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The phytochrome apoprotein family inArabidopsis is encoded by five genes: the sequences and expression ofPHYD andPHYE

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Abstract

Two novelArabidopsis phytochrome genes,PHYD andPHYE, are described and evidence is presented that, together with the previously describedPHYA, PHYB andPHYC genes, the primary structures of the complete phytochrome family of this plant are now known. ThePHYD- andPHYE-encoded proteins are of similar size to the other phytochrome apoproteins and show sequence similarity along their entire lengths. Hence, red/far-red light sensing in higher plants is mediated by a diverse but structurally conserved group of soluble photoreceptors. The proteins encoded by thePHYD andPHYE genes are more closely related to phytochrome B than to phytochromes A or C, indicating that the evolution of thePHY gene family inArabidopsis includes an expansion of a PHYB-related subgroup. The PHYB and PHYD phytochromes show greater than 80% amino acid sequence identity but the phenotypes ofphyB null mutants demonstrate that these receptor forms are not functionally redundant. The fivePHY mRNAs are, in general, expressed constitutively under varying light conditions, in different plant organs, and over the life cycle of the plant. These observations provide the first description of the structure and expression of a complete phytochrome family in a higher plant.

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References

  1. Ausubel FM, Brent R, Kingston RE, Moore DD, Seidman JG, Smith JA, Struhl K: Current Protocols in Molecular Biology. Greene Publishing Associates/Wiley-Interscience, New York (1989).

    Google Scholar 

  2. Butler WL, Norris KH, Siegelman HW, Hendricks SB: Detection, assay, and preliminary purification of the pigment controlling photoresponsive development of plants. Proc Natl Acad Sci USA 45: 1703–1708 (1959).

    Google Scholar 

  3. Chang C, Kwok SF, Bleeker AB, Meyerowitz EM:Arabidopsis ethylene-response geneETR1: similarity of product to two-component regulators. Science: 262, 539–544 (1993).

    Google Scholar 

  4. Cherry JR, Hondred D, Walker JM, Keller JM, Hershey HP, Vierstra RD: Carboxy-terminal deletion analysis of oat phytochrome A reveals the presence of separate domains required for structure and biological activity. Plant Cell 5: 565–575 (1993).

    Google Scholar 

  5. Cherry JR, Hondred D, Walker JM, Vierstra RD: Phytochrome requires the 6-kDa N-terminal domain for full biological activity. Proc Natl Acad Sci USA 89: 5039–5043 (1992).

    Google Scholar 

  6. Christensen AH, Quail PH: Structure and expression of a maize phytochrome-encoding gene. Gene 85: 381–390 (1989).

    Google Scholar 

  7. Crawford NM, Smith M, Bellissimo D, Davis RW: Sequence and nitrate regulation of theArabidopsis thaliana mRNA encoding nitrate reductase, a metalloflavoprotein with three functional domains. Proc Natl Acad Sci USA 85: 5006–5010 (1988).

    Google Scholar 

  8. Dehesh K, Franci C, Parks BM, Seeley KA, Short TW, Tepperman JM, Quail PH:Arabidopsis HY8 locus encodes phytochrome A. Plant Cell 5: 1081–1088 (1993).

    Google Scholar 

  9. Dehesh K, Franci C, Sharrock RA, Somers DE, Welsch J, Quail PH: TheArabidopsis phytochrome A gene has multiple transcription start sites and a promoter sequence motif homologous to the repressor element of monocot phytochrome A genes. Photochem Photobiol (in press).

  10. Dehesh K, Tepperman J, Christensen AH, Quail PH:phyB is evolutionarily conserved and constitutively expressed in rice seedling shoots. Mol Gen Genet 225: 305–313 (1991).

    Google Scholar 

  11. Edgerton MD, Jones AM: Localization of protein-protein interactions between subunits of phytochrome. Plant Cell 4: 161–171 (1992).

    Google Scholar 

  12. Edgerton MD, Jones AM: Subunit interactions in the carboxy-terminal domain of phytochrome. Biochemistry 32: 8239–8245 (1993).

    Google Scholar 

  13. Edwards K, Johnstone C, Thompson C: A simple and rapid method for the preparation of plant genomic DNA for PCR analysis. Nucl Acids Res 19: 1349 (1991).

    Google Scholar 

  14. Felsenstein J: PHYLIP — Phylogeny inference package (Version 3.2). Cladistics 5: 164–166 (1989).

    Google Scholar 

  15. Frohman MA, Dush MK, Martin GR: Rapid production of full-length cDNAs form rare transcripts: amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85: 8998–9002 (1988).

    Google Scholar 

  16. Furuya M: Phytochromes: their molecular species, gene families, and functions. Annu Rev Plant Physiol Plant Mol Biol 44: 617–645 (1993).

    Google Scholar 

  17. Heyer A, Gatz C: Isolation and characterization of a cDNA clone coding for potato type A phytochrome. Plant Mol Biol 18: 535–544 (1992).

    Google Scholar 

  18. Heyer A, Gatz C: Isolation and characterization of a cDNA clone coding for potato type B phytochrome. Plant Mol Biol 20: 589–600 (1992).

    Google Scholar 

  19. Hershey HP, Barker RF, Idler KB, Lissemore JL, Quail PH: Analysis of cloned cDNA and genomic sequences for phytochrome: amino acid sequences for two gene products expressed in etiolatedAvena. Nucl Acids Res 13: 8543–8559 (1985).

    Google Scholar 

  20. Hershey HP, Barker RF, Idler KB, Murray MG, Quail PH: Nucleotide sequence and characterization of a gene encoding the phytochrome polypeptide fromAvena. Gene 61: 339–348 (1987).

    Google Scholar 

  21. Jones AM, Quail PH: Quaternary structure of 124-kilodalton phytochrome fromAvena sativa L. Biochemistry 25: 2987–2995 (1986).

    Google Scholar 

  22. Jones AM, Vierstra RD, Daniels SM, Quail PH: The role of separate molecular domains in the structure of phytochrome from etiolatedAvena sativa L. Planta 164: 501–506 (1985).

    Google Scholar 

  23. Kay SA, Keith B, Shinozaki K, Chua N-H: The sequence of the rice phytochrome gene. Nucl Acids Res 17: 2865–2866 (1989).

    Google Scholar 

  24. Kimura M: The Neutral Theory of Molecular Evolution. Cambridge University Press, Cambridge (1983).

    Google Scholar 

  25. Maniatis T, Fritsch EF, Sambrook J: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY (1982).

    Google Scholar 

  26. Mathews S, Lavin M, Sharrock RA: Evolution of the phytochrome gene family and its utility for phylogenetic analyses of angiosperms. Ann Missouri Bot Gard (in press).

  27. Mendu N, Rines H, Silflow CD: Mapping of beta-tubulin genomic sequences in hexaploid oat (Avena sativa L.). Theor Appl Genet 86: 135–140 (1993).

    Google Scholar 

  28. Nagatani A, Reed JW, Chory J: Isolation and initial characterization ofArabidopsis mutants that are deficient in phytochrome A. Plant Physiol 102: 269–277 (1993).

    Google Scholar 

  29. Neuhaus G, Bowler C, Kern R, Chua N-H: Calcium/calmodulin-dependent and-independent phytochrome signal transduction pathways. Cell 73: 937–952 (1993).

    Google Scholar 

  30. Parks BM, Quail PH:hy8, a new class ofArabidopsis long hypocotyl mutants deficient in functional phytochrome A. Plant Cell 5: 39–48 (1993).

    Google Scholar 

  31. Putterill JJ, Gardner RC: Initiation of translation of the β-glucuronidase reporter gene at internal AUG codons in plant cells. Plant Sci 62: 199–205 (1989).

    Google Scholar 

  32. Quail PH: Phytochrome: a light-activated molecular switch that regulates plant gene expression. Ann Rev Genet 25: 389–409 (1991).

    Google Scholar 

  33. Reed JW, Nagpal P, Poole DS, Furuya M, Chory J: Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughoutArabidopsis development. Plant Cell 5: 147–157 (1993).

    Google Scholar 

  34. Roux SJ: Phytochrome and membranes. In: Kendrick RE, Kronenberg GHM (eds) Photomorphogenesis in Plants, pp. 115–136. Martinus Nijhoff Publishers, Dordrecht (1986).

    Google Scholar 

  35. Rüdiger W, Thümmler F: Phytochrome in lower plants. In: Thomas B, Johnson CB (eds) Phytochrome Properties and Biological Action, pp. 57–70. Springer-Verlag, Berlin (1991).

    Google Scholar 

  36. Sato N: Nucleotide sequence and expression of the phytochrome gene inPisum sativum: differential regulation by light of multiple transcripts. Plant Mol Biol 11: 697–710 (1988).

    Google Scholar 

  37. Schneider-Poetsch HAW: Signal transduction by phytochrome: Phytochromes have a module related to the transmitter modules of bacterial sensor proteins. Photochem Photobiol 56: 839–846 (1992).

    Google Scholar 

  38. Sharrock RA, Lissemore JL, Quail PH: Nucleotide and amino acid sequence of aCucurbita phytochrome cDNA clone: identification of conserved features by comparison withAvena phytochrome. Gene 47:287–295 (1986).

    Google Scholar 

  39. Sharrock RA, Quail PH: Novel phytochrome sequences inArabidopsis thaliana: structure, evolution, and differential expression of a plant regulatory photoreceptor family. Genes Devel 3: 1745–1757 (1989).

    Google Scholar 

  40. Smith H, Whitelam GC: Phytochrome, a family of photoreceptors with multiple physiological roles. Plant Cell Envir 13: 695–707 (1990).

    Google Scholar 

  41. Somers DE, Sharrock RA, Tepperman JM, Quail PH: Thehy3 long hypocotyl mutant ofArabidopsis is deficient in phytochrome B. Plant Cell 3: 1263–1274 (1991).

    Google Scholar 

  42. Stockhaus J, Nagatani A, Halfter U, Kay S, Furuya M, Chua N-H: Serine-to-alanine substitutions at the amino-terminal region of phytochrome A result in an increase in biological activity. Genes Devel 6: 2364–2372 (1992).

    Google Scholar 

  43. Thümmler F, Dufner M, Kreisl P, Dittrich P: Molecular cloning of a novel phytochrome gene of the mossCeratodon purpureus which encodes a putative light-regulated protein kinase. Plant Mol Biol 20: 1003–1017 (1992).

    Google Scholar 

  44. Valvekens D, Van Montagu M, Van Lijsebettens M:Agrobacterium tumefaciens-mediated transformation ofArabidopsis thaliana root explants by using kanamycin selection. Proc Natl Acad Sci USA 85: 5536–5540 (1988).

    Google Scholar 

  45. Wester L, Somers DE, Clack T, Sharrock RA: Transgenic complementation of thehy3 phytochrome B mutation and response toPHYB gene copy number inArabidopsis. Plant J 5: 261–272 (1994).

    Google Scholar 

  46. Whitelam GC, Johnson E, Peng J, Carol P, Anderson ML, Cowl JS, Harberd NP: Phytochrome A null mutants ofArabidopsis display a wild-type phenotype in white light. Plant Cell 5: 757–768 (1993).

    Google Scholar 

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  1. Department of Biology, Montana State University, 59717, Bozeman, MT, USA

    Ted Clack, Sarah Mathews & Robert A. Sharrock

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  1. Ted Clack
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  2. Sarah Mathews
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  3. Robert A. Sharrock
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Clack, T., Mathews, S. & Sharrock, R.A. The phytochrome apoprotein family inArabidopsis is encoded by five genes: the sequences and expression ofPHYD andPHYE . Plant Mol Biol 25, 413–427 (1994). https://doi.org/10.1007/BF00043870

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  • DOI: https://doi.org/10.1007/BF00043870

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