Auxin response factors ARF6 and ARF8 promote jasmonic acid production and flower maturation

Pollination in flowering plants requires that anthers release pollen when the gynoecium is competent to support fertilization. We show that in Arabidopsis thaliana, two paralogous auxin response transcription factors, ARF6 and ARF8, regulate both stamen and gynoecium maturation. arf6 arf8 double-null mutant flowers arrested as infertile closed buds with short petals, short stamen filaments, undehisced anthers that did not release pollen and immature gynoecia. Numerous developmentally regulated genes failed to be induced. ARF6 and ARF8 thus coordinate the transition from immature to mature fertile flowers. Jasmonic acid (JA) measurements and JA feeding experiments showed that decreased jasmonate production caused the block in pollen release, but not the gynoecium arrest. The double mutant had altered auxin responsive gene expression. However, whole flower auxin levels did not change during flower maturation, suggesting that auxin might regulate flower maturation only under specific environmental conditions, or in localized organs or tissues of flowers. arf6 and arf8 single mutants and sesquimutants (homozygous for one mutation and heterozygous for the other) had delayed stamen development and decreased fecundity, indicating that ARF6 and ARF8 gene dosage affects timing of flower maturation quantitatively.

[1]  P. Waterhouse,et al.  Total silencing by intronspliced hairpin RNAs , 2000 .

[2]  Edwards Allen,et al.  P1/HC-Pro, a viral suppressor of RNA silencing, interferes with Arabidopsis development and miRNA unction. , 2003, Developmental cell.

[3]  J. Mullet,et al.  Characterization of an Arabidopsis Lipoxygenase Gene Responsive to Methyl Jasmonate and Wounding , 1993, Plant physiology.

[4]  J. Callis,et al.  Auxin modulates the degradation rate of Aux/IAA proteins , 2001, Proceedings of the National Academy of Sciences of the United States of America.

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

[6]  J. Nemhauser,et al.  ETTIN patterns the Arabidopsis floral meristem and reproductive organs. , 1997, Development.

[7]  J. Cohen,et al.  A Rapid and Simple Procedure for Purification of Indole-3-Acetic Acid Prior to GC-SIM-MS Analysis. , 1988, Plant physiology.

[8]  P. M. Sanders,et al.  Anther developmental defects in Arabidopsis thaliana male-sterile mutants , 1999, Sexual Plant Reproduction.

[9]  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.

[10]  J. Reed,et al.  Arabidopsis SHY2/IAA3 Inhibits Auxin-Regulated Gene Expression Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010283. , 2002, The Plant Cell Online.

[11]  P. Arruda,et al.  An Arabidopsis gene induced by wounding functionally homologous to flavoprotein oxidoreductases , 2000, Plant Molecular Biology.

[12]  G. Hagen,et al.  Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4 , 2004, Development.

[13]  E. Liscum,et al.  MASSUGU2 Encodes Aux/IAA19, an Auxin-Regulated Protein That Functions Together with the Transcriptional Activator NPH4/ARF7 to Regulate Differential Growth Responses of Hypocotyl and Formation of Lateral Roots in Arabidopsis thaliana , 2004, The Plant Cell Online.

[14]  Elliot M. Meyerowitz,et al.  Genome-Wide Analysis of Spatial Gene Expression in Arabidopsis Flowers , 2004, The Plant Cell Online.

[15]  C. Hardtke,et al.  The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development , 1998, The EMBO journal.

[16]  J. D. Karron,et al.  Outcrossing rates of individual Mimulus ringens genets are correlated with anther–stigma separation , 1997, Heredity.

[17]  Yi Li,et al.  Auxin-induced expression of the soybean GH3 promoter in transgenic tobacco plants , 1991, Plant Molecular Biology.

[18]  G. Hagen,et al.  Auxin-responsive gene expression: genes, promoters and regulatory factors , 2002, Plant Molecular Biology.

[19]  G. Hagen,et al.  Dimerization and DNA binding of auxin response factors. , 1999, The Plant journal : for cell and molecular biology.

[20]  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.

[21]  J. Reed,et al.  Regulation of Arabidopsis SHY2/IAA3 protein turnover. , 2003, The Plant journal : for cell and molecular biology.

[22]  G. Hagen,et al.  Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. , 1997, The Plant cell.

[23]  G. Hagen,et al.  The Roles of Auxin Response Factor Domains in Auxin-Responsive Transcription Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.008417. , 2003, The Plant Cell Online.

[24]  AXR2 encodes a member of the Aux/IAA protein family. , 2000, Plant physiology.

[25]  C. Llave,et al.  P 1 / HC-Pro , a Viral Suppressor of RNA Silencing , Interferes with Arabidopsis Development and miRNA , 2003 .

[26]  M. Watahiki,et al.  The massugu1 Mutation of Arabidopsis Identified with Failure of Auxin-Induced Growth Curvature of Hypocotyl Confers Auxin Insensitivity to Hypocotyl and Leaf , 1997, Plant physiology.

[27]  G. Murphy Plant hormone receptors: Comparison of napthaleneacetic acid binding by maize extracts and by a non-plant protein , 1979 .

[28]  G. Jürgens,et al.  The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. , 1996, Development.

[29]  I. Tiryaki,et al.  An Arabidopsis Mutant Defective in Jasmonate Response Is Allelic to the Auxin-Signaling Mutant axr1 1 , 2002, Plant Physiology.

[30]  J. Reed,et al.  Arabidopsis SHY 2 / IAA 3 Inhibits Auxin-Regulated Gene Expression , 2002 .

[31]  G. Hagen,et al.  AUX/IAA Proteins Are Active Repressors, and Their Stability and Activity Are Modulated by Auxin Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010289. , 2001, The Plant Cell Online.

[32]  Neil A. Smith,et al.  Gene expression: Total silencing by intron-spliced hairpin RNAs , 2000, Nature.

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

[34]  T. J. Cooke,et al.  The Effects of Exogenous Auxins on Endogenous Indole-3-Acetic Acid Metabolism (The Implications for Carrot Somatic Embryogenesis) , 1996, Plant physiology.

[35]  J. Kim,et al.  Protein-protein interactions among the Aux/IAA proteins. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[36]  E. Farmer,et al.  Dinor-oxo-phytodienoic acid: a new hexadecanoid signal in the jasmonate family. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Christopher D Town,et al.  Development and evaluation of an Arabidopsis whole genome Affymetrix probe array. , 2004, The Plant journal : for cell and molecular biology.

[38]  J. Reed,et al.  Roles and activities of Aux/IAA proteins in Arabidopsis. , 2001, Trends in plant science.

[39]  T. Vision,et al.  Contrasting Modes of Diversification in the Aux/IAA and ARF Gene Families1[w] , 2004, Plant Physiology.

[40]  J. Bowman,et al.  Early flower development in Arabidopsis. , 1990, The Plant cell.

[41]  M. Schmid,et al.  Genome-Wide Insertional Mutagenesis of Arabidopsis thaliana , 2003, Science.

[42]  E. Liscum,et al.  Mutations of Arabidopsis in Potential Transduction and Response Components of the Phototropic Signaling Pathway , 1996, Plant physiology.

[43]  Adam M. Gustafson,et al.  microRNA-Directed Phasing during Trans-Acting siRNA Biogenesis in Plants , 2005, Cell.

[44]  Joseph R Ecker,et al.  NPH4/ARF7 and ARF19 promote leaf expansion and auxin-induced lateral root formation. , 2005, The Plant journal : for cell and molecular biology.

[45]  E. Liscum,et al.  Genetics of Aux/IAA and ARF action in plant growth and development , 2002, Plant Molecular Biology.

[46]  Stefan R. Henz,et al.  A gene expression map of Arabidopsis thaliana development , 2005, Nature Genetics.

[47]  Ottoline Leyser,et al.  Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins , 2001, Nature.

[48]  T. Koshiba,et al.  Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. , 2004, The Plant journal : for cell and molecular biology.

[49]  Anders Nordström,et al.  Auxin regulation of cytokinin biosynthesis in Arabidopsis thaliana: a factor of potential importance for auxin-cytokinin-regulated development. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[50]  G. Hagen,et al.  Activation and repression of transcription by auxin-response factors. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[51]  A. F. Motten,et al.  Heritability of stigma position and the effect of stigma-anther separation on outcrossing in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). , 2000, American journal of botany.

[52]  G. Jürgens,et al.  The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo , 1993 .

[53]  M. Rausher,et al.  THE ROLE OF INBREEDING DEPRESSION IN MAINTAINING THE MIXED MATING SYSTEM OF THE COMMON MORNING GLORY, IPOMOEA PURPUREA , 1999, Evolution; international journal of organic evolution.

[54]  R. E. Koning THE ROLES OF AUXIN, ETHYLENE, AND ACID GROWTH IN FILAMENT ELONGATION IN GAILLARDIA GRANDIFLORA (ASTERACEAE) , 1983 .

[55]  Dirk Inzé,et al.  GATEWAY vectors for Agrobacterium-mediated plant transformation. , 2002, Trends in plant science.

[56]  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.

[57]  E. Liscum,et al.  NPH4, a conditional modulator of auxin-dependent differential growth responses in Arabidopsis. , 1998, Plant physiology.

[58]  T. Vernoux,et al.  Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. , 2002, Development.

[59]  J. Ellis,et al.  In planta Agrobacterium mediated gene transfer by infiltration of adult Arabidopsis thaliana plants , 1993 .

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

[61]  E. Weiler,et al.  Structure and regulation of the Arabidopsis thaliana allene oxide synthase gene , 1999, Planta.

[62]  G. Jürgens,et al.  Local, Efflux-Dependent Auxin Gradients as a Common Module for Plant Organ Formation , 2003, Cell.

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