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Photomorphogenesis—from One Photoreceptor to 14: 40 Years of Progress

2012; Elsevier BV; Volume: 5; Issue: 3 Linguagem: Inglês

10.1093/mp/sss059

1674-2052

Winslow R. Briggs, Chentao Lin,

Plant Molecular Biology Research

In September of 1971, a group of plant biologists assembled for two weeks in Eretria on the Greek island of Euboea (Evia) under the sponsorship of NATO and the University of Athens to participate in a NATO school devoted to studies of role of light signaling in plants. Embedded in the conference was a mini-symposium entitled ‘Annual European Symposium on Photomorphogenesis’. The generous funding supported graduate-student and postdoctoral-fellow ­participation in the symposium. The meeting brought together and ­unified for the first time what was already a strong international group of scientists with a common interest in the ways in which light signaling impacts plants. (Three of the original participants—Peter Quail, Eberhard Schäfer, and Winslow Briggs—have contributed manuscripts to this issue of Molecular Plant—a measure of the long-term health of the field.) The meeting was truly seminal: it almost immediately spawned trans-ocean collaborations, exchange of younger (and a few older) scientists, and rapid progress. It was also the very first in a long list of international conferences—­variously in Europe, England, Japan, the USA, and, most recently, China. (For a number of years, they were called ‘Annual European Symposium on Photomorphogenesis’, although they did not remain annual and were no longer exclusively European.) Those of us who attended that first conference now have on our shelves a long list of symposium proceedings and review volumes that document the rapid progress in the field. The somewhat tortuous progression from ­physiology and biochemistry to molecular biology and biophysics and the powerful techniques of molecular genetics are beautifully documented in these volumes. In the intervening years, through the many remarkable changes and developments in the field, a combination of mutual interests, collegiality, and exchanges between labs has maintained a close-knit and immensely productive community of scientists. There is no single parent society but there is nevertheless overriding desire for the community to ­assemble together and exchange the latest findings every couple of years—a desire as strong now as it was then. In 1971, there was just one known photoreceptor: phytochrome. It was generally regarded as responsible for all red/far-red-reversible reactions in higher plants. Now, there are five known phytochromes. In 1971, there were no blue-light receptors known (indeed blue-light physiology was scarcely mentioned—essentially dismissed as boring). Now, there are at least eight known: two phototropins, three cryptochromes, and three photoactivated members of the F-box family. In 1971, a UV-B photoreceptor was unheard of. All of a sudden, we have one to study—UVR8—indeed, we even have a crystal structure (Christie, 2012Christie J.M. et al.Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges.Science. 2012; 335: 1492-1496Crossref PubMed Scopus (346) Google Scholar). Most of the thinking about signal-transduction ­pathways at the Eretria meeting was relatively simplistic—complete with naive expectations of a simple linear sequence of steps from photoactivated photoreceptor to plant response. We now know that there are multiple interactions between ­different photoreceptor pathways, and between photoreceptor and plant-hormone pathways. These produce a picture of complex regulatory networks that may require multiple transcription factors and targeted proteolysis. There is also ample evidence for photoreceptor redundancy in some cases and remarkable specificity in others. Simplistic thinking clearly did not work. January of 2008 marked the first appearance of a new international journal, Molecular Plant. The editors had decided that the best way to launch a new journal was to plan a series of deliberately themed issues. Plant photomorphogenesis was honored by being represented in Volume 1, issue 1 (http://mplant.oxfordjournals.org/content/1/1.toc). It was a themed issue that focused on plant photoreceptors and the complex signal-transduction pathways with which they interacted. There were some papers that delved into whole-plant physiology (Inoue et al., p. 15), circadian rhythms (Andronis et al., p. 58), photoreceptor properties (Hoang et al., p. 68; Sullivan et al., p. 178; Kneissl et al., p. 84), QTL analysis (Meng et al., p. 145), photoreceptor–hormone interactions (Staneloni et al., p. 75; Stone et al., p. 129; Cheng et al., p. 42), cell biology (Wan et al., 2008, p. 103), and numerous aspects of light-activated signal transduction (Lin et al., 2008, p. 42; Yang et al., p. 167) or UV-B action (Cloix and Jenkins, p. 118). We also learned of a photoreceptor working independently of light (Rosenfeldt et al., p. 4; Yang et al., p. 167), some pioneering proteomics (Gong et al., p. 27), and news of a prokaryote phytochrome (Kilian et al., p. 155). As the field has continued to move rapidly forward over the last 4 years, there has accumulated a fascinating body of new information in all of these areas. Thus, the editors decided that a second issue themed to plant photoreceptors and photomorphogenesis was timely. As another of the many focused symposia was to take place in the summer of 2011 in Beijing, that occasion was a perfect time to alert the community to the plan. Subsequently, e-mail invitations to contribute to this new issue went out to distant corners of the Earth. The response was gratifying—a real measure of the strength of the field. It was also a measure of the international makeup of the community. Once again, the authors provide remarkably broad coverage of the field. Papers explore very different aspects of circadian rhythms (Edwards et al., 2012Edwards C.E. Ewers B.E. McClung C.R. Lou P. Weinig C. Quantitative variation in water-use efficiency across water regimes and its relationship with circadian, vegetative, reproductive, and leaf gas-exchange traits.Mol. Plant. 2012; 5: 653-668Abstract Full Text Full Text PDF PubMed Scopus (62) Google Scholar; Herrero and Davis, 2012Herrero E. Davis S.J. Time for a nuclear meeting: protein trafficking and chromatin dynamics intersect in the plant circadian system.Mol. Plant. 2012; 5: 554-565Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar; Troncoso-Ponce and Mas, 2012Troncoso-Ponce M.A. Mas P. Newly described components and regulatory mechanisms of circadian clock function in Arabidopsis thaliana.Mol. Plant. 2012; 5: 545-553Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar; Sellaro et al., 2012Sellaro R. Pacín M. Casal J.J. Diurnal dependence of growth responses to shade in Arabidopsis: role of hormone, clock, and light signaling.Mol. Plant. 2012; 5: 619-628Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar); the crucial role of cytoplasmic–nuclear protein movement (Galstyan et al., 2012Galstyan A. Bou-Torrent J. Roig-Villanova I. Martínez-García J.F. A dual mechanism controls nuclear localization in the atypical basic-helix-loop-helix protein PAR1 of Arabidopsis thaliana..Mol. Plant. 2012; 5: 669-677Abstract Full Text Full Text PDF PubMed Scopus (13) Google Scholar; Herrero and Davis, 2012Herrero E. Davis S.J. Time for a nuclear meeting: protein trafficking and chromatin dynamics intersect in the plant circadian system.Mol. Plant. 2012; 5: 554-565Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar; Tsuboi et al., 2012Tsuboi H. Nakamura S. Schäfer E. Wada M. Red light-induced phytochrome relocation into the nucleus in Adiantum capillus-veneris..Mol. Plant. 2012; 5: 611-618Abstract Full Text Full Text PDF PubMed Scopus (22) Google Scholar); stomatal regulation (Chen et al., 2012Chen C. Xiao Y.G. Li X. Ni M. Light-regulated stomatal aperture in Arabidopsis..Mol. Plant. 2012; 5: 566-572Abstract Full Text Full Text PDF PubMed Scopus (71) Google Scholar; Eisinger et al., 2012Eisinger W.R. Ehrhardt D. Briggs W.R. Microtubules are essential for guard-cell function in Vicia and Arabidopsis..Mol. Plant. 2012; 5: 601-610Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar, Eisinger et al., 2012Eisinger W.R. Kirik V. Lewis C. Ehrhardt D. Briggs W.R. Quantitative changes in microtubule distribution correlate with guard cell function in Arabidopsis..Mol. Plant. 2012; 5: 716-725Abstract Full Text Full Text PDF PubMed Scopus (31) Google Scholar (two articles)); light and hormones (Fan, 2012Fan X.Y. et al.BZS1, a B-box protein, promotes photomorphogenesis downstream of both brassinosteroid and light signaling pathways.Mol. Plant. 2012; 5: 591-600Abstract Full Text Full Text PDF PubMed Scopus (108) Google Scholar; Shen et al., 2012); signal transduction (Hao et al., 2012Hao Y.Q. Oh E. Choi G. Liang Z.S. Wang Z.Y. Interactions between HLH and bHLH factors modulate light-regulated plant development.Mol. Plant. 2012; 5: 688-697Abstract Full Text Full Text PDF PubMed Scopus (123) Google Scholar; Kim et al., 2012Kim Y. Yeom M. Kim H. Lim J. Koo H.J. Hwang D. Somers D. Nam H.G. GIGANTEA and EARLY FLOWERING 4 in Arabidopsis exhibit differential phase-specific genetic influences over a diurnal cycle.Mol. Plant. 2012; 5: 678-687Abstract Full Text Full Text PDF PubMed Scopus (44) Google Scholar; Leivar et al., 2012Leivar P. Monte E. Cohn M.M. Quail P.H. Phytochrome signaling in green Arabidopsis seedlings: impact assessment of a mutually-negative phyB–PIF feedback loop.Mol. Plant. 2012; 5: 734-749Abstract Full Text Full Text PDF PubMed Scopus (74) Google Scholar); photoreceptor biochemistry (Zuo et al., 2012Zuo Z.C. Meng Y.Y. Yu X.H. Zhang Z.L. Feng D.S. Sun S.F. Liu B. Lin C.T. A study of the blue light-dependent phosphorylation, degradation and photobody formation of Arabidopsis CRY2.Mol. Plant. 2012; 5: 726-733Abstract Full Text Full Text PDF PubMed Scopus (46) Google Scholar); UV-B in defense against insects (Demkura and Ballaré, 2012Demkura P.V. Ballaré C.L. UVR8 mediates UV-B-induced Arabidopsis defense responses against Botrytis cinerea by controlling sinapate biosynthesis.Mol. Plant. 2012; 5: 642-652Abstract Full Text Full Text PDF PubMed Scopus (158) Google Scholar); photoreceptor structure and function (Song et al., 2012Song C. Essen L.O. Gärtner W. Hughes J. Matysik J. Solid-state NMR spectroscopic study of chromophore–protein interactions in the Pr ground state of plant phytochrome A.Mol. Plant. 2012; 5: 698-715Abstract Full Text Full Text PDF PubMed Scopus (26) Google Scholar; Viczián et al., 2012Viczián A. Ádám E. Wolf I. Bindics J. Kircher S. Heijde M. Ulm R. Schäfer E. Nagy F. A short amino-terminal part of Arabidopsis phytochrome A induces constitutive photomorphogenic response.Mol. Plant. 2012; 5: 629-641Abstract Full Text Full Text PDF PubMed Scopus (21) Google Scholar); the vital role of targeted proteolysis in signal transduction (Ito et al., 2012Ito S. Song Y.H. Imaizumi T. LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis..Mol. Plant. 2012; 5: 533-544Abstract Full Text Full Text PDF PubMed Scopus (131) Google Scholar; Shen et al., 2012Shen H. Zhu L. Bu Q.Y. Huq E. MAX2 affects multiple hormones to promote photomorphogenesis.Mol. Plant. 2012; 5: 750-762Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar); and chromatin remodeling (Van Zanten et al., 2012Van Zanten M. Tessadori F. Peeters A.J.M. Fransz P. Shedding light on large-scale chromatin re-organization in Arabidopsis thaliana..Mol. Plant. 2012; 5: 583-590Abstract Full Text Full Text PDF PubMed Scopus (38) Google Scholar). Among the several reviews is one on the burgeoning completely new field of optigenetics (Christie et al., 2012Christie J.M. Gawthorne J. Young G. Fraser N.J. Roe A.J. LOV to BLUF: flavoprotein contributions to the optogenetic toolkit.Mol. Plant. 2012; 5: 533-544Abstract Full Text Full Text PDF PubMed Scopus (105) Google Scholar). Taken together, these articles present a truly holistic view of plant responses to light: from protein structure through molecular genetics, biochemistry, cell biology, to whole-plant physiology. Authors are from Japan, Germany, Argentina, Hungary, Korea, China, Scotland, and the USA. The strength of the field remains worldwide and the future of the field is safely in gifted hands.