Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

Two molecular species of phytochrome A with distinct modes of action

V. Sineshchekov
+ Author Affiliations
- Author Affiliations

Biology Department, M.V. Lomonosov Moscow State University, Moscow, Russia. Email: vsineshchekov@gmail.com

Functional Plant Biology 46(2) 118-135 https://doi.org/10.1071/FP18156
Submitted: 15 June 2018  Accepted: 17 September 2018   Published: 26 October 2018

Abstract

Adaptation of plants to environmental light conditions is achieved via operation of a highly complex photoreceptor apparatus. It includes the phytochrome system comprising phytochromes A and B (phyA and phyB) as the major components. phyA differs from phyB by several properties, including its ability to mediate all three photoresponse modes – the very low and low fluence responses (VLFR and LFR respectively) and the high irradiance responses (HIR), whereas phyB is responsible for LFR. This review discusses the uniqueness of phyA in terms of its structural and functional heterogeneity. The photoreceptor is presented in monocots and dicots by two native molecular species, phyAʹ and phyAʹʹ, differing by spectroscopic, photochemical and phenomenological properties. phyA differentiation into substates includes post-translational phosphorylation of a serine residue(s) at the N-terminal extension of the molecule with phyAʹ being the phosphorylated species and phyAʹʹ, dephosphorylated. They differ also by their mode of action, which depends on the cellular context. The current working hypothesis is that phyAʹ mediates VLFR and phyAʹʹ, HIR and LFR. The content and functional activity of the two pools are regulated by light and by phosphatase/kinase equilibrium and pH in darkness, what contributes to the fine-tuning of the phytochrome system. Detection of the native pools of the cryptogamic plant fern Adiantum capillus-veneris phy1 (phy1ʹ and phy1ʹʹ) similar to those of phyA suggests that the structural and functional heterogeneity of phyA is not a unique phenomenon and may have arisen earlier in the molecular evolution of the phytochrome system than the appearance of the angiosperm phytochromes.


References

Apel K (1981) The protochlorophillide holochrome of barley (Hordeum vulgare, L.). Phytochrome induced decrease of transletable mRNA coding for the NADPH: protochlorophyllide oxidoreductase. European Journal of Biochemistry 120, 89–93.
The protochlorophillide holochrome of barley (Hordeum vulgare, L.). Phytochrome induced decrease of transletable mRNA coding for the NADPH: protochlorophyllide oxidoreductase.Crossref | GoogleScholarGoogle Scholar |

Bae G, Choi G (2008) Decoding of light signals by plant phytochromes and their interacting proteins. Annual Review of Plant Biology 59, 281–311.

Barnes SA, Nishizawa NK, Quaggio RB, Whitelam GC, Chua NH (1996) Far-red light blocks greening of Arabidopsis seedlings via a phytochrome A-mediated change in plastid development. The Plant Cell 8, 601–615.

Batschauer A (Ed.) (2004) ‘Photoreceptors and light signaling.’ (Royal Society of Chemistry: Cambridge, UK)

Batschauer A, Apel K (1984) An inverse control by phytochrome of the expression of two nuclear genes in barley (Hordeum vulgare L.). European Journal of Biochemistry 143, 593–597.
An inverse control by phytochrome of the expression of two nuclear genes in barley (Hordeum vulgare L.).Crossref | GoogleScholarGoogle Scholar |

Braslavsky SE, Gärtner W, Schaeffner K (1997) Phytochrome photoconversion. Plant, Cell & Environment 20, 700–706.
Phytochrome photoconversion.Crossref | GoogleScholarGoogle Scholar |

Briggs WR, Spudich JL (Eds.) (2005) ‘Handbook of photosensory receptors.’ (Wiley-VCH: Verlag Gmbh and Co. KgaA: Weinheim, Germany)

Brockmann J, Schäfer E (1982) Analysis of Pfr destruction in Amarantus caudatus L. – evidence for two pools of phytochrome. Photochemistry and Photobiology 35, 555–558.
Analysis of Pfr destruction in Amarantus caudatus L. – evidence for two pools of phytochrome.Crossref | GoogleScholarGoogle Scholar |

Burgie ES, Bussell AN, Walker JM, Dubiel K, Vierstra RD (2014) Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome. Proceedings of the National Academy of Sciences of the United States of America 111, 10179–10184.
Crystal structure of the photosensing module from a red/far-red light-absorbing plant phytochrome.Crossref | GoogleScholarGoogle Scholar |

Butler WL, Norris KH, Siegelman HW, Hendricks SB (1959) Detection, assay, and preliminary purification of the pigment controlling photoresponsive development in plants. Proceedings of the National Academy of Sciences of the United States of America 45, 1703–1708.
Detection, assay, and preliminary purification of the pigment controlling photoresponsive development in plants.Crossref | GoogleScholarGoogle Scholar |

Cantón F, Quail PH (1999) Both phyA and phyB mediate light-imposed repression of PHYA gene expression in Arabidopsis. Plant Physiology 121, 1207–1215.
Both phyA and phyB mediate light-imposed repression of PHYA gene expression in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Casal JJ (2000) Phytochromes, cryptochromes, phototropin: photoreceptor interactions in plants. Photochemistry and Photobiology 71, 1–11.
Phytochromes, cryptochromes, phototropin: photoreceptor interactions in plants.Crossref | GoogleScholarGoogle Scholar |

Casal JJ, Sánchez RA, Yanovsky MJ (1997) The function of phytochrome A. Plant, Cell & Environment 20, 813–819.
The function of phytochrome A.Crossref | GoogleScholarGoogle Scholar |

Casal JJ, Sánchez RA, Botto JF (1998) Modes of action of phytochromes. Journal of Experimental Botany 49, 127–138.

Casal JJ, Davis SJ, Kirchenbauer D, Viczian A, Yanovsky MJ, Clough RC, Kircher S, Jordan-Beebe ET, Schäfer E, Nagy F, Vierstra RD (2002) The serine-rich N-terminal domain of oat phytochrome a helps regulate light responses and subnuclear localization of the photoreceptor. Plant Physiology 129, 1127–1137.
The serine-rich N-terminal domain of oat phytochrome a helps regulate light responses and subnuclear localization of the photoreceptor.Crossref | GoogleScholarGoogle Scholar |

Casal JJ, Candia AN, Sellaro R (2014) Light perception and signaling by phytochrome A. Journal of Experimental Botany 65, 2835–2845.
Light perception and signaling by phytochrome A.Crossref | GoogleScholarGoogle Scholar |

Chen F, Li B, Li G, Charron JB, Dai M, Shi X, Deng XW (2014) Arabidopsis phytochrome A directly targets numerous promoters for individualized modulation of genes in a wide range of pathways. The Plant Cell 26, 1949–1966.
Arabidopsis phytochrome A directly targets numerous promoters for individualized modulation of genes in a wide range of pathways.Crossref | GoogleScholarGoogle Scholar |

Cherry JR, Hondred D, Walker JM, Vierstra RD (1992) Phytochrome requires the 6-kDa N-terminal domain for full biological activity. Proceedings of the National Academy of Sciences of the United States of America 89, 5039–5043.
Phytochrome requires the 6-kDa N-terminal domain for full biological activity.Crossref | GoogleScholarGoogle Scholar |

Debrieux D, Fankhauser C (2010) Light-induced degradation of phyA is promoted by transfer of the photoreceptor into the nucleus. Plant Molecular Biology 73, 687–695.
Light-induced degradation of phyA is promoted by transfer of the photoreceptor into the nucleus.Crossref | GoogleScholarGoogle Scholar |

Dong J, Ni W, Yu R, Deng XW, Chen H, Wei N (2017) Light-dependent degradation of PIF3 by SCFEBF1/2 promotes a photomorphogenic response in Arabidopsis. Current Biology 27, 2420–2430.
Light-dependent degradation of PIF3 by SCFEBF1/2 promotes a photomorphogenic response in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Emmler K, Stockhaus J, Chua NH, Schäfer E (1995) An amino-terminal deletion of rice phytochrome A results in a dominant negative suppression of tobacco phytochrome A activity in transgenic tobacco seedlings. Planta 197, 103–110.
An amino-terminal deletion of rice phytochrome A results in a dominant negative suppression of tobacco phytochrome A activity in transgenic tobacco seedlings.Crossref | GoogleScholarGoogle Scholar |

Fankhauser C (2001) The phytochromes, a family of red/far-red absorbing photoreceptors. The Journal of Biological Chemistry 276, 11453–11456.
The phytochromes, a family of red/far-red absorbing photoreceptors.Crossref | GoogleScholarGoogle Scholar |

Fankhauser C, Yeh KC, Clark J, Zhang H, Elich TD, Chory J (1999) PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284, 1539–1541.
PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Franciosini A, Serino G, Deng XW (2014)

Furuya M (1993) Phytochromes: their molecular species, gene families, and functions. Annual Review of Plant Physiology and Plant Molecular Biology 44, 617–645.
Phytochromes: their molecular species, gene families, and functions.Crossref | GoogleScholarGoogle Scholar |

Galvão VC, Fankhauser C (2015) Sensing the light environment in plants: photoreceptors and early signaling steps. Current Opinion in Neurobiology 34, 46–53.
Sensing the light environment in plants: photoreceptors and early signaling steps.Crossref | GoogleScholarGoogle Scholar |

Halliday KJ, Fankhauser C (2003) Phytochrome‐hormonal signalling networks. New Phytologist 157, 449–463.
Phytochrome‐hormonal signalling networks.Crossref | GoogleScholarGoogle Scholar |

Han Y-J, Kim H-S, Kim Y-M, Shin A-Y, Lee S-S, Bhoo SH, Song P-S, Kim J-I (2010) Functional characterization of phytochrome autophosphorylation in plant light signaling. Plant & Cell Physiology 51, 596–609.
Functional characterization of phytochrome autophosphorylation in plant light signaling.Crossref | GoogleScholarGoogle Scholar |

Heijde M, Ulm R (2012) UV-B photoreceptor-mediated signalling in plants. Trends in Plant Science 17, 230–237.
UV-B photoreceptor-mediated signalling in plants.Crossref | GoogleScholarGoogle Scholar |

Heyer AG, Mozley D, Landschutze V, Thomas B, Gatz C (1995) Function of phytochrome A in potato plants as revealed through the study of transgenic plants. Plant Physiology 109, 53–61.

Hiltbrunner A, Tscheuschler A, Viczian A, Kunkel T, Kircher S, Schäfer E (2006) FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor. Plant & Cell Physiology 47, 1023–1034.
FHY1 and FHL act together to mediate nuclear accumulation of the phytochrome A photoreceptor.Crossref | GoogleScholarGoogle Scholar |

Hsieh HL, Okamoto H (2014) Molecular interaction of jasmonate and phytochrome A signalling. Journal of Experimental Botany 65, 2847–2857.
Molecular interaction of jasmonate and phytochrome A signalling.Crossref | GoogleScholarGoogle Scholar |

Hughes J (2010) Phytochrome three-dimensional structures and functions. Biochemical Society Transactions 38, 710–716.
Phytochrome three-dimensional structures and functions.Crossref | GoogleScholarGoogle Scholar |

Hughes J (2013) Phytochrome cytopasmic signaling. Annual Review of Plant Biology 64, 377–402.
Phytochrome cytopasmic signaling.Crossref | GoogleScholarGoogle Scholar |

Hunt RE, Pratt LH (1980) Partial characterization of undegraded oat phytochrome. Biochemistry 19, 390–394.
Partial characterization of undegraded oat phytochrome.Crossref | GoogleScholarGoogle Scholar |

Iñigo S, Barber MR, Sánchez-Lamas M, Iglesias FM, Cerdán PD (2012) The photomorphogenic signal: an essential component of photoautotrophic life. In ‘Advances in photosynthesis-fundamental aspects’. (Ed. M Najafpour) pp. 191–294. (InTech: Rijeka, Croatia)

Inoue K, Nishihama R, Kohchi T (2017) Evolutionary origin of phytochrome responses and signaling in land plants. Plant, Cell & Environment 40, 2502–2508.
Evolutionary origin of phytochrome responses and signaling in land plants.Crossref | GoogleScholarGoogle Scholar |

Jarvis P, López-Juez E (2013) Biogenesis and homeostasis of chloroplasts and other plastids. Nature Reviews. Molecular Cell Biology 14, 787–802.
Biogenesis and homeostasis of chloroplasts and other plastids.Crossref | GoogleScholarGoogle Scholar |

Jordan ET, Cherry JR, Walker JM, Vierstra RD (1996) The amino‐terminus of phytochrome A contains two distinct functional domains. The Plant Journal 9, 243–257.
The amino‐terminus of phytochrome A contains two distinct functional domains.Crossref | GoogleScholarGoogle Scholar |

Jordan ET, Marita JM, Clough RC, Vierstra RD (1997) Characterization of regions within the N-terminal 6-kilodalton domain of phytochrome A that modulate its biological activity. Plant Physiology 115, 693–704.
Characterization of regions within the N-terminal 6-kilodalton domain of phytochrome A that modulate its biological activity.Crossref | GoogleScholarGoogle Scholar |

Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Current Topics in Developmental Biology 91, 29–66.

Kendrick RE, Kronenberg GH (Eds) (2012) ‘Photomorphogenesis in plants.’ (Springer Science & Business Media: Dordrecht, The Netherlands)

Kim J-I, Shen Y, Han Y-J, Park J-E, Kirchenbauer D, Soh M-S, Nagy F, Schäfer E, Song P-S (2004) Phytochrome phosphorylation modulates light signalling by influencing the protein-protein interaction. The Plant Cell 16, 2629–2640.
Phytochrome phosphorylation modulates light signalling by influencing the protein-protein interaction.Crossref | GoogleScholarGoogle Scholar |

Kim PW, Rockwell NC, Martin SS, Lagarias JC, Larsen DS (2014) Dynamic inhomogeneity in the photodynamics of cyanobacterial phytochrome Cph1. Biochemistry 53, 2818–2826.
Dynamic inhomogeneity in the photodynamics of cyanobacterial phytochrome Cph1.Crossref | GoogleScholarGoogle Scholar |

Kirchenbauer D, Viczián A, Ádám É, Hegedűs Z, Klose C, Leppert M, Hiltbrunner A, Kircher S, Schäfer E, Nagy F (2016) Characterization of photomorphogenic responses and signaling cascades controlled by phytochrome‐A expressed in different tissues. New Phytologist 211, 584–598.
Characterization of photomorphogenic responses and signaling cascades controlled by phytochrome‐A expressed in different tissues.Crossref | GoogleScholarGoogle Scholar |

Kircher S, Terecskei K, Wolf I, Sipos M, Adam E (2011) Phytochrome A-specific signaling in Arabidopsis thaliana. Plant Signaling & Behavior 6, 1714–1719.
Phytochrome A-specific signaling in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Klose C, Viczián A, Kircher S, Schäfer E, Nagy F (2015) Molecular mechanisms for mediating light‐dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors. New Phytologist 206, 965–971.
Molecular mechanisms for mediating light‐dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors.Crossref | GoogleScholarGoogle Scholar |

Kneissl J, Shinomura T, Furuya M, Bolle C (2008) A rice phytochrome A in Arabidopsis: the role of the N-terminus under red and far-red light. Molecular Plant 1, 84–102.
A rice phytochrome A in Arabidopsis: the role of the N-terminus under red and far-red light.Crossref | GoogleScholarGoogle Scholar |

Kobayashi K, Masuda T (2016) Transcriptional regulation of tetrapyrrole biosynthesis in Arabidopsis thaliana. Frontiers in Plant Science 7, 1811–1828.
Transcriptional regulation of tetrapyrrole biosynthesis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Kreslavski VD, Los DA, Schmitt FJ, Zharmukhamedov SK, Kuznetsov VV, Allakhverdiev SI (2018) The impact of the phytochromes on photosynthetic processes. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1859, 400–408.
The impact of the phytochromes on photosynthetic processes.Crossref | GoogleScholarGoogle Scholar |

Lamparter T, Lutterbuse P, Schneider-Poetsch HAW, Hertel R (1992) A study of membrane-associated phytochrome: hydrophobicity test and native size determination. Photochemistry and Photobiology 56, 697–707.
A study of membrane-associated phytochrome: hydrophobicity test and native size determination.Crossref | GoogleScholarGoogle Scholar |

Lapko VN, Wells TA, Song PS (1996) Protein kinase A catalyzed phosphorylation and its effect on conformation in phytochrome A. Biochemistry 35, 6585–6594.
Protein kinase A catalyzed phosphorylation and its effect on conformation in phytochrome A.Crossref | GoogleScholarGoogle Scholar |

Lapko VN, Jiang XY, Smith DL, Song PS (1997) Posttranslational modification of oat phytochrome A: phosphorylation of a specific serine in a multiple serine cluster. Biochemistry 36, 10595–10599.
Posttranslational modification of oat phytochrome A: phosphorylation of a specific serine in a multiple serine cluster.Crossref | GoogleScholarGoogle Scholar |

Lapko VN, Jiang XY, Smith DL, Song PS (1999) Mass spectrometric characterization of oat phytochrome A: isoforms and posttranslational modifications. Protein Science 8, 1032–1044.
Mass spectrometric characterization of oat phytochrome A: isoforms and posttranslational modifications.Crossref | GoogleScholarGoogle Scholar |

Lariguet P, Boccalandro HE, Alonso JM, Ecker JR, Chory J, Casal JJ, Fankhauser C (2003) A growth regulatory loop that provides homeostasis to phytochrome A signaling. The Plant Cell 15, 2966–2978.
A growth regulatory loop that provides homeostasis to phytochrome A signaling.Crossref | GoogleScholarGoogle Scholar |

Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Current Opinion in Plant Biology 13, 571–577.
Plant hormone signaling lightens up: integrators of light and hormones.Crossref | GoogleScholarGoogle Scholar |

Lau OS, Deng XW (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends in Plant Science 17, 584–593.
The photomorphogenic repressors COP1 and DET1: 20 years later.Crossref | GoogleScholarGoogle Scholar |

Lee N, Choi G (2017) Phytochrome-interacting factor from Arabidopsis to liverwort. Current Opinion in Plant Biology 35, 54–60.
Phytochrome-interacting factor from Arabidopsis to liverwort.Crossref | GoogleScholarGoogle Scholar |

Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends in Plant Science 16, 19–28.
PIFs: pivotal components in a cellular signaling hub.Crossref | GoogleScholarGoogle Scholar |

Li FW, Melkonian M, Rothfels CJ, Villarreal JC, Stevenson DW, Graham SW, et al (2015) Phytochrome diversity in green plants and the origin of canonical plant phytochromes. Nature Communications 6, 7852

Li J, Li G, Wang H, Wang Deng X (2011) Phytochrome signaling mechanisms. The Arabidopsis book 9,
Phytochrome signaling mechanisms.Crossref | GoogleScholarGoogle Scholar |

Liu P, Sharrock RA (2017) Biological activity and dimerization state of modified phytochrome A proteins. PLoS One 12,
Biological activity and dimerization state of modified phytochrome A proteins.Crossref | GoogleScholarGoogle Scholar |

Long C, Iino M (2001) Light-dependent osmoregulation in pea stem protoplasts. Photoreceptors, tissue specificity, ion regulation, and physiological implications. Plant Physiology 125, 1854–1869.
Light-dependent osmoregulation in pea stem protoplasts. Photoreceptors, tissue specificity, ion regulation, and physiological implications.Crossref | GoogleScholarGoogle Scholar |

Mailliet J, Psakis G, Feilke K, Sineshchekov V, Essen LO, Hughes J (2011) Spectroscopy and a high-resolution crystal structure of Tyr263 mutants of cyanobacterial phytochrome Cph1. Journal of Molecular Biology 413, 115–127.
Spectroscopy and a high-resolution crystal structure of Tyr263 mutants of cyanobacterial phytochrome Cph1.Crossref | GoogleScholarGoogle Scholar |

McMichael RW, Lagarias JC (1990) Phosphopeptide mapping of Avena phytochrome phosphorylated by protein kinazes in vitro. Biochemistry 29, 3872–3878.
Phosphopeptide mapping of Avena phytochrome phosphorylated by protein kinazes in vitro.Crossref | GoogleScholarGoogle Scholar |

Nagy F, Schäfer E (2002) Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants. Annual Review of Plant Biology 53, 329–355.
Phytochromes control photomorphogenesis by differentially regulated, interacting signaling pathways in higher plants.Crossref | GoogleScholarGoogle Scholar |

Obrucheva NV (1983) ‘Physiology of roots.’ (Amerind Publishing Co.: New Delhi)

Okamoto H, Sakamoto K, Tomizawa K-I, Nagatani A, Wada M (1997) Photoresponses of transgenic Arabidopsis overexpressing the fern Adiantum capillus-veneris PHY1. Plant Physiology 115, 79–85.
Photoresponses of transgenic Arabidopsis overexpressing the fern Adiantum capillus-veneris PHY1.Crossref | GoogleScholarGoogle Scholar |

Oyama H, Yamamoto K, Wada M (1990) Phytochrome in the fern, Adiantum capillus-veneris L.: spectrophotometric detection in vivo and partial purification. Plant & Cell Physiology 31, 1229–1238.

Peters WS, Felle HH (1999) The correlation of profiles of surface pH and elongation growth in maize roots. Plant Physiology 121, 905–912.
The correlation of profiles of surface pH and elongation growth in maize roots.Crossref | GoogleScholarGoogle Scholar |

Possart A, Hiltbrunner A (2013) An evolutionarily conserved signaling mechanism mediates far-red light responses in land plants. The Plant Cell 25, 102–114.
An evolutionarily conserved signaling mechanism mediates far-red light responses in land plants.Crossref | GoogleScholarGoogle Scholar |

Possart A, Fleck C, Hiltbrunner A (2014) Shedding (far-red) light on phytochrome mechanisms and responses in land plants. Plant Science 217–218, 36–46.
Shedding (far-red) light on phytochrome mechanisms and responses in land plants.Crossref | GoogleScholarGoogle Scholar |

Pratt LH (1994) Distribution and localization of phytochrome within the plant. In ‘Photomorphogenesis in plants’. (2nd edn) (Eds RE Kendrick, GHM Kronenberg) pp. 163–186. (Kluver Academic Publishers: London)

Quail PH (1994) Phytochrome genes and their expression. (2nd edn) In ‘Photomorphogenesis in plants’. (Eds RE Kendrick, GHM Kronenberg) pp. 71–104. (Kluver Academic Publishers: Dordrecht, The Netherlands)

Riemann M, Müller A, Korte A, Furuya M, Weiler EW, Nick P (2003) Impaired induction of the jasmonate pathway in the rice mutant hebiba. PlantPphysiology 133, 1820–1830.

Riemann M, Bouyer D, Hisada A, Müller A, Yatou O, Weiler EW, et al (2009) Phytochrome A requires jasmonate for photodestruction. Planta 229, 1035–1045.

Rockwell NC, Su Y-S, Lagarias JC (2006) Phytochrome structure and signaling mechanism. Annual Review of Plant Biology 57, 837–858.
Phytochrome structure and signaling mechanism.Crossref | GoogleScholarGoogle Scholar |

Rösler J, Jaedicke K, Zeidler M (2010) Cytoplasmic phytochrome action. Plant & Cell Physiology 51, 1248–1254.
Cytoplasmic phytochrome action.Crossref | GoogleScholarGoogle Scholar |

Runge S, Sperling U, Frick G, Apel K, Armstrong GA (1996) Distinct roles for light-dependent NADPH: protochlorophillide oxidoreductases A and B during greening in higher plants. The Plant Journal 9, 513–523.
Distinct roles for light-dependent NADPH: protochlorophillide oxidoreductases A and B during greening in higher plants.Crossref | GoogleScholarGoogle Scholar |

Schäfer E, Nagy F (Eds.) (2006) Photomorphogenesis in plants and bacteria (3rd edn) In ‘Function and signal transduction mechanisms’. (Springer Science & Business Media: Dordrecht, The Netherlands)

Sharrock RA, Quail PH (1989) Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulator photoreceptor family. Genes & Development 3, 1745–1757.
Novel phytochrome sequences in Arabidopsis thaliana: structure, evolution, and differential expression of a plant regulator photoreceptor family.Crossref | GoogleScholarGoogle Scholar |

Sheen J (1993) Protein phosphatase activity is required for light inducible gene expression in maize. The EMBO Journal 12, 3497–3505.
Protein phosphatase activity is required for light inducible gene expression in maize.Crossref | GoogleScholarGoogle Scholar |

Sheerin DJ, Hiltbrunner A (2017) Molecular mechanisms and ecological function of far‐red light signalling. Plant, Cell & Environment 40, 2509–2529.
Molecular mechanisms and ecological function of far‐red light signalling.Crossref | GoogleScholarGoogle Scholar |

Sheerin DJ, Menon C, zur Oven-Krockhaus S, Enderle B, Zhu L, Johnen P, Schleifenbaum F, Stierhof YD, Huq E, Hiltbrunner A (2015) Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex. The Plant Cell 27, 189–201.
Light-activated phytochrome A and B interact with members of the SPA family to promote photomorphogenesis in Arabidopsis by reorganizing the COP1/SPA complex.Crossref | GoogleScholarGoogle Scholar |

Shen Y, Zhou Z, Feng S, Li J, Tan-Wilson A, Qu L-J, Wang H, Deng X-W (2009) Phytochrome A mediates rapid red light-induced phosphorylation of Arabidopsis FAR-RED ELONGATED HYPOCOTYL1 in low fluence response. The Plant Cell 21, 494–506.
Phytochrome A mediates rapid red light-induced phosphorylation of Arabidopsis FAR-RED ELONGATED HYPOCOTYL1 in low fluence response.Crossref | GoogleScholarGoogle Scholar |

Shin A-Y, Han Y-J, Baek A, Ahn T, Kim SY, Nguyen TS, Son M, Lee KW, Shen Y, Song P-S, Kim J-I (2016) Evidence that phytochrome functions as a protein kinase in plant light signaling. Nature Communications 7, 11545
Evidence that phytochrome functions as a protein kinase in plant light signaling.Crossref | GoogleScholarGoogle Scholar |

Shinomura T, Nagatani A, Hanzawa A, Kubota H, Watanabe M, Furuya M (1996) Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 93, 8129–8133.
Action spectra for phytochrome A- and B-specific photoinduction of seed germination in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Shinomura T, Hanzawa H, Schäfer E, Furuya M (1998) Mode of phytochrome B action in the photoregulation of seed germination in Arabidopsis thaliana. The Plant Journal 13, 583–590.
Mode of phytochrome B action in the photoregulation of seed germination in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Shlumukov LR, Barro F, Barcelo P, Lazzeri P, Smith H (2001) Establishment of far‐red high irradiance responses in wheat through transgenic expression of an oat phytochrome A gene. Plant, Cell & Environment 24, 703–712.

Sineshchekov VA (1994) Two spectroscopically and photochemically distinguishable phytochromes in etiolated seedlings of monocots and dicots. Photochemistry and Photobiology 59, 77–85.
Two spectroscopically and photochemically distinguishable phytochromes in etiolated seedlings of monocots and dicots.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA (1995a) Photobiophysics and photobiochemistry of the heterogeneous phytochrome system. Biochim. Biophys. Acta (BBA)-. Bioenergetics 1228, 125–164.
Photobiophysics and photobiochemistry of the heterogeneous phytochrome system.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA (1995b) Evidence for the existence of two phytochrome A populations. Journal of Photochemistry and Photobiology. B, Biology 28, 53–55.
Evidence for the existence of two phytochrome A populations.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V (2004) Phytochrome A: functional diversity and polymorphism. Photochemical & Photobiological Sciences 3, 596–607.
Phytochrome A: functional diversity and polymorphism.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA (2005) Polymorphism of phytochrome A and its functional implications. In ‘Light sensing in plants’. (Eds M Wada, K Shimazaki, M Iino) pp. 95–102. (Springer-Verlag: Tokyo, Japan)

Sineshchekov VA (2006) Extreme dehydration of plant tissues irreversibly converts the major and variable phyAʹ into the minor and conserved phyAʹʹ. Journal of Photochemistry and Photobiology. B, Biology 85, 85–91.
Extreme dehydration of plant tissues irreversibly converts the major and variable phyAʹ into the minor and conserved phyAʹʹ.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA (2010) Fluorescence and photochemical investigations of phytochrome in higher plants. Journal of Botany 2010,
Fluorescence and photochemical investigations of phytochrome in higher plants.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Fankhauser C (2004) PKS1 and PKS2 affect the phyA state in etiolated Arabidopsis seedlings. Photochemical & Photobiological Sciences 3, 608–611.

Sineshchekov VA, Rüdiger W (1992) Fluorescence spectroscopy of stable and labile phytochrome in stems and roots of etiolated cress seedlings. Photochemistry and Photobiology 56, 735–742.
Fluorescence spectroscopy of stable and labile phytochrome in stems and roots of etiolated cress seedlings.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Sineshchekov AV (1989) Fluorescence of phytochrome in the cells of dark-grown plants and its connection with the phototransformations of the pigment. Photochemistry and Photobiology 49, 325–330.
Fluorescence of phytochrome in the cells of dark-grown plants and its connection with the phototransformations of the pigment.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Sineshchekov AV (1990) Different photoactive states of the red phytochrome form in the cells of etiolated pea and oat seedlings. Journal of Photochemistry and Photobiology. B, Biology 5, 197–217.
Different photoactive states of the red phytochrome form in the cells of etiolated pea and oat seedlings.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Weller JL (2004) Two modes of the light-induced phytochrome A decline – with and without changes in the relative content of its native pools (phyAʹ and phyAʹʹ): evidence from in-situ fluorescence investigations of wild-type and mutant phyA-3D pea. Journal of Photochemistry and Photobiology. B, Biology 75, 127–135.
Two modes of the light-induced phytochrome A decline – with and without changes in the relative content of its native pools (phyAʹ and phyAʹʹ): evidence from in-situ fluorescence investigations of wild-type and mutant phyA-3D pea.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Lamparter T, Hartmann E (1994) Evidence for the existence of membrane‐associated phytochrome in the cell. Photochemistry and Photobiology 60, 516–520.
Evidence for the existence of membrane‐associated phytochrome in the cell.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Frances S, White MJ (1995) Fluorescence and photochemical characterization of phytochrome in de-etiolated pea mutant lip. Journal of Photochemistry and Photobiology. B, Biology 28, 47–51.
Fluorescence and photochemical characterization of phytochrome in de-etiolated pea mutant lip.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Heyer AG, Gatz C (1996) Phytochrome states in transgenic potato plants with altered phytochrome A levels. Journal of Photochemistry and Photobiology. B, Biology 34, 137–142.
Phytochrome states in transgenic potato plants with altered phytochrome A levels.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Ogorodnikova OB, Devlin PF, Whitelam GC (1998) Fluorescence spectroscopy and photochemistry of phytochromes A and B in wild-type, mutant and transgenic strains of Arabidopsis thaliana. Journal of Photochemistry and Photobiology. B, Biology 42, 133–142.
Fluorescence spectroscopy and photochemistry of phytochromes A and B in wild-type, mutant and transgenic strains of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Ogorodnikova OB, Weller JL (1999a) Fluorescence and photochemical properties of phytochromes A and B in etiolated pea seedlings. Journal of Photochemistry and Photobiology. B, Biology 49, 204–211.
Fluorescence and photochemical properties of phytochromes A and B in etiolated pea seedlings.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Clough RC, Jordan-Beebe ET, Vierstra RD (1999b) Fluorescence analysis of oat phyA deletion mutants expressed in tobacco suggests that the N-terminal domain determines the photochemical and spectroscopic distinctions between phyAʹ and phyA. Photochemistry and Photobiology 69, 728–732.

Sineshchekov V, Ogorodnikova O, Thiele A, Gatz C (2000a) Fluorescence and photochemical characterization of phytochromes A and B in transgenic potato expressing Arabidopsis phytochrome B. Journal of Photochemistry and Photobiology. B, Biology 59, 139–146.
Fluorescence and photochemical characterization of phytochromes A and B in transgenic potato expressing Arabidopsis phytochrome B.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Hughes J, Lamparter T, Zeidler M (2000b) Recombinant phytochrome of the moss Ceratodon purpureus (CP2): fluorescence spectroscopy and photochemistry. Journal of Photochemistry and Photobiology. B, Biology 56, 145–153.
Recombinant phytochrome of the moss Ceratodon purpureus (CP2): fluorescence spectroscopy and photochemistry.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Hennig L, Lamparter T, Hughes J, Gärtner W, Schäfer E (2001a) Recombinant phytochrome A in yeast differs by its spectroscopic and photochemical properties from the major phyAʹ and is close to the minor phyAʹʹ: evidence for post-translational modification of the pigment in plants. Photochemistry and Photobiology 73, 692–696.
Recombinant phytochrome A in yeast differs by its spectroscopic and photochemical properties from the major phyAʹ and is close to the minor phyAʹʹ: evidence for post-translational modification of the pigment in plants.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Koppel L, Shlumukov L, Barro F, Barcelo P, Lazzeri P, Smith H (2001b) Fluorescence and photochemical properties of phytochromes in wild-type wheat and a transgenic line over-expressing an oat phytochrome A (PHYA) gene: functional implications. Plant, Cell & Environment 24, 1289–1297.
Fluorescence and photochemical properties of phytochromes in wild-type wheat and a transgenic line over-expressing an oat phytochrome A (PHYA) gene: functional implications.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Belyaeva O, Sudnitsin A (2004a) Phytochrome A positively regulates biosynthesis of the active protochlorophyllide in dicots under far-red light. Journal of Photochemistry and Photobiology. B, Biology 74, 47–54.
Phytochrome A positively regulates biosynthesis of the active protochlorophyllide in dicots under far-red light.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Loskovich AV, Riemann M, Nick P (2004b) The jasmonate-free rice mutant hebiba is affected in the response of phyAʹ/phyAʹʹ pools and protochlorophyllide biosynthesis to far-red light. Photochemical & Photobiological Sciences 3, 1058–1062.
The jasmonate-free rice mutant hebiba is affected in the response of phyAʹ/phyAʹʹ pools and protochlorophyllide biosynthesis to far-red light.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Loskovich A, Inagaki N, Takano M (2006) Two native pools of phytochrome a in monocots: evidence from fluorescence investigations of phytochrome mutants of rice. Photochemistry and Photobiology 82, 1116–1122.
Two native pools of phytochrome a in monocots: evidence from fluorescence investigations of phytochrome mutants of rice.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Koppel L, Shor E, Kochetova G, Galland P, Zeidler M (2013) Protein phosphatase activity and acidic/alkaline balance as factors regulating the state of phytochrome A and its two native pools in the plant cell. Photochemistry and Photobiology 89, 83–96.
Protein phosphatase activity and acidic/alkaline balance as factors regulating the state of phytochrome A and its two native pools in the plant cell.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Mailliet J, Psakis G, Feilke K, Kopycki J, Zeidler M, Essen LO, Hughes J (2014a) Tyrosine 263 in cyanobacterial phytochrome C ph1 optimizes photochemistry at the prelumi‐R→ lumi‐R step. Photochemistry and Photobiology 90, 786–795.

Sineshchekov V, Sudnitsin A, Adam E, Schäfer E, Viczian A (2014b) phyA-GFP is spectroscopically and photochemically similar to phyA and comprises both its native types, phyAʹ and phyAʹʹ. Photochemical & Photobiological Sciences 13, 1671–1679.
phyA-GFP is spectroscopically and photochemically similar to phyA and comprises both its native types, phyAʹ and phyAʹʹ.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov V, Koppel L, Okamoto H, Wada M (2014c) Fern Adiantum capillus-veneris phytochrome 1 comprises two native photochemical types similar to seed plant phytochrome A. Journal of Photochemistry and Photobiology. B, Biology 130, 20–29.
Fern Adiantum capillus-veneris phytochrome 1 comprises two native photochemical types similar to seed plant phytochrome A.Crossref | GoogleScholarGoogle Scholar |

Sineshchekov VA, Koppel LA, Bolle C (2018) Two native types of phytochrome A, phyAʹ and phyAʹʹ, differ by the state of phosphorylation at the N-terminus as revealed by fluorescence investigations of the Ser/Ala mutant of rice phyA expressed in transgenic Arabidopsis. Functional Plant Biology 45, 150–159.
Two native types of phytochrome A, phyAʹ and phyAʹʹ, differ by the state of phosphorylation at the N-terminus as revealed by fluorescence investigations of the Ser/Ala mutant of rice phyA expressed in transgenic Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Smith H (1995) Physiological and ecological function within the phytochrome family. Annual Review of Plant Biology 46, 289–315.
Physiological and ecological function within the phytochrome family.Crossref | GoogleScholarGoogle Scholar |

Smith H (1997) Photomorphogenesis. Plant, Cell & Environment 20, 657–844.

Sokolova V, Bindics J, Kircher S, Ádám É, Schäfer E, Nagy F, Viczián A (2012) Missense mutation in the amino terminus of phytochrome A disrupts the nuclear import of the photoreceptor. Plant Physiology 158, 107–118.
Missense mutation in the amino terminus of phytochrome A disrupts the nuclear import of the photoreceptor.Crossref | GoogleScholarGoogle Scholar |

Song P-S (1999) Inter-domain signal transduction within the phytochromes. Journal of Biochemistry and Molecular Biology 32, 215–225.

Stockhaus J, Nagatani A, Halfter U, Kay S, Furuya M, Chua NH (1992) Serine-to-alanine substitutions at the amino-terminal region of phytochrome A result in an increase in biological activity. Genes & Development 6, 2364–2372.
Serine-to-alanine substitutions at the amino-terminal region of phytochrome A result in an increase in biological activity.Crossref | GoogleScholarGoogle Scholar |

Sullivan S, Hart JE, Rasch P, Walker CH, Christie JM (2016) Phytochrome A mediates blue-light enhancement of second-positive phototropism in Arabidopsis. Frontiers of Plant Science 7, 290
Phytochrome A mediates blue-light enhancement of second-positive phototropism in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Svyatyna K, Riemann M (2012) Light-dependent regulation of the jasmonate pathway. Protoplasma 249, 137–145.
Light-dependent regulation of the jasmonate pathway.Crossref | GoogleScholarGoogle Scholar |

Takano M, Inagaki N, Xie X, Yuzurihara N, Hihara F, Ishizuka T, Yano M, Nishimura M, Miyao A, Hirochika H, Shinomura T (2005) Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice. The Plant Cell 17, 3311–3325.
Distinct and cooperative functions of phytochromes A, B, and C in the control of deetiolation and flowering in rice.Crossref | GoogleScholarGoogle Scholar |

Terry MJ, Hall JL, Thomas B (1992) The association of type I phytochrome with wheat leaf plasma membranes. Plant Physiology 140, 691–698.
The association of type I phytochrome with wheat leaf plasma membranes.Crossref | GoogleScholarGoogle Scholar |

Tokuhisa JG, Daniels SM, Quail PH (1985) Phytochrome in green tissue: spectral and immunochemical evidence for two distinct molecular species of phytochrome in light-grown Avena sativa L. Planta 164, 321–332.
Phytochrome in green tissue: spectral and immunochemical evidence for two distinct molecular species of phytochrome in light-grown Avena sativa L.Crossref | GoogleScholarGoogle Scholar |

Trupkin A, Debrieux D, Hiltbrunner A, Fankhauser C, Casal JJ (2007) The serine-rich N-terminal region of Arabidopsis phytochrome A is required for protein stability. Plant Molecular Biology 63, 669–678.
The serine-rich N-terminal region of Arabidopsis phytochrome A is required for protein stability.Crossref | GoogleScholarGoogle Scholar |

Tsuboi H, Nakamura S, Schäfer E, Wada M (2012) Red light-induced phytochrome relocation into the nucleus in Adiantum capillus-veneris. Molecular Plant 5, 611–618.
Red light-induced phytochrome relocation into the nucleus in Adiantum capillus-veneris.Crossref | GoogleScholarGoogle Scholar |

Tu S-L, Lagarias JC (2005) ‘The phytochromes’. In ‘Handbook of photosensory receptors’. (Eds WR Briggs, JL Spudich) pp. 122–139. (Wiley-VCH Verlag Gmbh and Co. KgaA: Weinheim, Germany)

van Tuinen A, Kerckhoffs LHJ, Nagatani A, Kendrick RE, Koornneef M (1995) Far-red light-insensitive, phytochrome A-deficient mutants of tomato. Molecular and General Genetics 246, 133–141.
Far-red light-insensitive, phytochrome A-deficient mutants of tomato.Crossref | GoogleScholarGoogle Scholar |

Wang H, Wang H (2015) Phytochrome signaling: time to tighten up the loose ends. Molecular Plant 8, 540–551.
Phytochrome signaling: time to tighten up the loose ends.Crossref | GoogleScholarGoogle Scholar |

Wasternack C, Forner S, Strnad M, Hause B (2013) Jasmonates in flower and seed development. Biochimie 95, 79–85.
Jasmonates in flower and seed development.Crossref | GoogleScholarGoogle Scholar |

Weller JL, Batge SL, Smith JJ, Kerckhoffs LHJ, Sineshchekov VA, Murfet IC, Reid JB (2004) A dominant mutation in the pea PHYA gene confers enhanced responses to light and impairs the light-dependent degradation of phytochrome A. Plant Physiology 135, 2186–2195.
A dominant mutation in the pea PHYA gene confers enhanced responses to light and impairs the light-dependent degradation of phytochrome A.Crossref | GoogleScholarGoogle Scholar |

Yang Y, Linke M, von Haimberg T, Matute R, Gonzalez L, Schmider P, Heyne K (2014) Active and silent chromophore isoforms for phytochrome Pr photoisomerizaton: an alternative evolutionary strategy to optimize photoreaction quantum yields. Structure and Dynamics 1,
Active and silent chromophore isoforms for phytochrome Pr photoisomerizaton: an alternative evolutionary strategy to optimize photoreaction quantum yields.Crossref | GoogleScholarGoogle Scholar |

Yeh KC, Lagarias JC (1998) Eukaryotic phytochromes: light-regulated serine/threonine protein kinazes with histidine kinaze ancestry. Proceedings of the National Academy of Sciences of the United States of America 95, 13976–13981.
Eukaryotic phytochromes: light-regulated serine/threonine protein kinazes with histidine kinaze ancestry.Crossref | GoogleScholarGoogle Scholar |

Zhou Q, Hare PD, Yang SW, Zeidler M, Huang L-F, Chua N-H (2005) FHL is required for full phytochrome signaling and shared overlapping functions with FHY1. The Plant Journal 43, 356–370.
FHL is required for full phytochrome signaling and shared overlapping functions with FHY1.Crossref | GoogleScholarGoogle Scholar |