Studies on the rice LEAF INCLINATION1 (LC1), an IAA-amido synthetase, reveal the effects of auxin in leaf inclination control.

The angle of rice leaf inclination is an important agronomic trait and closely related to the yields and architecture of crops. Although few mutants with altered leaf angles have been reported, the molecular mechanism remains to be elucidated, especially whether hormones are involved in this process. Through genetic screening, a rice gain-of-function mutant leaf inclination1, lc1-D, was identified from the Shanghai T-DNA Insertion Population (SHIP). Phenotypic analysis confirmed the exaggerated leaf angles of lc1-D due to the stimulated cell elongation at the lamina joint. LC1 is transcribed in various tissues and encodes OsGH3-1, an indole-3-acetic acid (IAA) amido synthetase, whose homolog of Arabidopsis functions in maintaining the auxin homeostasis by conjugating excess IAA to various amino acids. Indeed, recombinant LC1 can catalyze the conjugation of IAA to Ala, Asp, and Asn in vitro, which is consistent with the decreased free IAA amount in lc1-D mutant. lc1-D is insensitive to IAA and hypersensitive to exogenous BR, in agreement with the microarray analysis that reveals the altered transcriptions of genes involved in auxin signaling and BR biosynthesis. These results indicate the crucial roles of auxin homeostasis in the leaf inclination control.

[1]  E. K. Yoon,et al.  ‘Evidence of an auxin signal pathway, microRNA167-ARF8-GH3, and its response to exogenous auxin in cultured rice cells’ , 2006, Nucleic acids research.

[2]  C. Breton,et al.  PCR cloning and expression analysis of a cDNA encoding a pectinacetylesterase from Vigna radiata L , 1996, FEBS Letters.

[3]  A. Müller,et al.  Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. , 1998, Science.

[4]  B. Bernstein,et al.  SEMAPHORE1 functions during the regulation of ancestrally duplicated knox genes and polar auxin transport in maize. , 2002, Development.

[5]  G. Fink,et al.  ILR1, an amidohydrolase that releases active indole-3-acetic acid from conjugates. , 1995, Science.

[6]  K. Feldmann,et al.  Brassinosteroids Regulate Grain Filling in Rice[W][OA] , 2008, The Plant Cell Online.

[7]  H. Xue,et al.  A brassinolide-suppressed rice MADS-box transcription factor, OsMDP1, has a negative regulatory role in BR signaling. , 2006, The Plant journal : for cell and molecular biology.

[8]  P. Christou,et al.  ‘Green revolution’ genes encode mutant gibberellin response modulators , 1999, Nature.

[9]  Sheng-Wei Zhang,et al.  Altered Architecture and Enhanced Drought Tolerance in Rice via the Down-Regulation of Indole-3-Acetic Acid by TLD1/OsGH3.13 Activation1[C][W] , 2009, Plant Physiology.

[10]  J. Chory,et al.  A role for flavin monooxygenase-like enzymes in auxin biosynthesis. , 2001, Science.

[11]  B. Bartel,et al.  Auxin: regulation, action, and interaction. , 2005, Annals of botany.

[12]  J. Alvarez,et al.  Morphogenesis in pinoid mutants of Arabidopsis thaliana , 1995 .

[13]  H. Tsukaya.  Leaf shape: genetic controls and environmental factors. , 2005, The International journal of developmental biology.

[14]  A. Bleecker,et al.  A Mutation Altering Auxin Homeostasis and Plant Morphology in Arabidopsis. , 1995, The Plant cell.

[15]  Brown,et al.  Disruption of auxin transport is associated with aberrant leaf development in maize , 1999, Plant physiology.

[16]  Z. Hong,et al.  The Rice brassinosteroid-deficient dwarf2 Mutant, Defective in the Rice Homolog of Arabidopsis DIMINUTO/DWARF1, Is Rescued by the Endogenously Accumulated Alternative Bioactive Brassinosteroid, Dolichosterone , 2005, The Plant Cell Online.

[17]  DFL1, an auxin-responsive GH3 gene homologue, negatively regulates shoot cell elongation and lateral root formation, and positively regulates the light response of hypocotyl length. , 2001 .

[18]  Walter P. Suza,et al.  Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acidw⃞ , 2005, The Plant Cell Online.

[19]  M. Matsuoka,et al.  The rice SPINDLY gene functions as a negative regulator of gibberellin signaling by controlling the suppressive function of the DELLA protein, SLR1, and modulating brassinosteroid synthesis. , 2006, The Plant journal : for cell and molecular biology.

[20]  N. Mochizuki,et al.  Expression of the AtGH3a gene, an Arabidopsis homologue of the soybean GH3 gene, is regulated by phytochrome B. , 2002, Plant & cell physiology.

[21]  T. Setter,et al.  A GH3-like gene, CcGH3, isolated from Capsicum chinense L. fruit is regulated by auxin and ethylene* , 2005, Plant Molecular Biology.

[22]  T. Sinclair,et al.  Erect Leaves and Photosynthesis in Rice , 1999, Science.

[23]  F. B. Pickett,et al.  Mutations in the AXR3 gene of Arabidopsis result in altered auxin response including ectopic expression from the SAUR-AC1 promoter. , 1996, The Plant journal : for cell and molecular biology.

[24]  K. Ljung,et al.  A Family of Auxin-Conjugate Hydrolases That Contributes to Free Indole-3-Acetic Acid Levels during Arabidopsis Germination1 , 2004, Plant Physiology.

[25]  M. Bevan,et al.  GUS fusions: beta‐glucuronidase as a sensitive and versatile gene fusion marker in higher plants. , 1987, The EMBO journal.

[26]  Zhiqiang Ma,et al.  An Indole-3-Acetic Acid Carboxyl Methyltransferase Regulates Arabidopsis Leaf Developmentw⃞ , 2005, The Plant Cell Online.

[27]  J. Reed,et al.  Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene. , 1999, Development.

[28]  Harry Smith,et al.  Transgene-mediated auxin overproduction in Arabidopsis: hypocotyl elongation phenotype and interactions with the hy6-1 hypocotyl elongation and axr1 auxin-resistant mutants , 1995, Plant Molecular Biology.

[29]  T. Komari,et al.  Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. , 1994, The Plant journal : for cell and molecular biology.

[30]  M. Matsui,et al.  FIN219, an auxin-regulated gene, defines a link between phytochrome A and the downstream regulator COP1 in light control of Arabidopsis development. , 2000, Genes & development.

[31]  Allison E. Cocke,et al.  Light interacts with auxin during leaf elongation and leaf angle development in young corn seedlings , 2002, Planta.

[32]  Mukesh Jain,et al.  The auxin-responsive GH3 gene family in rice (Oryza sativa) , 2005, Functional & Integrative Genomics.

[33]  M. Matsuoka,et al.  Loss of Function of a Rice brassinosteroid insensitive1 Homolog Prevents Internode Elongation and Bending of the Lamina Joint , 2000, Plant Cell.

[34]  G. Sandberg,et al.  Over-expression of an Arabidopsis gene encoding a glucosyltransferase of indole-3-acetic acid: phenotypic characterisation of transgenic lines. , 2002, The Plant journal : for cell and molecular biology.

[35]  Masahiko Maekawa,et al.  LAX and SPA: Major regulators of shoot branching in rice , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[36]  C. Kuhlemeier,et al.  Auxin Regulates the Initiation and Radial Position of Plant Lateral Organs , 2000, Plant Cell.

[37]  G. An,et al.  Rice SVP-group MADS-box proteins, OsMADS22 and OsMADS55, are negative regulators of brassinosteroid responses. , 2008, The Plant journal : for cell and molecular biology.

[38]  Gerhard K. H. Przemeck,et al.  Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization , 2004, Planta.

[39]  Zhenying Shi,et al.  Over-expression of rice OsAGO7 gene induces upward curling of the leaf blade that enhanced erect-leaf habit , 2007, Planta.

[40]  M. Sussman,et al.  ABP1 is required for organized cell elongation and division in Arabidopsis embryogenesis. , 2001, Genes & development.

[41]  P. J. Davies.  Plant hormones : physiology, biochemistry and molecular biology , 1995 .

[42]  Yi Li,et al.  Expansins and cell growth. , 2003, Current opinion in plant biology.

[43]  M. Talón,et al.  The GH3 family in plants: genome wide analysis in rice and evolutionary history based on EST analysis. , 2006, Gene.

[44]  M. Matsui,et al.  ydk1-D, an auxin-responsive GH3 mutant that is involved in hypocotyl and root elongation. , 2004, The Plant journal : for cell and molecular biology.

[45]  H. Cao,et al.  Brassinosteroid-induced rice lamina joint inclination and its relation to indole-3-acetic acid and ethylene , 1995, Plant Growth Regulation.

[46]  D. Inzé,et al.  Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. , 1995, The Plant cell.

[47]  H. Brumer,et al.  The XTH Gene Family: An Update on Enzyme Structure, Function, and Phylogeny in Xyloglucan Remodeling1 , 2010, Plant Physiology.

[48]  S. Kikuchi,et al.  Isolation and Characterization of a Rice Dwarf Mutant with a Defect in Brassinosteroid Biosynthesis1 , 2002, Plant Physiology.

[49]  K. Chong,et al.  Functions of OsBZR1 and 14-3-3 proteins in brassinosteroid signaling in rice , 2007, Proceedings of the National Academy of Sciences.

[50]  Makoto Matsuoka,et al.  Production and characterization of auxin-insensitive rice by overexpression of a mutagenized rice IAA protein. , 2006, The Plant journal : for cell and molecular biology.

[51]  W. Liu,et al.  Roles of OsCKI1, a rice casein kinase I, in root development and plant hormone sensitivity. , 2003, The Plant journal : for cell and molecular biology.

[52]  A. Paterson,et al.  RFLP facilitated analysis of tiller and leaf angles in rice (Oryza sativa L.) , 1999, Euphytica.

[53]  G. An,et al.  Constitutively wilted 1, a member of the rice YUCCA gene family, is required for maintaining water homeostasis and an appropriate root to shoot ratio , 2007, Plant Molecular Biology.

[54]  M. Estelle,et al.  The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. , 2000, Development.

[55]  星川 清親.  The growing rice plant : an anatomical monograph , 1989 .

[56]  E. Liscum,et al.  The NPH4 Locus Encodes the Auxin Response Factor ARF7, a Conditional Regulator of Differential Growth in Aerial Arabidopsis Tissue , 2000, Plant Cell.

[57]  G. An,et al.  Mutations in the rice liguleless gene result in a complete loss of the auricle, ligule, and laminar joint , 2007, Plant Molecular Biology.

[58]  Y. Eshed,et al.  Auxin Response Factors Mediate Arabidopsis Organ Asymmetry via Modulation of KANADI Activityw⃞ , 2005, The Plant Cell Online.

[59]  G. Jürgens,et al.  The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. , 2002, Genes & development.

[60]  M. Matsuoka,et al.  Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice , 2006, Nature Biotechnology.

[61]  Cai-guo Xu,et al.  Activation of the Indole-3-Acetic Acid–Amido Synthetase GH3-8 Suppresses Expansin Expression and Promotes Salicylate- and Jasmonate-Independent Basal Immunity in Rice[W] , 2008, The Plant Cell Online.

[62]  N. Chua,et al.  The Arabidopsis Auxin-Inducible Gene ARGOS Controls Lateral Organ Size Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.013557. , 2003, The Plant Cell Online.

[63]  Fang-fang Fu,et al.  Studies on rice seed quality through analysis of a large-scale T-DNA insertion population , 2009, Cell Research.

[64]  G. Hagen,et al.  Rapid induction of selective transcription by auxins , 1985, Molecular and cellular biology.

[65]  B. Bartel,et al.  Characterization of a Family of IAA-Amino Acid Conjugate Hydrolases from Arabidopsis* , 2002, The Journal of Biological Chemistry.

[66]  Luis Herrera-Estrella,et al.  Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System1 , 2002, Plant Physiology.

[67]  M. Caboche,et al.  Sur2 mutations of Arabidopsis thaliana define a new locus involved in the control of auxin homeostasis. , 1998, The Plant journal : for cell and molecular biology.

[68]  Yukihisa Shimada,et al.  Loss-of-function of a rice brassinosteroid biosynthetic enzyme, C-6 oxidase, prevents the organized arrangement and polar elongation of cells in the leaves and stem. , 2002, The Plant journal : for cell and molecular biology.

[69]  M. Bennett,et al.  Regulation of phyllotaxis by polar auxin transport , 2003, Nature.

[70]  H. Xue,et al.  Arabidopsis Membrane Steroid Binding Protein 1 Is Involved in Inhibition of Cell Elongationw⃞ , 2005, The Plant Cell Online.

[71]  K. Mori,et al.  A Rice Lamina Inclination Test—A Micro-quantitative Bioassay for Brassinosteroids , 1984 .

[72]  Z. Hong,et al.  A Rice Brassinosteroid-Deficient Mutant, ebisu dwarf (d2), Is Caused by a Loss of Function of a New Member of Cytochrome P450 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014712. , 2003, The Plant Cell Online.

[73]  Pierre Frasse,et al.  The Tomato Aux/IAA Transcription Factor IAA9 Is Involved in Fruit Development and Leaf Morphogenesisw⃞ , 2005, The Plant Cell Online.

[74]  M. Matsuoka,et al.  Generating high-yielding varieties by genetic manipulation of plant architecture. , 2004, Current opinion in biotechnology.

[75]  K. Ljung,et al.  The SUR2 gene of Arabidopsis thaliana encodes the cytochrome P450 CYP83B1, a modulator of auxin homeostasis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[76]  Mariusz Kowalczyk,et al.  Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana , 2002, Plant Molecular Biology.

[77]  M. Matsui,et al.  DFL2, a new member of the Arabidopsis GH3 gene family, is involved in red light-specific hypocotyl elongation. , 2003, Plant & cell physiology.

[78]  H. Xue,et al.  Genome-Wide Analysis of the Complex Transcriptional Networks of Rice Developing Seeds , 2012, PloS one.

[79]  Zhang-liang Chen,et al.  Hormonal Regulation of Leaf Morphogenesis in Arabidopsis , 2007 .

[80]  Rita Sharma,et al.  Asymmetric Auxin Response Precedes Asymmetric Growth and Differentiation of asymmetric leaf1 and asymmetric leaf2 Arabidopsis Leaves , 2005, The Plant Cell Online.

[81]  Mukesh Jain,et al.  Structure and expression analysis of early auxin-responsive Aux/IAA gene family in rice (Oryza sativa) , 2005, Functional & Integrative Genomics.

[82]  T. Koshiba,et al.  NARROW LEAF 7 controls leaf shape mediated by auxin in rice , 2008, Molecular Genetics and Genomics.