Tetrapyrroles pp 221-234 | Cite as


Bilin-Linked Photoreceptors in Bacteria and Plants
  • Matthew J. Terry
  • Alex C. McCormac
Part of the Molecular Biology Intelligence Unit book series (MBIU)


The phytochromes and related prokaryotic photoreceptors utilise a linear tetrapyrrole chromophore to monitor the surrounding light environment. They are found in most photosynthetic organisms, and also some nonphotosynthetic bacteria from which they most likely evolved. A key feature of the phytochromes is that they respond to light in a photoreversible manner. In plants, red light leads to the formation of Pfr, the physiologically-active phytochrome species, while far-red light reverses this process to give the Pr form. Prokaryotic phytochromes are also photoreversible, and are thought to be involved in regulating processes such as chromatic adaptation, phototaxis and pigment synthesis. In the model plant Arabidopsis thaliana there are five phytochromes that are involved in regulating all stages of plant development from germination to flowering. They also play a key role in chloroplast development and the regulation of the tetrapyrrole pathway.


Histidine Kinase Domain phyB Mutant Photoactive Yellow Protein Plant Phytochrome Shade Avoidance Syndrome 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Montgomery BL, Lagarias JC. Phytochrome ancestory: Sensors of bilins and light. Trends Plant Sci 2002; 7:357–366.CrossRefPubMedGoogle Scholar
  2. 2.
    Lamparter T. Evolution of cyanobacterial and plant phytochromes. FEBS Lett 2004; 573:1–5.CrossRefPubMedGoogle Scholar
  3. 3.
    Sage LC. Pigment of the imagination. A History of Phytochrome Research. New York: Academic Press Inc, Harcourt Brace Jovanovich Publishers, 1992.Google Scholar
  4. 4.
    Terry MJ, Wahleithner JA, Lagarias JC. Biosynthesis of the plant photoreceptor phytochrome. Arch Biochem Biophys 1993; 306:1–15.CrossRefPubMedGoogle Scholar
  5. 5.
    Mathews S, Sharrock RA. Phytochrome gene diversity. Plant Cell Environ 1997; 20:666–671.CrossRefGoogle Scholar
  6. 6.
    Hughes J, Lamparter T, Mittmann F et al. A prokaryotic phytochrome. Nature 1997; 386:663–663.CrossRefPubMedGoogle Scholar
  7. 7.
    Yeh K-C, Wu S-H, Murphy JT et al. A cyanobacterial phytochrome two-component light sensory system. Science 1997; 277:1505–1508.CrossRefPubMedGoogle Scholar
  8. 8.
    Wu S-H, McDowell MT, Lagarias JC. Phycocyanobilin is the natural precursor of the phytochrome chromophore in the green alga Mesotaenium caldariorum. J Biol Chem 1997; 272:25700–25705.CrossRefPubMedGoogle Scholar
  9. 9.
    Hübschmann T, Börner T, Hartmann E et al. Characterization of the Cphl holo-phytochrome from Synechocystis sp. PCC 6803. Eur J Biochem 2001; 268:2055–2063.CrossRefPubMedGoogle Scholar
  10. 10.
    Bhoo S-H, Davis SJ, Walker J et al. Bacteriophytochromes are photochromic histidine kinases using a biliverdin chromophore. Nature 2001; 414:776–779.CrossRefPubMedGoogle Scholar
  11. 11.
    Terauchi K, Montgomery BL, Grossman AR et al. RcaE is a complementary chromatic adaptation photoreceptor required for green and red light responsiveness. Mol Microbiol 2004; 51:567–577.CrossRefPubMedGoogle Scholar
  12. 12.
    Yeh KC, Lagarias JC. Eukaryotic phytochromes: Light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proc Natl Acad Sci USA 1998; 95:13976–13981.CrossRefPubMedGoogle Scholar
  13. 13.
    Taylor BL, Zhulin IB. PAS domains: Internal sensors of oxygen, redox potential, and light. Microbiol Mol Biol Rev 1999; 63:479–506.PubMedGoogle Scholar
  14. 14.
    Matsushita T, Mochizuki N, Nagatani A. Dimers of the N-terminal domain of phytochrome B are functional in the nucleus. Nature 2003; 424:571–574.CrossRefPubMedGoogle Scholar
  15. 15.
    Nagatani A. Light-regulated nuclear localization of phytochromes. Curr Opin Plant Biol 2004; 7:708–711.CrossRefPubMedGoogle Scholar
  16. 16.
    Møller SG, Ingles PJ, Whitelam GC. The cell biology of phytochrome signalling. New Phytol 2002; 154:553–590.CrossRefGoogle Scholar
  17. 17.
    Quail PH. An emerging molecular map of the phytochromes. Plant Cell Environ 1997; 20:657–665.CrossRefGoogle Scholar
  18. 18.
    Nozue K, Kanegae T, Imaizumi T et al. A phytochrome from the fern Adiantum with features of the putative photoreceptor NPH1. Proc Natl Acad Sci USA 1998; 95:15826–15830.CrossRefPubMedGoogle Scholar
  19. 19.
    Kawai H, Kanegae T, Christensen S et al. Responses of ferns to red light are mediated by an unconventional photoreceptor. Nature 2003; 421:287–290.CrossRefPubMedGoogle Scholar
  20. 20.
    Jiang ZY, Swem LR, Rushing BG et al. Bacterial photoreceptor with similarity to photoactive yellow protein and plant phytochromes. Science 1999; 285:406–409.CrossRefPubMedGoogle Scholar
  21. 21.
    Karniol B, Vierstra RD. The pair of bacteriophytochromes from Agrobacterium tumefaciens are histidine kinases with opposing photobiological properties. Proc Natl Acad Sci USA 2003; 100:2807–2812.CrossRefPubMedGoogle Scholar
  22. 22.
    Mutsuda M, Michel K-P, Zhang X et al. Biochemical properties of CikA, an unusual phytochrome-like histidine protein kinase that resets the circadian clock in Synechococcus elongatus PCC 7942. J Biol Chem 2003; 278:19102–19110.CrossRefPubMedGoogle Scholar
  23. 23.
    Wu S-H, Lagarias JC. Defining the bilin lyase domain: Lessons from the extended phytochrome superfamily. Biochem 2000; 39:13487–13495.CrossRefGoogle Scholar
  24. 24.
    Lagarias JC, Kelly JM, Cyr KL et al. Comparative photochemical analysis of highly purified 124 kilodalton oat and rye phytochromes in vitro. Photochem Photobiol 1987; 46:5–13.CrossRefGoogle Scholar
  25. 25.
    Kneip C, Hildebrandt P, Schlamann W et al. Protonation state and structural changes of the tetrapyrrole chromophore during the Pr → Pfr phototransformation of phytochrome: A resonance raman spectroscopic study. Biochem 1999; 38:15185–15192.CrossRefGoogle Scholar
  26. 26.
    Andel IIIrd F, Murphy JT, Haas JA et al. Probing the photoreaction mechanism of phytochrome through analysis of resonance raman vibrational spectra of recombinant analogues. Biochem 2000; 39:2667–2676.CrossRefGoogle Scholar
  27. 27.
    Foerstendorf H, Benda C, Gärtner W et al. FTIR studies of phytochrome photoreactions reveal the C=O bands of the chromophore: Consequences for its protonation states, conformation, and protein interaction. Biochem 2001; 40:14952–14959.CrossRefGoogle Scholar
  28. 28.
    Braslavsky SE, Gärtner W, Schaffner K. Phytochrome photoconversion. Plant Cell Environ 1997; 20:700–706.CrossRefGoogle Scholar
  29. 29.
    Elich TD, Lagarias JC. Formation of a photoreversible phycocyanobilin-apophytochrome adduct in vitro. J Biol Chem 1989; 264:12902–12908.PubMedGoogle Scholar
  30. 30.
    Davis SJ, Vener AV, Vierstra RD. Bacteriophytochromes: Phytochrome-like photoreceptors from nonphotosynthetic eubacteria. Science 1999; 286:2517–2520.CrossRefPubMedGoogle Scholar
  31. 31.
    Lamparter T, Michael N, Mittmann F et al. Phytochrome from Agrobacterium tumefaciens has unusual spectral properties and reveals an N-terminal chromophore attachment site. Proc Natl Acad Sci USA 2002; 99:11628–11633.CrossRefPubMedGoogle Scholar
  32. 32.
    Lamparter T, Michael N, Caspani O et al. Biliverdin binds covalently to Agrobacterium phytochrome Agp1 via its ring A vinyl side chain. J Biol Chem 2003; 278:33786–33792.CrossRefPubMedGoogle Scholar
  33. 33.
    Lamparter T, Carrascal M, Michael N et al. The biliverdin chromophore binds covalently to a conserved cysteine residue in the N-terminus of Agrobacterium phytochrome Agp1. Biochem 2004; 43:3659–3669.CrossRefGoogle Scholar
  34. 34.
    Yoshihara S, Ikeuchi M. Photatactic motility in the unicellular cyanobacterium Synechocystis sp. PCC 6803. Photochem Photobiol Sci 2004; 3:512–518.CrossRefPubMedGoogle Scholar
  35. 35.
    Aravind L, Ponting CP. The GAF domain: An evolutionary link between diverse phototransducing proteins. Trends Biochem Sci 1997; 22:458–459.CrossRefPubMedGoogle Scholar
  36. 36.
    Lagarias JC, Lagarias DM. Self-assembly of synthetic phytochrome holoprotein in vitro. Proc Natl Acad Sci USA 1989; 86:5778–5780.CrossRefPubMedGoogle Scholar
  37. 37.
    Li L, Murphy JT, Lagarias JC. Continuous florescence assay of phytochrome assembly in vitro. Biochem 1995; 34:7923–7930.CrossRefGoogle Scholar
  38. 38.
    Borucki B, Otto H, Rottwinkel G et al. Mechanism of Cphl phytochrome assembly from stopped-flow kinetics and circular dichroism. Biochem 2003; 42:13684–13697.CrossRefGoogle Scholar
  39. 39.
    Quest B, Gärtner W. Chromophore selectivity in bacterial phytochromes. Dissecting the process of chromophore attachment. Eur J Biochem 2004; 271:1117–1126.CrossRefPubMedGoogle Scholar
  40. 40.
    Li L, Lagarias JC. Phytochrome assembly. Defining chromophore structural requirements for covalent attachment and photoreversibility. J Biol Chem 1992; 267:19204–19210.PubMedGoogle Scholar
  41. 41.
    Bhoo S-H, Hirano T, Jeong H-Y et al. Phytochrome photochromism probed by site-directed mutations and chromophore esterification. J Am Chem Soc 1997; 119:11717–11718.CrossRefGoogle Scholar
  42. 42.
    Hanzawa H, Inomata K, Kinoshita H et al. In vitro assembly of phytochrome B apoprotein with synthetic analogs of the phytochrome chromophore. Proc Natl Acad Sci USA 2001; 98:3612–3617.CrossRefPubMedGoogle Scholar
  43. 43.
    Hanzawa H, Shinomura T, Inomata K et al. Structural requirement of bilin chromophore for the photosensory specificity of phytochrome A and B. Proc Natl Acad Sci USA 2002; 99:4725–4729.CrossRefPubMedGoogle Scholar
  44. 44.
    Fiedler B, Broc D, Schubert H et al. Involvement of cyanobacterial phytochromes in growth under different light qualities and quantities. Photochem Photobiol 2004; 79:551–555.CrossRefPubMedGoogle Scholar
  45. 45.
    Wilde A, Fielder B, Börner T. The cyanobacterial photochrome Cph2 inhibits phototaxis towards blue light. Mol Microbiol 2002; 44:981–988.CrossRefPubMedGoogle Scholar
  46. 46.
    Giraud E, Fardoux J, Fourrier N et al. Bacteriophytochrome controls photosystem synthesis in anoxygenic bacteria. Nature 2002; 417:202–205.CrossRefPubMedGoogle Scholar
  47. 47.
    Kendrick RE, Kronenberg GHM, eds. Photomorphogenesis in Plants. 2nd ed. Dordrecht: Kluwer Academic Publishers, 1994.Google Scholar
  48. 48.
    Smith H. Physiological and ecological function within the phytochrome family. Ann Rev Plant Physiol Plant Mol Biol 1995; 46:289–315.CrossRefGoogle Scholar
  49. 49.
    Whitelam GC, Patel S, Devlin PF. Phytochromes and photomorphogenesis in Arabidopsis. Phil Trans R Soc Lond B 1998; 353:1445–1453.CrossRefGoogle Scholar
  50. 50.
    Smith H. Phytochromes and light signal perception by plants—An emerging synthesis. Nature 2000; 407:585–591.CrossRefPubMedGoogle Scholar
  51. 51.
    Nagy F, Schäfer E. Phytochromes control photomorphogeneis by differentially regulated, interacting signalling pathways in higher plants. Ann Rev Plant Biol 2002; 53:329–355.CrossRefGoogle Scholar
  52. 52.
    Wada M, Kadota A. Photomorphogenesis in lower green plants. Ann Rev Plant Physiol Plant Mol Biol 1989; 40:169–191.CrossRefGoogle Scholar
  53. 53.
    von Arnim A, Deng X-W. Light control of seedling development. Ann Rev Plant Physiol 1996; 47:215–243.CrossRefGoogle Scholar
  54. 54.
    Quail PH. Phytochrome photosensory signalling networks. Nature Rev Mol Cell Biol 2002; 3:85–93.CrossRefGoogle Scholar
  55. 55.
    Morelli G, Ruberti I. Light and shade in the photocontrol of Arabidopsis growth. Trends Plant Sci 2002; 7:399–404.CrossRefPubMedGoogle Scholar
  56. 56.
    Casal JJ. Phytochromes, cryptochromes, phototropin: Photoreceptor interactions in plants. Photochem Photobiol 2000; 71:1–11.CrossRefPubMedGoogle Scholar
  57. 57.
    Koornneef M, Rolff E, Spruit CJP. Genetic control of light-inhibited hypocotyl elongation in Arabidopsis thaliana (L.) Heynh. Z Pflanzenphysiol 1980; 100:147–160.Google Scholar
  58. 58.
    Reed JW, Nagatani A, Elich TD et al. Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiol 1994; 104:1139–1149.PubMedGoogle Scholar
  59. 59.
    Shinomura T, Nagatani A, Hanzawa H et al. Action spectra for phytochrome A-and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 1996; 93:8129–8133.CrossRefPubMedGoogle Scholar
  60. 60.
    Nagatani A, Reed JW, Chory J. Isolation and initial characterization of Arabidopsis mutants that are deficient in phytochrome A. Plant Physiol 1993; 102:269–277.PubMedGoogle Scholar
  61. 61.
    Whitelam GC, Johnson E, Peng J et al. Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 1993; 5:757–768.CrossRefPubMedGoogle Scholar
  62. 62.
    Shinomura T, Uchida K, Furuya M. Elementary processes of photoperception by phytochrome A for high-irradiance response of hypocotyl elongation in Arabidopsis. Plant Physiol 2000; 122:147–156.CrossRefPubMedGoogle Scholar
  63. 63.
    Casal JJ, Sanchez RA, Yanovsky MJ. The function of phytochrome A. Plant Cell Environ 1997; 20:813–819.CrossRefGoogle Scholar
  64. 64.
    Aukerman MJ, Hirschfeld M, Wester L et al. A deletion in the PHYD gene of the Arabidopsis Wassilewskija ecotype defines a role for phytochrome D in red/far-red light sensing. Plant Cell 1997; 9:1317–1326.CrossRefPubMedGoogle Scholar
  65. 65.
    Devlin PF, Robson PRH, Patel SR et al. Phytochrome D acts in the shade-avoidance syndrome in Arabidopsis by controlling elongation growth and flowering time. Plant Physiol 1999; 119:909–915.CrossRefPubMedGoogle Scholar
  66. 66.
    Devlin PF, Patel SR, Whitelam GC. Phytochrome E influences internode elongation and flowering time in Arabidopsis. Plant Cell 1998; 10:1479–1487.CrossRefPubMedGoogle Scholar
  67. 67.
    Hennig L, Stoddart WM, Dieterle M et al. Phytochrome E controls light-induced germination of Arabidopsis. Plant Physiol 2002; 128:194–200.CrossRefPubMedGoogle Scholar
  68. 68.
    Franklin KA, Davis SJ, Stoddart WM et al. Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. Plant Cell 2003; 15:1981–1989.CrossRefPubMedGoogle Scholar
  69. 69.
    Monte E, Alonso JM, Ecker JR et al. Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 2003; 15:1962–1980.CrossRefPubMedGoogle Scholar
  70. 70.
    Sharrock RA, Clack T. Patterns of expression and normalised levels of the five Arabidopsis phytochromes. Plant Physiol 2002; 130:442–456.CrossRefPubMedGoogle Scholar
  71. 71.
    Sharrock RA, Clack T. Heterodimerization of type II phytochromes in Arabidopsis. Proc Natl Acad Sci USA 2004; 101:11500–11505.CrossRefPubMedGoogle Scholar
  72. 72.
    Gyula P, Schäfer E, Nagy F. Light perception and signalling in higher plants. Curr Opin Plant Biol 2003; 6:446–452.CrossRefPubMedGoogle Scholar
  73. 73.
    Terry MJ. Phytochrome chromophore-deficient mutants. Plant Cell Environ 1997; 20:740–745.CrossRefGoogle Scholar
  74. 74.
    Tepperman JM, Hudson ME, Khanna R et al. Expression profiling of phyB mutant demonstrates substantial contribution of other phytochromes to red-light-regulated gene expression during seedling de-etiolation. Plant J 2004; 38:725–739.CrossRefPubMedGoogle Scholar
  75. 75.
    Terzaghi WB, Cashmore AR. Light-regulated transcription. Ann Rev Plant Physiol Plant Mol Biol 1995; 46:445–474.CrossRefGoogle Scholar
  76. 76.
    McCormac AC, Terry MJ. Light-signalling pathways leading to the coordinated expression of HEMA1 and Lhcb during chloroplast development in Arabidopsis thaliana. Plant J 2002; 32:549–559.CrossRefPubMedGoogle Scholar
  77. 77.
    Matsumoto F, Obayashi T, Sasaki-Sekimoto Y et al. Gene expression profiling of the tetrapyrrole metabolic pathway in Arabidopsis with a mini-array system. Plant Physiol 2004; 135:2379–2391.CrossRefPubMedGoogle Scholar
  78. 78.
    Kasemir H. Light control of chlorophyll accumulation in higher plants. In: Shropshire Jr W, Mohr H, eds. Encyclopedia of Plant Physiology, New Series, Vol 16B. Berlin: Springer-Verlag, 1983:662–686.Google Scholar
  79. 79.
    Huang L, Bonner BA, Castelfranco PA. Regulation of 5-aminolevulinic acid (ALA) synthesis in developing chloroplasts II. Regulation of ALA-synthesising capacity by phytochrome. Plant Physiol 1989; 90:1003–1008.CrossRefPubMedGoogle Scholar
  80. 80.
    McCormac AC, Terry MJ. Loss of nuclear gene expression during the phytochrome A-mediated far-red block of greening response. Plant Physiol 2002; 130:402–414.CrossRefPubMedGoogle Scholar
  81. 81.
    McCormac AC, Fischer A, Kumar AM et al. Regulation of HEMA1 expression by phytochrome and a plastid signal during de-etiolation in Arabidopsis thaliana. Plant J 2001; 25:549–561.CrossRefPubMedGoogle Scholar
  82. 82.
    Gray JC, Sullivan JA, Wang J-H et al. Coordination of plastid and nuclear gene expression. Phil Trans R Soc Lond B 2003; 358:135–145.CrossRefGoogle Scholar
  83. 83.
    Somers DE, Devlin PF, Kay SA. Phytochromes and cryptochromes in the entrainment of the Arabidopsis circadian clock. Science 1998; 282:1488–1490.CrossRefPubMedGoogle Scholar
  84. 84.
    Apel K. The protochlorophyllide holochrome of barley (Hordeum vulgare L). Phytochrome-induced decrease of translatable mRNA coding for the NADPH: protochlorophyllide oxidoreductase. Eur J Biochem 1981; 120:89–93.CrossRefPubMedGoogle Scholar
  85. 85.
    Eichenberg K, Bäurle I, Paulo N et al. Arabidopsis phytochromes C and E have different spectral characteristics from those of phytochromes A and B. FEBS Lett 2000; 470:107–112.CrossRefPubMedGoogle Scholar
  86. 86.
    Park C-M, Kim J-II, Yang S-S et al. A second photochromic bacteriophytochrome from Synechocystis sp. PCC 6803: Spectral analysis and down-regulation by light. Biochem 2000; 39:10840–10847.CrossRefGoogle Scholar
  87. 87.
    Milford MI. Biosynthesis, properties and structure of phytochrome photoreceptors from cyanobacteria. Ph. D. Thesis. University of Southampton, 2001.Google Scholar
  88. 88.
    Wagner JR, Brunzelle JS, Forest KT, Vierstra RD. A light-sensing knot revealed by the structure of the chromophore-binding domain of phytochrome. Nature 2005; 438:325–331.CrossRefPubMedGoogle Scholar
  89. 89.
    Wagner JR, Zhang JR, Brunzelle JS et al. High resolution structure of Deinococcus bacteriophytochrome yields new insights into phytochrome architecture and evolution. J Biol Chem 2007; 16:12298–12309.Google Scholar
  90. 90.
    Rockwell NC, Su YS, Lagarias JC. Phytochrome structure and signalling mechanisms. Ann Rev Plant Biol 2006; 57:837–858.CrossRefGoogle Scholar
  91. 91.
    Giraud E, Verméglio A. Bacteriophytochromes in anoxygenic photosynthetic bacteria. Photosyn Res 2008; 97:141–153.CrossRefPubMedGoogle Scholar
  92. 92.
    Ikeuchi M, Ishizuka T. Cyanobacteriochromes: a new superfamily of tetrapyrrole-binding photoreceptors in cyanobacteria. Photochem Photobiol Sci 2008; DOI: 10.1039/b802660m.Google Scholar

Copyright information

© Landes Bioscience and Springer Science+Business Media 2009

Authors and Affiliations

  1. 1.School of Biological SciencesUniversity of SouthamptonSouthamptonUK

Personalised recommendations