The Phytochromes, a Family of Red/Far-red Absorbing Photoreceptors

Because plants are photo-auxotrophic they are particularly sensitive to their light environment. To fine-tune their development according to light intensity, direction, spectral quality, and periodicity they possess a multiplicity of light sensors (1Kendrick R.E. Kronenberg G. Photomorphogenesis in Plants. Martinus Nijhoff Publishers, Dordrecht, Netherlands1994Crossref Google Scholar). InArabidopsis there are eight identified photoreceptors, but this list is still incomplete. It includes three UV-A/blue light receptors (phototropin, a photoreceptor to sense light direction, and two cryptochromes that mediate many photomorphogenic responses (2Briggs W.R. Huala E. Annu. Rev. Cell Dev. Biol. 1999; 15: 33-62Crossref PubMed Scopus (330) Google Scholar, 3Cashmore A.R. Jarillo J.A. Wu Y.J. Liu D. Science. 1999; 284: 760-765Crossref PubMed Scopus (785) Google Scholar)) and five phytochromes (phy) 1The abbreviations used are:phyphytochrome(s)BLDbilin lyase domainATEN-terminal extensionPRDPAS (PER/ARNT/SIM)-related domainHKRDhistidine kinase-related domainPYPphotoactive yellow proteinbHLHbasic helix-loop-helixnamed phyA–phyE that absorb mainly red/far-red light, with phyA also responding to broad-spectrum light (UV-A to far-red) of very low intensity (4Quail P.H. Boylan M.T. Parks B.M. Short T.W. Xu Y. Wagner D. Science. 1995; 268: 675-680Crossref PubMed Scopus (651) Google Scholar). All these photoreceptors bind to a chromophore, which for the phytochromes is a linear tetrapyrrole (phytochromobilin) (5Lagarias J.C. Rapoport H. J. Am. Chem. Soc. 1980; 102: 4821-4828Crossref Scopus (259) Google Scholar). Because many light effects are induced by the co-action of several photoreceptors and because some photoreceptors regulate multiple aspects of photomorphogenesis, a genetic approach was instrumental for dissecting the specific roles of individual photoreceptors (1Kendrick R.E. Kronenberg G. Photomorphogenesis in Plants. Martinus Nijhoff Publishers, Dordrecht, Netherlands1994Crossref Google Scholar). As a consequence, research has concentrated on a few species that are particularly well suited for molecular genetic studies, in particularArabidopsis (6Bevan M. Bancroft I. Mewes H.W. Martienssen R. McCombie R. Bioessays. 1999; 21: 110-120Crossref PubMed Scopus (28) Google Scholar). phytochrome(s) bilin lyase domain N-terminal extension PAS (PER/ARNT/SIM)-related domain histidine kinase-related domain photoactive yellow protein basic helix-loop-helix Phytochromes were originally defined as the receptors responsible for red, far-red reversible, plant responses (7Parker M.W. Hendricks S.B. Borthwick H.A. Went F.W. Am. J. Bot. 1949; 36: 194-204Crossref Google Scholar, 8Borthwick H.A. Hendricks S.B. Parker M.W. Toole E.H. Toole V.K. Proc. Natl. Acad. Sci. U. S. A. 1952; 38: 662-666Crossref PubMed Google Scholar, 9Borthwick H.A. Hendricks S.B. Parker M.W. Proc. Natl. Acad. Sci. U. S. A. 1952; 38: 929-934Crossref PubMed Google Scholar). Photobiological experiments led to the proposal that phy exists in two spectral forms: the inactive Pr form (red light absorbing) phototransforms into the active Pfr form (far-red light absorbing) upon absorption of red light. This reaction can be reversed when Pfr is converted to Pr upon absorption of far-red light. Purification of phy from plants confirmed the existence of those two spectrally interconvertible forms (10Butler W.L. Norris K.H. Siegelman H.W. Hendricks S.B. Proc. Natl. Acad. Sci. U. S. A. 1959; : 1703-1708Crossref PubMed Google Scholar). phy are classified into two groups; type I (phyA in Arabidopsis) is light-labile and type II (phyB–phyE in Arabidopsis) is light-stable (11Hirschfeld M. Tepperman J.M. Clack T. Quail P.H. Sharrock R.A. Genetics. 1998; 149: 523-535Crossref PubMed Google Scholar). Numerous recent reviews cover phy-mediated photomorphogenesis in detail (12Nagy F. Schaefer E. EMBO J. 2000; 19: 157-163Crossref PubMed Scopus (71) Google Scholar, 13Lin C. Plant Physiol. 2000; 123: 39-50Crossref PubMed Scopus (168) Google Scholar, 14Neff M.M. Fankhauser C. Chory J. Genes Dev. 2000; 14: 257-271Crossref PubMed Google Scholar, 15Deng X.W. Quail P.H. Semin. Cell Dev. Biol. 1999; 10: 121-129Crossref PubMed Scopus (169) Google Scholar, 16Osterlund M.T. Ang L.H. Deng X.W. Trends Cell Biol. 1999; 9: 113-118Abstract Full Text Full Text PDF PubMed Scopus (113) Google Scholar, 17Karniol B. Chamovitz D.A. Curr. Opin. Plant Biol. 2000; 3: 387-393Crossref PubMed Scopus (39) Google Scholar, 18Hughes J. Lamparter T. Plant Physiol. 1999; 121: 1059-1068Crossref PubMed Scopus (77) Google Scholar, 19Cashmore A.R. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 13358-13360Crossref PubMed Scopus (15) Google Scholar). Photobiological and genetic studies have revealed that this small gene family plays important roles in seed germination, seedling de-etiolation, neighbor perception and avoidance, and the transition from vegetative to reproductive growth (induction of flowering). At the molecular and cellular level phy responses include: development of the chloroplast, inhibition or promotion of cell growth (depending on the organ), ion fluxes at the plasma membrane, and gene expression responses (1Kendrick R.E. Kronenberg G. Photomorphogenesis in Plants. Martinus Nijhoff Publishers, Dordrecht, Netherlands1994Crossref Google Scholar). Genetic screens to identify loci implicated in phy responses have yielded four apoprotein mutants (phyA,phyB, phyD, and phyE), two chromophore mutants (hy1 and hy2), and numerous mutants implicated in phy-mediated signaling. The analysis of these mutants highlighted the role of phytochromes in sensing light quality, intensity, and the duration of the light cycle and revealed that type I and type II phy have distinct modes of photoperception (14Neff M.M. Fankhauser C. Chory J. Genes Dev. 2000; 14: 257-271Crossref PubMed Google Scholar, 15Deng X.W. Quail P.H. Semin. Cell Dev. Biol. 1999; 10: 121-129Crossref PubMed Scopus (169) Google Scholar). Light-stable phy are responsible for the classical red/far-red reversible phy responses. In Arabidopsis phyB plays the most prominent role; it is the major red light receptor for seedling de-etiolation, and it affects many light-regulated cell elongation responses, shade avoidance, and the regulation of flowering time by day length (20Reed J.W. Nagpal P. Poole D.S. Furuya M. Chory J. Plant Cell. 1993; 5: 147-157Crossref PubMed Scopus (762) Google Scholar). phyD and phyE mutants have more subtle phenotypes that are only revealed in double or triple mutant combinations (21Whitelam G.C. Devlin P.F. Plant Cell Environ. 1997; 20: 752-758Crossref Scopus (183) Google Scholar, 22Devlin P.F. Patel S.R. Whitelam G.C. Plant Cell. 1998; 10: 1479-1488Crossref PubMed Scopus (265) Google Scholar, 23Devlin P.F. Robson P.R. Patel S.R. Goosey L. Sharrock R.A. Whitelam G.C. Plant Physiol. 1999; 119: 909-915Crossref PubMed Scopus (215) Google Scholar). Because certain phytohormone mutants also display similar phenotypes, a subset of phy responses might be mediated by light-regulated hormonal signaling (14Neff M.M. Fankhauser C. Chory J. Genes Dev. 2000; 14: 257-271Crossref PubMed Google Scholar, 24Morelli G. Ruberti I. Plant Physiol. 2000; 122: 621-626Crossref PubMed Scopus (143) Google Scholar, 25Kamiya Y. Garcia-Martinez J.L. Curr. Opin. Plant Biol. 1999; 2: 398-403Crossref PubMed Scopus (131) Google Scholar, 26Hsieh H.L. Okamoto H. Wang M. Ang L.H. Matsui M. Goodman H. Deng X.W. Genes Dev. 2000; 14: 1958-1970PubMed Google Scholar). phyA, the only type I phy in Arabidopsis, plays a major role in gene expression and germination in response to very low fluences of broad spectrum light as well as in sensing day-length extension (27Johnson E. Bradley M. Harberd N.P. Whitelam G.C. Plant Physiol. 1994; 105: 141-149Crossref PubMed Scopus (42) Google Scholar, 28Shinomura T. Nagatani A. Hanzawa H. Kubota M. Watanabe M. Furuya M. Proc. Natl. Acad. Sci. U. S. A. 1996; 93: 8129-8133Crossref PubMed Scopus (427) Google Scholar, 29Botto J.F. Sanchez R.A. Whitelam G.C. Casal J.J. Plant Physiol. 1996; 110: 439-444Crossref PubMed Scopus (173) Google Scholar, 30Hamazato F. Shinomura T. Hanzawa H. Chory J. Furuya M. Plant Physiol. 1997; 115: 1533-1540Crossref PubMed Scopus (62) Google Scholar). phyA is also essential for de-etiolation in far-red enriched light (31Nagatani A. Reed R.W. Chory J. Plant Physiol. 1993; 102: 269-277Crossref PubMed Scopus (393) Google Scholar, 32Whitelam G.C. Johnson E. Peng J. Carol P. Anderson M.L. Cowl J.S. Harberd N.P. Plant Cell. 1993; 5: 757-768Crossref PubMed Scopus (483) Google Scholar, 33Dehesh K. Franci C. Parks B.M. Seeley K.A. Short T.W. Tepperman J.M. Quail P.H. Plant Cell. 1993; 5: 1081-1088PubMed Google Scholar). Such conditions are found when a young seedling develops under a dense canopy of plants. This is a particularly interesting phy function because, contrary to most phy responses, it is induced by far-red light and inhibited by red light (see above) (34Shinomura T. Uchida K. Furuya M. Plant Physiol. 2000; 122: 147-156Crossref PubMed Scopus (141) Google Scholar). This high irradiance response to far-red light identifies a novel form of active phy, Pr, that has been cycled through Pfr, which will be referred to as Pr*. Pr* has acquired novel properties that are distinct from Pr and Pfr, but the molecular nature of the distinction between Pr* and Pr is unknown (34Shinomura T. Uchida K. Furuya M. Plant Physiol. 2000; 122: 147-156Crossref PubMed Scopus (141) Google Scholar). As illustrated above, type I and type II phy play distinct roles; however, it must be pointed out that depending on the responses their role can be overlapping, coordinated, or even antagonistic (35Reed J.W. Nagatani A. Elich T.D. Fagan M. Chory J. Plant Physiol. 1994; 104: 1139-1149Crossref PubMed Scopus (526) Google Scholar, 36Robson P.R. McCormac A.C. Irvine A.S. Smith H. Nat. Biotechnol. 1996; 14: 995-998Crossref PubMed Scopus (137) Google Scholar, 37Smith H. Xu Y. Quail P.H. Plant Physiol. 1997; 114: 637-641Crossref PubMed Scopus (63) Google Scholar, 38Somers D.E. Devlin P.F. Kay S.A. Science. 1998; 282: 1488-1490Crossref PubMed Scopus (618) Google Scholar, 39Parks B.M. Spalding E.P. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 14142-14146Crossref PubMed Scopus (80) Google Scholar). Phytochromes bind phytochromobilin (PΦB) via a thioether linkage to a cysteine residue in the most conserved domain among phy (Fig.1). The first committed step in chromophore biosynthesis is the cleavage of the tetrapyrrole ring of heme (Fig. 1A). This reaction is catalyzed by a heme oxygenase encoded by the HY1 gene in Arabidopsis(40Davis S.J. Kurepa J. Vierstra R.D. Proc. Natl. Acad. Sci. U. S. A. 1999; 96: 6541-6546Crossref PubMed Scopus (177) Google Scholar, 41Muramoto T. Kohchi T. Yokota A. Hwang I. Goodman H.M. Plant Cell. 1999; 11: 335-348Crossref PubMed Scopus (271) Google Scholar). Hy2 mutants are most probably defective in the PΦB synthase enzyme; this step is followed by an isomerization in the C-3 double bond of PΦB (42Terry M.J. Plant Cell Environ. 1997; 20: 740-745Crossref Scopus (79) Google Scholar). The nature of the PΦB isomerase is still unclear, but phy itself is capable of catalyzing this reaction (42Terry M.J. Plant Cell Environ. 1997; 20: 740-745Crossref Scopus (79) Google Scholar). phy chromophore mutants can be mimicked by overexpression of a mammalian biliverdin reductase (43Lagarias D.M. Crepeau M.W. Maines M.D. Lagarias J.C. Plant Cell. 1997; 9: 675-688PubMed Google Scholar). phy apoprotein binds to the 3E-PΦB in the cytoplasm to yield the Pr form of the photoreceptor. This reaction requires the bilin lyase domain (BLD) of the photoreceptor. Absorption of red light triggers a "Z" to "E" isomerization in the C-15 double bond between the C and D rings of the linear tetrapyrrole, resulting in the far-red light-absorbing form Pfr (44Andel III, F. Lagarias J.C. Mathies R.A. Biochemistry. 1996; 35: 15997-16008Crossref PubMed Scopus (100) Google Scholar) (Fig. 1A). Conformational changes in the protein backbone are required to maintain this high energy state of the photoreceptor (45Song P.S. J. Biochem. Mol. Biol. 1999; 32: 215-225Google Scholar). Pfr can be converted to Pr either by a slow non-photoinduced reaction (dark reversion) or much faster upon absorption of far-red light. It is generally assumed that all phy have the same chromophore. Because of the very low levels of type II phy this has not been verified in vivo. Analysis of reconstituted recombinant phyA, phyB, phyC, and phyE reveals that they have similar but not identical spectral properties (46Remberg A. Ruddat A. Braslavsky S.E. Gartner W. Schaffner K. Biochemistry. 1998; 37: 9983-9990Crossref PubMed Scopus (28) Google Scholar, 47Elich T.D. Chory J. Plant Cell. 1997; 9: 2271-2280Crossref PubMed Scopus (69) Google Scholar, 48Eichenberg K. Baurle I. Paulo N. Sharrock R.A. Rudiger W. Schafer E. FEBS Lett. 2000; 470: 107-112Crossref PubMed Scopus (67) Google Scholar). Phytochromes are soluble homodimers composed of two functional domains: an N-terminal light-sensing domain and a C-terminal signaling domain (Fig. 1). The N-terminal portion is necessary and sufficient for photoperception and possesses the bilin lyase activity allowing attachment of the chromophore to the apoprotein (42Terry M.J. Plant Cell Environ. 1997; 20: 740-745Crossref Scopus (79) Google Scholar). The minimal BLD is actually less than 200 amino acids long (49Wu S.H. Lagarias J.C. Biochemistry. 2000; 39: 13487-13495Crossref PubMed Scopus (158) Google Scholar). The first 70 amino acids of the protein are dispensable for chromophore binding; they constitute the N-terminal extension (ATE). The ATE is poorly conserved, possibly accounting for some functional differences among phy. Structure function analysis has revealed that in phyA, the ATE is composed of two subdomains (50Stockhaus J. Nagatani A. Halfter U. Kay S. Furuya M. Chua N.H. 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This signaling domain is composed of a PAS (Per/Arndt/Sim)-related domain (PRD) and a histidine kinase-related domain (HKRD) (Fig. 1) (53Schneider-Poetsch H.A. Braun B. Marx S. Schaumburg A. FEBS Lett. 1991; 281: 245-249Crossref PubMed Scopus (92) Google Scholar, 54Yeh K.C. Lagarias J.C. Proc. Natl. Acad. Sci. U. S. A. 1998; 95: 13976-13981Crossref PubMed Scopus (351) Google Scholar). PAS domains have diverse functions; they can be used either as protein-protein interaction platforms or as co-factor binding domains (55Taylor B.L. Zhulin I.B. Microbiol. Mol. Biol. Rev. 1999; 63: 479-506Crossref PubMed Google Scholar). Interestingly such modules are used to bind the chromophore in various blue light receptors (2Briggs W.R. Huala E. Annu. Rev. Cell Dev. Biol. 1999; 15: 33-62Crossref PubMed Scopus (330) Google Scholar). In phytochromes, the PRD domain is required for interaction with phy signaling partners but might also play a role in stabilization of the Pfr form of phyB (4Quail P.H. 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