Phytochrome Kinase Substrate 4 is phosphorylated by the phototropin 1 photoreceptor

EMBO Journal

Volumn 31, Issue 16, 2012, Pages 3457-3467

  Demarsy, Emilie ^a   Schepens, Isabelle ^a,f   Okajima, Koji ^b   Hersch, Micha ^a,c   Bergmann, Sven ^a,c   Christie, John ^d   Shimazaki, Ken Ichiro ^e   Tokutomi, Satoru ^b   Fankhauser, Christian ^a  

^a UNIVERSITY OF LAUSANNE   (Switzerland)

^b Osaka Prefecture University   (Japan)

^c SWISS INSTITUTE OF BIOINFORMATICS   (Switzerland)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e KYUSHU UNIVERSITY   (Japan)

^f UNIVERSITY OF BERN   (Switzerland)

Author keywords

light activated protein kinase; photoreceptor co action; phototropin 1; phototropism; Phytochrome Kinase Substrate 4

Indexed keywords

AUXIN; PHOSPHOPROTEIN PHOSPHATASE 2; PHOTOTROPIN; PHOTOTROPIN 1; PHYTOCHROME; PHYTOCHROME KINASE SUBSTRATE 4; UNCLASSIFIED DRUG;

ARTICLE; BLUE LIGHT; CONTROLLED STUDY; DEPHOSPHORYLATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; NEGATIVE FEEDBACK; NONHUMAN; PHOTOMORPHOGENESIS; PHOTOTROPISM; PRIORITY JOURNAL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHOPROTEINS; PHOSPHORYLATION; PHOTOTROPHIC PROCESSES; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION;

ARABIDOPSIS;

EID: 84865227594     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2012.186     Document Type: Article

References (63)

1. Adams JA (2003) Activation loop phosphorylation and catalysis in protein kinases: is there functional evidence for the autoinhibitor model? Biochemistry 42: 601-607 (Pubitemid 36133283)
2. Aihara Y, Yamamoto T, Okajima K, Yamamoto K, Suzuki T, Tokutomi S, Tanaka K, Nagatani A (2012) Mutations in the N-terminal flanking region of the blue-light sensing domain LOV2 disrupt its repressive activity on the kinase domain in the Chlamydomonas phototropin. J Biol Chem 287: 9901-9909
3. Boccalandro HE, De Simone SN, Bergmann-Honsberger A, Schepens I, Fankhauser C, Casal JJ (2008) PHYTOCHROME KINASE SUBSTRATE1 regulates root phototropism and gravitropism. Plant Physiol 146: 108-115 (Pubitemid 351380041)
4. Cho HY, Tseng TS, Kaiserli E, Sullivan S, Christie JM, Briggs WR (2007) Physiological roles of the light, oxygen, or voltage domains of phototropin 1 and phototropin 2 in Arabidopsis. Plant Physiol 143: 517-529 (Pubitemid 46133654)
5. Christie JM (2007) Phototropin blue-light receptors. Annu Rev Plant Biol 58: 21-45 (Pubitemid 46986316)
6. Christie JM, Swartz TE, Bogomolni RA, Briggs WR (2002) Phototropin LOV domains exhibit distinct roles in regulating photoreceptor function. Plant J 32: 205-219 (Pubitemid 35249919)
7. Christie JM, Yang H, Richter GL, Sullivan S, Thomson CE, Lin J, Titapiwatanakun B, Ennis M, Kaiserli E, Lee OR, Adamec J, Peer WA, Murphy AS (2011) phot1 inhibition of ABCB19 primes lateral auxin fluxes in the shoot apex required for phototropism. PLoS Biol 9: e1001076
8. de Carbonnel M, Davis P, Roelfsema MR, Inoue S, Schepens I, Lariguet P, Geisler M, Shimazaki K, Hangarter R, Fankhauser C (2010) The Arabidopsis PHYTOCHROME KINASE SUBSTRATE2 protein is a phototropin signaling element that regulates leaf flattening and leaf positioning. Plant Physiol 152: 1391-1405
9. Deruere J, Jackson K, Garbers C, Soll D, Delong A (1999) The RCN1- encoded A subunit of protein phosphatase 2A increases phosphatase activity in vivo. Plant J 20: 389-399
10. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J, Fan Y, Morita MT, Tasaka M, Fankhauser C, Offringa R, Friml J (2011) Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat Cell Biol 13: 447-452
11. Duek PD, Fankhauser C (2003) HFR1, a putative bHLH transcription factor, mediates both phytochrome A and cryptochrome signalling. Plant J 34: 827-836 (Pubitemid 36796930)
12. Esmon CA, Tinsley AG, Ljung K, Sandberg G, Hearne LB, Liscum E (2006) A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proc Natl Acad Sci USA 103: 236-241 (Pubitemid 43076133)
13. Fankhauser C, Yeh KC, Lagarias JC, Zhang H, Elich TD, Chory J (1999) PKS1, a substrate phosphorylated by phytochrome that modulates light signaling in Arabidopsis. Science 284: 1539-1541
14. Folta KM, Spalding EP (2001) Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J 26: 471-478 (Pubitemid 32665046)
15. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G (2003) The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112: 219-230 (Pubitemid 36144111)
16. Han IS, Tseng TS, Eisinger W, Briggs WR (2008) Phytochrome A regulates the intracellular distribution of phototropin 1-green fluorescent protein in Arabidopsis thaliana. Plant Cell 20: 2835-2847 (Pubitemid 352844593)
17. Harper RM, Stowe-Evans EL, Luesse DR, Muto H, Tatematsu K, Watahiki MK, Yamamoto K, Liscum E (2000) The NPH4 locus encodes the auxin response factor ARF7, a conditional regulator of differential growth in aerial Arabidopsis tissue. Plant Cell 12: 757-770 (Pubitemid 30343586)
18. Harper SM, Christie JM, Gardner KH (2004) Disruption of the LOVJalpha helix interaction activates phototropin kinase activity. Biochemistry 43: 16184-16192 (Pubitemid 40041031)
19. Harper SM, Neil LC, Gardner KH (2003) Structural basis of a phototropin light switch. Science 301: 1541-1544 (Pubitemid 37128547)
20. Huala E, Oeller PW, Liscum E, Han IS, Larsen E, Briggs WR (1997) Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. Science 278: 2120-2123 (Pubitemid 28028321)
21. Iino M (2006) Toward understanding the ecological functions of tropisms: interactions among and effects of light on tropisms. Curr Opin Plant Biol 9: 89-93 (Pubitemid 43019259)
22. Inoue S, Kinoshita T, Matsumoto M, Nakayama KI, Doi M, Shimazaki K (2008a) Blue light-induced autophosphorylation of phototropin is a primary step for signaling. Proc Natl Acad Sci USA 105: 5626-5631 (Pubitemid 351753913)
23. Inoue S, Kinoshita T, Takemiya A, Doi M, Shimazaki K (2008b) Leaf positioning of Arabidopsis in response to blue light. Mol Plant 1: 15-26
24. Inoue S, Matsushita T, Tomokiyo Y, Matsumoto M, Nakayama KI, Kinoshita T, Shimazaki K (2011) Functional analyses of the activation loop of phototropin2 in Arabidopsis. Plant Physiol 156: 117-128
25. Janoudi AK, Poff KL (1991) Characterization of adaptation in phototropism of Arabidopsis thaliana. Plant Physiol 95: 517-521 (Pubitemid 21913843)
26. Janoudi AK, Whitelam GC, Gordon WR, Poff KL (1997) Both phytochrome A and phytochrome B are required for the normal expression of phototropism in Arabidopsis thaliana seedlings. Physiol Plant 101: 278-282 (Pubitemid 27447278)
27. Kagawa T, Sakai T, Suetsugu N, Oikawa K, Ishiguro S, Kato T, Tabata S, Okada K, Wada M (2001) Arabidopsis NPL1: a phototropin homolog controlling the chloroplast high-light avoidance response. Science 291: 2138-2141 (Pubitemid 32224442)
28. Kami C, Hersch M, Trevisan M, Genoud T, Hiltbrunner A, Bergmann S, Fankhauser C (2012) Nuclear Phytochrome A Signaling Promotes Phototropism in Arabidopsis. Plant Cell 24: 566-576
29. Kami C, Lorrain S, Hornitschek P, Fankhauser C (2010) Light-regulated plant growth and development. Curr Topics Dev Biol 91: 29-66
30. Keuskamp DH, Sasidharan R, Pierik R (2010) Physiological regulation and functional significance of shade avoidance responses to neighbors. Plant Signal Behav 5: 655-662
31. Konjevic R, Steinitz B, Poff KL (1989) Dependence of the phototropic response of Arabidopsis thaliana on fluence rate and wavelength. Proc Natl Acad Sci USA 86: 9876-9880 (Pubitemid 20030737)
32. 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. Plant Cell 15: 2966-2978 (Pubitemid 37546264)
33. Lariguet P, Fankhauser C (2004) Hypocotyl growth orientation in blue light is determined by phytochrome A inhibition of gravitropism and phototropin promotion of phototropism. Plant J 40: 826-834 (Pubitemid 39623255)
34. Lariguet P, Schepens I, Hodgson D, Pedmale UV, Trevisan M, Kami C, de Carbonnel M, Alonso JM, Ecker JR, Liscum E, Fankhauser C (2006) PHYTOCHROME KINASE SUBSTRATE 1 is a phototropin 1 binding protein required for phototropism. Proc Natl Acad Sci USA 103: 10134-10139 (Pubitemid 43993635)
35. Li YM, Mackintosh C, Casida JE (1993) Protein phosphatase 2A and its [3H]cantharidin/[3H]endothall thioanhydride binding site. Inhibitor specificity of cantharidin and ATP analogues. Biochem Pharmacol 46: 1435-1443 (Pubitemid 23319314)
36. Liscum E, Briggs WR (1996) Mutations of Arabidopsis in potential transduction and response components of the phototropic signaling pathway. Plant Physiol 112: 291-296 (Pubitemid 26368229)
37. Lorrain S, Allen T, Duek PD, Whitelam GC, Fankhauser C (2008) Phytochrome-mediated inhibition of shade avoidance involves degradation of growth-promoting bHLH transcription factors. Plant J 53: 312-323
38. Matsuoka D, Tokutomi S (2005) Blue light-regulated molecular switch of Ser/Thr kinase in phototropin. Proc Natl Acad Sci USA 102: 13337-13342 (Pubitemid 41325024)
39. Mockler T, Yang H, Yu X, Parikh D, Cheng YC, Dolan S, Lin C (2003) Regulation of photoperiodic flowering by Arabidopsis photoreceptors. Proc Natl Acad Sci USA 100: 2140-2145 (Pubitemid 36254587)
40. Molas ML, Kiss JZ (2008) PKS1 plays a role in red-light-based positive phototropism in roots. Plant Cell Environ 31: 842-849 (Pubitemid 351667681)
41. Nagashima A, Suzuki G, Uehara Y, Saji K, Furukawa T, Koshiba T, Sekimoto M, Fujioka S, Kuroha T, Kojima M, Sakakibara H, Fujisawa N, Okada K, Sakai T (2008) Phytochromes and cryptochromes regulate the differential growth of Arabidopsis hypocotyls in both a PGP19-dependent and a PGP19-independent manner. Plant J 53: 516-529 (Pubitemid 351172021)
42. Ohgishi M, Saji K, Okada K, Sakai T (2004) Functional analysis of each blue light receptor, cry1, cry2, phot1, and phot2, by using combinatorial multiple mutants in Arabidopsis. Proc Natl Acad Sci USA 101: 2223-2228 (Pubitemid 38269293)
43. Okajima K, Matsuoka D, Tokutomi S (2011) LOV2-linker-kinase phosphorylates LOV1-containing N-terminal polypeptide substrate via photoreaction of LOV2 in Arabidopsis phototropin1. FEBS Lett 585: 3391-3395
44. Pantin F, Simonneau T, Rolland G, Dauzat M, Muller B (2011) Control of leaf expansion: a developmental switch from metabolics to hydraulics. Plant Physiol 156: 803-815
45. Parks BM, Quail PH, Hangarter RP (1996) Phytochrome A regulates red-light induction of phototropic enhancement in Arabidopsis. Plant Physiol 110: 155-162
46. Pedmale UV, Liscum E (2007) Regulation of phototropic signaling in Arabidopsis via phosphorylation state changes in the phototropin 1-interacting protein NPH3. J Biol Chem 282: 19992-20001 (Pubitemid 47100126)
47. Rizzini L, Favory JJ, Cloix C, Faggionato D, O'Hara A, Kaiserli E, Baumeister R, Schafer E, Nagy F, Jenkins GI, Ulm R (2011) Perception of UV-B by the Arabidopsis UVR8 protein. Science 332: 103-106
48. Salomon M, Knieb E, von Zeppelin T, Rudiger W (2003) Mapping of low- and high-fluence autophosphorylation sites in phototropin 1. Biochemistry 42: 4217-4225 (Pubitemid 36418315)
49. Schepens I, Boccalandro HE, Kami C, Casal JJ, Fankhauser C (2008) PHYTOCHROME KINASE SUBSTRATE4 modulates phytochromemediated control of hypocotyl growth orientation. Plant Physiol 147: 661-671 (Pubitemid 352844313)
50. Sellaro R, Hoecker U, Yanovsky M, Chory J, Casal JJ (2009) Synergism of red and blue light in the control of Arabidopsis gene expression and development. Curr Biol 19: 1216-1220
51. Stowe-Evans EL, Luesse DR, Liscum E (2001) The enhancement of phototropin-induced phototropic curvature in Arabidopsis occurs via a photoreversible phytochrome A-dependent modulation of auxin responsiveness. Plant Physiol 126: 826-834 (Pubitemid 32566631)
52. Strasser B, Sanchez-Lamas M, Yanovsky MJ, Casal JJ, Cerdan PD (2010) Arabidopsis thaliana life without phytochromes. Proc Natl Acad Sci USA 107: 4776-4781
53. Sullivan S, Thomson CE, Kaiserli E, Christie JM (2009) Interaction specificity of Arabidopsis 14-3-3 proteins with phototropin receptor kinases. FEBS Lett 583: 2187-2193
54. Sullivan S, Thomson CE, Lamont DJ, Jones MA, Christie JM (2008) In vivo phosphorylation site mapping and functional characterization of Arabidopsis phototropin 1. Mol Plant 1: 178-194
55. Tokutomi S, Matsuoka D, Zikihara K (2008) Molecular structure and regulation of phototropin kinase by blue light. Biochim Biophys Acta 1784: 133-142
56. Tseng TS, Briggs WR (2010) The Arabidopsis rcn1-1 mutation impairs dephosphorylation of Phot2, resulting in enhanced blue light responses. Plant Cell 22: 392-402
57. Tsuchida-Mayama T, Nakano M, Uehara Y, Sano M, Fujisawa N, Okada K, Sakai T (2008) Mapping of the phosphorylation sites on the phototropic transducer, NPH3. Plant Sci 174: 626-633
58. Tsuchida-Mayama T, Sakai T, Hanada A, Uehara Y, Asami T, Yamaguchi S (2010) Role of the phytochrome and cryptochrome signaling pathways in hypocotyl phototropism. Plant J 62: 653-662
59. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59: 573-594 (Pubitemid 351813043)
60. Ueno K, Kinoshita T, Inoue S, Emi T, Shimazaki K (2005) Biochemical characterization of plasma membrane H-ATPase activation in guard cell protoplasts of Arabidopsis thaliana in response to blue light. Plant Cell Physiol 46: 955-963 (Pubitemid 41435483)
61. Wan YL, Eisinger W, Ehrhardt D, Kubitscheck U, Baluska F, Briggs W (2008) The subcellular localization and blue-light-induced movement of phototropin 1-GFP in etiolated seedlings of Arabidopsis thaliana. Mol Plant 1: 103-117
62. Whippo CW, Hangarter RP (2003) Second positive phototropism results from coordinated co-action of the phototropins and cryptochromes. Plant Physiol 132: 1499-1507 (Pubitemid 36872898)
63. Whippo CW, Hangarter RP (2004) Phytochrome modulation of bluelight- induced phototropism. Plant Cell Environ 27: 1223-1228 (Pubitemid 39415192)