Comprehensive Transcriptome Analysis of Phytohormone Biosynthesis and Signaling Genes in Microspore/Pollen and Tapetum of Rice

To investigate the involvement of phytohormones during rice microspore/pollen (MS/POL) development, endogenous levels of IAA, gibberellins (GAs), cytokinins (CKs) and abscisic acid (ABA) in the mature anther were analyzed. We also analyzed the global expression profiles of genes related to seven phytohormones, namely auxin, GAs, CKs, brassinosteroids, ethylene, ABA and jasmonic acids, in MS/POL and tapetum (TAP) using a 44K microarray combined with a laser microdissection technique (LM-array analysis). IAA and GA4 accumulated in a much higher amount in the mature anther compared with the other tissues, while CKs and ABA did not. LM-array analysis revealed that sets of genes required for IAA and GA synthesis were coordinately expressed during the later stages of MS/POL development, suggesting that these genes are responsible for the massive accumulation of IAA and GA4 in the mature anther. In contrast, genes for GA signaling were preferentially expressed during the early developmental stages of MS/POL and throughout TAP development, while their expression was down-regulated at the later stages of MS/POL development. In the case of auxin signaling genes, such mirror-imaged expression observed in GA synthesis and signaling genes was not observed. IAA receptor genes were mostly expressed during the late stages of MS/POL development, and various sets of AUX/IAA and ARF genes were expressed during the different stages of MS/POL or TAP development. Such cell type-specific expression profiles of phytohormone biosynthesis and signaling genes demonstrate the validity and importance of analyzing the expression of phytohormone-related genes in individual cell types independently of other cells/tissues.

[1]  Eran Pichersky,et al.  The Tomato Homolog of CORONATINE-INSENSITIVE1 Is Required for the Maternal Control of Seed Maturation, Jasmonate-Signaled Defense Responses, and Glandular Trichome Development Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org , 2004, The Plant Cell Online.

[2]  M. Matsuoka,et al.  Loss-of-function mutations of the rice GAMYB gene impair alpha-amylase expression in aleurone and flower development. , 2004, The Plant cell.

[3]  J. Browse,et al.  The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[4]  Masashi Yamada,et al.  Plant development is regulated by a family of auxin receptor F box proteins. , 2005, Developmental cell.

[5]  M. Kojima,et al.  Overexpression of a petunia zinc-finger gene alters cytokinin metabolism and plant forms. , 2004, The Plant journal : for cell and molecular biology.

[6]  C. Wasternack,et al.  Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana , 2003, Plant Molecular Biology.

[7]  G. Agrawal,et al.  Screening of the rice viviparous mutants generated by endogenous retrotransposon Tos17 insertion. Tagging of a zeaxanthin epoxidase gene and a novel ostatc gene. , 2001, Plant physiology.

[8]  M. Endo,et al.  Separated Transcriptomes of Male Gametophyte and Tapetum in Rice: Validity of a Laser Microdissection (LM) Microarray , 2008, Plant & cell physiology.

[9]  M. Matsuoka,et al.  slender Rice, a Constitutive Gibberellin Response Mutant, Is Caused by a Null Mutation of the SLR1 Gene, an Ortholog of the Height-Regulating Gene GAI/RGA/RHT/D8 , 2001, Plant Cell.

[10]  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.

[11]  A. Peeters,et al.  The Arabidopsis aldehyde oxidase 3 (AAO3) gene product catalyzes the final step in abscisic acid biosynthesis in leaves. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[12]  R. Solano,et al.  JASMONATE-INSENSITIVE1 Encodes a MYC Transcription Factor Essential to Discriminate between Different Jasmonate-Regulated Defense Responses in Arabidopsis , 2004, The Plant Cell Online.

[13]  E. Nambara,et al.  A Unique Short-Chain Dehydrogenase/Reductase in Arabidopsis Glucose Signaling and Abscisic Acid Biosynthesis and Functions , 2002, The Plant Cell Online.

[14]  D. Ohta,et al.  Tomato cytochrome P450 CYP734A7 functions in brassinosteroid catabolism. , 2006, Phytochemistry.

[15]  E. Zažímalová,et al.  Points of regulation for auxin action , 2003, Plant Cell Reports.

[16]  Hua Jin,et al.  Regulation of brassinosteroid signaling. , 2007, Trends in plant science.

[17]  Masatomo Kobayashi,et al.  Expression of novel rice gibberellin 2-oxidase gene is under homeostatic regulation by biologically active gibberellins , 2003, Journal of Plant Research.

[18]  Yukihisa Shimada,et al.  GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. , 2006, The Plant journal : for cell and molecular biology.

[19]  J. C. Cook,et al.  Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen , 1979, Nature.

[20]  G. Fink,et al.  Arabidopsis mutants resistant to the auxin effects of indole-3-acetonitrile are defective in the nitrilase encoded by the NIT1 gene. , 1997, The Plant cell.

[21]  H. Miyagawa,et al.  Metabolic profiling of tryptophan-overproducing rice calli that express a feedback-insensitive alpha subunit of anthranilate synthase. , 2005, Plant & cell physiology.

[22]  J. Noel,et al.  Methylation of Gibberellins by Arabidopsis GAMT1 and GAMT2[W] , 2007, The Plant Cell Online.

[23]  M. Matsuoka,et al.  Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? , 2003, The Plant journal : for cell and molecular biology.

[24]  Anna N. Stepanova,et al.  TAA1-Mediated Auxin Biosynthesis Is Essential for Hormone Crosstalk and Plant Development , 2008, Cell.

[25]  D. Grierson,et al.  Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants , 1990, Nature.

[26]  Masatomo Kobayashi,et al.  An Overview of Gibberellin Metabolism Enzyme Genes and Their Related Mutants in Rice1[w] , 2004, Plant Physiology.

[27]  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.

[28]  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.

[29]  Mukesh Jain,et al.  Genomic Survey and Gene Expression Analysis of the Basic Leucine Zipper Transcription Factor Family in Rice1[W][OA] , 2007, Plant Physiology.

[30]  P. Hugueney,et al.  Molecular identification of zeaxanthin epoxidase of Nicotiana plumbaginifolia, a gene involved in abscisic acid biosynthesis and corresponding to the ABA locus of Arabidopsis thaliana. , 1996, The EMBO journal.

[31]  D. Botstein,et al.  Cluster analysis and display of genome-wide expression patterns. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[32]  Anthony L. Schilmiller,et al.  COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine , 2008, Proceedings of the National Academy of Sciences.

[33]  G. Sembdner,et al.  Jasmonates from pine pollen , 1995 .

[34]  A. Webb,et al.  ABI1 Protein Phosphatase 2C Is a Negative Regulator of Abscisic Acid Signaling , 1999, Plant Cell.

[35]  T. Young,et al.  Programmed cell death during endosperm development , 2000, Plant Molecular Biology.

[36]  D. Swartzfager,et al.  Indole-3-acetic Acid Levels of Plant Tissue as Determined by a New High Performance Liquid Chromatographic Method. , 1978, Plant physiology.

[37]  Hitoshi Sakakibara,et al.  The GID1-Mediated Gibberellin Perception Mechanism Is Conserved in the Lycophyte Selaginella moellendorffii but Not in the Bryophyte Physcomitrella patens[W] , 2007, The Plant Cell Online.

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

[39]  J. Sheen,et al.  Advances in Cytokinin Signaling , 2007, Science.

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

[41]  Masatomo Kobayashi,et al.  GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin , 2005, Nature.

[42]  J. B. Reid,et al.  MYC2 Differentially Modulates Diverse Jasmonate-Dependent Functions in Arabidopsis[W] , 2007, The Plant Cell Online.

[43]  Anna N. Stepanova,et al.  A Link between Ethylene and Auxin Uncovered by the Characterization of Two Root-Specific Ethylene-Insensitive Mutants in Arabidopsis , 2005, The Plant Cell Online.

[44]  Y. Kamiya,et al.  ELONGATED UPPERMOST INTERNODE Encodes a Cytochrome P450 Monooxygenase That Epoxidizes Gibberellins in a Novel Deactivation Reaction in Rice[W] , 2006, The Plant Cell Online.

[45]  J. Ecker,et al.  Functional Genomic Analysis of the AUXIN/INDOLE-3-ACETIC ACID Gene Family Members in Arabidopsis thaliana[W] , 2005, The Plant Cell Online.

[46]  T. Adachi,et al.  Molecular cloning of the gene for indolepyruvate decarboxylase from Enterobacter cloacae , 1991, Molecular and General Genetics MGG.

[47]  S. Tabata,et al.  Ultrastructural characterization of exine development of the transient defective exine 1 mutant suggests the existence of a factor involved in constructing reticulate exine architecture from sporopollenin aggregates. , 2008, Plant & cell physiology.

[48]  Joseph J. Kieber,et al.  Cytokinin signaling: two-components and more. , 2008, Trends in plant science.

[49]  S. Prat,et al.  Conserved MYC transcription factors play a key role in jasmonate signaling both in tomato and Arabidopsis. , 2004, Genes & development.

[50]  Joanne Chory,et al.  Rapid Synthesis of Auxin via a New Tryptophan-Dependent Pathway Is Required for Shade Avoidance in Plants , 2008, Cell.

[51]  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.

[52]  M. Matsuoka,et al.  Ectopic Expression of KNOTTED 1-Like Homeobox Protein Induces Expression of Cytokinin Biosynthesis Genes in Rice 1 [ W ] , 2006 .

[53]  C. Wasternack,et al.  Allene oxide synthases of barley (Hordeum vulgare cv. Salome): tissue specific regulation in seedling development. , 2000, The Plant journal : for cell and molecular biology.

[54]  J. Chory,et al.  BAS1: A gene regulating brassinosteroid levels and light responsiveness in Arabidopsis. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[55]  I. Tiryaki,et al.  The Oxylipin Signal Jasmonic Acid Is Activated by an Enzyme That Conjugates It to Isoleucine in Arabidopsis , 2004, The Plant Cell Online.

[56]  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.

[57]  Shihshieh Huang,et al.  Transgenic Studies on the Involvement of Cytokinin and Gibberellin in Male Development , 2003, Plant Physiology.

[58]  M. Matsuoka,et al.  A Rice Semi-Dwarf Gene, Tan-Ginbozu (D35), Encodes the Gibberellin Biosynthesis Enzyme, ent-Kaurene Oxidase , 2004, Plant Molecular Biology.

[59]  S. Ishiguro,et al.  The DEFECTIVE IN ANTHER DEHISCENCE1 Gene Encodes a Novel Phospholipase A1 Catalyzing the Initial Step of Jasmonic Acid Biosynthesis, Which Synchronizes Pollen Maturation, Anther Dehiscence, and Flower Opening in Arabidopsis , 2001, The Plant Cell Online.

[60]  T. Yokota,et al.  C-23 Hydroxylation by Arabidopsis CYP90C1 and CYP90D1 Reveals a Novel Shortcut in Brassinosteroid Biosynthesis[W] , 2006, The Plant Cell Online.

[61]  M. Ishitani,et al.  The Arabidopsis LOS5/ABA3 Locus Encodes a Molybdenum Cofactor Sulfurase and Modulates Cold Stress– and Osmotic Stress–Responsive Gene Expression , 2001, The Plant Cell Online.

[62]  Masatomo Kobayashi,et al.  Accumulation of Phosphorylated Repressor for Gibberellin Signaling in an F-box Mutant , 2003, Science.

[63]  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.

[64]  K. Shinozaki,et al.  A genome-wide gain-of-function analysis of rice genes using the FOX-hunting system , 2007, Plant Molecular Biology.

[65]  Makoto Matsuoka,et al.  Auxin Biosynthesis by the YUCCA Genes in Rice1[W][OA] , 2007, Plant Physiology.

[66]  F. Wightman,et al.  Gas chromatography-mass spectrometry evidence for several endogenous auxins in pea seedling organs , 1985, Planta.

[67]  T. Kuromori,et al.  ABA-Hypersensitive Germination3 Encodes a Protein Phosphatase 2C (AtPP2CA) That Strongly Regulates Abscisic Acid Signaling during Germination among Arabidopsis Protein Phosphatase 2Cs1[W] , 2005, Plant Physiology.

[68]  Anthony L. Schilmiller,et al.  Role of β-Oxidation in Jasmonate Biosynthesis and Systemic Wound Signaling in Tomatow⃞ , 2005, The Plant Cell Online.

[69]  J. Micol,et al.  The JAZ family of repressors is the missing link in jasmonate signalling , 2007, Nature.

[70]  G. S. Khush,et al.  Green revolution: A mutant gibberellin-synthesis gene in rice , 2002, Nature.

[71]  S. Clouse.  Arabidopsis Mutants Reveal Multiple Roles for Sterols in Plant Development , 2002, The Plant Cell Online.

[72]  Q. Qian,et al.  Cytokinin Oxidase Regulates Rice Grain Production , 2005, Science.

[73]  B. Rubinstein.  Regulation of cell death in flower petals , 2000, Plant Molecular Biology.

[74]  Z. Hong,et al.  The Role of OsBRI 1 and Its Homologous Genes , OsBRL 1 and OsBRL 3 , in Rice 1 , 2006 .

[75]  K. Asano,et al.  Gibberellin Regulates Pollen Viability and Pollen Tube Growth in Rice[W] , 2007, The Plant Cell Online.

[76]  G. C. Medlow,et al.  Identification of IAA in phloem and root pressure saps of Ricinus communis L. by mass spectrometry , 1974, Planta.

[77]  N. Takahashi,et al.  Jasmonic Acid and Methyl Jasmonate in Pollens and Anthers of Three Camellia Species , 1982 .

[78]  Joseph R. Ecker,et al.  Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation , 2005, Development.

[79]  M. Matsuoka,et al.  Ectopic Expression of KNOTTED1-Like Homeobox Protein Induces Expression of Cytokinin Biosynthesis Genes in Rice1[W] , 2006, Plant Physiology.

[80]  Y. Choi,et al.  Jasmonic acid carboxyl methyltransferase: A key enzyme for jasmonate-regulated plant responses , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[81]  G. Howe,et al.  Identification of a Peroxisomal Acyl-activating Enzyme Involved in the Biosynthesis of Jasmonic Acid in Arabidopsis*♦ , 2006, Journal of Biological Chemistry.

[82]  Hitoshi Sakakibara,et al.  Cytokinins: activity, biosynthesis, and translocation. , 2006, Annual review of plant biology.

[83]  Masatomo Kobayashi,et al.  Quantitative Analysis of Endogenous Gibberellins in Normal and Dwarf Cultivars of Rice , 1989 .

[84]  M. Kojima,et al.  Overexpression of a type-A response regulator alters rice morphology and cytokinin metabolism. , 2007, Plant & cell physiology.

[85]  P. M. Sanders,et al.  The Arabidopsis DELAYED DEHISCENCE1 Gene Encodes an Enzyme in the Jasmonic Acid Synthesis Pathway , 2000, Plant Cell.

[86]  T. Hough,et al.  Effect of Brassinolide and other Growth Regulators on the Germination and Growth of Pollen Tubes of Prunus avium using a Multiple Hanging-drop Assay , 1985 .

[87]  Charlie Chang,et al.  Functional Genomic Analysis of the AUXIN RESPONSE FACTOR Gene Family Members in Arabidopsis thaliana: Unique and Overlapping Functions of ARF7 and ARF19w⃞ , 2005, The Plant Cell Online.

[88]  M. Drew,et al.  Programmed cell death and aerenchyma formation in roots. , 2000, Trends in plant science.

[89]  Thorsten Hamann,et al.  Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators , 2005, The EMBO journal.

[90]  J E Mullet,et al.  A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[91]  M. Caboche,et al.  Higher activity of an aldehyde oxidase in the auxin-overproducing superroot1 mutant of Arabidopsis thaliana. , 1998, Plant physiology.

[92]  Neel G. Barnaby,et al.  Potential Sites of Bioactive Gibberellin Production during Reproductive Growth in Arabidopsis[W] , 2008, The Plant Cell Online.

[93]  M. Kumar,et al.  Whole-Genome Analysis of Oryza sativa Reveals Similar Architecture of Two-Component Signaling Machinery with Arabidopsis1[W] , 2006, Plant Physiology.

[94]  D. J. Lee,et al.  Molecular Cloning of GA 2-Oxidase3 from Spinach and Its Ectopic Expression in Nicotiana sylvestris1 , 2005, Plant Physiology.

[95]  Patrick S Schnable,et al.  Laser-capture microdissection, a tool for the global analysis of gene expression in specific plant cell types: identification of genes expressed differentially in epidermal cells or vascular tissues of maize. , 2003, The Plant cell.

[96]  M. Matsuoka,et al.  GID1-mediated gibberellin signaling in plants. , 2008, Trends in Plant Science.

[97]  J. Chory,et al.  A Putative Leucine-Rich Repeat Receptor Kinase Involved in Brassinosteroid Signal Transduction , 1997, Cell.

[98]  J. B. Reid,et al.  The Distribution of Gibberellins in Vegetative Tissues of Pisum sativum L. : I. Biological and Biochemical Consequences of the le Mutation. , 1992, Plant physiology.

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

[100]  D. Xie,et al.  COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. , 1998, Science.

[101]  Nori Kurata,et al.  Identification and characterization of cytokinin-signalling gene families in rice. , 2006, Gene.

[102]  F. Nagy,et al.  Brassinosteroids Rescue the Deficiency of CYP90, a Cytochrome P450, Controlling Cell Elongation and De-etiolation in Arabidopsis , 1996, Cell.

[103]  P. M. Sanders,et al.  Anther development: basic principles and practical applications. , 1993, The Plant cell.

[104]  M. Hamberg,et al.  Molecular Cloning of Allene Oxide Cyclase , 2000, The Journal of Biological Chemistry.

[105]  C. Wasternack,et al.  Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. , 2007, Annals of botany.

[106]  D. McCarty,et al.  Specific oxidative cleavage of carotenoids by VP14 of maize. , 1997, Science.

[107]  Y. Kamiya,et al.  The Arabidopsis cytochrome P450 CYP707A encodes ABA 8′‐hydroxylases: key enzymes in ABA catabolism , 2004, The EMBO journal.

[108]  G. Falasca,et al.  Auxin Regulates Arabidopsis Anther Dehiscence, Pollen Maturation, and Filament Elongation[W] , 2008, The Plant Cell Online.

[109]  B. Han,et al.  Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). , 2007, Gene.

[110]  S. Tabata,et al.  ARR1, a Transcription Factor for Genes Immediately Responsive to Cytokinins , 2001, Science.

[111]  O. Miersch,et al.  A jasmonic acid conjugate, N-[(—)-jasmonoyl]-tyramine, from Petunia pollen , 1998 .

[112]  J. Ecker,et al.  Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. , 2002, Genes & development.

[113]  A. Gunawardena.  Programmed cell death and tissue remodelling in plants. , 2008, Journal of experimental botany.

[114]  S. Jacobsen,et al.  SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[115]  Joseph R. Ecker,et al.  CTR1, a negative regulator of the ethylene response pathway in arabidopsis, encodes a member of the Raf family of protein kinases , 1993, Cell.

[116]  M. Matsuoka,et al.  Overexpression of a GRAS protein lacking the DELLA domain confers altered gibberellin responses in rice. , 2005, The Plant journal : for cell and molecular biology.

[117]  R. Bensen,et al.  Detection of endogenous gibberellins and their relationship to hypocotyl elongation in soybean seedlings. , 1990, Plant physiology.

[118]  Wenyu Yang,et al.  AtPLAI Is an Acyl Hydrolase Involved in Basal Jasmonic Acid Production and Arabidopsis Resistance to Botrytis cinerea* , 2007, Journal of Biological Chemistry.

[119]  P. Gaskin,et al.  The endogenous gibberellins of dwarf mutants of lettuce. , 1991, Plant physiology.

[120]  M. Matsuoka,et al.  Cloning and functional analysis of two gibberellin 3β-hydroxylase genes that are differently expressed during the growth of rice , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[121]  T. Mizuno,et al.  A Link between Cytokinin and ASL9 (ASYMMETRIC LEAVES 2 LIKE 9) That Belongs to the AS2/LOB (LATERAL ORGAN BOUNDARIES) Family Genes in Arabidopsis thaliana , 2007, Bioscience, biotechnology, and biochemistry.

[122]  C. Wasternack,et al.  Jasmonate‐induced lipoxygenase forms are localized in chloroplasts of barley leaves (Hordeum vulgare cv. Salome) , 1995 .

[123]  J. Micol,et al.  The Short-Chain Alcohol Dehydrogenase ABA2 Catalyzes the Conversion of Xanthoxin to Abscisic Aldehyde Online version contains Web-only data. Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002477. , 2002, The Plant Cell Online.

[124]  B. Mueller‐Roeber,et al.  Auxin Flow in Anther Filaments is Critical for Pollen Grain Development through Regulating Pollen Mitosis , 2006, Plant Molecular Biology.

[125]  Cristina Martinez,et al.  Gene-Specific Involvement of β-Oxidation in Wound-Activated Responses in Arabidopsis1 , 2004, Plant Physiology.

[126]  H. Kamada,et al.  Anther-specific expression of mutated melon ethylene receptor gene Cm-ERS1/H70A affected tapetum degeneration and pollen grain production in transgenic tobacco plants , 2006, Plant Cell Reports.

[127]  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.

[128]  T. Kuromori,et al.  ABA-Hypersensitive Germination 3 Encodes a Protein Phosphatase 2 C ( AtPP 2 CA ) That Strongly Regulates Abscisic Acid Signaling during Germination among Arabidopsis Protein Phosphatase 2 Cs 1 [ W ] , 2005 .

[129]  Bryan C Thines,et al.  JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling , 2007, Nature.

[130]  K. Ohmiya,et al.  The seed-specific transcription factor VP1 (OSVP1) is expressed in rice suspension-cultured cells. , 1996, Plant & cell physiology.

[131]  Z. Hong,et al.  The Role of OsBRI1 and Its Homologous Genes, OsBRL1 and OsBRL3, in Rice1 , 2006, Plant Physiology.

[132]  P. Bethke,et al.  Programmed cell death in cereal aleurone , 2000, Plant Molecular Biology.

[133]  M. Yano,et al.  A Novel Cytochrome P450 Is Implicated in Brassinosteroid Biosynthesis via the Characterization of a Rice Dwarf Mutant, dwarf11, with Reduced Seed Length , 2005, The Plant Cell Online.

[134]  Judith L. Flippen-Anderson,et al.  Plant Growth-Promoting Brassinosteroids , 1988 .

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

[136]  Yi Lin,et al.  IAA stimulates pollen tube growth and mediates the modification of its wall composition and structure in Torenia fournieri , 2008, Journal of experimental botany.

[137]  G. An,et al.  T-DNA tagged knockout mutation of rice OsGSK1, an orthologue of Arabidopsis BIN2, with enhanced tolerance to various abiotic stresses , 2007, Plant Molecular Biology.

[138]  Signaling in plants. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[139]  S. Kepinski.  The anatomy of auxin perception. , 2007, BioEssays : news and reviews in molecular, cellular and developmental biology.

[140]  G. Howe,et al.  Tomato allene oxide synthase and fatty acid hydroperoxide lyase, two cytochrome P450s involved in oxylipin metabolism, are targeted to different membranes of chloroplast envelope. , 2001, Plant physiology.

[141]  J. Kyozuka,et al.  Direct control of shoot meristem activity by a cytokinin-activating enzyme , 2007, Nature.

[142]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[143]  J. Chory,et al.  Brassinosteroid Signaling: A Paradigm for Steroid Hormone Signaling from the Cell Surface , 2006, Science.

[144]  P. McCourt,et al.  Plant hormone receptors: perception is everything. , 2006, Genes & development.

[145]  S. Tabata,et al.  Distinct and overlapping roles of two gibberellin 3-oxidases in Arabidopsis development. , 2006, The Plant journal : for cell and molecular biology.