Updated on 2021/09/21

写真b

 
HORIGUCHI Gorou
 
*Items subject to periodic update by Rikkyo University (The rest are reprinted from information registered on researchmap.)
Affiliation*
College of Science Department of Life Science
Graduate School of Science Field of Study: Life Science
Graduate School of Science Field of Study: Life Science
Title*
Professor
Degree
博士(理学) ( 九州大学 )
Contact information
Mail Address
Research Theme*
  • 顕花植物のモデルであるシロイヌナズナを用いて、器官形態形成に関する研究を行っている。具体的には、①細胞増殖と細胞伸長を統御し、葉のサイズを決定する機構、②葉の表と裏の領域を決定し、扁平な葉の構造を作り出す機構、③根の枝分かれを生み出す機構について、遺伝学的、発生学的、分子生物学的手法を用いて解析を進めている。

  • Research Interests
  • molecular biology

  • Plant developmental biology

  • Campus Career*
    • 4 2018 - Present 
      College of Science   Department of Life Science   Professor
    • 4 2018 - Present 
      Graduate School of Science   Field of Study: Life Science   Professor
    • 4 2018 - Present 
      Graduate School of Science   Field of Study: Life Science   Professor
    • 10 2008 - 3 2018 
      College of Science   Department of Life Science   Associate Professor
     

    Research Areas

    • Life Science / Plant molecular biology and physiology

    Research History

    • 4 2018 - Present 
      RIKKYO UNIVERSITY   College of Science Department of Life Science   Professor

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    • 4 2018 - Present 
      RIKKYO UNIVERSITY   Graduate School of Science Field of Study: Life Science   Professor

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    • 4 2018 - Present 
      RIKKYO UNIVERSITY   Graduate School of Science Field of Study: Life Science   Professor

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    • 10 2008 - 3 2018 
      RIKKYO UNIVERSITY   College of Science Department of Life Science   Associate Professor

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    • 11 2006 - 9 2008 
      The University of Tokyo   Graduate School of Science

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    • 5 2002 - 10 2006 
      国立岡崎共同研究機構基礎生物学研究所統合バイオサイエンスセンター   助手

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    • 4 2004 - 3 2006 
      自然科学研究機構・岡崎統合バイオサイエンスセンター   助手

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    • 4 2004 - 3 2006 
      自然科学研究機構・岡崎統合バイオサイエンスセンター   助手

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    • 4 2001 - 4 2002 
      理化学研究所植物科学研究センター   研究員

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    • 4 2001 - 4 2002 
      理化学研究所植物科学研究センター   研究員

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    • 4 1999 - 3 2001 
      日本学術振興会特別研究員PD   日本学術振興会特別研究員

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    • 4 1999 - 3 2001 
      日本学術振興会特別研究員PD   日本学術振興会特別研究員

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    • 4 1996 - 3 1999 
      日本学術振興会特別研究員DC1   日本学術振興会特別研究員

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    • 4 1996 - 3 1999 
      日本学術振興会特別研究員DC1   日本学術振興会特別研究員

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    Education

    • - 3 1999 
      Kyushu University   Graduate School, Division of Natural Science   Department of Biology

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      Country: Japan

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    • - 3 1994 
      Kyushu University   Faculty of Science

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      Country: Japan

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    Committee Memberships

    • 4 2018 - Present 
      日本植物形態学会   Plant Morphology 編集委員長

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    • 2010 - Present 
      Frontiers in Plant Science Review Editor

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    • 2018 - 2021 
      日本植物生理学会   代議員

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    • 4 2015 - 3 2018 
      日本植物学会   Journal of Plant Research Editorial Board

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    • 4 2009 - 3 2013 
      日本植物学会   ホームページ委員

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      Committee type:Academic society

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    Awards

    • 9 2008  
      日本植物学会  日本植物学会 奨励賞 
       
      堀口吾朗

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      Award type:Award from Japanese society, conference, symposium, etc.  Country:Japan

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    • 9 2006  
      日本植物形態学会  日本植物形態学会 奨励賞 
       
      堀口吾朗

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      Award type:Award from Japanese society, conference, symposium, etc.  Country:Japan

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    Papers

    • Stem integrity in Arabidopsis thaliana requires a load-bearing epidermis. International journal

      Mariko Asaoka, Mao Ooe, Shizuka Gunji, Pascale Milani, Gaël Runel, Gorou Horiguchi, Olivier Hamant, Shinichiro Sawa, Hirokazu Tsukaya, Ali Ferjani

      Development (Cambridge, England)148 ( 4 )   26 2 2021

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      Language:English   Publishing type:Research paper (scientific journal)  

      Because plant cells are glued to each other via their cell walls, failure to coordinate growth among adjacent cells can create cracks in tissues. Here, we find that the unbalanced growth of inner and outer tissues in the clavata3 de-etiolated3 (clv3 det3) mutant of Arabidopsis thaliana stretched epidermal cells, ultimately generating cracks in stems. Stem growth slowed before cracks appeared along clv3 det3 stems, whereas inner pith cells became drastically distorted and accelerated their growth, yielding to stress, after the appearance of cracks. This is consistent with a key role of the epidermis in restricting growth. Mechanical property measurements recorded using an atomic force microscope revealed that epidermal cell wall stiffness decreased in det3 and clv3 det3 epidermises. Thus, we hypothesized that stem integrity depends on the epidermal resistance to mechanical stress. To formally test this hypothesis, we used the DET3 gene as part of a tissue-specific strategy to complement cell expansion defects. Epidermis-driven DET3 expression restored growth and restored the frequency of stem cracking to 20% of the clv3 det3 mutant, demonstrating the DET3-dependent load-bearing role of the epidermis.

      DOI: 10.1242/dev.198028

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    • Metabolic Control of Gametophore Shoot Formation through Arginine in the Moss Physcomitrium patens. International journal

      Kensuke Kawade, Gorou Horiguchi, Yuu Hirose, Akira Oikawa, Masami Yokota Hirai, Kazuki Saito, Tomomichi Fujita, Hirokazu Tsukaya

      Cell reports32 ( 10 ) 108127 - 108127   8 9 2020

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      Shoot formation is accompanied by active cell proliferation and expansion, requiring that metabolic state adapts to developmental control. Despite the importance of such metabolic reprogramming, it remains unclear how development and metabolism are integrated. Here, we show that disruption of ANGUSTIFOLIA3 orthologs (PpAN3s) compromises gametophore shoot formation in the moss Physcomitrium patens due to defective cell proliferation and expansion. Trans-omics analysis reveals that the downstream activity of PpAN3 is linked to arginine metabolism. Elevating arginine level by chemical treatment leads to stunted gametophores and causes Ppan3 mutant-like transcriptional changes in the wild-type plant. Furthermore, ectopic expression of AtAN3 from Arabidopsis thaliana ameliorates the defective arginine metabolism and promotes gametophore formation in Ppan3 mutants. Together, these findings indicate that arginine metabolism is a key pathway associated with gametophore formation and provide evolutionary insights into the establishment of the shoot system in land plants through the integration of developmental and metabolic processes.

      DOI: 10.1016/j.celrep.2020.108127

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    • an3-Mediated Compensation Is Dependent on a Cell-Autonomous Mechanism in Leaf Epidermal Tissue.

      Mamoru Nozaki, Kensuke Kawade, Gorou Horiguchi, Hirokazu Tsukaya

      Plant & cell physiology61 ( 6 ) 1181 - 1190   1 6 2020

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      Leaves are formed by coordinated growth of tissue layers driven by cell proliferation and expansion. Compensation, in which a defect in cell proliferation induces compensated cell enlargement (CCE), plays an important role in cell-size determination during leaf development. We previously reported that CCE triggered by the an3 mutation is observed in epidermal and subepidermal layers in Arabidopsis thaliana (Arabidopsis) leaves. Interestingly, CCE is induced in a non-cell autonomous manner between subepidermal cells. However, whether CCE in the subepidermis affects cell size in the adjacent epidermis is still unclear. We induced layer-specific expression of AN3 in an3 leaves and found that CCE in the subepidermis had little impact on cell-size determination in the epidermis, and vice versa, suggesting that CCE is induced in a tissue-autonomous manner. Examination of the epidermis in an3 leaves having AN3-positive and -negative sectors generated by Cre/loxP revealed that, in contrast to the subepidermis, CCE occurred exclusively in AN3-negative epidermal cells, indicating a cell autonomous action of an3-mediated compensation in the epidermis. These results clarified that the epidermal and subepidermal tissue layers have different cell autonomies in CCE. In addition, quantification of cell-expansion kinetics in epidermal and subepidermal tissues of the an3 showed that the tissues exhibited a similar temporal profile to reach a peak cell-expansion rate as compared to wild type. This might be one feature representing that the two tissue layers retain their growth coordination even in the presence of CCE.

      DOI: 10.1093/pcp/pcaa048

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    • Suppression of class I compensated cell enlargement by xs2 mutation is mediated by salicylic acid signaling. Peer-reviewed International journal

      Ushio Fujikura, Kazune Ezaki, Gorou Horiguchi, Mitsunori Seo, Yuri Kanno, Yuji Kamiya, Michael Lenhard, Hirokazu Tsukaya

      PLoS genetics16 ( 6 ) e1008873 - e1008873   6 2020

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:Public Library of Science (PLoS)  

      The regulation of leaf size has been studied for decades. Enhancement of post-mitotic cell expansion triggered by impaired cell proliferation in Arabidopsis is an important process for leaf size regulation, and is known as compensation. This suggests a key interaction between cell proliferation and cell expansion during leaf development. Several studies have highlighted the impact of this integration mechanism on leaf size determination; however, the molecular basis of compensation remains largely unknown. Previously, we identified extra-small sisters (xs) mutants which can suppress compensated cell enlargement (CCE) via a specific defect in cell expansion within the compensation-exhibiting mutant, angustifolia3 (an3). Here we revealed that one of the xs mutants, namely xs2, can suppress CCE not only in an3 but also in other compensation-exhibiting mutants erecta (er) and fugu2. Molecular cloning of XS2 identified a deleterious mutation in CATION CALCIUM EXCHANGER 4 (CCX4). Phytohormone measurement and expression analysis revealed that xs2 shows hyper activation of the salicylic acid (SA) response pathway, where activation of SA response can suppress CCE in compensation mutants. All together, these results highlight the regulatory connection which coordinates compensation and SA response.

      DOI: 10.1371/journal.pgen.1008873

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    • The bRPS6-Family Protein RFC3 Prevents Interference by the Splicing Factor CFM3b during Plastid rRNA Biogenesis in Arabidopsis thaliana. Peer-reviewed International journal

      Yumi Nagashima, Katsutomo Ohshiro, Akiyasu Iwase, Miyuki T Nakata, Shugo Maekawa, Gorou Horiguchi

      Plants (Basel, Switzerland)9 ( 3 ) 328 - 328   4 3 2020

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:MDPI AG  

      Plastid ribosome biogenesis is important for plant growth and development. REGULATOR OF FATTY ACID COMPOSITION3 (RFC3) is a member of the bacterial ribosomal protein S6 family and is important for lateral root development. rfc3-2 dramatically reduces the plastid rRNA level and produces lateral roots that lack stem cells. In this study, we isolated a suppressor of rfc three2 (sprt2) mutant that enabled recovery of most rfc3 mutant phenotypes, including abnormal primary and lateral root development and reduced plastid rRNA level. Northern blotting showed that immature and mature plastid rRNA levels were reduced, with the exception of an early 23S rRNA intermediate, in rfc3-2 mutants. These changes were recovered in rfc3-2 sprt2-1 mutants, but a second defect in the processing of 16S rRNA appeared in this line. The results suggest that rfc3 mutants may be defective in at least two steps of plastid rRNA processing, one of which is specifically affected by the sprt2-1 mutation. sprt2-1 mutants had a mutation in CRM FAMILY MEMBER 3b (CFM3b), which encodes a plastid-localized splicing factor. A bimolecular fluorescence complementation (BiFC) assay suggested that RFC3 and SPRT2/CFM3b interact with each other in plastids. These results suggest that RFC3 suppresses the nonspecific action of SPRT2/CFM3b and improves the accuracy of plastid rRNA processing.

      DOI: 10.3390/plants9030328

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    • tRNA Wobble Modification Affects Leaf Cell Development in Arabidopsis thaliana. Peer-reviewed

      Yumi Nakai, Gorou Horiguchi, Kosei Iwabuchi, Akiko Harada, Masato Nakai, Ikuko Hara-Nishimura, Takato Yano

      Plant & cell physiology60 ( 9 ) 2026 - 2039   1 9 2019

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      The tRNA modification at the wobble position of Lys, Glu and Gln (wobbleU* modification) is responsible for the fine-tuning of protein translation efficiency and translation rate. This modification influences organism function in accordance with growth and environmental changes. However, the effects of wobbleU* modification at the cellular, tissue, or individual level have not yet been elucidated. In this study, we show that sulfur modification of wobbleU* of the tRNAs affects leaf development in Arabidopsis thaliana. The sulfur modification was impaired in the two wobbleU*-modification mutants: the URM1-like protein-defective mutant and the Elongator complex-defective mutants. Analyses of the mutant phenotypes revealed that the deficiency in the wobbleU* modification increased the airspaces in the leaves and the leaf size without affecting the number and the area of palisade mesophyll cells. On the other hand, both mutants exhibited increased number of leaf epidermal pavement cells but with reduced cell size. The deficiency in the wobbleU* modification also delayed the initiation of the endoreduplication processes of mesophyll cells. The phenotype of ASYMMETRIC LEAVES2-defective mutant was enhanced in the Elongator-defective mutants, while it was unchanged in the URM1-like protein-defective mutant. Collectively, the findings of this study suggest that the tRNA wobbleU* modification plays an important role in leaf morphogenesis by balancing the development between epidermal and mesophyll tissues.

      DOI: 10.1093/pcp/pcz064

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    • Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana. Peer-reviewed International journal

      Miyuki T Nakata, Mayuko Sato, Mayumi Wakazaki, Nozomi Sato, Koji Kojima, Akihiko Sekine, Shiori Nakamura, Toshiharu Shikanai, Kiminori Toyooka, Hirokazu Tsukaya, Gorou Horiguchi

      Biology open7 ( 2 )   5 2 2018

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      The plastid evolved from a symbiotic cyanobacterial ancestor and is an essential organelle for plant life, but its developmental roles in roots have been largely overlooked. Here, we show that plastid translation is connected to the stem cell patterning in lateral root primordia. The RFC3 gene encodes a plastid-localized protein that is a conserved bacterial ribosomal protein S6 of β/γ proteobacterial origin. The rfc3 mutant developed lateral roots with disrupted stem cell patterning and associated with decreased leaf photosynthetic activity, reduced accumulation of plastid rRNAs in roots, altered root plastid gene expression, and changes in expression of several root stem cell regulators. These results suggest that deficiencies in plastid function affect lateral root stem cells. Treatment with the plastid translation inhibitor spectinomycin phenocopied the defective stem cell patterning in lateral roots and altered plastid gene expression observed in the rfc3 mutant. Additionally, when prps17 defective in a plastid ribosomal protein was treated with low concentrations of spectinomycin, it also phenocopied the lateral root phenotypes of rfc3 The spectinomycin treatment and rfc3 mutation also negatively affected symplasmic connectivity between primary root and lateral root primordia. This study highlights previously unrecognized functions of plastid translation in the stem cell patterning in lateral roots.

      DOI: 10.1242/bio.028175

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    • OLIGOCELLULA1/HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 Promotes Cell Proliferation With HISTONE DEACETYLASE9 and POWERDRESS During Leaf Development in Arabidopsis thaliana. Peer-reviewed International journal

      Marina Suzuki, Nanae Shinozuka, Tomohiro Hirakata, Miyuki T Nakata, Taku Demura, Hirokazu Tsukaya, Gorou Horiguchi

      Frontiers in plant science9   580 - 580   2018

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      Organ size regulation is dependent on the precise spatial and temporal regulation of cell proliferation and cell expansion. A number of transcription factors have been identified that play a key role in the determination of aerial lateral organ size, but their functional relationship to various chromatin modifiers has not been well understood. To understand how leaf size is regulated, we previously isolated the oligocellula1 (oli1) mutant of Arabidopsis thaliana that develops smaller first leaves than the wild type (WT) mainly due to a reduction in the cell number. In this study, we further characterized oli1 leaf phenotypes and identified the OLI1 gene as well as interaction partners of OLI1. Detailed characterizations of leaf development suggested that the cell proliferation rate in oli1 leaf primordia is lower than that in the WT. In addition, oli1 was associated with a slight delay of the progression from the juvenile to adult phases of leaf traits. A classical map-based approach demonstrated that OLI1 is identical to HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENES15 (HOS15). HOS15/OLI1 encodes a homolog of human transducin β-like protein1 (TBL1). TBL1 forms a transcriptional repression complex with the histone deacetylase (HDAC) HDAC3 and either nuclear receptor co-repressor (N-CoR) or silencing mediator for retinoic acid and thyroid receptor (SMRT). We found that mutations in HISTONE DEACETYLASE9 (HDA9) and a switching-defective protein 3, adaptor 2, N-CoR, and transcription factor IIIB-domain protein gene, POWERDRESS (PWR), showed a small-leaf phenotype similar to oli1. In addition, hda9 and pwr did not further enhance the oli1 small-leaf phenotype, suggesting that these three genes act in the same pathway. Yeast two-hybrid assays suggested physical interactions, wherein PWR probably bridges HOS15/OLI1 and HDA9. Earlier studies suggested the roles of HOS15, HDA9, and PWR in transcriptional repression. Consistently, transcriptome analyses showed several genes commonly upregulated in the three mutants. From these findings, we propose a possibility that HOS15/OLI1, PWR, and HDA9 form an evolutionary conserved transcription repression complex that plays a positive role in the regulation of final leaf size.

      DOI: 10.3389/fpls.2018.00580

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    • The 5’ UTR intron-mediated enhancement of constitutive splicing of the tobacco microsome w-3 fatty acid desaturase gene Peer-reviewed

      Ohta, S, Nakagawara, S, Hirai, S, Miyaghishima, K, Horiguchi, G, Kodama, H

      Plant Biotechnology12   105 - 114   2018

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    • Evidence for a Role of ANAC082 as a Ribosomal Stress Response Mediator Leading to Growth Defects and Developmental Alterations in Arabidopsis. Peer-reviewed International journal

      Iwai Ohbayashi, Chung-Yi Lin, Naoki Shinohara, Yoko Matsumura, Yasunori Machida, Gorou Horiguchi, Hirokazu Tsukaya, Munetaka Sugiyama

      The Plant cell29 ( 10 ) 2644 - 2660   10 2017

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:AMER SOC PLANT BIOLOGISTS  

      Ribosome-related mutants in Arabidopsis thaliana share several notable characteristics regarding growth and development, which implies the existence of a common pathway that responds to disorders in ribosome biogenesis. As a first step to explore this pathway genetically, we screened a mutagenized population of root initiation defective2 (rid2), a temperature-sensitive mutant that is impaired in pre-rRNA processing, and isolated suppressor of root initiation defective two1 (sriw1), a suppressor mutant in which the defects of cell proliferation observed in rid2 at the restrictive temperature was markedly rescued. sriw1 was identified as a missense mutation of the NAC transcription factor gene ANAC082 The sriw1 mutation greatly alleviated the developmental abnormalities of rid2 and four other tested ribosome-related mutants, including rid3 However, the impaired pre-rRNA processing in rid2 and rid3 was not relieved by sriw1 Expression of ANAC082 was localized to regions where phenotypic effects of ribosome-related mutations are readily evident and was elevated in rid2 and rid3 compared with the wild type. These findings suggest that ANAC082 acts downstream of perturbation of biogenesis of the ribosome and may mediate a set of stress responses leading to developmental alterations and cell proliferation defects.

      DOI: 10.1105/tpc.17.00255

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    • Spatially Different Tissue-Scale Diffusivity Shapes ANGUSTIFOLIA3 Gradient in Growing Leaves. Peer-reviewed International journal

      Kensuke Kawade, Hirokazu Tanimoto, Gorou Horiguchi, Hirokazu Tsukaya

      Biophysical journal113 ( 5 ) 1109 - 1120   5 9 2017

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:CELL PRESS  

      The spatial gradient of signaling molecules is pivotal for establishing developmental patterns of multicellular organisms. It has long been proposed that these gradients could arise from the pure diffusion process of signaling molecules between cells, but whether this simplest mechanism establishes the formation of the tissue-scale gradient remains unclear. Plasmodesmata are unique channel structures in plants that connect neighboring cells for molecular transport. In this study, we measured cellular- and tissue-scale kinetics of molecular transport through plasmodesmata in Arabidopsis thaliana developing leaf primordia by fluorescence recovery assays. These trans-scale measurements revealed biophysical properties of diffusive molecular transport through plasmodesmata and revealed that the tissue-scale diffusivity, but not the cellular-scale diffusivity, is spatially different along the leaf proximal-to-distal axis. We found that the gradient in cell size along the developmental axis underlies this spatially different tissue-scale diffusivity. We then asked how this diffusion-based framework functions in establishing a signaling gradient of endogenous molecules. ANGUSTIFOLIA3 (AN3) is a transcriptional co-activator, and as we have shown here, it forms a long-range signaling gradient along the leaf proximal-to-distal axis to determine a cell-proliferation domain. By genetically engineering AN3 mobility, we assessed each contribution of cell-to-cell movement and tissue growth to the distribution of the AN3 gradient. We constructed a diffusion-based theoretical model using these quantitative data to analyze the AN3 gradient formation and demonstrated that it could be achieved solely by the diffusive molecular transport in a growing tissue. Our results indicate that the spatially different tissue-scale diffusivity is a core mechanism for AN3 gradient formation. This provides evidence that the pure diffusion process establishes the formation of the long-range signaling gradient in leaf development.

      DOI: 10.1016/j.bpj.2017.06.072

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    • Double-stranded RNA-binding protein DRB3 negatively regulates anthocyanin biosynthesis by modulating PAP1 expression in Arabidopsis thaliana. Peer-reviewed

      Hikaru Sawano, Takuma Matsuzaki, Tomoyuki Usui, Midori Tabara, Akihito Fukudome, Akihiro Kanaya, Daichi Tanoue, Akihiro Hiraguri, Gorou Horiguchi, Misato Ohtani, Taku Demura, Toshinori Kozaki, Kazuo Ishii, Hiromitsu Moriyama, Toshiyuki Fukuhara

      Journal of plant research130 ( 1 ) 45 - 55   1 2017

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      The model plant Arabidopsis thaliana has five double-stranded RNA-binding proteins (DRB1-DRB5), two of which, DRB1 and DRB4, are well characterized. In contrast, the functions of DRB2, DRB3 and DRB5 have yet to be elucidated. In this study, we tried to uncover their functions using drb mutants and DRB-over-expressed lines. In over-expressed lines of all five DRB genes, the over-expression of DRB2 or DRB3 (DRB2ox or DRB3ox) conferred a downward-curled leaf phenotype, but the expression profiles of ten small RNAs were similar to that of the wild-type (WT) plant. Phenotypes were examined in response to abiotic stresses. Both DRB2ox and DRB3ox plants exhibited salt-tolerance. When these plants were exposed to cold stress, drb2 and drb3 over-accumulated anthocyanin but DRB2ox and DRB3ox did not. Therefore, the over-expression of DRB2 or DRB3 had pleiotropic effects on host plants. Microarray and deep-sequencing analyses indicated that several genes encoding key enzymes for anthocyanin biosynthesis, including chalcone synthase (CHS), dihydroflavonol reductase (DFR) and anthocyanidin synthase (ANS), were down-regulated in DRB3ox plants. When DRB3ox was crossed with the pap1-D line, which is an activation-tagged transgenic line that over-expresses the key transcription factor PAP1 (Production of anthocyanin pigmentation1) for anthocyanin biosynthesis, over-expression of DRB3 suppressed the expression of PAP1, CHS, DFR and ANS genes. DRB3 negatively regulates anthocyanin biosynthesis by modulating the level of PAP1 transcript. Since two different small RNAs regulate PAP1 gene expression, a possible function of DRB3 for small RNA biogenesis is discussed.

      DOI: 10.1007/s10265-016-0886-0

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    • Two Nucleolar Proteins, GDP1 and OLI2, Function As Ribosome Biogenesis Factors and Are Preferentially Involved in Promotion of Leaf Cell Proliferation without Strongly Affecting Leaf Adaxial-Abaxial Patterning in Arabidopsis thaliana. Peer-reviewed International journal

      Koji Kojima, Junya Tamura, Hiroto Chiba, Kanae Fukada, Hirokazu Tsukaya, Gorou Horiguchi

      Frontiers in plant science8   2240 - 2240   2017

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:Frontiers Media S.A.  

      Leaf abaxial-adaxial patterning is dependent on the mutual repression of leaf polarity genes expressed either adaxially or abaxially. In Arabidopsis thaliana, this process is strongly affected by mutations in ribosomal protein genes and in ribosome biogenesis genes in a sensitized genetic background, such as asymmetric leaves2 (as2). Most ribosome-related mutants by themselves do not show leaf abaxialization, and one of their typical phenotypes is the formation of pointed rather than rounded leaves. In this study, we characterized two ribosome-related mutants to understand how ribosome biogenesis is linked to several aspects of leaf development. Previously, we isolated oligocellula2 (oli2) which exhibits the pointed-leaf phenotype and has a cell proliferation defect. OLI2 encodes a homolog of Nop2 in Saccharomyces cerevisiae, a ribosome biogenesis factor involved in pre-60S subunit maturation. In this study, we found another pointed-leaf mutant that carries a mutation in a gene encoding an uncharacterized protein with a G-patch domain. Similar to oli2, this mutant, named g-patch domain protein1 (gdp1), has a reduced number of leaf cells. In addition, gdp1 oli2 double mutants showed a strong genetic interaction such that they synergistically impaired cell proliferation in leaves and produced markedly larger cells. On the other hand, they showed additive phenotypes when combined with several known ribosomal protein mutants. Furthermore, these mutants have a defect in pre-rRNA processing. GDP1 and OLI2 are strongly expressed in tissues with high cell proliferation activity, and GDP1-GFP and GFP-OLI2 are localized in the nucleolus. These results suggest that OLI2 and GDP1 are involved in ribosome biogenesis. We then examined the effects of gdp1 and oli2 on adaxial-abaxial patterning by crossing them with as2. Interestingly, neither gdp1 nor oli2 strongly enhanced the leaf polarity defect of as2. Similar results were obtained with as2 gdp1 oli2 triple mutants although they showed severe growth defects. These results suggest that the leaf abaxialization phenotype induced by ribosome-related mutations is not merely the result of a general growth defect and that there may be a sensitive process in the ribosome biogenesis pathway that affects adaxial-abaxial patterning when compromised by a mutation.

      DOI: 10.3389/fpls.2017.02240

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    • Nitrogen dioxide regulates organ growth by controlling cell proliferation and enlargement in Arabidopsis Peer-reviewed

      Misa Takahashi, Takamasa Furuhashi, Naoko Ishikawa, Gorou Horiguchi, Atsushi Sakamoto, Hirokazu Tsukaya, Hiromichi Morikawa

      NEW PHYTOLOGIST201 ( 4 ) 1304 - 1315   3 2014

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:WILEY-BLACKWELL  

      To gain more insight into the physiological function of nitrogen dioxide (NO2), we investigated the effects of exogenous NO2 on growth in Arabidopsis thaliana.
      Plants were grown in air without NO2 for 1 wk after sowing and then grown for 1-4 wk in air with (designated treated plants) or without (control plants) NO2. Plants were irrigated semiweekly with a nutrient solution containing 19.7 mM nitrate and 10.3 mM ammonium.
      Five-week-old plants treated with 50 ppb NO2 showed a <= 2.8-fold increase in biomass relative to controls. Treated plants also showed early flowering. The magnitude of the effects of NO2 on leaf expansion, cell proliferation and enlargement was greater in developing than in maturing leaves. Leaf areas were 1.3-8.4 times larger on treated plants than corresponding leaves on control plants. The NO2-induced increase in leaf size was largely attributable to cell proliferation in developing leaves, but was attributable to both cell proliferation and enlargement in maturing leaves. The expression of different sets of genes for cell proliferation and/or enlargement was induced by NO2, but depended on the leaf developmental stage.
      Collectively, these results indicated that NO2 regulates organ growth by controlling cell proliferation and enlargement.

      DOI: 10.1111/nph.12609

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    • Nitrogen dioxide regulates organ growth by controlling cell proliferation and enlargement in Arabidopsis. International journal

      Misa Takahashi, Takamasa Furuhashi, Naoko Ishikawa, Gorou Horiguchi, Atsushi Sakamoto, Hirokazu Tsukaya, Hiromichi Morikawa

      The New phytologist201 ( 4 ) 1304 - 1315   3 2014

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      • To gain more insight into the physiological function of nitrogen dioxide (NO₂), we investigated the effects of exogenous NO₂ on growth in Arabidopsis thaliana. • Plants were grown in air without NO₂ for 1 wk after sowing and then grown for 1-4 wk in air with (designated treated plants) or without (control plants) NO₂. Plants were irrigated semiweekly with a nutrient solution containing 19.7 mM nitrate and 10.3 mM ammonium. • Five-week-old plants treated with 50 ppb NO₂ showed a ≤ 2.8-fold increase in biomass relative to controls. Treated plants also showed early flowering. The magnitude of the effects of NO₂ on leaf expansion, cell proliferation and enlargement was greater in developing than in maturing leaves. Leaf areas were 1.3-8.4 times larger on treated plants than corresponding leaves on control plants. The NO₂-induced increase in leaf size was largely attributable to cell proliferation in developing leaves, but was attributable to both cell proliferation and enlargement in maturing leaves. The expression of different sets of genes for cell proliferation and/or enlargement was induced by NO₂, but depended on the leaf developmental stage. • Collectively, these results indicated that NO₂ regulates organ growth by controlling cell proliferation and enlargement.

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    • Enhanced cell expansion in a KRP2 overexpressor is mediated by increased V-ATPase activity. Peer-reviewed

      Ali Ferjani, Kazuki Ishikawa, Mariko Asaoka, Masanori Ishida, Gorou Horiguchi, Masayoshi Maeshima, Hirokazu Tsukaya

      Plant & cell physiology54 ( 12 ) 1989 - 98   12 2013

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      Decreased cell numbers during leaf development often trigger increased cell size, a phenomenon called compensation. In compensation-exhibiting mutants, the unusually high cell expansion activity occurs through two different mechanisms during the post-mitotic stage of leaf development, except in the KIP-RELATED PROTEIN 2-overexpressing line (KRP2 o/e), whose cell sizes are 2-fold greater during proliferative growth. However, the molecular basis of compensated cell expansion (CCE) has not been characterized. The det3-1 mutant has a mutation in the C-subunit of the vacuolar-type H(+)-ATPase (V-ATPase) complex that causes a 50% decrease in its activity and cell size. To determine the contribution of V-ATPase activity to CCE, the cellular phenotypes of double mutants between det3-1 and compensation-exhibiting fugu5-1, an3-4, fas1-5 and KRP2 o/e were analyzed in detail. Interestingly, while decreased V-ATPase activity caused by det3-1 did not suppress CCE in fugu5-1, fas1-5 and an3-4, CCE in KRP2 o/e was totally suppressed. Furthermore, measurements revealed that the activity and quantity of the A-subunit of the V-ATPase complex were significantly increased in the shoots of KRP2 o/e plants. Importantly, the unusually increased size of actively dividing KRP2 o/e cells was restored to normal in the det3-1 background. Taken together, our data strongly suggest that CCE in KRP2 o/e, but not in other compensation-exhibiting mutants, occurs exclusively through the increase of V-ATPase activity.

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    • Class III compensation, represented by KRP2 overexpression, depends on V-ATPase activity in proliferative cells. Peer-reviewed International journal

      Ali Ferjani, Kazuki Ishikawa, Mariko Asaoka, Masanori Ishida, Gorou Horiguchi, Masayoshi Maeshima, Hirokazu Tsukaya

      Plant signaling & behavior8 ( 11 ) e27204 - e27204   11 2013

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      Compensation refers to an increase in cell size when the cell number is significantly decreased due to the mutation or gain of function of a gene that negatively affects the cell cycle. Given the importance of coordinated growth during organogenesis in both animal and plant systems, compensation is important to understand the mechanism of size regulation. In leaves, cell division precedes cell differentiation (which involves cell expansion); therefore, a decrease in cell number triggers enhanced cell expansion (compensated cell expansion; hereafter, CCE). Functional analyses of genes for which a loss or gain of function triggers compensation have increased our understanding of the molecular mechanisms underlying the decrease in cell number. Nevertheless, the mechanisms that induce enhanced cell expansion (the link between cell cycling and expansion), as well as the cellular machinery mediating CCE, have not been characterized. We recently characterized an important pathway involved in cell enlargement in KRP2-overexpressing plants. Here, we discuss the potential axial role of plant KRPs in triggering enlargement in cells with meristematic features.

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    • Promotion of chloroplast proliferation upon enhanced post-mitotic cell expansion in leaves. Peer-reviewed International journal

      Kensuke Kawade, Gorou Horiguchi, Naoko Ishikawa, Masami Yokota Hirai, Hirokazu Tsukaya

      BMC plant biology13 ( 1 ) 143 - 143   28 9 2013

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      BACKGROUND: Leaves are determinate organs; hence, precise control of cell proliferation and post-mitotic cell expansion is essential for their growth. A defect in cell proliferation often triggers enhanced post-mitotic cell expansion in leaves. This phenomenon is referred to as 'compensation'. Several lines of evidence from studies on compensation have shown that cell proliferation and post-mitotic cell expansion are coordinately regulated during leaf development. Therefore, compensation has attracted much attention to the mechanisms for leaf growth. However, our understanding of compensation at the subcellular level remains limited because studies of compensation have focused mainly on cellular-level phenotypes. Proper leaf growth requires quantitative control of subcellular components in association with cellular-level changes. To gain insight into the subcellular aspect of compensation, we investigated the well-known relationship between cell area and chloroplast number per cell in compensation-exhibiting lines, and asked whether chloroplast proliferation is modulated in response to the induction of compensation. RESULTS: We first established a convenient and reliable method for observation of chloroplasts in situ. Using this method, we analyzed Arabidopsis thaliana mutants fugu5 and angustifolia3 (an3), and a transgenic line KIP-RELATED PROTEIN2 overexpressor (KRP2 OE), which are known to exhibit typical features of compensation. We here showed that chloroplast number per cell increased in the subepidermal palisade tissue of these lines. We analyzed tetraploidized wild type, fugu5, an3 and KRP2 OE, and found that cell area itself, but not nuclear ploidy, is a key parameter that determines the activity of chloroplast proliferation. In particular, in the case of an3, we uncovered that promotion of chloroplast proliferation depends on the enhanced post-mitotic cell expansion. The expression levels of chloroplast proliferation-related genes are similar to or lower than that in the wild type during this process. CONCLUSIONS: This study demonstrates that chloroplast proliferation is promoted in compensation-exhibiting lines. This promotion of chloroplast proliferation takes place in response to cell-area increase in post-mitotic phase in an3. The expression of chloroplast proliferation-related genes were not promoted in compensation-exhibiting lines including an3, arguing that an as-yet-unknown mechanism is responsible for modulation of chloroplast proliferation in these lines.

      DOI: 10.1186/1471-2229-13-143

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    • The ATM-dependent DNA damage response acts as an upstream trigger for compensation in the fas1 mutation during Arabidopsis leaf development. Peer-reviewed International journal

      Tetsuya Hisanaga, Ali Ferjani, Gorou Horiguchi, Naoko Ishikawa, Ushio Fujikura, Minoru Kubo, Taku Demura, Hiroo Fukuda, Takashi Ishida, Keiko Sugimoto, Hirokazu Tsukaya

      Plant physiology162 ( 2 ) 831 - 41   6 2013

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      During leaf development, a decrease in cell number often triggers an increase in cell size. This phenomenon, called compensation, suggests that some system coordinates cell proliferation and cell expansion, but how this is mediated at the molecular level is still unclear. The fugu2 mutants in Arabidopsis (Arabidopsis thaliana) exhibit typical compensation phenotypes. Here, we report that the FUGU2 gene encodes FASCIATA1 (FAS1), the p150 subunit of Chromatin Assembly Factor1. To uncover how the fas1 mutation induces compensation, we performed microarray analyses and found that many genes involved in the DNA damage response are up-regulated in fas1. Our genetic analysis further showed that activation of the DNA damage response and the accompanying decrease of cell number in fas1 depend on ATAXIA TELANGIECTASIA MUTATED (ATM) but not on ATM AND RAD3 RELATED. Kinematic analysis suggested that the delay in the cell cycle leads to a decrease in cell number in fas1 and that loss of ATM partially restores this phenotype. Consistently, both cell size phenotypes and high ploidy phenotypes of fas1 are also suppressed by atm, supporting that the ATM-dependent DNA damage response leads to these phenotypes. Altogether, these data suggest that the ATM-dependent DNA damage response acts as an upstream trigger in fas1 to delay the cell cycle and promote entry into the endocycle, resulting in compensated cell expansion.

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    • ANGUSTIFOLIA3 signaling coordinates proliferation between clonally distinct cells in leaves. Peer-reviewed International journal

      Kensuke Kawade, Gorou Horiguchi, Takeshi Usami, Masami Yokota Hirai, Hirokazu Tsukaya

      Current biology : CB23 ( 9 ) 788 - 92   6 5 2013

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      Coordinated proliferation between clonally distinct cells via inter-cell-layer signaling largely determines the size and shape of plant organs. Nonetheless, the signaling mechanism underlying this coordination in leaves remains elusive because of a lack of understanding of the signaling molecule (or molecules) involved. ANGUSTIFOLIA3 (AN3, also called GRF-INTERACTING FACTOR1) encodes a putative transcriptional coactivator with homology to human synovial sarcoma translocation protein. AN3 transcripts accumulate in mesophyll cells but are not detectable in leaf epidermal cells. However, we found here that in addition to mesophyll cells, epidermal cells of an3 leaves show defective proliferation. This spatial difference between the accumulation pattern of AN3 transcripts and an3 leaf phenotype is explained by AN3 protein movement across cell layers. AN3 moves into epidermal cells after being synthesized within mesophyll cells and helps control epidermal cell proliferation. Interference with AN3 movement results in abnormal leaf size and shape, indicating that AN3 signaling is indispensable for normal leaf development. AN3 movement does not require type II chaperonin activity, which is needed for movement of some mobile proteins. Taking these findings together, we present a novel model emphasizing the role of mesophyll cells as a signaling source coordinating proliferation between clonally independent leaf cells.

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    • The ATM-dependent DNA damage response acts as an upstream trigger for compensation in the fas1 mutation during Arabidopsis leaf development Peer-reviewed

      Hisanaga, T, Ferjani, A, Horiguchi, G, Ishikawa, N, Fujikura, U, Kubo, M, Demura, T, Fukuda, H, Ishida, T, Sugimoto, K, Tsukaya, H

      Plant Physiology   2013

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    • Berberine enhances defects in the establishment of leaf polarity in asymmetric leaves1 and asymmetric leaves2 of Arabidopsis thaliana. Peer-reviewed International journal

      Ayami Nakagawa, Hiro Takahashi, Shoko Kojima, Nobuo Sato, Kazuomi Ohga, Byung Yoon Cha, Je-Tae Woo, Kazuo Nagai, Gorou Horiguchi, Hirokazu Tsukaya, Yasunori Machida, Chiyoko Machida

      Plant molecular biology79 ( 6 ) 569 - 81   8 2012

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      Leaves develop as flat lateral organs from the indeterminate shoot apical meristem. The establishment of polarity along three-dimensional axes, proximal-distal, medial-lateral, and adaxial-abaxial axes, is crucial for the growth of normal leaves. The mutations of ASYMMETRIC LEAVES1 (AS1) and AS2 of Arabidopsis thaliana cause defects in repression of the indeterminate state and the establishment of axis formation in leaves. Although many mutations have been identified that enhance the adaxial-abaxial polarity defects of as1 and as2 mutants, the roles of the causative genes in leaf development are still unknown. In this study, we found that wild-type plants treated with berberine produced pointed leaves, which are often observed in the single mutants that enhance phenotypes of as1 and as2 mutants. The berberine-treated as1 and as2 mutants formed abaxialized filamentous leaves. Berberine, an isoquinoline alkaloid compound naturally produced in various plant sources, has a growth inhibitory effect on plants that do not produce berberine. We further showed that transcript levels of meristem-specific class 1 KNOX homeobox genes and abaxial determinant genes were increased in berberine-treated as1 and as2. Berberine treated plants carrying double mutations of AS2 and the large subunit ribosomal protein gene RPL5B showed more severe defects in polarity than did the as2 single mutant plants. We suggest that berberine inhibits (a) factor(s) that might be required for leaf adaxial cell differentiation through a pathway independent of AS1 and AS2. Multiple pathways might play important roles in the formation of flat symmetric leaves.

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    • Stable establishment of cotyledon identity during embryogenesis in Arabidopsis by ANGUSTIFOLIA3 and HANABA TARANU Peer-reviewed

      Mari Kanei, Gorou Horiguchi, Hirokazu Tsukaya

      DEVELOPMENT139 ( 13 ) 2436 - 2446   7 2012

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      In seed plants, the shoot apical and root apical meristems form at the apical and basal poles of the embryonic axis, and leaves form at the flanks of the shoot apical meristem. ANGUSTIFOLIA3/GRF INTERACTING FACTOR1 (AN3/GIF1) encodes a putative transcriptional co-activator involved in various aspects of shoot development, including the maintenance of shoot apical meristems, cell proliferation and expansion in leaf primordia, and adaxial/abaxial patterning of leaves. Here, we report a novel function of AN3 involved in developmental fate establishment. We characterised an an3-like mutant that was found to be an allele of hanaba taranu (han), named han-30, and examined its genetic interactions with an3. an3 han double mutants exhibited severe defects in cotyledon development such that ectopic roots were formed at the apical region of the embryo, as confirmed by pWOX5::GFP expression. Additionally, gif2 enhanced the ectopic root phenotype of an3 han. Although the auxin accumulation pattern of the embryo was correct in an3 han-30, based on DR5rev::GFP expression at the globular stage, expression of the PLETHORA1 (PLT1), a master regulator of root development, expanded from the basal embryonic region to the apical region during the same developmental stage. Furthermore, the plt1 mutation suppressed ectopic root formation in an3 han. These data suggest that establishing cotyledon identity requires both AN3 and HAN to repress ectopic root formation by repressing PLT1 expression.

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    • Regulation of pyrophosphate levels by H+-PPase is central for proper resumption of early plant development Peer-reviewed

      Ali Ferjani, Shoji Segami, Gorou Horiguchi, Azusa Sakata, Masayoshi Maeshima, Hirokazu Tsukaya

      Plant Signaling and Behavior7 ( 1 ) 38 - 42   2012

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:Landes Bioscience  

      The synthesis of DNA, RNA, and de novo proteins is fundamental for early development of the seedling after germination, but such processes release pyrophosphate (PPi) as a byproduct of ATP hydrolysis. The over-accumulation of the inhibitory metabolite PPi in the cytosol hinders these biosynthetic reactions. All living organisms possess ubiquitous enzymes collectively called inorganic pyrophosphatases (PPases), which catalyze the hydrolysis of PPi into two orthophosphate (Pi) molecules. Defects in PPase activity cause severe developmental defects and/or growth arrest in several organisms. In higher plants, a proton-translocating vacuolar PPase (H+-PPase) uses the energy of PPi hydrolysis to acidify the vacuole. However, the biological implications of PPi hydrolysis are vague due to the widespread belief that the major role of H+-PPase in plants is vacuolar acidification. We have shown that the Arabidopsis fugu5 mutant phenotype, caused by a defect in H+-PPase activity, is rescued by complementation with the yeast cytosolic PPase IPP1. In addition, our analyses have revealed that increased cytosolic PPi levels impair postgerminative development in fugu5 by inhibiting gluconeogenesis. This led us to the conclusion that the role of H+-PPase as a proton-pump is negligible. Here, we present further evidence of the growth-boosting effects of removing PPi in later stages of plant vegetative development, and briefly discuss the biological role of PPases and their potential applications in different disciplines and in various organisms. © 2012 Landes Bioscience.

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    • ANGUSTIFOLIA, a plant homolog of CtBP/BARS, functions outside the nucleus Peer-reviewed

      Naoko Minamisawa, Mayuko Sato, Kiu-Hyung Cho, Hanako Ueno, Katsuaki Takechi, Masataka Kajikawa, Katsuyuki T. Yamato, Kanji Ohyama, Kiminori Toyooka, Gyung-Tae Kim, Gorou Horiguchi, Hiroyoshi Takano, Takashi Ueda, Hirokazu Tsukaya

      PLANT JOURNAL68 ( 5 ) 788 - 799   12 2011

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      CtBP/BARS is a unique protein family in having quite diversified cellular functions, intercellular localizations, and developmental roles. ANGUSTIFOLIA (AN) is the sole homolog of CtBP/BARS from Arabidopsis thaliana, although it has plant AN-specific motifs and a long C-terminus. Previous studies suggested that AN would function in the nucleus as a transcriptional co-repressor, as CtBPs function in animals; however, precise verification has been lacking. In this paper, we isolated a homologous gene (MAN) of AN from liverwort, Marchantia polymorpha. Transformation of the Arabidopsis an-1 mutant with 35S-driven MAN completely complemented the an-1 phenotype, although it lacks the putative nuclear localization signal (NLS) that exists in AN proteins isolated from other plant species. We constructed several plasmids for expressing modified ANs with amino acid substitutions in known motifs. The results clearly indicated that modified AN with mutations in the putative NLS-like domain could complement the an-1 phenotype. Therefore, we re-examined localization of AN using several techniques. Our results demonstrated that AN localizes on punctuate structures around the Golgi, partially overlapping with a trans-Golgi network resident, which highlighted an unexpected link between leaf development and membrane trafficking. We should reconsider the roles and evolutionary traits of AN based on these findings.

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    • Key Proliferative Activity in the Junction between the Leaf Blade and Leaf Petiole of Arabidopsis Peer-reviewed

      Yasunori Ichihashi, Kensuke Kawade, Takeshi Usami, Gorou Horiguchi, Taku Takahashi, Hirokazu Tsukaya

      PLANT PHYSIOLOGY157 ( 3 ) 1151 - 1162   11 2011

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      Leaves are the most important, fundamental units of organogenesis in plants. Although the basic form of a leaf is clearly divided into the leaf blade and leaf petiole, no study has yet revealed how these are differentiated from a leaf primordium. We analyzed the spatiotemporal pattern of mitotic activity in leaf primordia of Arabidopsis (Arabidopsis thaliana) in detail using molecular markers in combination with clonal analysis. We found that the proliferative zone is established after a short interval following the occurrence of a rod-shaped early leaf primordium; it is separated spatially from the shoot apical meristem and seen at the junction region between the leaf blade and leaf petiole and produces both leaf-blade and leaf-petiole cells. This proliferative region in leaf primordia is marked by activity of the ANGUSTIFOLIA3 (AN3) promoter as a whole and seems to be differentiated into several spatial compartments: activities of the CYCLIN D4;2 promoter and SPATULA enhancer mark parts of it specifically. Detailed analyses of the an3 and blade-on-petiole mutations further support the idea that organogenesis of the leaf blade and leaf petiole is critically dependent on the correct spatial regulation of the proliferative region of leaf primordia. Thus, the proliferative zone of leaf primordia is spatially differentiated and supplies both the leaf-blade and leaf-petiole cells.

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    • Keep an Eye on PPi: The Vacuolar-Type H+-Pyrophosphatase Regulates Postgerminative Development in Arabidopsis Peer-reviewed

      Ali Ferjani, Shoji Segami, Gorou Horiguchi, Yukari Muto, Masayoshi Maeshima, Hirokazu Tsukaya

      PLANT CELL23 ( 8 ) 2895 - 2908   8 2011

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      Postgerminative growth of seed plants requires specialized metabolism, such as gluconeogenesis, to support heterotrophic growth of seedlings until the functional photosynthetic apparatus is established. Here, we show that the Arabidopsis thaliana fugu5 mutant, which we show to be defective in AVP1 (vacuolar H+-pyrophosphatase), failed to support heterotrophic growth after germination. We found that exogenous supplementation of Suc or the specific removal of the cytosolic pyrophosphate (PPi) by the heterologous expression of the cytosolic inorganic pyrophosphatase1 (IPP1) gene from budding yeast (Saccharomyces cerevisiae) rescued fugu5 phenotypes. Furthermore, compared with the wild-type and AVP1(Pro):IPP1 transgenic lines, hypocotyl elongation in the fugu5 mutant was severely compromised in the dark but recovered upon exogenous supply of Suc to the growth media. Measurements revealed that the peroxisomal beta-oxidation activity, dry seed contents of storage lipids, and their mobilization were unaffected in fugu5. By contrast, fugu5 mutants contained similar to 2.5-fold higher PPi and similar to 50% less Suc than the wild type. Together, these results provide clear evidence that gluconeogenesis is inhibited due to the elevated levels of cytosolic PPi. This study demonstrates that the hydrolysis of cytosolic PPi, rather than vacuolar acidification, is the major function of AVP1/FUGU5 in planta. Plant cells optimize their metabolic function by eliminating PPi in the cytosol for efficient postembryonic heterotrophic growth.

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    • Differential contributions of ribosomal protein genes to Arabidopsis thaliana leaf development Peer-reviewed

      Gorou Horiguchi, Almudena Molla-Morales, Jose Manuel Perez-Perez, Kouji Kojima, Pedro Robles, Maria Rosa Ponce, Jose Luis Micol, Hirokazu Tsukaya

      PLANT JOURNAL65 ( 5 ) 724 - 736   3 2011

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      P>In Arabidopsis thaliana, mutations in genes encoding ribosomal proteins (r-proteins) perturb various developmental processes. Whether these perturbations are caused by overall ribosome insufficiency or partial dysfunction of the ribosome caused by deficiency of a particular ribosomal protein is not known. To distinguish these possibilities, a comparative study using several r-protein mutants was required. Here, we identified mutations in 11 r-protein genes from previously isolated denticulata and pointed-leaves mutants. Most of these mutations were associated with pointed leaves, with reduced growth due to a decrease in the number or size of palisade mesophyll and pavement cells. In addition, leaf abaxialization was usually observed when these r-protein mutations were combined with asymmetric leaves1 (as1) and as2 mutations. These results suggest that the establishment of leaf polarity is highly sensitive to ribosome functionality in general. However, several r-protein mutants showed a preference towards a specific developmental defect. For example, rpl4d mutations did not affect cell proliferation but caused strong abaxialization of leaves in the as1 and as2 backgrounds. On the other hand, rps28b enhanced leaf abaxialization of as2 to a weaker extent than expected on the basis of its negative effect on cell proliferation. In addition, hypomorphic rps6a alleles had the strongest effects on most of the phenotypes examined. These findings suggest that deficiencies in these three r-protein genes lead to production of dysfunctional ribosomes. Depending on their structural abnormalities, dysfunctional ribosomes may affect translation of specific transcripts involved in the regulation of some leaf developmental processes.

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    • ANGUSTIFOLIA3 Plays Roles in Adaxial/Abaxial Patterning and Growth in Leaf Morphogenesis Peer-reviewed

      Gorou Horiguchi, Hokuto Nakayama, Naoko Ishikawa, Minoru Kubo, Taku Demura, Hiroo Fukuda, Hirokazu Tsukaya

      PLANT AND CELL PHYSIOLOGY52 ( 1 ) 112 - 124   1 2011

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      Leaf morphogenesis relies on adaxial/abaxial patterning and extensive growth. This study investigated the role of ANGUSTIFOLIA3 (AN3) from Arabidopsis thaliana in these processes. The an3 mutants produce narrower leaves that contain significantly fewer cells than the wild type. We examined the genetic interaction between an3 and asymmetric leaves2 (as2), which has a weak adaxial defect. The an3 as2 mutants developed trumpet-like leaves and accumulated transcripts of abaxially expressed genes at higher levels than an3 and as2. Gene expression analyses suggested that an3 altered the expression of a number of genes. Many of them were involved in metabolism, and several genes that promote adaxial identity cooperatively with as2 were down-regulated. Next, we performed detailed developmental analyses to examine the relationship between the narrow-leaf phenotype of an3 and leaf polarity. As a result, we showed that AN3 is required during a specific phase after an oblong shape is established in early leaf primordia. During this phase, the angle of the cell division plane relative to the longitudinal axis of the leaf primordium is more variable than in the earlier phase where transverse divisions were dominant in both the wild type and an3. Correlated with this dynamic change in cell division pattern, the leaf primordium became rounder. In an3, mitotic activity was reduced more rapidly than in the wild type, causing premature termination of the morphometric change. These results suggest that AN3 promotes cell proliferation during a specific developmental phase that is also required to correct abaxial/adaxial patterning in concert with AS2.

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    • ROTUNDIFOLIA4 Regulates Cell Proliferation Along the Body Axis in Arabidopsis Shoot Peer-reviewed

      Momoko Ikeuchi, Takahiro Yamaguchi, Toshiya Kazama, Tasuku Ito, Gorou Horiguchi, Hirokazu Tsukaya

      PLANT AND CELL PHYSIOLOGY52 ( 1 ) 59 - 69   1 2011

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      Molecular genetics has been successful in identifying leaf-size regulators such as transcription factors, phytohormones, and signal molecules. Among them, a ROTUNDIFOLIA4-LIKE/DEVIL (RTFL/DVL) family of Arabidopsis, genes encoding peptides with no secretion-signal sequence, is unique in that their overexpressors have a reduced number of leaf cells specifically along the proximodistal axis. However, because the RTFL/DVL lack any obvious homology with functionally identified domains, and because of genetic redundancy among RTFL/DVL, their molecular and developmental roles are unclear. In this study we focused on one member in the family, ROTUNDIFOLIA4 (ROT4), and identified the core functional region within it and we found no proteolytic processing in planta. Developmental analysis of leaf primordia revealed that ROT4 overexpression reduces the meristematic zone size within the leaf blade. Moreover, induced local overexpression demonstrated that ROT4 acts as a regulator of the leaf shape via a change in positional cue along the longitudinal axis. Similarly, ROT4 overexpression results in a protrusion of the main inflorescence stem, again indicating a change in positional cue along the longitudinal axis. These results suggest that ROT4 affects the positional cue and cell proliferation along the body axis.

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    • Non-cell-autonomously coordinated organ size regulation in leaf development Peer-reviewed

      Kensuke Kawade, Gorou Horiguchi, Hirokazu Tsukaya

      Development137 ( 24 ) 4221 - 4227   15 12 2010

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      The way in which the number and size of cells in an organ are determined poses a central challenge in our understanding of organ size control. Compensation is an unresolved phenomenon, whereby a decrease in cell proliferation below some threshold level triggers enhanced postmitotic cell expansion in leaf primordia. It suggests an interaction between these cellular processes during organogenesis and provides clues relevant to an understanding of organ size regulation. Although much attention has been given to compensation, it remains unclear how the cellular processes are coordinated. Here, we used a loss-of-function mutation in the transcriptional coactivator gene ANGUSTIFOLIA3 (AN3), which causes typical compensation in Arabidopsis thaliana. We established Cre/lox systems to generate leaves chimeric for AN3 expression and investigated whether compensation occurs in a cell-autonomous or non-cell-autonomous manner. We found that an3-dependent compensation is a non-cellautonomous process, and that an3 cells seem to generate and transmit an intercellular signal that enhances postmitotic cell expansion. The range of signalling was restricted to within one-half of a leaf partitioned by the midrib. Additionally, we also demonstrated that overexpression of the cyclin-dependent kinase inhibitor gene KIP-RELATED PROTEIN2 resulted in cellautonomous compensation. Together, our results revealed two previously unknown pathways that coordinate cell proliferation and postmitotic cell expansion for organ size control in plants.

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    • Non-cell-autonomously coordinated organ size regulation in leaf development Peer-reviewed

      Kensuke Kawade, Gorou Horiguchi, Hirokazu Tsukaya

      DEVELOPMENT137 ( 24 ) 4221 - 4227   12 2010

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:COMPANY OF BIOLOGISTS LTD  

      The way in which the number and size of cells in an organ are determined poses a central challenge in our understanding of organ size control. Compensation is an unresolved phenomenon, whereby a decrease in cell proliferation below some threshold level triggers enhanced postmitotic cell expansion in leaf primordia. It suggests an interaction between these cellular processes during organogenesis and provides clues relevant to an understanding of organ size regulation. Although much attention has been given to compensation, it remains unclear how the cellular processes are coordinated. Here, we used a loss-of-function mutation in the transcriptional coactivator gene ANGUSTIFOLIA3 (AN3), which causes typical compensation in Arabidopsis thaliana. We established Cre/lox systems to generate leaves chimeric for AN3 expression and investigated whether compensation occurs in a cell-autonomous or non-cell-autonomous manner. We found that an3-dependent compensation is a non-cell-autonomous process, and that an3 cells seem to generate and transmit an intercellular signal that enhances postmitotic cell expansion. The range of signalling was restricted to within one-half of a leaf partitioned by the midrib. Additionally, we also demonstrated that overexpression of the cyclin-dependent kinase inhibitor gene KIP-RELATED PROTEIN2 resulted in cell-autonomous compensation. Together, our results revealed two previously unknown pathways that coordinate cell proliferation and postmitotic cell expansion for organ size control in plants.

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    • Involvement of Auxin and Brassinosteroid in the Regulation of Petiole Elongation under the Shade Peer-reviewed

      Toshiaki Kozuka, Junko Kobayashi, Gorou Horiguchi, Taku Demura, Hitoshi Sakakibara, Hirokazu Tsukaya, Akira Nagatani

      PLANT PHYSIOLOGY153 ( 4 ) 1608 - 1618   8 2010

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:AMER SOC PLANT BIOLOGISTS  

      Plants grown under a canopy recognize changes in light quality and modify their growth patterns; this modification is known as shade avoidance syndrome. In leaves, leaf blade expansion is suppressed, whereas petiole elongation is promoted under the shade. However, the mechanisms that control these responses are largely unclear. Here, we demonstrate that both auxin and brassinosteroid (BR) are required for the normal leaf responses to shade in Arabidopsis (Arabidopsis thaliana). The microarray analysis of leaf blades and petioles treated with end-of-day far-red light (EODFR) revealed that almost half of the genes induced by the treatment in both parts were previously identified as auxin-responsive genes. Likewise, BR-responsive genes were overrepresented in the EODFR-induced genes. Hence, the auxin and BR responses were elevated by EODFR treatment in both leaf blades and petioles, although opposing growth responses were observed in these two parts. The analysis of the auxin-deficient doc1/big mutant and the BR-deficient rot3/cyp90c1 mutant further indicates that auxin and BR were equally required for the normal petiole elongation response to the shade stimulus. In addition, the spotlight irradiation experiment revealed that phytochrome in leaf blades but not that in petioles regulated petiole elongation, which was probably mediated through regulation of the auxin/BR responses in petioles. On the basis of these findings, we conclude that auxin and BR cooperatively promote petiole elongation in response to the shade stimulus under the control of phytochrome in the leaf blade.

      DOI: 10.1104/pp.110.156802

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    • Mechanisms of leaf tooth formation in Arabidopsis (共著) Peer-reviewed

      Kawamura E, Horiguchi G, Tsukaya H

      The Plant Journal   2 2010

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    • The bHLH Transcription Factor SPATULA Controls Final Leaf Size in Arabidopsis thaliana Peer-reviewed

      Yasunori Ichihashi, Gorou Horiguchi, Stefan Gleissberg, Hirokazu Tsukaya

      PLANT AND CELL PHYSIOLOGY51 ( 2 ) 252 - 261   2 2010

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      Leaves possess intrinsic information about their final size, but the developmental mechanisms setting the limits of growth are not well characterized. By screening enhancer trap lines that show a specific expression pattern in leaf primordia, we isolated one line, 576. This line contains a T-DNA insertion upstream of the basic helixloophelix (bHLH) transcription factor SPATULA (SPT) gene, and shows expression in the basal region of young leaves, where cell proliferation is active. An spt loss-of-function mutation increased leaf size and total cell number within a leaf, while SPT overexpression decreased leaf size and total cell number within a leaf. Although spt mutations did not affect cell size, SPT overexpression decreased the cell size in fully expanded leaves. Genetic analysis suggested that SPT acts independently from another set of cell proliferation-dependent organ size regulators ANGUSTIFOLIA3 (AN3) and GROWTH REGULATING FACTOR5 (AtGRF5). Detailed analysis of spt leaf development showed that the spt mutation enlarged the size of the meristematic region in leaf primordia, while overexpression of AtGRF5 promoted cell proliferation without affecting the enlargement of the meristematic region. These results suggest that SPT functions as a repressor of leaf growth and that meristematic region size in young leaf primordia, in terms of proliferative cell number within leaf primordia, is another target of leaf size determination, which previously had not been identified.

      DOI: 10.1093/pcp/pcp184

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    • Impact of segmental chromosomal duplications on leaf size in the grandifolia-D mutants of Arabidopsis thaliana Peer-reviewed

      Gorou Horiguchi, Nathalie Gonzalez, Gerrit T. S. Beemster, Dirk Inze, Hirokazu Tsukaya

      PLANT JOURNAL60 ( 1 ) 122 - 133   10 2009

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:WILEY-BLACKWELL PUBLISHING, INC  

      The number of cells in an organ is a major factor that specifies its size. However, the genetic basis of cell number determination is not well understood. To obtain insight into this genetic basis, three grandifolia-D (gra-D) mutants of Arabidopsis thaliana were characterized that developed huge leaves with two to three times more cells than the wild-type. Genetic and microarray analyses showed that a large segmental duplication had occurred in all the gra-D mutants, consisting of the lower part of chromosome 4. In the duplications, genes were found that encode AINTEGUMENTA (ANT), a factor that extends the duration of cell proliferation, and CYCD3;1, a G(1)/S cyclin. The expression levels of both genes increased and the duration of cell proliferation in the leaf primordia was extended in the gra-D mutants. Data obtained by RNAi-mediated knockdown of ANT expression suggested that ANT contributed to the huge-leaf phenotype, but that it was not the sole factor. Introduction of an extra genomic copy of CYCD3;1 into the wild-type partially mimicked the gra-D phenotype. Furthermore, combined elevated expression of ANT and CYCD3;1 enhanced cell proliferation in a cumulative fashion. These results indicate that the duration of cell proliferation in leaves is determined in part by the interaction of ANT and CYCD3;1, and also demonstrate the potential usefulness of duplication mutants in the elucidation of genetic relationships that are difficult to uncover by standard single-gene mutations or gain-of-function analysis. We also discuss the potential effect of chromosomal duplication on evolution of organ size.

      DOI: 10.1111/j.1365-313X.2009.03940.x

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    • Coordination of cell proliferation and cell expansion mediated by ribosome-related processes in the leaves of Arabidopsis thaliana Peer-reviewed

      Ushio Fujikura, Gorou Horiguchi, Maria Rosa Ponce, Jose Luis Micol, Hirokazu Tsukaya

      PLANT JOURNAL59 ( 3 ) 499 - 508   8 2009

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      P>Co-ordination of cell proliferation and cell expansion is a key regulatory process in leaf-size determination, but its molecular details are unknown. In Arabidopsis thaliana, mutations in a positive regulator of cell proliferation often trigger excessive cell enlargement post-mitotically in leaves. This phenomenon, called compensation syndrome, is seen in the mutant angustifolia3 (an3), which is defective in a transcription co-activator. Such compensation, however, does not occur in response to a decrease in cell number in oligocellula (oli). oli2, oli5 and oli7 did not exhibit compensation and the reduction in cell number in these mutants was moderate. However, when an oli mutation was combined with a different oli mutation to create a double mutant, cell number was further reduced and compensation was induced. Similarly, weak suppression of AN3 expression reduced cell number moderately but did not induce compensation compared with an an3 null mutant. Furthermore, double mutants of either oli2, oli5 or oli7 and an3 showed markedly enhanced compensation. These results suggest that compensation is triggered when cell proliferation regulated by OLI2/OLI5/OLI7 and AN3 is compromised in a threshold-dependent manner. OLI2 encodes a Nop2 homolog in Saccharomyces cerevisiae that is involved in ribosome biogenesis, whereas OLI5 and OLI7 encode ribosome proteins RPL5A and RPL5B, respectively. This suggests that a factor involved in the induction of compensation may be under the dual control of AN3 and a ribosome-related process.

      DOI: 10.1111/j.1365-313X.2009.03886.x

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    • The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty Peer-reviewed

      Takeshi Usami, Gorou Horiguchi, Satoshi Yano, Hirokazu Tsukaya

      DEVELOPMENT136 ( 6 ) 955 - 964   3 2009

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:COMPANY OF BIOLOGISTS LTD  

      Regulation of cell number and cell size is essential for controlling the shape and size of leaves. Here, we report a novel class of Arabidopsis thaliana mutants, more and smaller cells 1 (msc1)-msc3, which have increased cell number and decreased cell size in leaves. msc1 has a miR156-resistant mutation in the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 15 (SPL15) gene. msc2 and msc3 are new alleles of paused and squint mutants, respectively. All msc mutants showed accelerated heteroblasty, a phenomenon in which several morphological traits of leaves change along with phase change. Consistent with this finding, in the wild type, leaves at higher nodes (adult leaves) also have increased cell number and reduced cell size compared with those at lower nodes (juvenile leaves). These facts indicate that precocious acquisition of adult leaf characteristics in the msc mutants may cause alterations in the number and size of cells, and that heteroblasty plays an important role in the regulation of cell number and size. In agreement with this suggestion, such heteroblasty-associated changes in cell number and size are severely inhibited by the constitutive overexpression of miR156 and are promoted by the elevated expression of miR156-insensitive forms of SPL genes. By contrast, rdr6, sgs3, zip, arf3 and arf4 mutations, which affect progression of heteroblasty, had little or no effect on number or size of cells. These results suggest that cell number and size are mainly regulated by an SPL-dependent pathway rather than by a tasiR-ARF-dependent pathway.

      DOI: 10.1242/dev.028613

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    • Structurally related Arabidopsis ANGUSTIFOLIA is functionally distinct from the transcriptional corepressor CtBP Peer-reviewed

      Stern Mark D, Aihara Hitoshi, Cho Kiu-Hyung, Kim Gyung-Tae, Horiguchi Gorou, Roccaro Giorgio A, Guevara Elizabeth, Sun Huan Huan, Negeri Dereje, Tsukaya Hirokazu, Nibu Yutaka

      DEVELOPMENT GENES AND EVOLUTION217 ( 11-12 ) 759 - 769   12 2007

    • Compensated cell enlargement is induced postmitotically in fugu mutants and is mediated by two different expansion-regulatory pathways Peer-reviewed

      Ferjani Ali, Ishikawa Naoko, Hisanaga Tetsuya, Fujikura Ushio, Kubo Minoru, Demura Taku, Horiguchi Gorou, Fukuda Hiroo, Tsukaya Hirokazu

      PLANT AND CELL PHYSIOLOGY48   S192   2007

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    • Functions of phytohormones on leaf morphogenesis

      Yamaguchi Takahiro, Horiguchi Gorou, Tsukaya Hirokazu

      Regulation of Plant Growth & Development41 ( 2 ) 122 - 130   20 12 2006

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      Language:Japanese   Publisher:植物化学調節学会  

      DOI: 10.18978/jscrp.41.2_122

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    • Classification of compensated cell enlargement by the extra-small sisters mutations

      FUJIKURA Ushio, FERJANI Ali, HORIGUCHI Gorou, TSUKAYA Hirokazu

      Journal of plant research119   148 - 149   1 12 2006

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    • Compensated cell enlargement occurs post-mitotically and is achieved by several different mechanisms

      FERJANI Ali, FUJIKURA Ushio, HORIGUCHI Gorou, TSUKAYA Hirokazu

      Journal of plant research119   1 12 2006

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    • Microarray analysis of compensated cell enlargement in angustifolia3

      HORIGUCHI Gorou, ISHIKAWA Naoko, KUBO Minoru, DEMURA Taku, FUKUDA Hiroo, TSUKAYA Hirokazu

      Journal of plant research119   1 12 2006

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    • Large-scale histological analysis of leaf mutants using two simple leaf observation methods: Identification of novel genetic pathways governing the size and shape of leaves Peer-reviewed

      Horiguchi G, Fujikura U, Ferjani A, Ishikawa N, Tsukaya H

      The Plant Journal48   638 - 644   12 2006

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      DOI: 10.1111/j.1365-313X.2006.02896.x

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    • Dissection of Enhanced Cell Expansion Processes in Leaves Triggered by a Defect in Cell Proliferation, with Reference to Roles of Endoreduplication

      FUJIKURA Ushio, HORIGUCHI Gorou, TSUKAYA Hirokazu

      Plant and Cell Physiology48 ( 2 ) 278 - 286   1 2 2006

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      Language:English   Publisher:Japanese Society of Plant Physiologists  

      DOI: 10.1093/pcp/pcm002

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    • Gravitropism in leaves of Arabidopsis thaliana (L.) Heynh. Peer-reviewed

      E Mano, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY47 ( 2 ) 217 - 223   2 2006

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:OXFORD UNIV PRESS  

      In higher plants, stems and roots show negative and positive gravitropism, respectively. However, current knowledge on the graviresponse of leaves is lacking. In this study, we analyzed the positioning and movement of rosette leaves of Arabidopsis thaliana under light and dark conditions. We found that the radial positioning of rosette leaves was not affected by the direction of gravity under continuous white light. In contrast, when plants were shifted to darkness, the leaves moved upwards, suggesting negative gravitropism. Analysis of the phosphoglucomutase and shoot gravitropism 2-1 mutants revealed that the sedimenting amyloplasts in the leaf petiole are important for gravity perception, as is the case in stems and roots. In addition, our detailed physiological analyses revealed a unique feature of leaf movement after the shift to darkness, i.e. movement could be divided into negative gravitropism and nastic movement. The orientation of rosette leaves is ascribed to a combination of these movements.

      DOI: 10.1093/pcp/pci237

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    • Transcription switches for protoxylem and metaxylem vessel formation. Peer-reviewed

      Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T

      Genes & development19 ( 16 ) 1855 - 1860   8 2005

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    • The transcription factor AtGRF5 and the transcription coactivator AN3 regulate cell proliferation in leaf primordia of Arabidopsis thaliana Peer-reviewed

      G Horiguchi, GT Kim, H Tsukaya

      PLANT JOURNAL43 ( 1 ) 68 - 78   7 2005

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      Language:English   Publishing type:Research paper (scientific journal)   Publisher:BLACKWELL PUBLISHING  

      The development of the flat morphology of leaf blades is dependent on the control of cell proliferation as well as cell expansion. Each process has a polarity with respect to the longitudinal and transverse axes of the leaf blade. However, only a few regulatory components of these processes have been identified to date. We have characterized two genes from Arabidopsis thaliana: ANGUSTIFOLIA3 (AN3), which encodes a homolog of the human transcription coactivator SYT, and GROWTH-REGULATING FACTOR5 (AtGRF5), which encodes a putative transcription factor. AN3 is identical to GRF-INTERACTING FACTOR1 (AtGIF1). The an3 and atgrf5 mutants exhibit narrow-leaf phenotypes due to decreases in cell number. Conversely, cell proliferation in leaf primordia is enhanced and leaves grow larger than normal when AN3 or AtGRF5 is overexpressed. Both genes are expressed in leaf primordia, and in the yeast two-hybrid assay, the gene products were found to interact with each other through their N-terminal domains. These results suggest that AN3 and AtGRF5 act together and are required for the development of appropriate leaf size and shape through the promotion and/or maintenance of cell proliferation activity in leaf primordia.

      DOI: 10.1111/j.1365-313X.2005.02429.x

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    • 葉の形態形成 (発生システムのダイナミクス) -- (組織・器官形成)

      塚谷 裕一, 堀口 吾朗

      蛋白質核酸酵素50 ( 6 ) 627 - 632   5 2005

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    • The ATE genes are responsible for the repression of the transdifferentiation into xylem cells in Arabidopsis. Peer-reviewed

      Sawa, S, Demura, T, Horiguchi, G, Kubo, M, Fukuda, H

      Plant Physiol.137 ( 1 ) 141 - 148   2005

    • The different growth responses of the Arabidopsis thaliana leaf blade and the petiole during shade avoidance are regulated by Photoreceptors and sugar Peer-reviewed

      Kozuka T, Horiguchi G, Kim G. T, Ohgishi M, Sakai T, Tsukaya H

      Plant and Cell Physiology46 ( 1 ) 213 - 223   2005

    • Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana. Peer-reviewed

      Narita NN, Moore S, Horiguchi G, Kubo M, Demura T, Fukuda H, Goodrich J, Tsukaya H

      The Plant journal : for cell and molecular biology38   699 - 713   5 2004

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    • Visualization by comprehensive microarray analysis of gene expression programs during transdifferentition of mesophyll cells into xylem cells. Peer-reviewed

      Demura, T, Tashiro, G, Horiguchi, G, Kishimoto, N, Kubo, M, Matsuoka, N, Minami, A, Nagata-Hiwatashi, M, Nakamura, K, Okamura, Y, Sassa, N, Suzuki, S, Yazaki, J, Kikuchi, S, Fukuda, H

      Proc. Natl. Acad. Sci. USA.99 ( 24 ) 15794 - 15799   2002

    • Characterization of Arabidopsis mutants that are associated with altered C18 unsaturated fatty acid metabolism. (共著) Peer-reviewed

      HORIGUCHI G, KODAMA H, IBA K

      Plant Sci.161 ( 6 ) 1117 - 1123   2001

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      Publishing type:Research paper (scientific journal)  

      DOI: 10.1016/S0168-9452(01)00523-4

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    Misc.

    • リボソームの生合成と植物の発生 Invited Peer-reviewed

      堀口 吾朗

      生物科学68   232 - 239   2017

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    • as2 rpl4dで引き起こされる葉の背軸化に必要なSZK1の発現解析

      井上幹人, 中田未友希, 塚谷裕一, 堀口吾朗, 堀口吾朗

      日本植物学会大会研究発表記録79th   153   1 9 2015

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      J-GLOBAL

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    • シロイヌナズナおよびコケ植物におけるAN3,GRF,SWI2の分子的機能保存性の検討

      長野夏未, 名和美聡, 中田未友希, 西浜竜一, 河内孝之, 塚谷裕一, 堀口吾朗, 堀口吾朗

      Plant Morphology27 ( 1 ) 59   4 2015

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    • 細胞サイズが小型化するシロイヌナズナxs1変異株の原因遺伝子の同定と解析

      宮田和裕, 依藤絵里, 中田未友希, 塚谷裕一, 堀口吾朗, 堀口吾朗

      Plant Morphology27 ( 1 ) 60   4 2015

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    • 根のプラスチドリボソームの損傷は側根の発生異常を引き起こす

      中田未友希, 塚谷裕一, 堀口吾朗

      日本植物生理学会年会要旨集56th   210   9 3 2015

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    • 原核型リボソーム阻害剤がシロイヌナズナの根の発生に与える影響

      中田未友希, 塚谷裕一, 堀口吾朗

      日本植物学会大会研究発表記録78th   242   1 9 2014

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    • Roles of the vacuolar H<sup>+</sup>-PPase in seed storage oil mobilization and plant development. Invited Peer-reviewed

      Ferjani, A, Segami, S, Horiguchi, G, Muto, Y, Maeshima, M, Tsukaya, H

      Plant Morphology26   45-51   6 2014

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    • リボソームタンパク質RPL4DのGFP標識とその機能性についての解析

      堀口吾朗, 中田未友希, 塚谷裕一

      日本植物生理学会年会要旨集55th   268   11 3 2014

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      J-GLOBAL

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    • 根の発生におけるプラスチドタンパク質RFC3の機能解析

      中田未友希, 塚谷裕一, 堀口吾朗

      日本植物生理学会年会要旨集55th   351   11 3 2014

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    • How do 'housekeeping' genes control organogenesis?--Unexpected new findings on the role of housekeeping genes in cell and organ differentiation.

      Hirokazu Tsukaya, Mary E Byrne, Gorou Horiguchi, Munetaka Sugiyama, Mieke Van Lijsebettens, Michael Lenhard

      Journal of plant research126 ( 1 ) 3 - 15   1 2013

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      Language:English   Publisher:SPRINGER JAPAN KK  

      In recent years, an increasing number of mutations in what would appear to be 'housekeeping genes' have been identified as having unexpectedly specific defects in multicellular organogenesis. This is also the case for organogenesis in seed plants. Although it is not surprising that loss-of-function mutations in 'housekeeping' genes result in lethality or growth retardation, it is surprising when (1) the mutant phenotype results from the loss of function of a 'housekeeping' gene and (2) the mutant phenotype is specific. In this review, by defining housekeeping genes as those encoding proteins that work in basic metabolic and cellular functions, we discuss unexpected links between housekeeping genes and specific developmental processes. In a surprising number of cases housekeeping genes coding for enzymes or proteins with functions in basic cellular processes such as transcription, post-transcriptional modification, and translation affect plant development.

      DOI: 10.1007/s10265-012-0518-2

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    • Ribosomes and translation in plant developmental control

      Gorou Horiguchi, Mieke Van Lijsebettens, Hector Candela, Jose Luis Micol, Hirokazu Tsukaya

      PLANT SCIENCE191   24 - 34   8 2012

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      Language:English   Publishing type:Book review, literature introduction, etc.   Publisher:ELSEVIER IRELAND LTD  

      Ribosomes play a basic housekeeping role in global translation. However, a number of ribosomal-protein-defective mutants show common and rare developmental phenotypes including growth defects, changes in leaf development, and auxin-related phenotypes. This suggests that translational regulation may be occurring during development. In addition, proteomic and bioinformatic analyses have demonstrated a high heterogeneity in ribosome composition. Although this might be a sign of unequal roles of individual ribosomal proteins, it does not explain every ribosomal-protein-defective phenotype. Moreover, comprehensive interpretations concerning the relationship between ribosomal-protein-defective phenotypes and molecular changes in ribosome status are lacking. In this review, we address these phenotypes based on three models, ribosome insufficiency, heterogeneity, and aberrancy, to consider how ribosomes play developmental roles. We propose that the three models are not mutually exclusive, and ribosomal-protein-defective phenotypes can be explained with one or more of these models. The three models with reference to genetic, biochemical, and bioinformatic knowledge will serve as a foundation for future studies of translational regulation. (C) 2012 Elsevier Ireland Ltd. All rights reserved.

      DOI: 10.1016/j.plantsci.2012.04.008

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    • Organ size regulation in plants: insights from compensation

      Gorou Horiguchi, Hirokazu Tsukaya

      FRONTIERS IN PLANT SCIENCE2   24   2011

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      Language:English   Publishing type:Book review, literature introduction, etc.   Publisher:FRONTIERS RESEARCH FOUNDATION  

      The regulation of organ size in higher organisms is a fundamental issue in developmental biology. In flowering plants, a phenomenon called "compensation" has been observed where a cell proliferation defect in developing leaf primordia triggers excessive cell expansion. As a result, final leaf size is not significantly reduced compared to that expected from the reduction in leaf cell numbers. Recent genetic studies have revealed several key features of the compensation phenomenon. Compensation is induced either cell autonomously or non-cell autonomously depending on the trigger that impairs cell proliferation; a certain type of compensation is induced only when cell proliferation is impaired beyond a threshold level. Excessive cell expansion is achieved by either an increased cell expansion rate or a prolonged period of cell expansion via genetic pathways that are also required for normal cell expansion. These results indicate that cell proliferation and cell expansion are coordinated through multiple pathways during leaf size determination. Further classification of compensation pathways and their characterization at the molecular level will provide a deeper understanding of organ size regulation.

      DOI: 10.3389/fpls.2011.00024

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    • Organ size control in Arabidopsis: insights from compensation studies

      Ferjani A, Horiguchi G, Tsuyaka H

      Plant Morphology22   65 - 71   8 4 2010

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      Language:English   Publishing type:Article, review, commentary, editorial, etc. (other)   Publisher:日本植物形態学会  

      DOI: 10.5685/plmorphol.22.65

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    • Control of leaf morphogenesis by long- and short-distance signaling: Differentiation of leaves into sun or shade types and compensated cell enlargement

      Ali Ferjani, Satoshi Yano, Gorou Horiguchi, Hirokazu Tsukaya

      Plant Cell Monographs10   47 - 62   2008

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      Language:English   Publishing type:Article, review, commentary, editorial, etc. (scientific journal)  

      The flattened, thin lamina of leaves captures sunlight for photosynthesis and facilitates gas exchange. Therefore, the size and shape of a leaf are fundamentally important features of its integrity and function. Progress in developmental studies has suggested that long- and short-distance signaling pathways are involved in leaf formation. In this chapter, we introduce these signaling pathways, both of which can control final leaf shape and structure: a long-distance signaling pathway that governs the differentiation of leaves into sun and shade types, and a short-distance signaling pathway that appears to be involved in an organ-wide system that integrates cell proliferation and cell enlargement. Although none of the molecules involved in these two pathways have been identified, plausible mechanisms of these pathways are discussed based on present data. © 2008 Springer-Verlag Berlin Heidelberg.

      DOI: 10.1007/7089_2007_148

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    • Ferjani Ali, Horiguchi Gorou*, Yano Satoshi, Tsukaya Hirokazu (2007) Analysis of Leaf Development in fugu Mutants of Arabidopsis Reveals Three Compensation Modes That Modulate Cell Expansion in Determinate Organs

      Ferjani Ali, Horiguchi Gorou, Yano Satoshi, Tsukaya Hirokazu

      PLANT PHYSIOLOGY144 ( (2): ) 988 - 999   6 2007

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    • Analysis on the reverse compensation

      Takeshi Usami, Gorou Horiguchi, Hirokazu Tsukaya

      PLANT AND CELL PHYSIOLOGY48   S55 - S55   2007

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      Language:English   Publishing type:Research paper, summary (international conference)   Publisher:OXFORD UNIV PRESS  

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    • Effect of mutations that stimulate cell proliferation on compensated cell enlargement induced by the angustifolia3 mutation

      Gorou Horiguchi, Hirokazu Tsukaya

      PLANT AND CELL PHYSIOLOGY48   S54 - S54   2007

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    • Genetic relationship between Angustifolia3 and Extra-Small Sisters highlights novel mechanisms controlling leaf size

      Ushio Fujikura, Gorou Horiguchi, Hirokazu Tsukaya

      Plant Signaling and Behavior2 ( 5 ) 378 - 380   2007

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      Language:English   Publishing type:Article, review, commentary, editorial, etc. (scientific journal)   Publisher:Landes Bioscience  

      DOI: 10.4161/psb.2.5.4525

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    • Is endoreduplication governed by topo IV essential for cell-size regulation?

      Hirokazu Tsukuya, Christian Breuer, Nicola Stacey, Ushio Fujikura, Gorou Horiguchi, Keiko Sugimoto

      PLANT AND CELL PHYSIOLOGY48   S54 - S54   2007

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    • Coordination of cell proliferation and cell expansion in the control of leaf size in Arabidopsis thaliana

      G Horiguchi, A Ferjani, U Fujikura, H Tsukaya

      JOURNAL OF PLANT RESEARCH119 ( 1 ) 37 - 42   1 2006

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      Language:English   Publishing type:Article, review, commentary, editorial, etc. (scientific journal)   Publisher:SPRINGER TOKYO  

      Size is an important parameter in the characterization of organ morphology and function. To understand the mechanisms that control leaf size, we previously isolated a number of Arabidopsis thaliana mutants with altered leaf size. Because leaf morphogenesis depends on determinate cell proliferation, the size of a mature leaf is controlled by variation in cell size and number. Therefore, leaf-size mutants should be classified according to the effects of the mutations on the cell number and/or size. A group of mutants represented by angustifolia3/grf-interacting factor1 and aintegumenta exhibits an intriguing cellular phenotype termed compensation: when the leaf cell number is decreased due to the mutation, the leaf cell size increases, leading to compensation in leaf area. Several lines of genetic evidence suggest that compensation is probably not a result of the uncoupling of cell division from cell growth. Rather, the evidence suggests an organ-wide mechanism that coordinates cell proliferation with cell expansion during leaf development. Our results provide a key, novel concept that explains how leaf size is controlled at the organ level.

      DOI: 10.1007/s10265-005-0232-4

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    • A mechanism that monitors the number of leaf cells and its role in the determination of cell size and leaf size

      G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY47   S118 - S118   2006

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    • Characterization of leaf positioning in Arabidopsis thaliana.

      E Mano, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY47   S234 - S234   2006

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    • Coordination of cell proliferation and cell expansion during leaf morphogenesis: Cell enlargement observed in compensation is mediated by two different mechanisms

      A Ferjani, U Fujikura, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY47   S176 - S176   2006

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    • Genetic analysis of compensation system in leaf development: identification of mutants defective in cell expansion activated by compensation

      U Fujikura, A Ferjani, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY47   S118 - S118   2006

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    • 高等植物における道管形成のマスター制御因子であるVND6とVND7

      久保稔, 宇田川真理子, 西窪伸之, 堀口吾朗, 山口雅利, 井藤純, 三村徹郎, 福田裕穂, 出村拓

      日本分子生物学会年会講演要旨集28th   718   25 11 2005

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    • Coordination of cell proliferation and cell expansion during leaf morphogenesis in Arabidopsis: Compensatory system

      A Ferjani, U Fujikura, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY46   S195 - S195   2005

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    • Genetic analysis of compensation system(s) in leaf development

      U Fujikura, A Ferjani, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY46   S195 - S195   2005

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    • Regulation of petiole elongation during shade-avoidance response is highly dependent on ROT3 and DOC1

      T Kozuka, G Horiguchi, GT Kim, H Tsukaya

      PLANT AND CELL PHYSIOLOGY46   S208 - S208   2005

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    • The gravity response of leaves

      E Mano, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY46   S115 - S115   2005

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    • grandifolia mutants produce large leaves due to an extended duration of cell proliferation

      G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY46   S195 - S195   2005

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    • Basic analysis of controls of periclinal division in Arabidopsis mesophyll cells

      N Narita, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY45   S163 - S163   2004

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    • Is there any gravitropism in leaves?

      E Mano, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY45   S144 - S144   2004

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    • RNA silencing in plants: A shortcut to functional analysis

      Gorou Horiguchi

      Differentiation72 ( 2-3 ) 65 - 73   2004

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      RNA silencing is a rapidly expanding research field, not only because it is a fundamental biological issue but also because its application in the control of gene expression is highly promising. Post-transcriptional gene silencing in plants is a form of RNA silencing by which target RNA is degraded in a sequence-specific manner. Findings regarding the central role that double-stranded RNA plays in triggering RNA silencing have prompted the development of many modified methods for RNA silencing. These methods, in combination with the development of genomic resources, have provided rapid and efficient means by which to investigate gene function in a wide range of plant species. This review addresses the technical aspects of RNA silencing in plants by introducing the principles of several methods of RNA silencing, as well as the advantages and disadvantages of each method. © International Society of Differentiation 2004.

      DOI: 10.1111/j.1432-0436.2004.07202005.x

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    • Role of ANGUSTIFOLIA3 and its interacting proteins for cell proliferation-dependent leaf morphogenesis

      G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY45   S163 - S163   2004

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    • Characterization of Arabidopsis T-DNA tag line with dwarfism and depressed leaves

      N Narita, G Horiguchi, J Goodrich, H Tsukaya

      PLANT AND CELL PHYSIOLOGY44   S107 - S107   2003

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    • Characterization of a narrow leaf mutant of Arabidopsis, angustifolia3, suggests the presence of a mechanism controlling cell division orientation in the leaf-width direction

      G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY44   S107 - S107   2003

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    • The study of mechanisms that regulate the elongation of leaf blade and petiole in various light conditions

      T Kozuka, GT Kim, G Horiguchi, H Tsukaya

      PLANT AND CELL PHYSIOLOGY44   S161 - S161   2003

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    • Construction of GATEWAY binary vectors for high throughput analyses of vascular formation related genes

      M Kubo, G Horiguchi, N Sassa, HJ Pyo, H Fukuda, T Demura

      PLANT AND CELL PHYSIOLOGY43   S38 - S38   2002

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    Presentations

    • シロイヌナズナ小型葉変異株oligocellula1の抑圧変異株の探索

      鈴木 真里奈, 篠塚 奈々絵, 塚谷 裕一, 堀口 吾朗

      第29回日本植物形態学会大会  7 9 2017 

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    • ゼニゴケの発生におけるAN3-GRF-BRM複合体の役割の解析

      齋藤 美永子, 長野 夏未, 塚谷 裕一, 堀口 吾朗

      第29回日本植物形態学会大会  7 9 2017 

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    • 幹細胞を欠く側根を形成するシロイヌナズナrfc3の抑圧変異株の解析

      長嶋 友美, 大城 克友, 岩瀬 晃康, 中村 栞理, 中田 未友希, 堀口 吾朗

      7 9 2017 

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    • 葉の成長に多面的に関わるシロイヌナズナAN3およびGRFの発現制御機構の解析

      佐藤 晃圭, 皆吉 彩, 池田 奨, 塚谷 裕一

      第29回日本植物形態学会大会  7 9 2017 

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    • Analysis on the suppressors of as2 rpl4d reveals relationship among genes involved in the ribosomal protein-dependent regulation of leaf polarity

      Takahara, M, Tsukaya, H, Horiguchi, G

      48th annual meeting of the Japanese society of developmental biologist  2 6 2015 

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      Event date: 5 6 2015

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    • Inhibition of plastid translation alters expression of stem cell-regulatory genes in lateral roots of Arabidopsis thaliana.

      Nakata, M, Tsukaya, H, Horiguchi, G

      48th annual meeting of the Japanese society of developmental biologists  2 6 2015 

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    • SUZAKU1, a NAC-domain transcription factor gene promotes leaf abaxialization in response to as2-enhancer mutations in Arabidopsis thaliana

      Horiguchi, G, Inoue, M, Masuda, H, Nakata, M, Tsukaya, H

      48th annual meeting of the Japanese society of developmental biologists  2 6 2015 

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    • AN3, HAN, TPLが子葉の 属性維持に果たす役割の解析

      堀口吾朗, 大池 諒, 秋間健太, 塚谷裕一

      第56回日本植物生理学会年会  16 3 2015 

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    • シロイヌナズナOLIGOCELLULA1による葉サイズ決定機構の解析

      篠塚 奈々絵, 平方 智大, 藤倉 潮, 出村 拓, 塚谷 裕一, 堀口 吾朗

      第56回日本植物生理学会年会  16 3 2015 

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    • 根のプラスチドリボソームの損傷は側根の発生異常を引き起こす

      中田 未友希, 塚谷 裕一, 堀口 吾朗

      第56回日本植物生理学会年会  16 3 2015 

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    • 葉の細胞数が減少するシロイヌナズナのoligocellula6-D変異株の解析

      佐藤翔紀, 塚谷裕一, 堀口吾朗

      第56回日本植物生理学会年会  16 3 2015 

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    • as2 rpl4d背景での葉の裏側化を抑制する変異体の遺伝学および発生学的解析

      高原正裕, 塚谷裕一, 堀口吾朗

      第56回日本植物生理学会年会  16 3 2015 

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    • リボソームタンパク質RPL4の質と量が葉の背腹性に及ぼす効果の解析

      増田英典, 塚谷裕一, 堀口吾朗

      日本植物学会第78回大会  12 9 2014 

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    • リボソームタンパク質変異体で過剰発現するSZK1の解析

      井上幹人, 中田未友希, 塚谷裕一, 堀口吾朗

      日本植物学会第78回大会  12 9 2014 

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    • 原核型リボソーム阻害剤がシロイヌナズナの根の発生に与える影響

      中田未友希, 塚谷裕一, 堀口吾朗

      日本植物学会第78回大会  12 9 2014 

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    • 子葉における根の異所形成を抑制するAN3とHANの解析

      大池 諒, 秋間健太, 塚谷裕一, 堀口吾朗

      日本植物学会78回大会  12 9 2014 

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    • シロイヌナズナおよびコケ植物におけるAN3, GRF, SWI2の分子的機能保存性の検討

      長野夏未, 名和美聡, 中田未友希, 西浜竜一, 河内孝之, 塚谷裕一, 堀口吾朗

      日本植物形態学会第 26 回大会  11 9 2014 

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    • 細胞サイズが小型化するシロイヌナズナxs1変異株の原因遺伝子の同定と解析

      宮田和裕, 依藤絵里, 中田未友希, 塚谷裕一, 堀口吾朗

      日本植物形態学会第 26 回大会  11 9 2014 

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    • 葉の細胞数が減少するシロイヌナズナのoligocellula6変異株の解析

      佐藤翔紀, 塚谷裕一, 堀口吾朗

      日本植物形態学会第 26回大会  11 9 2014 

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    • How mutations in ribosomal protein genes affect leaf polarity in the asymmetric leaves 2 genetic background International conference

      Gorou Horiguchi, Mikito Inoue, Hidenori Masuda, Miyuki Nakata, Iwai Ohbayashi, Munetaka Sugiyama, Hirokazu Tsukaya

      24th International conference on Arabidopsis Research  28 7 2014 

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    • NAC型転写因子をコードするSZK1遺伝子の高発現が葉の背腹性に及ぼす効果の解析

      堀口 吾朗, 塚谷 裕一

      日本植物学会第77回大会  13 9 2013 

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    • シロイヌナズナのWD40リピートタンパク質をコードするOLIGOCELLULA1は異形葉性を通じて葉のサイズ制御に関わる

      篠塚 奈々絵, 平方 智大, 藤倉 潮, 出村 拓, 塚谷 裕一, 堀口 吾朗

      日本植物学会第77回大会  13 9 2013 

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    • シロイヌナズナの器官サイズ異常変異株little princeはミトコンドリアnad6 mRNAのエディティング異常を示す

      石橋幸大, 濱田ゆかり, 中村崇裕, 塚谷裕一, 堀口吾朗

      日本植物形態学会第 24回大会  12 9 2013 

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    • Mutations in a NAC-domain transcription factor gene, SUZAKU1, suppress leaf abaxialization caused by the defects of ribosomal proteins International conference

      Gorou Horiguchi, Hiroki Shimada, Tatsuya Watanabe, Hirokazu Tsukaya

      2013 FASEB Science Research Conferences Mechanisms in Plant Development  11 8 2013 

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    • NAC転写因子の機能欠損によるas2 rpl4d が示す葉の背軸化の抑制

      堀口吾朗, 島田浩貴, 渡辺達矢, 大林 祝, 杉山宗隆, 塚谷裕一

      第54回日本植物生理学会年会  21 3 2013 

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    • 細胞層をまたぐANGUSTIFOLIA3の移動様式

      川出 健介, 堀口 吾朗, 平井 優美, 塚谷 裕一

      第54回日本植物生理学会年会  21 3 2013 

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    • rpl4d as2の葉が背軸化する表現型を抑圧するszk1-D変異株の解析

      島田浩貴, 渡辺達矢, 大林 祝, 杉山宗隆, 塚谷裕一, 堀口吾朗

      日本植物学会第76回大会  15 9 2012 

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    • rpl4dが示す花序形態異常の解析

      尾内紀之, 塚谷裕一, 堀口吾朗

      日本植物形態学会第 24回大会  14 9 2012 

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    • Promotion of chloroplast proliferation upon enhanced post-mitotic cell expansion in leaves International conference

      Kensuke Kawade, Gorou Horiguchi, Naoko Ishikawa, Masami Y. Hirai, Hirokazu Tsukaya

      23rd International conference on Arabidopsis Research  3 7 2012 

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    • 細胞増殖を促すANGUSTIFOLIA3の葉原基における時空間的な発現動態

      川出 健介, 谷本 博一, 堀口 吾朗, 平井 優美, 塚谷 裕一

      第53回日本植物生理学会年会  16 3 2012 

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    • Organ-level control of leaf size in Arabidopsis

      Hirokazu Tsukaya, Gorou Horiguchi

      日本植物学会第75回大会  17 9 2011 

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    • シロイヌナズナのrpl4d as2 における葉の 向背軸異常を抑圧する突然変異株の解析

      堀口吾朗, 塚谷裕一

      日本植物学会第75回大会  17 9 2011 

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    • 葉の発生過程においてANGUSTIFOLIA3が細胞層間を移動する重要性

      川出 健介, 堀口 吾朗, 平井 優美, 塚谷 裕一

      日本植物学会第75回大会  17 9 2011 

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    • ANGUSTIFOLIA3を介した細胞層間シグナリングは葉で特徴的に増殖の協調性を担う

      川出健介, 堀口吾朗, 平井優美, 塚谷裕一

      日本植物形態学会第 23回大会  16 9 2011 

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    • GENERAL AND SPECIFIC ROLES OF THE RIBOSOME IN LEAF DEVELOPMENT International conference

      Gorou Horiguchi, Hirokazu Tsukaya

      XVIII International Botanical Congress  24 7 2011 

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    • Inter-cell-layer movement of ANGUSTIFOLIA3 coordinates cell proliferation between clonally distinct tissues in leaves International conference

      Kensuke Kawade, Gorou Horiguchi, Hirokazu Tsukaya

      XVIII International Botanical Congress  24 7 2011 

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    • Removal of cytosolic PPi is a prerequisite for proper resumption of post-germinative development in Arabidopsis thaliana International conference

      Ali Ferjani, Yukari Muto, Gorou Horiguchi, Masayoshi Maeshima, Hirokazu Tsukaya

      XVIII International Botanical Congress  24 7 2011 

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    • EXPRESSION GRADIENT OF ANGUSTIFOLIA3 AND PROLIFERATION DYNAMICS OF LEAF CELLS International conference

      Kensuke Kawade, Hirokazu Tanimoto, Gorou Horiguchi, Masami Y. Hirai, Hirokazu Tsukaya

      22nd International conference on Arabidopsis Research  22 6 2011 

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    • ANGUSTIFOLIA3による葉の細胞層間をまたいだ細胞増殖の協調的な制御

      川出 健介, 堀口 吾朗, 塚谷 裕一

      第52回日本植物生理学会年会  20 3 2011 

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    • RPL4Dの部位特異的発現がas2 rpl4dの葉の背腹性異常の抑制に及ぼす効果

      小島 幸治, 塚谷 裕一, 堀口 吾朗

      第52回日本植物生理学会年会  20 3 2011 

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    • シロイヌナズナのリボソームタンパク質RPL4Dが葉の発生に果たす役割の解析

      堀口吾朗, 塚谷裕一

      第52回日本植物生理学会年会  20 3 2011 

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    • AN3 とそのエンハン サーは胚における根の形 成位置の制御に必要であ る

      兼井 麻利, 堀口 吾朗, 塚谷 裕一

      日本植物学会第74回大会  9 9 2010 

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      Venue:中部大学  

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    • an3依存的な補償作用でみられる細胞間シグナリングの性質

      川出 健介, 堀口 吾朗, 塚谷 裕一

      日本植物学会第74回大会  9 9 2010 

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    • fugu5変異体におけるピロリン酸の蓄積は貯蔵脂質由来のスクロースの生合成を阻害し補償作用を引き起こす

      Ferjani Ali, 武藤由香里, 堀口吾朗, 前島正義, 塚谷裕一

      日本植物学会第74回大会  9 9 2010 

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    • シロイヌナズナG-PATCH DOMAIN PROTEIN 1のリボゾーム生合成における役割

      小島幸治, 田村洵也, 塚谷裕一, 堀口吾朗

      日本植物学会第74回大会  9 9 2010 

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    • リボソームタンパク質による葉の発生制御

      堀口吾朗, 塚谷裕一

      日本植物学会第74回大会  9 9 2010 

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      Venue:中部大学  

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    • as2 rpl4d変異株が示す葉の向背軸異常を抑圧する突然変異株の単離と解析

      堀口吾朗, 関根美紀, 塚谷裕一

      日本植物学会第74回大会  9 9 2010 

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    • 葉の形態形成におけるリボソームタンパク質パラログの役割 International conference

      堀口吾朗, 小澤記史, 塚谷裕一

      日本植物形態学会第 22 回大会  8 9 2010 

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    • 葉緑体数は細胞分裂後において調節されている

      川出健介, 堀口吾朗, 塚谷裕一

      日本植物形態学会第22回大会  8 9 2010 

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      Venue:中部大学  

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    • fugu5変異体により明らかなる、ピロリン酸の代謝とショ糖の生合成の初期生育に果たす役割

      Ferjani Ali, 武藤由香里, 堀口吾朗, 前島正義, 塚谷裕一

      日本植物形態学会第 22 回大会  8 9 2010 

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    • Characterization of intercellular signaling that coordinates cell proliferation with postmitotic cell expansion during leaf development International conference

      Kensuke Kawade, Gorou Horiguchi, Hirokazu Tsukaya

      21st International conference on Arabidopsis Research  6 6 2010 

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    • GDP1, a novel nucleolar protein, is involved in ribosome biogenesis International conference

      Gorou Horiguchi, Koji Kojima, Junya Tamura, Hirokazu Tsukaya

      21st International conference on Arabidopsis Research  6 6 2010 

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    • Toward an understanding of leaf size regulation - Relationship between salicylic-acid response and compensation in leaf development International conference

      Ushio Fujikura, Gorou Horiguchi, Taku Demura, Hirokazu Tsukaya

      21st International conference on Arabidopsis Research  6 6 2010 

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    • fugu5 変異体におけるピロリン酸の蓄積は細胞増殖を阻害し補償作用を引き起こす

      Ali Ferjani, 武藤由香里, 堀口吾朗, 前島正義, 塚谷裕一

      第51回日本植物生理学会年会  18 3 2010 

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      Venue:熊本大学  

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    • シロイヌナズナの葉の向背軸極性分化における核小体タンパク質ヌクレオリンの役割

      氣多澄江, 中川彩美, 小島久恵, 堀口吾朗, 塚谷裕一, 中村研三, 町田泰則, 町田千代子

      第51回日本植物生理学会年会  18 3 2010 

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      Venue:熊本大学  

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    • 細胞間コミュニケーションを介した an3 変 異体での補償作用

      川出健介, 堀口吾朗, 塚谷裕一

      第51回日本植物生理学会年会  18 3 2010 

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      Language:Japanese   Presentation type:Oral presentation (general)  

      Venue:熊本大学  

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    • 葉の横方向への極性伸長制御因子・ANGUSTIFOLIA の細胞内局在性および機能解析

      南澤直子, 上田貴志, 佐藤真由子, 豊岡公徳, 堀口吾朗, 中野明彦, 塚谷裕一

      第51回日本植物生理学会年会  18 3 2010 

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      Language:Japanese   Presentation type:Oral presentation (general)  

      Venue:熊本大学  

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    • 補償作用を示す fugu2 変異体において発現変動する遺伝子群の葉の形成における役 割

      久永哲也, Ali Ferjani, 堀口吾朗, 藤倉潮, 石川直子, 出村拓, 福田裕穂, 塚谷裕一

      第51回日本植物生理学会年会  18 3 2010 

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      Language:Japanese   Presentation type:Oral presentation (general)  

      Venue:熊本大学  

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    • 補償作用抑制能を持つ xs2 の機能解析 ~サリチル酸応答と補償作用の関係につ いて

      藤倉潮, 堀口吾朗, 出村拓, 塚谷裕一

      第51回日本植物生理学会年会  18 3 2010 

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      Language:Japanese   Presentation type:Oral presentation (general)  

      Venue:熊本大学  

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    • KRP2過剰発現により誘導される補償作用経路は細胞自律的である

      川出 健介, 堀口 吾朗, 塚谷 裕一

      日本植物学会第73回大会  17 9 2009 

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    • SPT-AN3-AtGRFネットワークは葉メリステムにおける細胞分裂活性を制御する

      市橋 泰範, 堀口 吾朗, Stefan Gleissberg, 塚谷 裕一

      日本植物学会第73回大会  17 9 2009 

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    • fugu5変異体におけるピロリン酸の蓄積と補償作用との関係

      Ferjani Ali, 武藤 由香理, 堀口 吾朗, 前島 正義, 塚谷 裕一

      日本植物学会第73回大会  17 9 2009 

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    • 種々のリボソームタンパク欠損変異とas2変異との相互作用に関する解析

      堀口吾朗, 塚谷裕一

      日本植物学会第73回大会  17 9 2009 

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    • 胚において異所的な根の形成を引き起こすシロイヌナズナ変異株における解析

      兼井麻利, 堀口吾朗, 塚谷裕一

      日本植物学会第73回大会  17 9 2009 

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    • 補償作用抑制能を持つxs変異原因遺伝子のクローニングと機能解析

      藤倉潮, 堀口吾朗, 塚谷裕一

      日本植物学会第73回大会  17 9 2009 

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    • Leaf size is regulated by a cell-autonomous system linking cell proliferation and post- mitotic cell enlargement International conference

      Kensuke Kawade, Gorou Horiguchi, Hirokazu Tsukaya

      第20回国際シロイヌナズナ会議  30 6 2009 

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      Language:English   Presentation type:Oral presentation (invited, special)  

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    • CRE/Loxシステムにより誘導したKRP2モザイク葉における補償作用の解析

      川出 健介, 堀口 吾朗, 塚谷 裕一

      第50回日本植物生理学会年会  21 3 2009 

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    • ROT4ペプチドはシロイヌナズナの成長をいかに制御するのか

      池内 桃子, 山口 貴大, 堀口 吾朗, 塚谷 裕一

      第50回日本植物生理学会年会  21 3 2009 

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    • fugu2変異株を用いた補償作用の分子機構解明のための網羅的発現解析 International conference

      久永 哲也, Ferjani Ali, 堀口 吾朗, 石川 直子, 久保 稔, 出村 拓, 福田 裕穂, 塚谷 裕一

      第50回日本植物生理学会年会  21 3 2009 

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    • 発芽後の成長および器官サイズ制御におけるFUGU5/AVP1の役割

      Ferjani Ali, 武藤 由香理, 堀口 吾朗, 前島 正義, 塚谷 裕一

      第50回日本植物生理学会年会  21 3 2009 

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    • 種々のリボソーム関連変異株がas1/as2の背腹性異常に及ぼす効果の解析

      堀口 吾朗, Micol Jose Luis, Ponce Maria Rosa, 塚谷 裕一

      第50回日本植物生理学会年会  21 3 2009 

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    • 葉メリステムにおけるBLADE-ON-PETIOLEとLEAFY PETIOLEの役割

      市橋 泰範, 堀口 吾朗, 塚谷 裕一

      第50回日本植物生理学会年会  21 3 2009 

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    • as2 rpl4dで引き起こされる葉の背軸化に必要なSZK1の発現解析

      井上 幹人, 中田 未友希, 塚谷 裕一, 堀口 吾朗

      日本植物学会第79回大会 

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      Event date: 6 9 2015 - 8 9 2015

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    • シロイヌナズナOLI1, HDA9, SANT1による葉の細胞増殖制御機構の解析

      鈴木 真里奈, 篠塚 奈々絵, 出村 拓, 塚谷 裕一, 堀口 吾朗

      第59回日本植物生理学会年会 

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      Event date: 28 3 2018 - 30 3 2018

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    • シロイヌナズナas2 rpl4dにおける葉の背軸化を抑圧するリボソームタンパク質 変異の解析

      深田 かなえ, 高原 正裕, 塚谷 裕一, 堀口 吾朗

      日本植物学会第81回大会 

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      Event date: 8 9 2017 - 10 9 2017

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    • シロイヌナズナにおけるOLI1とHDA9による葉サイズ制御機構の解析

      鈴木 真里奈, 出村 拓, 塚谷 裕一, 堀口 吾朗

      日本植物学会第80回大会 

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      Event date: 16 9 2016 - 18 9 2016

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    • シロイヌナズナのas2 rpl4d変異株における葉の背軸化は、変異型RPL4D mRNAの蓄積、RING finger タンパク質SZK2を介して、NAC型転写因子遺伝子SZK1の発現上昇によって引き起こされる

      堀口吾朗, 増田英典, 井上幹人, 高原正裕, 中田未友希, 塚谷裕一

      第5回植物RNA研究者ネットワークシンポジウム 

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      Event date: 8 1 2016 - 9 1 2016

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    • シロイヌナズナのmiR396過剰発現体が示す地上部と地下部の境界異常の解析

      堀口 吾朗, 塚谷 裕一

      日本植物学会第81回大会 

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      Event date: 8 9 2017 - 10 9 2017

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    • シロイヌナズナの葉サイズを正に制御するOLI1およびHDA9とともに働く因子とその下流因子の探索

      鈴木 真里奈, 篠塚 奈々絵, 出村 拓, 塚谷 裕一, 堀口 吾朗

      日本植物学会第81回大会 

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      Event date: 8 9 2017 - 10 9 2017

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    • リボソーム生合成関連因子GDP1とOLI2が葉の発生に果たす役割の解析

      深田 かなえ, 塚谷 裕一, 堀口 吾朗

      日本植物学会第80回大会 

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      Event date: 16 9 2016 - 18 9 2016

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    • 側根の分裂組織形成不全を示すシロイヌナズナrfc3の組織特異的相補性の解析

      伊藤 将太, 中田 未友希, 堀口吾朗

      日本植物学会第81回大会 

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      Event date: 8 9 2017 - 10 9 2017

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    • 幹細胞を欠く側根を形成するシロイヌナズナrfc3 の抑圧変異株の解析

      長嶋 友美, 大城 克友, 岩瀬 晃康, 中村 栞理, 中田 未友希, 堀口 吾朗

      第59回日本植物生理学会年会 

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      Event date: 28 3 2018 - 30 3 2018

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    • 異なるrpl4dおよびrpl4aアリルで蓄積している変異型mRNAの構造決定とその背腹性制御に及ぼす影響の解析

      増田 英典, 塚谷 裕一, 堀口 吾朗

      日本植物学会第79回大会 

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      Event date: 6 9 2015 - 8 9 2015

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    • 葉の成長に多面的に関わるシロイヌナズナAN3およびGRFの制御機構の解析

      佐藤 晃圭, 皆吉 彩, 池田 奨, 塚谷 裕一, 堀口 吾朗

      日本植物学会第80回大会 

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      Event date: 16 9 2016 - 18 9 2016

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    • A quartet of NAC transcription factor genes is upregulated in response to abnormal ribosomal proteins and enhances leaf abaxialization in asymmetric leaves2

      Horiguchi, G, Ohbayashi, I, Sugiyama, M, Tsukaya, H

      the 59th Annual Meeting of the Japanese Society of Plant Physiologists 

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      Event date: 28 3 2018

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    • Horiguchi, G., Inoue, M., Masuda, H., Nakata, M., Tsukaya, H.: Mutations in ribosomal protein genes induce the expression of NAC transcription factor gene, SUZAKU1, and promote leaf abaxialization in asymmetric leaves2

      Horiguchi, G, Inoue, M, Masuda, H, Nakata, M, Tsukaya, H

      27th International Conference on Arabidopsis Research 

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      Event date: 29 6 2016 - 3 7 2016

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    • How mutations in ribosome-related genes affect leaf adaxial-abaxial patterning in Arabidopsis thaliana

      Horiguchi, G, Tsukaya, H

      50th annual meeting of the Japanese society of developmental biologists 

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      Event date: 10 5 2017 - 13 5 2017

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    • Importance of RFC3 function and plastid translation in root plastids.

      Nakata, M, Sato, M, Wakazaki, M, Satom N, Shikanai, T, Toyooka, K, Tsukaya, H, Horiguchi, G

      The 57th Annual Meeting of The Japanese Society of Plant Physiologists 

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      Event date: 18 3 2016 - 20 3 2016

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    • Leaf abaxialization in rpl4 as2 mutants requires aberrant rpl4 transcript accumulation, a RING finger protein gene SZK2, and upregulation of a NAC transcription factor gene SZK1.

      Horiguchi, G, Inoue, M, Masuda, H, Takahara, M, Nakata, M, Tsukaya, H

      The 57th Annual Meeting of The Japanese Society of Plant Physiologists 

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      Event date: 18 3 2016 - 20 3 2016

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    • Suppression of homeotic change of cotyledons into roots by AN3, GRF, HAN and TPL/TPR in Arabidopsis thaliana.

      Horiguchi, G, Ohike, G, Akima, K, Tsukaya, H

      International ERATO Higashiyama Live-Holonics Symposium 2015, “Organogenesis from Eggs to Mature Plants”. 

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    Professional Memberships

    Research Projects

    • Mechanisms of basic mechanisms and diverity in leaf development

      Japan Society for the Promotion of Science  Grants-in-Aid for Scientific Research Grant-in-Aid for Scientific Research on Innovative Areas (Research in a proposed research area) 

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      6 2019 - 3 2024

      Grant number:19H05672

      Grant amount:\127530000 ( Direct Cost: \98100000 、 Indirect Cost:\29430000 )

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    • 植物におけるリボソームストレスの感知とその情報伝達機構の解析

      日本学術振興会  科学研究費助成事業 基盤研究(C) 

      堀口 吾朗, 古賀 皓之, 前川 修吾

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      4 2019 - 3 2022

      Grant number:19K06714

      Grant amount:\4420000 ( Direct Cost: \3400000 、 Indirect Cost:\1020000 )

      真核生物はリボソーム生合成異常を監視しそれに対処するためのリボソームストレス応答機構を備えている。我々はシロイヌナズナをモデルに植物のリボソームストレス応答に関わる因子を同定している。RINGタンパク質の一種であるSZK2およびリボソームタンパク質のRPL12の下流にSZK1をはじめとした4種のNAC型転写因子を位置付けている。本研究では、「異常型リボソームタンパク質の存在下では、RPL12によってSZK2が活性化され、下流のNAC型転写因子を活性化することでリボソームストレス応答が誘導される」という仮説を立て、その検証を進めている。
      本年度、SZK2とRPL12Bの機能解析にある程度の進展が見られた。RINGドメインを持つタンパク質はユビキチンリガーゼとして働く場合が多い。In vitroユビキチン化アッセイからSZK2の自己ユビキチン可能が検出された。イースト2ハイブリッド法と共免疫沈降法からはSZK2とRPL12Bの相互作用が検出された。既知のアミノ酸置換型RPL12B変異タンパク質は、SZK2との相互作用能を失っていた。また、タバコ葉での共発現、野生型およびT-DNA挿入を持つszk2-2変異株の細胞抽出物を用いた実験から、RPL12BはSZK2依存的に不安定化することを見出した。興味深いことにSZK2には2種のスプライスバリアントが存在し、そのうちの片方のみがRPL12Bを不安定化した。
      上記の実験と並行して、as2 rpl4dおよびas2 rpl4d szk2のサプレッサー変異株の変異部位の同定を進めた。前者のサプレッサーはリボソームストレス応答が誘導できない変異株、後者はリボソームストレス応答誘導能が回復した変異株である。合計10系統のリシーケンスを行い、szk1やszk2の新規アリルに加え、数種の新規変異遺伝子候補を見出した。

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    • Quiescent center-specific regulation of ribosome levels and elucidation of its developmental function

      Japan Society for the Promotion of Science  Grants-in-Aid for Scientific Research Grant-in-Aid for Scientific Research (C) 

      HORIGUCHI Gorou

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      4 2015 - 3 2018

      Grant number:15K07115

      Grant type:Competitive

      Quiescent center (QC) resides in the center of a root apical meristem and has a very low mitotic activity. To establish this quiescence, the amount of ribosomes is assumed to be maintained at a low level. In this study, overexpression of ribosomal protein fused with GFP revealed that at least several distinct ribosomal proteins are maintained at a low level in the QC cells. This regulation is counteracted by the exogenous application of brassinosteroids or cytokinins. In addition, such quantitative regulation of ribosomal proteins requires two mechanisms: one of them suppresses ribosome production in the QC cells and the other eliminates ribosomal proteins produced in excess in entire root apical meristem.

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    • 葉の発生ロジックの多元的開拓

      文部科学省  科学研究費助成事業 

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      6 2013 - 3 2018

      Grant type:Competitive

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    • 位置価に基づく葉形・サイズのホロニック制御機構の解明

      日本学術振興会  科学研究費助成事業 

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      4 2012 - 3 2015

      Grant type:Competitive

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    • リボソームによる植物発生制御機構の解明

      日本学術振興会  科学研究費助成事業 

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      3 2012 - 3 2015

      Grant type:Competitive

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    • 器官サイズ制御の分子基盤-補償作用の分子遺伝学的解明

      科学研究費助成事業 

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      4 2006 - 3 2010

      Grant type:Competitive

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    • 葉の細胞数をモニターする情報の実体とその器官サイズ制御における役割の解明

      科学研究費助成事業 

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      4 2006 - 3 2009

      Grant type:Competitive

      Grant amount:\3300000 ( Direct Cost: \3300000 )

      シロイヌナズナでは葉の細胞数が減少すると、それが引き金となり細胞サイズが大型化する補償作用が知られている。この現象の背景にある分子機構を明らかにするため、転写コア口ベーターをコードするAN3遺伝子の欠損変異株を補償作用のモデルとした解析を行っている。

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    • 葉器官形成における細胞増殖統合システムの解明

      日本学術振興会  科学研究費助成事業 

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      4 2005 - 3 2009

      Grant type:Competitive

      Grant amount:\50700000 ( Direct Cost: \39000000 、 Indirect Cost:\11700000 )

      葉の細胞増殖に関わる様々な因子の単離を目的として、細胞数が減少した突然変異株から、遺伝子単離を進めた。また、これらの因子が補償作用をいかにしてい引き起こすのかについても解析を進めた。その結果、補償作用はいくつかの異なる仕組みによって引き起こされていることが明らかになった。

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    • 細胞数とサイズの調節を介した葉器官サイズ決定機構の解析

      日本学術振興会  科学研究費助成事業 

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      4 2003 - 3 2006

      Grant type:Competitive

      Grant amount:\3600000 ( Direct Cost: \3600000 )

      葉のサイズ制御機構を明らかにするため、シロイヌナズナを用い葉の大きさや形態が変化した突然変異株を網羅的に収集し、その表現型解析を行った。その結果、細胞増殖、細胞伸長のいずれかに特異的な異常を持つ変異株を単離した他、細胞数が減少し、細胞サイズが増加する補償作用を示すもの、これと逆の表現型を示すもの等様々な突然変異株が得られた。

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    • 細胞数とサイズの調節を介した葉器官サイズ決定機構の解析

      日本学術振興会  科学研究費助成事業 若手研究(B) 

      堀口 吾朗

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      2003 - 2005

      Grant number:15770034

      Grant amount:\3600000 ( Direct Cost: \3600000 )

      本研究の目的は、葉のサイズを制御する遺伝学的ネットワークを明らかにすることである。これまでに、葉のサイズに異常を示すシロイヌナズナ突然変異株を多数収集し、それらを葉細胞の数あるいはサイズの増減に応じクラス分けした。本年度はそれらの中でも特徴的な表現型を示す4種の突然変異株について原因遺伝子の特定を行った。
      葉原基における細胞増殖期間を延長することで、葉細胞数を増加させるgrandifolia1-D (gla1-D)変異は、4番染色体の重複に起因することが示唆された。この領域は葉の細胞数を正に制御するAINTEGUMENTA (ANT)の遺伝子を含む。従って、gla1-Dにおける細胞数の増加は、ANTのコピー数の増加が引き金である可能性が示唆された。gra-1D変異が全ての葉組織の細胞を一様に増加させるのに対し、elongata1 (elo1),elo3変異は特に表皮の細胞増殖を強く促進することが判明した。これらの変異株では、表皮とその直下の組織の細胞増殖の調和が乱され、最終的に通常よりも広い細胞間隙を持つ大型かつ長い葉身が形成される。ELO1,ELO3遺伝子をT-DNA tagging法、map-based法でそれぞれ特定したところ、これらの遺伝子はRNA polymerase IIによる転写産物の伸長を制御するElongator複合体の異なるサブユニットをコードすることが明らかになった。これらの結果から、細胞増殖を介する葉サイズ制御機構には、器官全体をカバーするGRA経路、表皮を特に制御するELO経路の最低2種類が存在することが明らかとなった。
      増殖を終えた葉細胞は、液胞化により急激に細胞伸長を行う。この過程に欠損を示す#116変異株の原因遺伝子をmap-based法で特定したところ、cellulose synthaseをコードするIRREGULAR XYLEM3 (IRX3)であることが判明した。IRX3は未成熟な道管特異的に発現し、道管の2次細胞壁肥厚を司る。irx3では道管の2次細胞壁が正常に形成されず、非常に道管がもろくなる。従って、葉の細胞が十分伸長するためには、通道組織からの正常な物質供給が必須であること、またこれとは対照的に、そのような欠損は細胞増殖にはほとんど影響を及ぼさないことが明らかとなった。

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    • 高等植物における脂肪酸不飽和化の真核経路の制御機構とその生理的意義の解明

      科学研究費助成事業 

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      4 1999 - 3 2001

      Grant type:Competitive

      Grant amount:\2800000 ( Direct Cost: \2800000 )

      植物では、低温依存的に生体膜脂質の構成成分であるトリエン脂肪酸が増加する。トリエン脂肪酸を合成するw-3脂肪酸不飽和化酵素遺伝子の発現は翻訳レベルで制御されており、その発現制御に関わる新規変異株の取得を目的とした研究を行った

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    • 高等植物の温度環境適応における生体膜脂質のトリエン脂肪酸含量の調節機構

      科学研究費助成事業 

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      4 1996 - 3 1999

      Grant type:Competitive

      高等植物の脂肪酸組成は温度依存的に変化する。その中でもとり得ん脂肪酸含量は低温によって顕著に蓄積量が増加する。このような増加の背景にある分子機構を明らかにするため、コムギからトリエン脂肪酸を合成するw-3 脂肪酸不飽和化酵素遺伝子(TaFAD3) を単離し、その発現を解析した。その結果、低温依存的にTaFAD3遺伝子の翻訳レベルが増加することが明らかになった

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