Photoreceptor Specificity in the Light-Induced and COP1-Mediated Rapid Degradation of the Repressor of Photomorphogenesis SPA2 in Arabidopsis


Plants have evolved photoreceptors that initiate a signaling cascade to adjust growth and development to the ambient light environment. The CUL4-dependent COP1/SPA E3 ubiquitin ligase is a key negative regulator of light signaling whose function is repressed by light. Recent research has identified mechanisms that are common to both phytochrome and cryptochrome photoreceptors. Here, we have identified a mechanism of light-induced COP1/SPA repression that is specific to phytochrome photoreceptors. We show that the SPA2 protein is very rapidly degraded in red, far-red and blue light in a phytochrome-dependent fashion. We further show that SPA2 degradation in the light depends on COP1 and on the interaction of SPA2 with COP1. Hence, our results suggest a light-induced degradation of SPA2, but not of COP1, by the COP1/SPA2 ubiquitin ligase. The human ortholog of COP1, which functions without the plant-specific SPA proteins, is known to be regulated by autodegradation following DNA damage. Hence, autodegradation of components of this E3 ligase is a regulatory mechanism used in both humans and plants.


Vyšlo v časopise: Photoreceptor Specificity in the Light-Induced and COP1-Mediated Rapid Degradation of the Repressor of Photomorphogenesis SPA2 in Arabidopsis. PLoS Genet 11(9): e32767. doi:10.1371/journal.pgen.1005516
Kategorie: Research Article
prolekare.web.journal.doi_sk: 10.1371/journal.pgen.1005516

Souhrn

Plants have evolved photoreceptors that initiate a signaling cascade to adjust growth and development to the ambient light environment. The CUL4-dependent COP1/SPA E3 ubiquitin ligase is a key negative regulator of light signaling whose function is repressed by light. Recent research has identified mechanisms that are common to both phytochrome and cryptochrome photoreceptors. Here, we have identified a mechanism of light-induced COP1/SPA repression that is specific to phytochrome photoreceptors. We show that the SPA2 protein is very rapidly degraded in red, far-red and blue light in a phytochrome-dependent fashion. We further show that SPA2 degradation in the light depends on COP1 and on the interaction of SPA2 with COP1. Hence, our results suggest a light-induced degradation of SPA2, but not of COP1, by the COP1/SPA2 ubiquitin ligase. The human ortholog of COP1, which functions without the plant-specific SPA proteins, is known to be regulated by autodegradation following DNA damage. Hence, autodegradation of components of this E3 ligase is a regulatory mechanism used in both humans and plants.


Zdroje

1. 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 20705178

2. 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 23373700

3. Casal JJ, Candia AN, Sellaro R (2014) Light perception and signalling by phytochrome A. J Exp Bot 65: 2835–2845. doi: 10.1093/jxb/ert379 24220656

4. Franklin KA, Quail PH (2010) Phytochrome functions in Arabidopsis development. J Exp Bot 61: 11–24. doi: 10.1093/jxb/erp304 19815685

5. Chaves I, Pokorny R, Byrdin M, Hoang N, Ritz T, 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 21526969

6. Liu H, Liu B, Zhao C, Pepper M, Lin C (2011) The action mechanisms of plant cryptochromes. Trends Plant Sci 16: 684–691. doi: 10.1016/j.tplants.2011.09.002 21983106

7. Su YS, Lagarias JC (2007) Light-independent phytochrome signaling mediated by dominant GAF domain tyrosine mutants of Arabidopsis phytochromes in transgenic plants. Plant Cell 19: 2124–2139. 17660358

8. Gu NN, Zhang YC, Yang HQ (2012) Substitution of a conserved glycine in the PHR domain of Arabidopsis cryptochrome 1 confers a constitutive light response. Mol Plant 5: 85–97. doi: 10.1093/mp/ssr052 21765176

9. Yang HQ, Wu YJ, Tang RH, Liu DM, Liu Y, et al. (2000) The C termini of Arabidopsis cryptochromes mediate a constitutive light response. Cell 103: 815–827. 11114337

10. Viczian A, Adam E, Wolf I, Bindics J, Kircher S, 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 22498774

11. Tilbrook K, Arongaus AB, Binkert M, Heijde M, Yin R, et al. (2013) The UVR8 UV-B photoreceptor: perception, signaling and response. Arabidopsis Book 11: e0164. doi: 10.1199/tab.0164 23864838

12. Jenkins GI (2014) The UV-B photoreceptor UVR8: from structure to physiology. Plant Cell 26: 21–37. doi: 10.1105/tpc.113.119446 24481075

13. 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 22705257

14. Huang X, Ouyang X, Deng XW (2014) Beyond repression of photomorphogenesis: role switching of COP/DET/FUS in light signaling. Curr Opin Plant Biol 21C: 96–103.

15. Weidler G, Zur Oven-Krockhaus S, Heunemann M, Orth C, Schleifenbaum F, 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 22739826

16. Seo HS, Watanabe E, Tokutomi S, Nagatani A, Chua NH (2004) Photoreceptor ubiquitination by COP1 E3 ligase desensitizes phytochrome A signaling. Genes Dev 18: 617–622. 15031264

17. Shalitin D, Yang HY, Mockler TC, Maymon M, Guo HW, et al. (2002) Regulation of Arabidopsis cryptochrome 2 by blue-light-dependent phosphorylation. Nature 417: 763–767. 12066190

18. Debrieux D, Trevisan M, Fankhauser C (2013) Conditional involvement of CONSTITUTIVE PHOTOMORPHOGENIC1 in the degradation of phytochrome A. Plant Physiol 161: 2136–2145. doi: 10.1104/pp.112.213280 23391578

19. Zhu D, Maier A, Lee JH, Laubinger S, Saijo Y, 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 18812498

20. Ranjan A, Dickopf S, Ullrich KK, Rensing SA, Hoecker U (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 24985152

21. Deng X-W, Caspar T, Quail PH (1991) cop1: A regulatory locus involved in light-controlled development and gene expression in Arabidopsis. Genes Dev 5: 1172–1182. 2065972

22. 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. 15308756

23. Ordonez-Herrera N, Fackendahl P, Yu X, Schaefer S, Koncz C, 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 25667004

24. Laubinger S, Marchal V, Gentilhomme J, Wenkel S, Adrian 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. 16854975

25. Rolauffs S, Fackendahl P, Sahm J, Fiene G, Hoecker U (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 23093358

26. Maier A, Schrader A, Kokkelink L, Falke C, Welter B, 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 23425305

27. Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W, 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 18388858

28. Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, et al. (2008) 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 18296627

29. Wang CQ, Sarmast MK, Jiang J, Dehesh K (2015) The transcriptional regulator BBX19 promotes hypocotyl growth by facilitating COP1-mediated EARLY FLOWERING3 degradation in Arabidopsis. Plant Cell: 27: 1128–1139. doi: 10.1105/tpc.15.00044 25841036

30. Ranjan A, Fiene G, Fackendahl P, Hoecker U (2011) The Arabidopsis repressor of light signaling SPA1 acts in the phloem to regulate seedling de-etiolation, leaf expansion and flowering time. Development 138: 1851–1862. doi: 10.1242/dev.061036 21447551

31. Jang IC, Yang JY, Seo HS, Chua NH (2005) HFR1 is targeted by COP1 E3 ligase for post-translational proteolysis during phytochrome A signaling. Genes Dev 19: 593–602. 15741320

32. Yang J, Lin R, Hoecker U, Liu B, Xu L, et al. (2005) Repression of light signaling by Arabidopsis SPA1 involves post-translational regulation of HFR1 protein accumulation. Plant J 43: 131–141. 15960622

33. Hoecker U, Xu Y, Quail PH (1998) SPA1: A new genetic locus involved in phytochrome A-specific signal transduction. Plant Cell 10: 19–33. 9477570

34. Jackson S, Xiong Y (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 34: 562–570. doi: 10.1016/j.tibs.2009.07.002 19818632

35. Biedermann S, Hellmann H (2011) WD40 and CUL4-based E3 ligases: lubricating all aspects of life. Trends Plant Sci 16: 38–46. doi: 10.1016/j.tplants.2010.09.007 20965772

36. Chen H, Huang X, Gusmaroli G, Terzaghi W, Lau OS, 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 20061554

37. 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. 11461903

38. Saijo Y, Sullivan JA, Wang H, Yang J, Shen Y, et al. (2003) The COP1-SPA1 interaction defines a critical step in phytochrome A-mediated regulation of HY5 activity. Genes Dev 17: 2642–2647. 14597662

39. Holm M, Hardtke CS, Gaudet R, Deng XW (2001) Identification of a structural motif that confers specific interaction with the WD40 repeat domain of Arabidopsis COP1. EMBO J 20: 118–127. 11226162

40. Hoecker U, Tepperman JM, Quail PH (1999) SPA1, a WD-repeat protein specific to phytochrome A signal transduction. Science 284: 496–499. 10205059

41. Deng XW, Matsui M, Wei N, Wagner D, Chu AM, 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. 1423630

42. Balcerowicz M, Fittinghoff K, Wirthmueller L, Maier A, Fackendahl P, 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 21235648

43. Pacin M, Legris M, Casal JJ (2014) Rapid decline in nuclear CONSTITUTIVE PHOTOMORPHOGENESIS1 abundance anticipates the stabilization of its target ELONGATED HY5 in the light. Plant Physiol 164: 1134–1138. doi: 10.1104/pp.113.234245 24434030

44. 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. 8001131

45. Fankhauser C, Ulm R (2011) Light-regulated interactions with SPA proteins underlie cryptochrome-mediated gene expression. Genes Dev 25: 1004–1009. doi: 10.1101/gad.2053911 21576261

46. Liu B, Zuo Z, Liu H, Liu X, Lin C (2011) 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 21511871

47. Lian HL, He SB, Zhang YC, Zhu DM, Zhang JY, 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 21511872

48. Lu XD, Zhou CM, Xu PB, Luo Q, Lian HL, 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 25744387

49. Sheerin DJ, Menon C, zur Oven-Krockhaus S, Enderle B, Zhu L, 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 25627066

50. Zuo Z, Liu H, Liu B, Liu X, Lin C (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 21514160

51. Fittinghoff K, Laubinger S, Nixdorf M, Fackendahl P, Baumgardt RL, et al. (2006) Functional and expression analysis of Arabidopsis SPA genes during seedling photomorphogenesis and adult growth. Plant J 47: 577–590. 16813571

52. Osterlund MT, Deng XW (1998) Multiple photoreceptors mediate the light-induced reduction of GUS-COP1 from Arabidopsis hypocotyl nuclei. Plant J 16: 201–208. 9839465

53. Osterlund MT, Wei N, Deng XW (2000) The roles of photoreceptor systems and the COP1-targeted destabilization of HY5 in light control of arabidopsis seedling development. Plant Physiol 124: 1520–1524. 11115869

54. 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. 12244439

55. Laubinger S, Hoecker U (2003) The SPA1-like proteins SPA3 and SPA4 repress photomorphogenesis in the light. Plant J 35: 373–385. 12887588

56. Xu D, Lin F, Jiang Y, Huang X, Li J, et al. (2014) The RING-finger E3 ubiquitin ligase COP1 SUPPRESSOR1 negatively regulates COP1 abundance in maintaining COP1 homeostasis in dark-grown Arabidopsis seedlings. Plant Cell 26: 1981–1991. 24838976

57. Dornan D, Shimizu H, Mah A, Dudhela T, Eby M, et al. (2006) ATM engages autodegradation of the E3 ubiquitin ligase COP1 after DNA damage. Science 313: 1122–1126. 16931761

58. 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. 12232154

59. Parks BM, Quail PH (1993) Hy8, a new class of Arabidopsis long hypocotyl mutants deficient in functional phytochrome A. Plant Cell 5: 39–48. 8439743

60. Quail PH, Briggs WR, Chory J, Hangarter RP, Harberd NP, et al. (1994) Spotlight on phytochrome nomenclature. Plant Cell 6: 468–471. 12244245

61. 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. 9193095

62. Mazzella MA, Cerdan PD, Staneloni RJ, Casal JJ (2001) Hierarchical coupling of phytochromes and cryptochromes reconciles stability and light modulation of Arabidopsis development. Development 128: 2291–2299. 11493548

63. Deng XW, Quail PH (1992) Genetic and phenotypic characterization of cop1 mutants of Arabidopsis thaliana. Plant J 2: 83–95.

64. McNellis TW, Von Arnim AG, Araki T, Komeda Y, Miséra S, 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. 8205001

65. Yoo SY, Bomblies K, Yoo SK, Yang JW, Choi MS, et al. (2005) The 35S promoter used in a selectable marker gene of a plant transformation vector affects the expression of the transgene. Planta 221: 523–530. 15682278

66. Xia YJ, Nikolau BJ, Schnable PS (1997) Developmental and hormonal regulation of the Arabidopsis CER2 gene that codes for a nuclear-localized protein required for the normal accumulation of cuticular waxes. Plant Physiology 115: 925–937. 9390429

67. Lin C, Ahmad M, Gordon D, Cashmore AR (1995) Expression of an Arabidopsis cryptochrome gene in transgenic tobacco results in hypersensitivity to blue, UV-a, and green light. Proc NatAcad Sci USA 92: 8423–8427.

68. Ahmad M, Jarillo JA, Cashmore AR (1998) Chimeric proteins between cry1 and cry2 Arabidopsis blue light photoreceptors indicate overlapping functions and varying protein stability. Plant Cell 10: 197–207. 9490743

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2015 Číslo 9

Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Eozinofilní granulomatóza s polyangiitidou
nový kurz

Betablokátory a Ca antagonisté z jiného úhlu
Autori: prof. MUDr. Michal Vrablík, Ph.D., MUDr. Petr Janský

Autori: doc. MUDr. Petr Čáp, Ph.D.

Farmakoterapie akutní a chronické bolesti

Získaná hemofilie - Povědomí o nemoci a její diagnostika

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Nemáte účet?  Registrujte sa

Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa