PIN Auxin Efflux Carriers Are Necessary for Pulse-Induced But Not Continuous Light-Induced Phototropism in Arabidopsis1[W][OA]

Auxin efflux carrier PIN-FORMED (PIN) proteins are thought to have central roles in regulating asymmetrical auxin translocation during tropic responses, including gravitropism and phototropism, in plants. Although PIN3 is known to be involved in phototropism in Arabidopsis (Arabidopsis thaliana), no severe defects of phototropism in any of the pin mutants have been reported. We show here that the pulse-induced, first positive phototropism is impaired partially in pin1, pin3, and pin7 single mutants, and severely in triple mutants. In contrast, such impairment was not observed in continuous-light-induced second positive phototropism. Analysis with an auxin-reporter gene demonstrated that PIN3-mediated auxin gradients participate in pulse-induced phototropism but not in continuous-light-induced phototropism. Similar functional separation was also applicable to PINOID, a regulator of PIN localization. Our results strongly suggest the existence of functionally distinct mechanisms i.e. a PIN-dependent mechanism in which transient stimulation is sufficient to induce phototropism, and a PIN-independent mechanism that requires continuous stimulation and does not operate in the former phototropism process. Although a previous study has proposed that blue-light photoreceptors, the phototropins, control PIN localization through the transcriptional down-regulation of PINOID, we could not detect this blue-light-dependent down-regulation event, suggesting that other as yet unknown mechanisms are involved in phototropin-mediated phototropic responses.

[1]  Ioan Vlad Uilecan,et al.  HYPOTrace: Image Analysis Software for Measuring Hypocotyl Growth and Shape Demonstrated on Arabidopsis Seedlings Undergoing Photomorphogenesis1[OA] , 2009, Plant Physiology.

[2]  T. Koshiba,et al.  Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. , 2007, The Plant journal : for cell and molecular biology.

[3]  J. Christie,et al.  Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. , 2002, The Plant journal : for cell and molecular biology.

[4]  J. Adamec,et al.  phot1 Inhibition of ABCB19 Primes Lateral Auxin Fluxes in the Shoot Apex Required For Phototropism , 2011, PLoS biology.

[5]  R. Hangarter,et al.  Phototropism: Bending towards Enlightenment , 2006, The Plant Cell Online.

[6]  I. Han,et al.  Phytochrome A Regulates the Intracellular Distribution of Phototropin 1–Green Fluorescent Protein in Arabidopsis thaliana[W] , 2008, The Plant Cell Online.

[7]  A. Murphy,et al.  Auxin transporters--why so many? , 2010, Cold Spring Harbor perspectives in biology.

[8]  M. Iino.  Desensitization by red and blue light of phototropism in maize coleoptiles , 1988, Planta.

[9]  Klaus Palme,et al.  The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots , 2005, Nature.

[10]  T. Wada,et al.  RPT2: A Signal Transducer of the Phototropic Response in Arabidopsis , 2000, Plant Cell.

[11]  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.

[12]  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.

[13]  Jing Zhang,et al.  Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter , 2009, Nature.

[14]  M. Iino,et al.  Roles Played by Auxin in Phototropism and Photomorphogenesis , 2005 .

[15]  K. Okada,et al.  Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[16]  M. Iino.  Action of red light on indole-3-acetic-acid status and growth in coleoptiles of etiolated maize seedlings , 1982, Planta.

[17]  J. Ecker,et al.  PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[18]  R. Hangarter,et al.  Phytochrome modulation of blue-light-induced phototropism , 2004 .

[19]  C. Bell,et al.  Requirement of the Auxin Polar Transport System in Early Stages of Arabidopsis Floral Bud Formation. , 1991, The Plant cell.

[20]  J. Christie.  Phototropin blue-light receptors. , 2007, Annual review of plant biology.

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

[22]  M. Iino.  Phototropism : mechanisms and ecological implications , 1990 .

[23]  A. Murphy,et al.  Enhanced gravi- and phototropism in plant mdr mutants mislocalizing the auxin efflux protein PIN1 , 2003, Nature.

[24]  T. Sakai,et al.  The ABC subfamily B auxin transporter AtABCB19 is involved in the inhibitory effects of N-1-naphthyphthalamic acid on the phototropic and gravitropic responses of Arabidopsis hypocotyls. , 2008, Plant & cell physiology.

[25]  A. Murphy,et al.  Multidrug Resistance–like Genes of Arabidopsis Required for Auxin Transport and Auxin-Mediated Development Article, publication date, and citation information can be found at www.aspb.org/cgi/doi/10.1105/tpc.010350. , 2001, The Plant Cell Online.

[26]  M. Takano,et al.  The Rice COLEOPTILE PHOTOTROPISM1 Gene Encoding an Ortholog of Arabidopsis NPH3 Is Required for Phototropism of Coleoptiles and Lateral Translocation of Auxinw⃞ , 2005, The Plant Cell Online.

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

[28]  K. L. Poff,et al.  Influence of hook position on phototropic and gravitropic curvature by etiolated hypocotyls of Arabidopsis thaliana. , 1989, Plant physiology.

[29]  K. Ljung,et al.  A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[30]  J. Kiss,et al.  Restoration of gravitropic sensitivity in starch-deficient mutants of Arabidopsis by hypergravity. , 2001, Journal of experimental botany.

[31]  T. Kinoshita,et al.  Blue-Light- and Phosphorylation-Dependent Binding of a 14-3-3 Protein to Phototropins in Stomatal Guard Cells of Broad Bean1 , 2003, Plant Physiology.

[32]  Jiří Friml,et al.  Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis , 2011, Nature Cell Biology.

[33]  Miguel A Blázquez,et al.  Polarization of PIN3-dependent auxin transport for hypocotyl gravitropic response in Arabidopsis thaliana. , 2011, The Plant journal : for cell and molecular biology.

[34]  Hongyu Zhao,et al.  Light Control of Arabidopsis Development Entails Coordinated Regulation of Genome Expression and Cellular Pathways , 2001, The Plant Cell Online.

[35]  M. Iino,et al.  Asymmetric distribution of auxin correlates with gravitropism and phototropism but not with autostraightening (autotropism) in pea epicotyls. , 2006, Journal of experimental botany.

[36]  K. L. Poff,et al.  Both phytochrome A and phytochrome B are required for the normal expression of phototropism in Arabidopsis thaliana seedlings , 1997 .

[37]  G. Fink,et al.  EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. , 1998, Genes & development.

[38]  K. L. Poff,et al.  Characterization of adaptation in phototropism of Arabidopsis thaliana. , 1991, Plant physiology.

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

[40]  P. Oeller,et al.  Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. , 1997, Science.

[41]  Jan Petrásek,et al.  Auxin transport routes in plant development , 2009, Development.

[42]  G. Choi,et al.  Phytochromes inhibit hypocotyl negative gravitropism by regulating the development of endodermal amyloplasts through phytochrome-interacting factors , 2011, Proceedings of the National Academy of Sciences.

[43]  E. Liscum,et al.  Arabidopsis NPH3: A NPH1 photoreceptor-interacting protein essential for phototropism. , 1999, Science.

[44]  W. Briggs.  Chapter 8 – PHOTOTROPISM IN HIGHER PLANTS1 , 1964 .

[45]  M. Iino.  Mediation of tropisms by lateral translocation of endogenous indole‐3‐acetic acid in maize coleoptiles , 1991 .

[46]  Emmanuel Liscum,et al.  Understanding phototropism: from Darwin to today. , 2009, Journal of experimental botany.

[47]  Emmanuel Liscum,et al.  Phototropism: Mechanisms and Outcomes , 2002 .

[48]  K. Nakayama,et al.  Blue light-induced autophosphorylation of phototropin is a primary step for signaling , 2008, Proceedings of the National Academy of Sciences.