Differential petiole growth in Arabidopsis thaliana: photocontrol and hormonal regulation.

Environmental challenges such as low light intensity induce differential growth-driven upward leaf movement (hyponastic growth) in Arabidopsis thaliana. However, little is known about the physiological regulation of this response. Here, we studied how low light intensity is perceived and translated into a differential growth response in Arabidopsis. We used mutants defective in light, ethylene and auxin signaling, and in polar auxin transport, as well as chemical inhibitors, to analyze the mechanisms of low light intensity-induced differential growth. Our data indicate that photosynthesis-derived signals and blue light wavelengths affect petiole movements and that rapid induction of hyponasty by low light intensity involves functional cryptochromes 1 and 2, phytochrome-A and phytochrome-B photoreceptor proteins. The response is independent of ethylene signaling. Auxin and polar auxin transport, by contrast, play a role in low light intensity-induced differential petiole growth. We conclude that low light intensity-induced differential petiole growth requires blue light, auxin signaling and polar auxin transport and is, at least in part, genetically separate from well-characterized ethylene-induced differential growth.

[1]  P. Davis,et al.  Isolation and initial characterization of the BRCA2 promoter , 1999, Oncogene.

[2]  R. Pierik,et al.  New perspectives in flooding research: the use of shade avoidance and Arabidopsis thaliana. , 2005, Annals of botany.

[3]  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.

[4]  É. Hideg,et al.  The Genetic Basis of Singlet Oxygen–Induced Stress Responses of Arabidopsis thaliana , 2004, Science.

[5]  J. Friml,et al.  Polar auxin transport – old questions and new concepts? , 2002, Plant Molecular Biology.

[6]  R. Pierik,et al.  Auxin and Ethylene Regulate Elongation Responses to Neighbor Proximity Signals Independent of Gibberellin and DELLA Proteins in Arabidopsis1[C][W][OA] , 2009, Plant Physiology.

[7]  Klaus Palme,et al.  Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis , 2002, Nature.

[8]  P. Falkowski,et al.  Light intensity regulation of cab gene transcription is signaled by the redox state of the plastoquinone pool. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Thomas D. Schmittgen,et al.  Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. , 2001, Methods.

[10]  J. Ecker,et al.  HOOKLESS1, an Ethylene Response Gene, Is Required for Differential Cell Elongation in the Arabidopsis Hypocotyl , 1996, Cell.

[11]  M. L. Anderson,et al.  Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. , 1993, The Plant cell.

[12]  T. Kohchi,et al.  The Arabidopsis HY2 Gene Encodes Phytochromobilin Synthase, a Ferredoxin-Dependent Biliverdin Reductase , 2001, Plant Cell.

[13]  M. Estelle,et al.  Reduced naphthylphthalamic acid binding in the tir3 mutant of Arabidopsis is associated with a reduction in polar auxin transport and diverse morphological defects. , 1997, The Plant cell.

[14]  G. Whitelam,et al.  Gating of the rapid shade-avoidance response by the circadian clock in plants , 2003, Nature.

[15]  Frank F. Millenaar,et al.  Plant Movement. Submergence-Induced Petiole Elongation inRumex palustris Depends on Hyponastic Growth1 , 2003, Plant Physiology.

[16]  L. Voesenek,et al.  1-aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence. , 1999, Plant physiology.

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

[18]  G. Morelli,et al.  Shade avoidance responses. Driving auxin along lateral routes. , 2000, Plant physiology.

[19]  R. Hangarter,et al.  Gravity, light and plant form. , 1997, Plant, cell & environment.

[20]  P. Geigenberger,et al.  Redox regulation of carbon storage and partitioning in response to light and sugars. , 2005, Journal of experimental botany.

[21]  L. Voesenek,et al.  Functional Significance of Shade‐Induced Leaf Senescence in Dense Canopies: An Experimental Test Using Transgenic Tobacco , 2006, The American Naturalist.

[22]  J. Benschop,et al.  The Roles of Ethylene, Auxin, Abscisic Acid, and Gibberellin in the Hyponastic Growth of Submerged Rumex palustris Petioles1 , 2004, Plant Physiology.

[23]  M. Koornneef,et al.  A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana , 1991, Molecular and General Genetics MGG.

[24]  M. Wilkins.  The physiology of plant growth and development , 1969 .

[25]  R. Pierik,et al.  The Regulation of Cell Wall Extensibility during Shade Avoidance: A Study Using Two Contrasting Ecotypes of Stellaria longipes1[C][OA] , 2008, Plant Physiology.

[26]  Filip Vandenbussche,et al.  Ethylene and Auxin Control the Arabidopsis Response to Decreased Light Intensity1 , 2003, Plant Physiology.

[27]  J. Ecker,et al.  Phototropin-related NPL1 controls chloroplast relocation induced by blue light , 2001, Nature.

[28]  J. Chory,et al.  Isolation and Initial Characterization of Arabidopsis Mutants That Are Deficient in Phytochrome A , 1993, Plant physiology.

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

[30]  C. Ballaré,et al.  RESPONSES OF LIGHT‐GROWN WILD‐TYPE and LONG‐HYPOCOTYL MUTANT CUCUMBER SEEDLINGS TO NATURAL and SIMULATED SHADE LIGHT * , 1991 .

[31]  J. Casal,et al.  Hierarchical coupling of phytochromes and cryptochromes reconciles stability and light modulation of Arabidopsis development. , 2001, Development.

[32]  R. Pierik,et al.  Interactions between Ethylene and Gibberellins in Phytochrome-Mediated Shade Avoidance Responses in Tobacco1 , 2004, Plant Physiology.

[33]  Masahiro Kasahara,et al.  Arabidopsis nph1 and npl1: Blue light receptors that mediate both phototropism and chloroplast relocation , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[34]  S. Mayfield,et al.  Light-regulated translation of chloroplast messenger RNAs through redox potential. , 1994, Science.

[35]  J. Ecker,et al.  Genetic analysis of ethylene signal transduction in Arabidopsis thaliana: five novel mutant loci integrated into a stress response pathway. , 1995, Genetics.

[36]  N. Harberd,et al.  High Temperature-Mediated Adaptations in Plant Architecture Require the bHLH Transcription Factor PIF4 , 2009, Current Biology.

[37]  O. Smirnova,et al.  Cryptochrome blue-light photoreceptors of Arabidopsis implicated in phototropism , 1998, Nature.

[38]  E. Meyerowitz,et al.  Arabidopsis ethylene-response gene ETR1: similarity of product to two-component regulators. , 1993, Science.

[39]  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.

[40]  Laurentius A. C. J. Voesenek,et al.  Growth responses of Rumex species in relation to submergence and ethylene , 1989 .

[41]  E. Knee,et al.  Interactions of light and ethylene in hypocotyl hook maintenance in Arabidopsis thaliana seedlings. , 2000, Physiologia plantarum.

[42]  R. Pierik,et al.  The Janus face of ethylene: growth inhibition and stimulation. , 2006, Trends in Plant Science.

[43]  J. Ecker,et al.  Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. , 1990, The Plant cell.

[44]  In-Jung Lee,et al.  Phytochrome B and the Regulation of Circadian Ethylene Production in Sorghum , 1998 .

[45]  K. Apel,et al.  EXECUTER1- and EXECUTER2-dependent transfer of stress-related signals from the plastid to the nucleus of Arabidopsis thaliana , 2007, Proceedings of the National Academy of Sciences.

[46]  J. Harborne.  Encyclopedia of plant physiology, New series , 1978 .

[47]  V. Paakkarinen,et al.  Chloroplast-mediated regulation of nuclear genes in Arabidopsis thaliana in the absence of light stress. , 2006, Physiological genomics.

[48]  S. Ishiguro,et al.  Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. , 2001, Science.

[49]  J. Benschop,et al.  Abscisic Acid Antagonizes Ethylene-Induced Hyponastic Growth in Arabidopsis1[OA] , 2006, Plant Physiology.

[50]  Frank F. Millenaar,et al.  Ethylene-Induced Differential Growth of Petioles in Arabidopsis. Analyzing Natural Variation, Response Kinetics, and Regulation1 , 2005, Plant Physiology.

[51]  R. Firn,et al.  The Establishment of Tropic Curvatures in Plants , 1980 .

[52]  R. Pierik,et al.  Ethylene is required in tobacco to successfully compete with proximate neighbours , 2003 .

[53]  Hsiao-Ching Yen,et al.  An Ethylene-Inducible Component of Signal Transduction Encoded by Never-ripe , 1995, Science.

[54]  D. Straeten,et al.  Ethylene can stimulate Arabidopsis hypocotyl elongation in the light. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[55]  M. Yanovsky,et al.  A quadruple photoreceptor mutant still keeps track of time , 2000, Current Biology.

[56]  Chentao Lin.  Blue Light Receptors and Signal Transduction Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.000646. , 2002, The Plant Cell Online.

[57]  E. Liscum,et al.  Mutations in the NPH1 locus of Arabidopsis disrupt the perception of phototropic stimuli. , 1995, The Plant cell.

[58]  Cynthia Weinig,et al.  Shade avoidance and the regulation of leaf inclination in Arabidopsis. , 2006, Plant, cell & environment.

[59]  M. Feinleib,et al.  Physiology of movements , 1979 .

[60]  Michael Sauer,et al.  Efflux-dependent auxin gradients establish the apical–basal axis of Arabidopsis , 2003, Nature.

[61]  J. Friml,et al.  Auxin transport - shaping the plant. , 2003, Current opinion in plant biology.

[62]  J. Casal,et al.  Conditional synergism between cryptochrome 1 and phytochrome B is shown by the analysis of phyA, phyB, and hy4 simple, double, and triple mutants in Arabidopsis. , 1998, Plant physiology.

[63]  M. Koornneef,et al.  Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) , 1980 .

[64]  M. Estelle,et al.  The F-box protein TIR1 is an auxin receptor , 2005, Nature.

[65]  T. Mockler,et al.  Regulation of flowering time by Arabidopsis photoreceptors. , 1998, Science.

[66]  J. Chory,et al.  Genetic interactions between phytochrome A, phytochrome B, and cryptochrome 1 during Arabidopsis development. , 1998, Plant physiology.

[67]  R. Pierik,et al.  Canopy studies on ethylene-insensitive tobacco identify ethylene as a novel element in blue light and plant-plant signalling. , 2004, The Plant journal : for cell and molecular biology.

[68]  John Okyere,et al.  How to decide? Different methods of calculating gene expression from short oligonucleotide array data will give different results , 2006, BMC Bioinformatics.

[69]  Ottoline Leyser,et al.  The Arabidopsis F-box protein TIR1 is an auxin receptor , 2005, Nature.

[70]  A. Nilsson,et al.  Photosynthetic control of chloroplast gene expression , 1999, Nature.

[71]  A. Cashmore,et al.  HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor , 1993, Nature.

[72]  J R Ecker,et al.  EIN4 and ERS2 Are Members of the Putative Ethylene Receptor Gene Family in Arabidopsis , 1998, Plant Cell.

[73]  J. Görlach,et al.  Growth Stage–Based Phenotypic Analysis of Arabidopsis , 2001, The Plant Cell Online.

[74]  J. Ecker,et al.  Chloroplast to nucleus communication triggered by accumulation of Mg-protoporphyrinIX , 2003, Nature.

[75]  K. Apel,et al.  FLU: A negative regulator of chlorophyll biosynthesis in Arabidopsis thaliana , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[76]  C. Ballaré,et al.  Keeping up with the neighbours: phytochrome sensing and other signalling mechanisms. , 1999, Trends in plant science.

[77]  J. Ecker,et al.  Regulation of differential growth in the apical hook of Arabidopsis. , 1999, Development.