Abstract
Main conclusion
In this review we focus on the role of SPA proteins in light signalling and discuss different aspects, including molecular mechanisms, specificity, and evolution.
The ability of plants to perceive and respond to their environment is key to their survival under ever-changing conditions. The abiotic factor light is of particular importance for plants. Light provides plants energy for carbon fixation through photosynthesis, but also is a source of information for the adaptation of growth and development to the environment. Cryptochromes and phytochromes are major photoreceptors involved in control of developmental decisions in response to light cues, including seed germination, seedling de-etiolation, and induction of flowering. The SPA protein family acts in complex with the E3 ubiquitin ligase COP1 to target positive regulators of light responses for degradation by the 26S proteasome to suppress photomorphogenic development in darkness. Light-activated cryptochromes and phytochromes both repress the function of COP1, allowing accumulation of positive photomorphogenic factors in light. In this review, we highlight the role of the SPA proteins in this process and discuss recent advances in understanding how SPAs link light-activation of photoreceptors and downstream signaling.
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References
Alabadí D, Gallego-Bartolomé J, Orlando L et al (2008) Gibberellins modulate light signaling pathways to prevent Arabidopsis seedling de-etiolation in darkness. Plant J 53:324–335. doi:10.1111/j.1365-313X.2007.03346.x
Al-Sady B, Ni W, Kircher S et al (2006) Photoactivated phytochrome induces rapid PIF3 phosphorylation prior to proteasome-mediated degradation. Mol Cell 23:439–446. doi:10.1016/j.molcel.2006.06.011
Balcerowicz M, Fittinghoff K, Wirthmueller L et al (2011) Light exposure of Arabidopsis seedlings causes rapid de-stabilization as well as selective post-translational inactivation of the repressor of photomorphogenesis SPA2. Plant J 65:712–723. doi:10.1111/j.1365-313X.2010.04456.x
Bauer D, Viczián A, Kircher S et al (2004) CONSTITUTIVE PHOTOMORPHOGENESIS 1 and multiple photoreceptors control degradation of PHYTOCHROME INTERACTING FACTOR 3, a transcription factor required for light signaling in Arabidopsis. Plant Cell 16:1433–1445. doi:10.1105/tpc.021568
Baumgardt RL, Oliverio KA, Casal JJ, Hoecker U (2002) SPA1, a component of phytochrome A signal transduction, regulates the light signaling current. Planta 215:745–753. doi:10.1007/s00425-002-0801-x
Boccalandro HE, Rossi MC, Saijo Y et al (2004) Promotion of photomorphogenesis by COP1. Plant Mol Biol 56:905–915. doi:10.1007/s11103-004-5919-8
Botto JF, Sanchez RA, Whitelam GC, Casal JJ (1996) Phytochrome A mediates the promotion of seed germination by very low fluences of light and canopy shade light in Arabidopsis. Plant Physiol 110:439–444. doi:10.1104/pp.110.2.439
Bou-Torrent J, Toledo-Ortiz G, Ortiz-Alcaide M et al (2015) Regulation of carotenoid biosynthesis by shade relies on specific subsets of antagonistic transcription factors and co-factors. Plant Physiol 169:1584–1594. doi:10.1104/pp.15.00552
Cao D, Lin Y, Cheng CL (2000) Genetic interactions between the chlorate-resistant mutant cr88 and the photomorphogenic mutants cop1 and hy5. Plant Cell 12:199–210. doi:10.1105/tpc.12.2.199
Casal JJ (2012) Shade avoidance. Arabidopsis Book 10:e0157. doi:10.1199/tab.0157
Casal JJ (2013) Photoreceptor signaling networks in plant responses to shade. Annu Rev Plant Biol 64:403–427. doi:10.1146/annurev-arplant-050312-120221
Casson S, Franklin KA, Gray JE et al (2009) Phytochrome B and PIF4 regulate stomatal development in response to light quantity. Curr Biol 19:229–234. doi:10.1016/j.cub.2008.12.046
Catalá R, Medina J, Salinas J (2011) Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci USA 108:16475–16480. doi:10.1073/pnas.1107161108
Chang C-SJ, Maloof JN, Wu S-H (2011) COP1-mediated degradation of BBX22/LZF1 optimizes seedling development in Arabidopsis. Plant Physiol 156:228–239. doi:10.1104/pp.111.175042
Chaves I, Pokorny R, Byrdin M et al (2011) The cryptochromes: blue light photoreceptors in plants and animals. Annu Rev Plant Biol 62:335–364. doi:10.1146/annurev-arplant-042110-103759
Chen H, Huang X, Gusmaroli G et al (2010) Arabidopsis CULLIN4-DAMAGED DNA BINDING PROTEIN 1 interacts with CONSTITUTIVELY PHOTOMORPHOGENIC1-SUPPRESSOR OF PHYA complexes to regulate photomorphogenesis and flowering time. Plant Cell 22:108–123. doi:10.1105/tpc.109.065490
Chen A, Li C, Hu W et al (2014) PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod. Proc Natl Acad Sci 111:10037–10044. doi:10.1073/pnas.1409795111
Chen S, Lory N, Stauber J, Hoecker U (2015) Photoreceptor specificity in the light-induced and COP1-mediated rapid degradation of the repressor of photomorphogenesis SPA2 in Arabidopsis. PLoS Genet 11:e1005516. doi:10.1371/journal.pgen.1005516
Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58:21–45. doi:10.1146/annurev.arplant.58.032806.103951
Christie JM, Arvai AS, Baxter KJ et al (2012) Plant UVR8 photoreceptor senses UV-B by tryptophan-mediated disruption of cross-dimer salt bridges. Science 335:1492–1497. doi:10.1126/science.1218091
Christie JM, Blackwood L, Petersen J, Sullivan S (2015) Plant flavoprotein photoreceptors. Plant Cell Physiol 56:401–413. doi:10.1093/pcp/pcu196
de Wit M, Lorrain S, Fankhauser C (2014) Auxin-mediated plant architectural changes in response to shade and high temperature. Physiol Plant 151:13–24. doi:10.1111/ppl.12099
Debrieux D, Trevisan M, Fankhauser C (2013) Conditional involvement of CONSTITUTIVE PHOTOMORPHOGENIC 1 in the degradation of phytochrome A. Plant Physiol 161:2136–2145. doi:10.1104/pp.112.213280
Deng XW, Caspar T, Quail PH (1991) COP1: a regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev 5:1172–1182. doi:10.1101/gad.5.7.1172
Deng XW, Matsui M, Wei N et al (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71:791–801. doi:10.1016/0092-8674(92)90555-Q
Dong J, Tang D, Gao Z et al (2014) Arabidopsis DE-ETIOLATED1 represses photomorphogenesis by positively regulating PHYTOCHROME INTERACTING FACTORs in the dark. Plant Cell. doi:10.1105/tpc.114.130666
Duek PD, Elmer MV, van Oosten VR, Fankhauser C (2004) The degradation of HFR1, a putative bHLH class transcription factor involved in light signaling, is regulated by phosphorylation and requires COP1. Curr Biol 14:2296–2301. doi:10.1016/j.cub.2004.12.026
Fankhauser C, Christie JMM (2015) Plant phototropic growth. Curr Biol 25:R384–R389. doi:10.1016/j.cub.2015.03.020
Favory J-J, Stec A, Gruber H et al (2009) Interaction of COP1 and UVR8 regulates UV-B-induced photomorphogenesis and stress acclimation in Arabidopsis. EMBO J 28:591–601. doi:10.1038/emboj.2009.4
Fittinghoff K, Laubinger S, Nixdorf M et al (2006) Functional and expression analysis of Arabidopsis SPA genes during seedling photomorphogenesis and adult growth. Plant J 47:577–590. doi:10.1111/j.1365-313X.2006.02812.x
Franklin KA, Davis SJ, Stoddart WM et al (2003a) Mutant analyses define multiple roles for phytochrome C in Arabidopsis photomorphogenesis. Plant Cell 15:1981–1989. doi:10.1105/tpc.015164
Franklin KA, Praekelt U, Stoddart WM et al (2003b) Phytochromes B, D, and E act redundantly to control multiple physiological responses in Arabidopsis. Plant Physiol 131:1340–1346. doi:10.1104/pp.102.015487
Franklin KA, Lee SHH, Patel D et al (2011) PHYTOCHROME-INTERACTING FACTOR 4 (PIF4) regulates auxin biosynthesis at high temperature. Proc Natl Acad Sci USA 108:20231–20235. doi:10.1073/pnas.1110682108
Gangappa SN, Crocco CD, Johansson H et al (2013) The Arabidopsis B-BOX protein BBX25 interacts with HY5, negatively regulating BBX22 expression to suppress seedling photomorphogenesis. Plant Cell 25:1243–1257. doi:10.1105/tpc.113.109751
Hardtke CS, Gohda K, Osterlund MT et al (2000) HY5 stability and activity in Arabidopsis is regulated by phosphorylation in its COP1 binding domain. EMBO J 19:4997–5006. doi:10.1093/emboj/19.18.4997
Heijde M, Binkert M, Yin R et al (2013) Constitutively active UVR8 photoreceptor variant in Arabidopsis. Proc Natl Acad Sci USA 110:20326–20331. doi:10.1073/pnas.1314336110
Hennig L, Stoddart WM, Dieterle M et al (2002) Phytochrome E controls light-induced germination of Arabidopsis. Plant Physiol 128:194–200. doi:10.1104/pp.010559
Hoecker U, Quail PH (2001) The phytochrome A-specific signaling intermediate SPA1 interacts directly with COP1, a constitutive repressor of light signaling in Arabidopsis. J Biol Chem 276:38173–38178. doi:10.1074/jbc.M103140200
Hoecker U, Xu Y, Quail PH (1998) SPA1: a new genetic locus involved in phytochrome A-specific signal transduction. Plant Cell 10:19–33. doi:10.1105/tpc.10.1.19
Hoecker U, Tepperman JM, Quail PH (1999) SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science 284:496–499. doi:10.1126/science.284.5413.496
Holm M, Ma L-G, Qu L-J, Deng X-W (2002) Two interacting bZIP proteins are direct targets of COP1-mediated control of light-dependent gene expression in Arabidopsis. Genes Dev 16:1247–1259. doi:10.1101/gad.969702
Hornitschek P, Lorrain S, Zoete V et al (2009) Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28:3893–3902. doi:10.1038/emboj.2009.306
Hornitschek P, Kohnen MV, Lorrain S et al (2012) Phytochrome interacting factors 4 and 5 control seedling growth in changing light conditions by directly controlling auxin signaling. Plant J 71:699–711. doi:10.1111/j.1365-313X.2012.05033.x
Hotton SK, Callis J (2008) Regulation of cullin RING ligases. Annu Rev Plant Biol 59:467–489. doi:10.1146/annurev.arplant.58.032806.104011
Huang X, Ouyang X, Yang P et al (2013) Conversion from CUL4-based COP1–SPA E3 apparatus to UVR8–COP1–SPA complexes underlies a distinct biochemical function of COP1 under UV-B. Proc Natl Acad Sci 110:16669–16674. doi:10.1073/pnas.1316622110
Huang X, Ouyang X, Deng XW (2014) Beyond repression of photomorphogenesis: role switching of COP/DET/FUS in light signaling. Curr Opin Plant Biol 21:96–103. doi:10.1016/j.pbi.2014.07.003
Indorf M, Cordero J, Neuhaus G, Rodríguez-Franco M (2007) SALT TOLERANCE (STO), a stress-related protein, has a major role in light signalling. Plant J 51:563–574. doi:10.1111/j.1365-313X.2007.03162.x
Ishikawa M, Kiba T, Chua NH (2006) The Arabidopsis SPA1 gene is required for circadian clock function and photoperiodic flowering. Plant J 46:736–746. doi:10.1111/j.1365-313X.2006.02737.x
Ito S, Song YH, Imaizumi T (2012) LOV domain-containing F-box proteins: light-dependent protein degradation modules in Arabidopsis. Mol Plant 5:573–582. doi:10.1093/mp/sss013
Jang I-C, Yang J-Y, Seo HS, Chua N-H (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev 19:593–602. doi:10.1101/gad.1247205
Jang S, Marchal V, Panigrahi KCS et al (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J 27:1277–1288. doi:10.1038/emboj.2008.68
Jang I-C, Henriques R, Seo HS et al (2010) Arabidopsis PHYTOCHROME INTERACTING FACTOR proteins promote phytochrome B polyubiquitination by COP1 E3 ligase in the nucleus. Plant Cell 22:2370–2383. doi:10.1105/tpc.109.072520
Jang K, Gil Lee H, Jung S-J et al (2015) The E3 ubiquitin ligase COP1 regulates thermosensory flowering by triggering GI degradation in Arabidopsis. Sci Rep 5:12071. doi:10.1038/srep12071
Jenkins GI (2014) The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell 26:21–37. doi:10.1105/tpc.113.119446
Jiao Y, Ma L, Strickland E, Deng XW (2005) Conservation and divergence of light-regulated genome expression patterns during seedling development in rice and Arabidopsis. Plant Cell 17:3239–3256. doi:10.1105/tpc.105.035840
Johnson E, Bradley M, Harberd NP, Whitelam GC (1994) Photoresponses of light-grown phyA mutants of Arabidopsis: phytochrome A is required for the perception of daylength extensions. Plant Physiol 105:141–149. doi:10.1104/pp.105.1.141
Kaiserli E, Jenkins GI (2007) UV-B promotes rapid nuclear translocation of the Arabidopsis UV-B specific signaling component UVR8 and activates its function in the nucleus. Plant Cell 19:2662–2673. doi:10.1105/tpc.107.053330
Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Top Dev Biol 91:29–66. doi:10.1016/S0070-2153(10)91002-8
Klose C, Viczián A, Kircher S et al (2015) Molecular mechanisms for mediating light-dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors. New Phytol 206:965–971. doi:10.1111/nph.13207
Koini MA, Alvey L, Allen T et al (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413. doi:10.1016/j.cub.2009.01.046
Lau OS, Deng XW (2010) Plant hormone signaling lightens up: integrators of light and hormones. Curr Opin Plant Biol 13:571–577. doi:10.1016/j.pbi.2010.07.001
Lau OS, Deng XW (2012) The photomorphogenic repressors COP1 and DET1: 20 years later. Trends Plant Sci 17:584–593. doi:10.1016/j.tplants.2012.05.004
Laubinger S, Hoecker U (2003) The SPA1-like proteins SPA3 and SPA4 repress photomorphogenesis in the light. Plant J 35:373–385. doi:10.1046/j.1365-313X.2003.01813.x
Laubinger S, Fittinghoff K, Hoecker U (2004) The SPA quartet: a family of WD-repeat proteins with a central role in suppression of photomorphogenesis in Arabidopsis. Plant Cell 16:2293–2306. doi:10.1105/tpc.104.024216
Laubinger S, Marchal V, Le Gourrierec J et al (2006) Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 133:3213–3222. doi:10.1242/dev.02481
Leivar P, Monte E (2014) PIFs: systems integrators in plant development. Plant Cell 26:56–78. doi:10.1105/tpc.113.120857
Leivar P, Quail PH (2011) PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci 16:19–28. doi:10.1016/j.tplants.2010.08.003
Leivar P, Monte E, Oka Y et al (2008) Multiple phytochrome-interacting bHLH transcription factors repress premature seedling photomorphogenesis in darkness. Curr Biol 18:1815–1823. doi:10.1016/j.cub.2008.10.058
Leivar P, Tepperman JM, Monte E et al (2009) Definition of early transcriptional circuitry involved in light-induced reversal of PIF-imposed repression of photomorphogenesis in young Arabidopsis seedlings. Plant Cell 21:3535–3553. doi:10.1105/tpc.109.070672
Leivar P, Monte E, Cohn MM, Quail PH (2012) Phytochrome signaling in green Arabidopsis seedlings: impact assessment of a mutually negative phyB-PIF feedback loop. Mol Plant 5:734–749. doi:10.1093/mp/sss031
Li J, Li G, Wang H, Wang Deng X (2011) Phytochrome signaling mechanisms. Arabidopsis Book 9:e0148. doi:10.1199/tab.0148
Li L, Ljung K, Breton G et al (2012) Linking photoreceptor excitation to changes in plant architecture. Genes Dev 26:785–790. doi:10.1101/gad.187849.112
Li F, Sun J, Wang D et al (2014) The B-box family gene STO (BBX24) in Arabidopsis thaliana regulates flowering time in different pathways. PLoS One 9:e87544. doi:10.1371/journal.pone.0087544
Lian H-L, He S-B, Zhang Y-C et al (2011) Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism. Genes Dev 25:1023–1028. doi:10.1101/gad.2025111
Lin C, Yang H, Guo H et al (1998) Enhancement of blue-light sensitivity of Arabidopsis seedlings by a blue light receptor cryptochrome 2. Proc Natl Acad Sci USA 95:2686–2690. doi:10.1073/pnas.95.5.2686
Liu H, Yu X, Li K et al (2008a) Photoexcited CRY2 interacts with CIB1 to regulate transcription and floral initiation in Arabidopsis. Science 322:1535–1539. doi:10.1126/science.1163927
Liu L-J, Zhang Y-C, Li Q-H et al (2008b) COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20:292–306. doi:10.1105/tpc.107.057281
Liu B, Zuo Z, Liu H et al (2011a) Arabidopsis cryptochrome 1 interacts with SPA1 to suppress COP1 activity in response to blue light. Genes Dev 25:1029–1034. doi:10.1101/gad.2025011
Liu H, Liu B, Zhao C et al (2011b) The action mechanisms of plant cryptochromes. Trends Plant Sci 16:684–691. doi:10.1016/j.tplants.2011.09.002
Liu Y, Li X, Li K et al (2013) Multiple bHLH proteins form heterodimers to mediate CRY2-dependent regulation of flowering-time in Arabidopsis. PLoS Genet 9:e1003861. doi:10.1371/journal.pgen.1003861
Lorrain S, Trevisan M, Pradervand S, Fankhauser C (2009) PHYTOCHROME INTERACTING FACTORs 4 and 5 redundantly limit seedling de-etiolation in continuous far-red light. Plant J 60:449–461. doi:10.1111/j.1365-313X.2009.03971.x
Lu X-D, Zhou C-M, Xu P-B et al (2015) Red-light-dependent interaction of phyB with SPA1 promotes COP1–SPA1 dissociation and photomorphogenic development in Arabidopsis. Mol Plant 8:467–478. doi:10.1016/j.molp.2014.11.025
Luo X-M, Lin W-H, Zhu S et al (2010) Integration of light- and brassinosteroid-signaling pathways by a GATA transcription factor in Arabidopsis. Dev Cell 19:872–883. doi:10.1016/j.devcel.2010.10.023
Ma L, Li J, Qu L et al (2001) Light control of Arabidopsis development entails coordinated regulation of genome expression and cellular pathways. Plant Cell 13:2589–2607. doi:10.1105/tpc.010229
Ma L, Gao Y, Qu L et al (2002) Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell 14:2383–2398. doi:10.1105/tpc.004416
Maier A, Schrader A, Kokkelink L et al (2013) Light and the E3 ubiquitin ligase COP1/SPA control the protein stability of the MYB transcription factors PAP1 and PAP2 involved in anthocyanin accumulation in Arabidopsis. Plant J 74:638–651. doi:10.1111/tpj.12153
Mancinelli AL (1994) The physiology of phytochrome action. In: Kendrick RE, Kronenberg GHM (eds) Photomorphogenesis in Plants, 2nd edn. Kluwer Academic Publishers, Dordrecht, pp 211–269
Mathews S (2006) Phytochrome-mediated development in land plants: red light sensing evolves to meet the challenges of changing light environments. Mol Ecol 15:3483–3503. doi:10.1111/j.1365-294X.2006.03051.x
McNellis TW, von Arnim AG, Araki T et al (1994) Genetic and molecular analysis of an allelic series of cop1 mutants suggests functional roles for the multiple protein domains. Plant Cell 6:487–500. doi:10.1105/tpc.6.4.487
Monte E, Alonso JM, Ecker JR et al (2003) Isolation and characterization of phyC mutants in Arabidopsis reveals complex crosstalk between phytochrome signaling pathways. Plant Cell 15:1962–1980. doi:10.1105/tpc.012971
Ni M, Tepperman JM, Quail PH (1998) PIF3, a phytochrome-interacting factor necessary for normal photoinduced signal transduction, is a novel basic helix-loop-helix protein. Cell 95:657–667
Ni W, Xu S-L, Tepperman JM et al (2014) A mutually assured destruction mechanism attenuates light signaling in Arabidopsis. Science 344:1160–1164. doi:10.1126/science.1250778
Nishida H, Ishihara D, Ishii M et al (2013) Phytochrome C is a key factor controlling long-day flowering in barley. Plant Physiol 163:804–814. doi:10.1104/pp.113.222570
Oh E, Kim J, Park E et al (2004) PIL5, a phytochrome-interacting basic helix-loop-helix protein, is a key negative regulator of seed germination in Arabidopsis thaliana. Plant Cell 16:3045–3058. doi:10.1105/tpc.104.025163.1
Oh E, Yamaguchi S, Kamiya Y et al (2006) Light activates the degradation of PIL5 protein to promote seed germination through gibberellin in Arabidopsis. Plant J 47:124–139. doi:10.1111/j.1365-313X.2006.02773.x
Oravecz A, Baumann A, Máté Z et al (2006) CONSTITUTIVELY PHOTOMORPHOGENIC1 is required for the UV-B response in Arabidopsis. Plant Cell 18:1975–1990. doi:10.1105/tpc.105.040097
Ordoñez-Herrera N, Fackendahl P, Yu X et al (2015) A cop1 spa mutant deficient in COP1 and SPA proteins reveals partial co-action of COP1 and SPA during Arabidopsis post-embryonic development and photomorphogenesis. Mol Plant 8:479–481. doi:10.1016/j.molp.2014.11.026
Osterlund MT, Deng X-W (1998) Multiple photoreceptors mediate the light-induced reduction of GUS-COP1 from Arabidopsis hypocotyl nuclei. Plant J 16:201–208. doi:10.1046/j.1365-313X.1998.00290.x
Osterlund MT, Hardtke CS, Wei N, Deng XW (2000) Targeted destabilization of HY5 during light-regulated development of Arabidopsis. Nature 405:462–466. doi:10.1038/35013076
Pacín M, Legris M, Casal JJ (2013) COP1 re-accumulates in the nucleus under shade. Plant J 75:631–641. doi:10.1111/tpj.12226
Pacín M, Legris M, Casal JJ (2014) Rapid decline in nuclear COP1 abundance anticipates the stabilisation of its target HY5 in the light. Plant Physiol 164:1134–1138. doi:10.1104/pp.113.234245
Park E, Park J, Kim J et al (2012) Phytochrome B inhibits binding of PHYTOCHROME INTERACTING FACTORs to their target promoters. Plant J 72:537–546. doi:10.1111/j.1365-313X.2012.05114.x
Peschke F, Kretsch T (2011) Genome-wide analysis of light-dependent transcript accumulation patterns during early stages of Arabidopsis seedling deetiolation. Plant Physiol 155:1353–1366. doi:10.1104/pp.110.166801
Ranjan A, Dickopf S, Ullrich KK et al (2014) Functional analysis of COP1 and SPA orthologs from Physcomitrella and rice during photomorphogenesis of transgenic Arabidopsis reveals distinct evolutionary conservation. BMC Plant Biol 14:178. doi:10.1186/1471-2229-14-178
Rausenberger J, Tscheuschler A, Nordmeier W et al (2011) Photoconversion and nuclear trafficking cycles determine phytochrome A’s response profile to far-red light. Cell 146:813–825. doi:10.1016/j.cell.2011.07.023
Richardt S, Lang D, Reski R et al (2007) PlanTAPDB, a phylogeny-based resource of plant transcription-associated proteins. Plant Physiol 143:1452–1466. doi:10.1104/pp.107.095760
Rizzini L, Favory J-J, Cloix C et al (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332:103–106. doi:10.1126/science.1200660
Rolauffs S, Fackendahl P, Sahm J et al (2012) Arabidopsis COP1 and SPA genes are essential for plant elongation but not for acceleration of flowering time in response to a low red light to far-red light ratio. Plant Physiol 160:2015–2027. doi:10.1104/pp.112.207233
Saijo Y, Sullivan JA, Wang H et al (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17:2642–2647. doi:10.1101/gad.1122903
Sellaro R, Crepy M, Trupkin SA et al (2010) Cryptochrome as a sensor of the blue/green ratio of natural radiation in Arabidopsis. Plant Physiol 154:401–409. doi:10.1104/pp.110.160820
Seo HS, Yang J-Y, Ishikawa M et al (2003) LAF1 ubiquitination by COP1 controls photomorphogenesis and is stimulated by SPA1. Nature 423:995–999. doi:10.1038/nature01696
Seo HS, Watanabe E, Tokutomi S et al (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev 18:617–622. doi:10.1101/gad.1187804
Shalitin D, Yang H, Mockler TC et al (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417:763–767. doi:10.1038/nature00815
Sharrock RA, Clack T (2002) Patterns of expression and normalized levels of the five Arabidopsis phytochromes. Plant Physiol 130:442–456. doi:10.1104/pp.005389
Sheerin DJ, Menon C, zur Oven-Krockhaus S et al (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. Plant Cell 27:189–201. doi:10.1105/tpc.114.134775
Shen H, Moon J, Huq E (2005) PIF1 is regulated by light-mediated degradation through the ubiquitin-26S proteasome pathway to optimize photomorphogenesis of seedlings in Arabidopsis. Plant J 44:1023–1035. doi:10.1111/j.1365-313X.2005.02606.x
Shi H, Zhong S, Mo X et al (2013) HFR1 sequesters PIF1 to govern the transcriptional network underlying light-initiated seed germination in Arabidopsis. Plant Cell 25:3770–3784. doi:10.1105/tpc.113.117424
Shimizu M, Ichikawa K, Aoki S (2004) Photoperiod-regulated expression of the PpCOL1 gene encoding a homolog of CO/COL proteins in the moss Physcomitrella patens. Biochem Biophys Res Commun 324:1296–1301. doi:10.1016/j.bbrc.2004.09.194
Shin J, Kim K, Kang H et al (2009) Phytochromes promote seedling light responses by inhibiting four negatively-acting PHYTOCHROME INTERACTING FACTORs. Proc Natl Acad Sci USA 106:7660–7665. doi:10.1073/pnas.0812219106
Smirnova OG, Stepanenko IL, Shumnyi VK (2011) The role of the COP1, SPA, and PIF proteins in plant photomorphogenesis. Biol Bull Rev 1:314–324. doi:10.1134/S2079086411040098
Smirnova OG, Stepanenko IL, Shumny VK (2012) Mechanism of action and activity regulation of COP1, a constitutive repressor of photomorphogenesis. Russ J Plant Physiol 59:155–166. doi:10.1134/S102144371202015X
Smith H, Xu Y, Quail PH (1997) Antagonistic but complementary actions of phytochromes A and B allow seedling de-etiolation. Plant Physiol 114:637–641. doi:10.1104/pp.114.2.637
Sun J, Qi L, Li Y et al (2012) PIF4–mediated activation of YUCCA8 expression integrates temperature into the auxin pathway in regulating Arabidopsis hypocotyl growth. PLoS Genet 8:e1002594. doi:10.1371/journal.pgen.1002594
Takemiya A, Inoue S-I, Doi M et al (2005) Phototropins promote plant growth in response to blue light in low light environments. Plant Cell 17:1120–1127. doi:10.1105/tpc.104.030049
Tilbrook K, Arongaus AB, Binkert M et al (2013) The UVR8 UV-B photoreceptor: perception, signaling and response. Arabidopsis Book 11:e0164. doi:10.1199/tab.0164
Vandenbussche F, Habricot Y, Condiff AS et al (2007) HY5 is a point of convergence between cryptochrome and cytokinin signalling pathways in Arabidopsis thaliana. Plant J 49:428–441. doi:10.1111/j.1365-313X.2006.02973.x
Viczián A, Ádám É, Wolf I et al (2012) A short amino-terminal part of Arabidopsis phytochrome A induces constitutive photomorphogenic response. Mol Plant 5:629–641. doi:10.1093/mp/sss035
von Arnim AG, Deng X-W (1994) Light inactivation of Arabidopsis photomorphogenic repressor COP1 involves a cell-specific regulation of its nucleocytoplasmic partitioning. Cell 79:1035–1045. doi:10.1016/0092-8674(94)90034-5
von Arnim AG, Osterlund MT, Kwok SF, Deng XW (1997) Genetic and developmental control of nuclear accumulation of COP1, a repressor of photomorphogenesis in Arabidopsis. Plant Physiol 114:779–788. doi:10.1104/pp.114.3.779
Wang H, Wang H (2015) Phytochrome signaling: time to tighten up the loose ends. Mol Plant 8:540–551. doi:10.1016/j.molp.2014.11.021
Weidler G, Zur Oven-Krockhaus S, Heunemann M et al (2012) Degradation of Arabidopsis CRY2 is regulated by SPA proteins and phytochrome A. Plant Cell 24:2610–2623. doi:10.1105/tpc.112.098210
Whitelam GC, Johnson E, Peng J et al (1993) Phytochrome A null mutants of Arabidopsis display a wild-type phenotype in white light. Plant Cell 5:757–768. doi:10.1105/tpc.5.7.757
Wu D, Hu Q, Yan Z et al (2012) Structural basis of ultraviolet-B perception by UVR8. Nature 484:214–219. doi:10.1038/nature10931
Xu X, Paik I, Zhu L et al (2014) PHYTOCHROME INTERACTING FACTOR1 enhances the E3 ligase activity of CONSTITUTIVE PHOTOMORPHOGENIC1 to synergistically repress photomorphogenesis in Arabidopsis. Plant Cell 26:1992–2006. doi:10.1105/tpc.114.125591
Yamawaki S, Yamashino T, Nakanishi H, Mizuno T (2011) Functional characterization of HY5 homolog genes involved in early light-signaling in Physcomitrella patens. Biosci Biotechnol Biochem 75:1533–1539. doi:10.1271/bbb.110219
Yang J, Wang H (2006) The central coiled-coil domain and carboxyl-terminal WD-repeat domain of Arabidopsis SPA1 are responsible for mediating repression of light signaling. Plant J 47:564–576. doi:10.1111/j.1365-313X.2006.02811.x
Yang J, Lin R, Hoecker U et al (2005a) Repression of light signaling by Arabidopsis SPA1 involves post-translational regulation of HFR1 protein accumulation. Plant J 43:131–141. doi:10.1111/j.1365-313X.2005.02433.x
Yang J, Lin R, Sullivan J et al (2005b) Light regulates COP1-mediated degradation of HFR1, a transcription factor essential for light signaling in Arabidopsis. Plant Cell 17:804–821. doi:10.1105/tpc.104.030205
Yanovsky MJ, Casal JJ, Whitelam GC (1995) Phytochrome A, phytochrome B and HY4 are involved in hypocotyl growth-responses to natural radiation in Arabidopsis: weak de-etiolation of the phyA mutant under dense canopies. Plant Cell Environ 18:788–794. doi:10.1111/j.1365-3040.1995.tb00582.x
Yu J-WW, Rubio V, Lee N-YY et al (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630. doi:10.1016/j.molcel.2008.09.026
Zeng X, Ren Z, Wu Q et al (2015) Dynamic crystallography reveals early signalling events in ultraviolet photoreceptor UVR8. Nat Plants 1:14006. doi:10.1038/nplants.2014.6
Zheng X, Wu S, Zhai H et al (2013) Arabidopsis phytochrome B promotes SPA1 nuclear accumulation to repress photomorphogenesis under far-red light. Plant Cell 25:115–133. doi:10.1105/tpc.112.107086
Zhu D, Maier A, Lee J-H et al (2008) Biochemical characterization of Arabidopsis complexes containing CONSTITUTIVELY PHOTOMORPHOGENIC1 and SUPPRESSOR OF PHYA proteins in light control of plant development. Plant Cell 20:2307–2323. doi:10.1105/tpc.107.056580
Zhu L, Bu Q, Xu X et al (2015) CUL4 forms an E3 ligase with COP1 and SPA to promote light-induced degradation of PIF1. Nat Commun 6:7245. doi:10.1038/ncomms8245
Zobell O, Coupland G, Reiss B (2005) The family of CONSTANS-like genes in Physcomitrella patens. Plant Biol (Stuttg) 7:266–275. doi:10.1055/s-2005-865621
Zuo Z, Liu H, Liu B et al (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21:841–847. doi:10.1016/j.cub.2011.03.048
Acknowledgments
We thank Klaus Harter, Centre for Plant Molecular Biology (ZMBP), University of Tübingen, for hosting CM and the two anonymous reviewers for carefully reading the manuscripts and providing excellent feedback. Work in the laboratory of AH was supported by the Excellence Initiative of the German Federal and State Governments (EXC 294, project C20) and grants from the German Research Foundation (DFG; HI 1369/4-1 and HI 1369/5-1) and the Human Frontier Science Program (HFSP; RGP0025/2013) to AH.
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C. Menon and D. J. Sheerin equally contributing first authors.
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Menon, C., Sheerin, D.J. & Hiltbrunner, A. SPA proteins: SPAnning the gap between visible light and gene expression. Planta 244, 297–312 (2016). https://doi.org/10.1007/s00425-016-2509-3
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DOI: https://doi.org/10.1007/s00425-016-2509-3