Differential phosphorylation of the N-terminal extension regulates phytochrome B signaling.
dark reversion
phosphorylation
phyB NTE
phytochrome
thermal reversion
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
02 2020
02 2020
Historique:
received:
17
07
2019
accepted:
24
09
2019
pubmed:
10
10
2019
medline:
10
4
2021
entrez:
10
10
2019
Statut:
ppublish
Résumé
Phytochrome B (phyB) is an excellent light quality and quantity sensor that can detect subtle changes in the light environment. The relative amounts of the biologically active photoreceptor (phyB Pfr) are determined by the light conditions and light independent thermal relaxation of Pfr into the inactive phyB Pr, termed thermal reversion. Little is known about the regulation of thermal reversion and how it affects plants' light sensitivity. In this study we identified several serine/threonine residues on the N-terminal extension (NTE) of Arabidopsis thaliana phyB that are differentially phosphorylated in response to light and temperature, and examined transgenic plants expressing nonphosphorylatable and phosphomimic phyB mutants. The NTE of phyB is essential for thermal stability of the Pfr form, and phosphorylation of S86 particularly enhances the thermal reversion rate of the phyB Pfr-Pr heterodimer in vivo. We demonstrate that S86 phosphorylation is especially critical for phyB signaling compared with phosphorylation of the more N-terminal residues. Interestingly, S86 phosphorylation is reduced in light, paralleled by a progressive Pfr stabilization under prolonged irradiation. By investigating other phytochromes (phyD and phyE) we provide evidence that acceleration of thermal reversion by phosphorylation represents a general mechanism for attenuating phytochrome signaling.
Substances chimiques
Apoproteins
0
Arabidopsis Proteins
0
PHYE protein, Arabidopsis
0
Phytochrome
11121-56-5
Phytochrome B
136250-22-1
PHYD protein, Arabidopsis
158379-16-9
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1635-1650Informations de copyright
© 2019 The Authors. New Phytologist © 2019 New Phytologist Trust.
Références
Ádám É, Hussong A, Bindics J, Wüst F, Viczián A, Essing M, Medzihradszky M, Kircher S, Schäfer E, Nagy F. 2011. Altered dark- and photoconversion of phytochrome B mediate extreme light sensitivity and loss of photoreversibility of the phyB-401 mutant. PLoS ONE 6: e27250.
Ádám É, Kircher S, Liu P, Mérai Z, González-Schain N, Hörner M, Viczián A, Monte E, Sharrock RA, Schäfer E et al. 2013. Comparative functional analysis of full-length and N-terminal fragments of phytochrome C, D and E in red light-induced signaling. New Phytologist 200: 86-96.
Burgie ES, Bussell AN, Lye S-H, Wang T, Hu W, McLoughlin KE, Weber EL, Li H, Vierstra RD. 2017. Photosensing and thermosensing by phytochrome B require both proximal and distal allosteric features within the dimeric photoreceptor. Scientific Reports 7: 13648.
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, USA 111: 10179-10184.
Chen M, Tao Y, Lim J, Shaw A, Chory J. 2005. Regulation of phytochrome B nuclear localization through light-dependent unmasking of nuclear-localization signals. Current Biology 15: 637-642.
Chen Z, Cole PA. 2015. Synthetic approaches to protein phosphorylation. Current Opinion in Chemical Biology 28: 115-122.
Clough SJ, Bent AF. 1998. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal 16: 735-743.
Enderle B, Sheerin DJ, Paik I, Kathare PK, Schwenk P, Klose C, Ulbrich MH, Huq E, Hiltbrunner A. 2017. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nature Communications 8: 2221.
Frosch S, Jabben M, Bergfeld R, Kleinig H, Mohr H. 1979. Inhibition of carotenoid biosynthesis by the herbicide SAN 9789 and its consequences for the action of phytochrome on plastogenesis. Planta 145: 497-505.
Halliday KJ, Whitelam GC. 2003. Changes in photoperiod or temperature alter the functional relationships between phytochromes and reveal roles for phyD and phyE. Plant Physiology 131: 1913-1920.
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.
Honda M, Okuno Y, Yoo J, Ha T, Spies M. 2011. Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding. EMBO Journal 30: 3368-3382.
von Horsten S, Straß S, Hellwig N, Gruth V, Klasen R, Mielcarek A, Linne U, Morgner N, Essen L-O. 2016. Mapping light-driven conformational changes within the photosensory module of plant phytochrome B. Scientific Reports 6: 34366.
Huang H, McLoughlin KE, Sorkin ML, Burgie ES, Bindbeutel RK, Vierstra RD, Nusinow DA. 2019. PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis. Proceedings of the National Academy of Sciences, USA 116: 8603-8608.
Huang H, Yoo CY, Bindbeutel R, Goldsworthy J, Tielking A, Alvarez S, Naldrett MJ, Evans BS, Chen M, Nusinow DA. 2016. PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis. eLife 5: e13292.
Jabben M, Deitzer GF. 1978. A method for measuring phytochrome in plants grown in white light. Photochemistry and Photobiology 27: 799-802.
Jabben M, Deitzer GF. 1979. Effects of the herbicide san 9789 on photomorphogenic responses. Plant Physiology 63: 481-485.
Jung J-H, Domijan M, Klose C, Biswas S, Ezer D, Gao M, Khattak AK, Box MS, Charoensawan V, Cortijo S et al. 2016. Phytochromes function as thermosensors in Arabidopsis. Science 354: 886-889.
Kikis EA, Oka Y, Hudson ME, Nagatani A, Quail PH. 2009. Residues clustered in the light-sensing knot of phytochrome B are necessary for conformer-specific binding to signaling partner PIF3. PLOS Genetics 5: e1000352.
Kim D-H, Kang J-G, Yang S-S, Chung K-S, Song P-S, Park C-M. 2002. A phytochrome-associated protein phosphatase 2A modulates light signals in flowering time control in Arabidopsis. Plant cell 14: 3043-3056.
Kircher S, Gil P, Kozma-Bognár L, Fejes E, Speth V, Husselstein-Muller T, Bauer D, Adám E, Schäfer E, Nagy F. 2002. Nucleocytoplasmic partitioning of the plant photoreceptors phytochrome A, B, C, D, and E is regulated differentially by light and exhibits a diurnal rhythm. Plant Cell 14: 1541-1555.
Klement E, Gyula P, Viczián A. 2019. Detection of phytochrome phosphorylation in plants. Methods in Molecular Biology 2026: 41-67.
Klose C. 2019. In vivo spectroscopy. Methods in Molecular Biology 2026: 113-120.
Klose C, Venezia F, Hussong A, Kircher S, Schafer E, Fleck C. 2015. Systematic analysis of how phytochrome B dimerization determines its specificity. Nature Plants 1: 15090.
Kretsch T, Poppe C, Schäfer E. 2000. A new type of mutation in the plant photoreceptor phytochrome B causes loss of photoreversibility and an extremely enhanced light sensitivity. The Plant Journal 22: 177-186.
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.
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.
Legris M, Klose C, Burgie ES, Rojas CCR, Neme M, Hiltbrunner A, Wigge PA, Schäfer E, Vierstra RD, Casal JJ. 2016. Phytochrome B integrates light and temperature signals in Arabidopsis. Science 354: 897-900.
McMichael RW, Lagarias JC. 1990. Phosphopeptide mapping of Avena phytochrome phosphorylated by protein kinases in vitro. Biochemistry 29: 3872-3878.
Medzihradszky M, Bindics J, Ádám É, Viczián A, Klement É, Lorrain S, Gyula P, Mérai Z, Fankhauser C, Medzihradszky KF et al. 2013. Phosphorylation of phytochrome B inhibits light-induced signaling via accelerated dark reversion in Arabidopsis. Plant Cell 25: 535-544.
Nagatani A. 2010. Phytochrome: structural basis for its functions. Current Opinion in Plant Biology 13: 565-570.
Nito K, Wong CC, Yates JR, Chory J. 2013. Tyrosine phosphorylation regulates the activity of phytochrome photoreceptors. Cell Reports 3: 1970-1979.
Phee B-K, Kim J-I, Shin DH, Yoo J, Park K-J, Han Y-J, Kwon Y-K, Cho M-H, Jeon J-S, Bhoo SH et al. 2008. A novel protein phosphatase indirectly regulates phytochrome-interacting factor 3 via phytochrome. The Biochemical journal 415: 247-255.
Qiu Y, Pasoreck EK, Reddy AK, Nagatani A, Ma W, Chory J, Chen M. 2017. Mechanism of early light signaling by the carboxy-terminal output module of Arabidopsis phytochrome B. Nature Communications 8: 1905.
Quail PH. 2002. Phytochrome photosensory signalling networks. Nature Reviews Molecular Cell Biology 3: 85-93.
Rausenberger J, Hussong A, Kircher S, Kirchenbauer D, Timmer J, Nagy F, Schäfer E, Fleck C. 2010. An integrative model for phytochrome B mediated photomorphogenesis: from protein dynamics to physiology. PLoS ONE 5: e10721.
Reed JW, Nagatani A, Elich TD, Fagan M, Chory J. 1994. Phytochrome A and phytochrome B have overlapping but distinct functions in Arabidopsis development. Plant Physiology 104: 1139-1149.
Reed JW, Nagpal P, Poole DS, Furuya M, Chory J. 1993. Mutations in the gene for the red/far-red light receptor phytochrome B alter cell elongation and physiological responses throughout Arabidopsis development. Plant Cell 5: 147-157.
Rockwell NC, Su Y-S, Lagarias JC. 2006. Phytochrome structure and signaling mechanisms. Annual Review of Plant Biology 57: 837-858.
Ryu JS, Kim J-I, Kunkel T, Kim BC, Cho DS, Hong SH, Kim S-H, Fernández AP, Kim Y, Alonso JM et al. 2005. Phytochrome-specific type 5 phosphatase controls light signal flux by enhancing phytochrome stability and affinity for a signal transducer. Cell 120: 395-406.
Sánchez-Lamas M, Lorenzo CD, Cerdán PD. 2016. Bottom-up assembly of the phytochrome network. PLOS Genetics 12: e1006413.
Sellaro R, Smith RW, Legris M, Fleck C, Casal JJ. 2019. Phytochrome B dynamics departs from photoequilibrium in the field. Plant, Cell & Environment 42: 606-617.
Shin A-Y, Han Y-J, Baek A, Ahn T, Kim SY, Nguyen TS, Son M, Lee KW, Shen Y, Song P-S et al. 2016. Evidence that phytochrome functions as a protein kinase in plant light signalling. Nature Communications 7: 11545.
Smith H. 2000. Phytochromes and light signal perception by plants-an emerging synthesis. Nature 407: 585-591.
Sweere U, Eichenberg K, Lohrmann J, Mira-Rodado V, Bäurle I, Kudla J, Nagy F, Schafer E, Harter K. 2001. Interaction of the response regulator ARR4 with phytochrome B in modulating red light signaling. Science 294: 1108-1111.
Velázquez Escobar F, Buhrke D, Fernandez Lopez M, Shenkutie SM, von Horsten S, Essen L-O, Hughes J, Hildebrandt P. 2017. Structural communication between the chromophore-binding pocket and the N-terminal extension in plant phytochrome phyB. FEBS letters 591: 1258-1265.
Viczián A, Klose C, Ádám É, Nagy F. 2017. New insights of red light-induced development. Plant, Cell & Environment 40: 2457-2468.
Wagner D, Tepperman JM, Quail PH. 1991. Overexpression of phytochrome B induces a short hypocotyl phenotype in transgenic Arabidopsis. Plant Cell 3: 1275-1288.
Yamaguchi R, Nakamura M, Mochizuki N, Kay SA, Nagatani A. 1999. Light-dependent translocation of a phytochrome B-GFP fusion protein to the nucleus in transgenic Arabidopsis. Journal of Cell Biology 145: 437-445.
Yeh KC, Lagarias JC. 1998. Eukaryotic phytochromes: light-regulated serine/threonine protein kinases with histidine kinase ancestry. Proceedings of the National Academy of Sciences, USA 95: 13976-13981.
Zhang S, Li C, Zhou Y, Wang X, Li H, Feng Z, Chen H, Qin G, Jin D, Terzaghi W et al. 2018. TANDEM ZINC-FINGER/PLUS3 is a key component of phytochrome A signaling. Plant Cell 30: 835-852.
Zhou Y, Yang L, Duan J, Cheng J, Shen Y, Wang X, Han R, Li H, Li Z, Wang L et al. 2018. Hinge region of Arabidopsis phyA plays an important role in regulating phyA function. Proceedings of the National Academy of Sciences, USA 115: E11864-E11873.