Understanding phototropism: from Darwin to today.

Few individuals have had the lasting impact on such a breadth of science as Charles Darwin. While his writings about time aboard the HMS Beagle, his study of the Galapagos islands (geology, fauna, and flora), and his theories on evolution are well known, less appreciated are his studies on plant growth responses to a variety of environmental stimuli. In fact, Darwin, together with the help of his botanist son Francis, left us an entire book, 'The power of movements in plants', describing his many, varied, and insightful observations on this topic. Darwin's findings have provided an impetus for an entire field of study, the study of plant tropic responses, or differential growth (curvature) of plant organs in response to directional stimuli. One tropic response that has received a great deal of attention is the phototropic response, or curvature response to directional light. This review summarizes many of the most significant advancements that have been made in our understanding of this response and place these recent findings in the context of Darwin's initial observations.

[1]  Yunde Zhao,et al.  NPY1, a BTB-NPH3-like protein, plays a critical role in auxin-regulated organogenesis in Arabidopsis , 2007, Proceedings of the National Academy of Sciences.

[2]  W. Rüdiger,et al.  Dimerization of the plant photoreceptor phototropin is probably mediated by the LOV1 domain , 2004, FEBS letters.

[3]  K. Moffat,et al.  Primary reactions of the LOV2 domain of phototropin, a plant blue-light photoreceptor. , 2003, Biochemistry.

[4]  R. Offringa,et al.  Plant evolution: AGC kinases tell the auxin tale. , 2007, Trends in plant science.

[5]  Masahiko Furutani,et al.  The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level , 2007, Development.

[6]  Ullas V. Pedmale,et al.  Regulation of Phototropic Signaling in Arabidopsis via Phosphorylation State Changes in the Phototropin 1-interacting Protein NPH3* , 2007, Journal of Biological Chemistry.

[7]  Ken-ichiro Shimazaki,et al.  phot1 and phot2 mediate blue light regulation of stomatal opening , 2001, Nature.

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

[9]  P. Quail,et al.  Multiple Phytochromes Are Involved in Red-Light-Induced Enhancement of First-Positive Phototropism in Arabidopsis thaliana , 1997, Plant physiology.

[10]  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.

[11]  Ottoline Leyser,et al.  Dynamic Integration of Auxin Transport and Signalling , 2006, Current Biology.

[12]  F. W. Went Wuchsstoff und Wachstum , 1927 .

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

[14]  E. Koonin,et al.  Gleaning non-trivial structural, functional and evolutionary information about proteins by iterative database searches. , 1999, Journal of molecular biology.

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

[16]  Yoshikatsu Sato,et al.  Chloroplast movement. , 2003, Annual review of plant biology.

[17]  John B. Shoven,et al.  I , Edinburgh Medical and Surgical Journal.

[18]  Kevin H. Gardner,et al.  Structural Basis of a Phototropin Light Switch , 2003, Science.

[19]  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.

[20]  S. Yoshida,et al.  Function analysis of phototropin2 using fern mutants deficient in blue light-induced chloroplast avoidance movement. , 2004, Plant & cell physiology.

[21]  W. Krek BTB proteins as henchmen of Cul3-based ubiquitin ligases , 2003, Nature Cell Biology.

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

[23]  Winslow R. Briggs,et al.  The Photocycle of a Flavin-binding Domain of the Blue Light Photoreceptor Phototropin* , 2001, The Journal of Biological Chemistry.

[24]  E. Liscum,et al.  Light-Sensing in Roots , 2007, Plant signaling & behavior.

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

[26]  K. Moffat,et al.  Structure of a flavin-binding plant photoreceptor domain: Insights into light-mediated signal transduction , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[27]  Michal Sharon,et al.  Mechanism of auxin perception by the TIR1 ubiquitin ligase , 2007, Nature.

[28]  M. Estelle,et al.  The IAA1 protein is encoded by AXR5 and is a substrate of SCF(TIR1). , 2004, The Plant journal : for cell and molecular biology.

[29]  J C Watson,et al.  The Phototropin Family of Photoreceptors , 2001, Plant Cell.

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

[31]  Keith Moffat,et al.  Photoexcited Structure of a Plant Photoreceptor Domain Reveals a Light-Driven Molecular Switch Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010475. , 2002, The Plant Cell Online.

[32]  R. Bogomolni,et al.  Intramolecular Proton Transfers and Structural Changes during the Photocycle of the LOV2 Domain of Phototropin 1* , 2003, The Journal of Biological Chemistry.

[33]  J. Chory,et al.  PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. , 1999, Science.

[34]  Yunde Zhao,et al.  NPY genes and AGC kinases define two key steps in auxin-mediated organogenesis in Arabidopsis , 2008, Proceedings of the National Academy of Sciences.

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

[36]  A. Murphy,et al.  Relocalization of the PIN1 Auxin Efflux Facilitator Plays a Role in Phototropic Responses1[w] , 2004, Plant Physiology.

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

[38]  J. Christie,et al.  LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[39]  S. Yoshihara,et al.  Oligomeric structure of LOV domains in Arabidopsis phototropin , 2009, FEBS letters.

[40]  J. Christie,et al.  Physiological Roles of the Light, Oxygen, or Voltage Domains of Phototropin 1 and Phototropin 2 in Arabidopsis1[OA] , 2006, Plant Physiology.

[41]  P. Hegemann,et al.  Phot-LOV1: photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii. , 2003, Biophysical journal.

[42]  Robert D. Finn,et al.  The Pfam protein families database , 2004, Nucleic Acids Res..

[43]  N. Mochizuki,et al.  Blue light-induced association of phototropin 2 with the Golgi apparatus. , 2006, The Plant journal : for cell and molecular biology.

[44]  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.

[45]  Rossana Henriques,et al.  Growth signalling pathways in Arabidopsis and the AGC protein kinases. , 2003, Trends in plant science.

[46]  K. Sakamoto,et al.  Cellular and Subcellular Localization of Phototropin 1 Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.003293. , 2002, The Plant Cell Online.

[47]  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.

[48]  M. Jones,et al.  In vivo phosphorylation site mapping and functional characterization of Arabidopsis phototropin 1. , 2008, Molecular plant.

[49]  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.

[50]  S. Heuvel Protein Degradation: CUL-3 and BTB – Partners in Proteolysis , 2004, Current Biology.

[51]  E. Liscum,et al.  The enhancement of phototropin-induced phototropic curvature in Arabidopsis occurs via a photoreversible phytochrome A-dependent modulation of auxin responsiveness. , 2001, Plant physiology.

[52]  T. Kinoshita,et al.  Biochemical evidence for the requirement of 14-3-3 protein binding in activation of the guard-cell plasma membrane H+-ATPase by blue light. , 2002, Plant & cell physiology.

[53]  J. Christie,et al.  Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. , 2000, Biochemistry.

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

[55]  H. Kandori,et al.  Primary Processes During the Light‐signal Transduction of Phototropin , 2007, Photochemistry and photobiology.

[56]  P Reymond,et al.  Arabidopsis NPH1: a flavoprotein with the properties of a photoreceptor for phototropism. , 1998, Science.

[57]  P. Defossez,et al.  Born to bind: the BTB protein–protein interaction domain , 2006, BioEssays : news and reviews in molecular, cellular and developmental biology.

[58]  K. Gardner,et al.  Disruption of the LOV-Jalpha helix interaction activates phototropin kinase activity. , 2004, Biochemistry.

[59]  M. Nakasako,et al.  Light-induced structural changes of LOV domain-containing polypeptides from Arabidopsis phototropin 1 and 2 studied by small-angle X-ray scattering. , 2004, Biochemistry.

[60]  S. A. Gordon,et al.  Hormonal Relations in the Phototropic Response: III. The Movement of C-labeled and Endogenous Indoleacetic Acid in Phototropically Stimulated Zea Coleoptiles. , 1966, Plant physiology.

[61]  B. Pickard,et al.  Transport and Distribution of Auxin during Tropistic Response. II. The Lateral Migration of Auxin in Phototropism of Coleoptiles. , 1964, Plant physiology.

[62]  N. Cholodny Beiträge zur hormonalen Theorie von Tropismen , 1928, Planta.

[63]  E. Liscum,et al.  Phototropism: A “Simple” Physiological Response Modulated by Multiple Interacting Photosensory-response Pathways¶ , 2000, Photochemistry and photobiology.

[64]  Ulrich Kubitscheck,et al.  The subcellular localization and blue-light-induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. , 2008, Molecular plant.

[65]  H. Fukuzawa,et al.  Photochemical Properties of the Flavin Mononucleotide-Binding Domains of the Phototropins from Arabidopsis, Rice, andChlamydomonas reinhardtii 1 , 2002, Plant Physiology.

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

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

[68]  A. Lupas,et al.  The structure of alpha-helical coiled coils. , 2005, Advances in protein chemistry.

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

[70]  P. Quail,et al.  Phytochrome A Regulates Red-Light Induction of Phototropic Enhancement in Arabidopsis , 1996, Plant physiology.

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

[72]  Jin-Young Park,et al.  Mutation in domain II of IAA1 confers diverse auxin-related phenotypes and represses auxin-activated expression of Aux/IAA genes in steroid regulator-inducible system. , 2002, The Plant journal : for cell and molecular biology.

[73]  K. Bennett,et al.  The power of movement in plants. , 1998, Trends in ecology & evolution.

[74]  W. Briggs Mediation of Phototropic Responses of Corn Coleoptiles by Lateral Transport of Auxin. , 1963, Plant physiology.

[75]  J. Wilson,et al.  Phototropic auxin redistribution in corn coleoptiles. , 1957, Science.

[76]  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.

[77]  Matthias Peter,et al.  Cullin‐based ubiquitin ligases: Cul3–BTB complexes join the family , 2004, The EMBO journal.

[78]  Keith Moffat,et al.  The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. , 2003, Biochemistry.

[79]  K. Okada,et al.  RPT2 Is a Signal Transducer Involved in Phototropic Response and Stomatal Opening by Association with Phototropin 1 in Arabidopsis thaliana , 2004, The Plant Cell Online.

[80]  M. Terazima,et al.  Conformational dynamics of phototropin 2 LOV2 domain with the linker upon photoexcitation. , 2005, Journal of the American Chemical Society.

[81]  Mike Tyers,et al.  A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. , 2004, Biochimica et biophysica acta.

[82]  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.

[83]  P. Hegemann,et al.  Crystal structures and molecular mechanism of a light-induced signaling switch: The Phot-LOV1 domain from Chlamydomonas reinhardtii. , 2003, Biophysical journal.

[84]  D. Matsuoka,et al.  Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

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

[86]  K. Ljung,et al.  Disruptions in Aux1-dependent Auxin Influx Alter Hypocotyl Phototropism in Arabidopsis , 2022 .

[87]  M. Lourdes,et al.  Phytohormones , 1938, Nature.

[88]  R. Bogomolni,et al.  Vibration spectroscopy reveals light-induced chromophore and protein structural changes in the LOV2 domain of the plant blue-light receptor phototropin 1. , 2002, Biochemistry.

[89]  M. Wilkins,et al.  IAA transport during the phototropic responses of intact Zea and Avena coleoptiles , 2004, Planta.

[90]  D. Nozaki,et al.  Comparative investigation of the LOV1 and LOV2 domains in Adiantum phytochrome3. , 2005, Biochemistry.

[91]  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.

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

[93]  Andrei N. Lupas,et al.  The structure of α-helical coiled coils , 2005 .

[94]  Ullas V. Pedmale,et al.  Signaling in Phototropism , 2009 .

[95]  K. Moffat,et al.  The LOV2 domain of phototropin: a reversible photochromic switch. , 2004, Journal of the American Chemical Society.

[96]  E. Liscum,et al.  Functional ecology of a blue light photoreceptor: effects of phototropin-1 on root growth enhance drought tolerance in Arabidopsis thaliana. , 2007, The New phytologist.

[97]  P. Stogios,et al.  Sequence and structural analysis of BTB domain proteins , 2005, Genome Biology.

[98]  Phototropins and Associated Signaling: Providing the Power of Movement in Higher Plants ¶ , 2005, Photochemistry and photobiology.

[99]  E. Liscum,et al.  AN EXPERIMENTAL TEST OF THE ADAPTIVE EVOLUTION OF PHOTOTROPINS: BLUE‐LIGHT PHOTORECEPTORS CONTROLLING PHOTOTROPISM IN ARABIDOPSIS THALIANA , 2004, Evolution; international journal of organic evolution.