O-GlcNAcylation of master growth repressor DELLA by SECRET AGENT modulates multiple signaling pathways in Arabidopsis

Genes and Development

Volumn 30, Issue 2, 2016, Pages 164-176

  Zentella, Rodolfo ^a   Hu, Jianhong ^a   Hsieh, Wen Ping ^a   Matsumoto, Peter A ^b   Dawdy, Andrew ^c   Barnhill, Benjamin ^c   Oldenhof, Harriëtte ^b,f   Hartweck, Lynn M ^b,g   Maitra, Sushmit ^c   Thomas, Stephen G ^a,h   Cockrell, Shelley ^a,i   Boyce, Michael ^d   Shabanowitz, Jeffrey ^c   Hunt, Donald F ^c,e   Olszewski, Neil E ^b   Sun, Tai Ping ^a  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY OF VIRGINIA   (United States)

^f UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^g UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^h ROTHAMSTED RESEARCH   (United Kingdom)

ⁱ UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

DELLA interacting proteins; Gibberellin signaling; Hormone signaling; O GlcNAc transferase; O GlcNAcylation of DELLA; SECRET AGENTs

Indexed keywords

ARABIDOPSIS PROTEIN; BRASSINAZOLE RESISTANT 1 PROTEIN; BRASSINOSTEROID; GIBBERELLIN; JASMONATE ZIM DOMAIN 1 PROTEIN; JASMONIC ACID; N ACETYLGLUCOSAMINE; PHYTOHORMONE INTERACTING FACTOR 3; PHYTOHORMONE INTERACTING FACTOR 4; PROTEIN DELLA; PROTEIN SECRET AGENT; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; TRANSFERASE; UNCLASSIFIED DRUG; GAI PROTEIN, ARABIDOPSIS; N ACETYLGLUCOSAMINYLTRANSFERASE; PROTEIN BINDING; SECRET AGENT PROTEIN, ARABIDOPSIS;

ACYLATION; ARABIDOPSIS; ARTICLE; CONTROLLED STUDY; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION; LIGHT; MASS SPECTROMETRY; MUTANT; NONHUMAN; NULL ALLELE; O GLCNACYLATION; PEPTIDE MAPPING; PHENOTYPE; PLANT DEVELOPMENT; PLANT STEM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY;

ACYLATION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; GENE EXPRESSION REGULATION, PLANT; GIBBERELLINS; MUTATION; N-ACETYLGLUCOSAMINYLTRANSFERASES; PROTEIN BINDING; SIGNAL TRANSDUCTION;

EID: 84954553651     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.270587.115     Document Type: Article

References (61)

1. An F, Zhang X, Zhu Z, Ji Y, He W, Jiang Z, Li M, Guo H. 2012. Coordinated regulation of apical hook development by gibberellins and ethylene in etiolated Arabidopsis seedlings. Cell Res 22: 915-927.
2. Bai MY, Shang JX, Oh E, Fan M, Bai Y, Zentella R, Sun T-P, Wang Z-Y. 2012. Brassinosteroid, gibberellin, and phytochrome signalling pathways impinge on a common transcription module in Arabidopsis. Nat Cell Biol 14: 810-817.
3. Berk JM, Maitra S, Dawdy AW, Shabanowitz J, Hunt DF, Wilson KL. 2013. O-GlcNAc regulates emerin binding to BAF in a chromatinand lamin B-enriched ‘niche’. J Biol Chem 288: 30192-30209.
4. Bond MR, Hanover JA. 2013. O-GlcNAc cycling: a link between metabolism and chronic disease. Annu Rev Nutr 33: 205-229
5. Boyce M, Carrico IS, Ganguli AS, Yu SH, Hangauer MJ, Hubbard SC, Kohler JJ, Bertozzi CR. 2011. Metabolic cross-talk allows labeling of O-linked β-N-acetylglucosamine-modified proteins via the N-acetylgalactosamine salvage pathway. Proc Natl Acad Sci 108: 3141-3146.
6. Comer FI, Vosseller K, Wells L, Accavitti MA, Hart GW. 2001. Characterization of a mouse monoclonal antibody specific for O-linked N-acetylglucosamine. Anal Biochem 293: 169-177.
7. Conti L, Nelis S, Zhang C, Woodcock A, Swarup R, Galbiati M, Tonelli C, Napier R, Hedden P, Bennett M, et al. 2014. Small ubiquitin-like modifier protein SUMO enables plants to control growth independently of the phytohormone gibberellin. Dev Cell 28: 102-110.
8. Czechowski T, Stitt M, Altmann T, Udvardi MK, Scheible WR. 2005. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17.
9. Dai C, Xue HW. 2010. Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellins signalling. EMBO J 29: 1916-1927.
10. Daviere JM, Achard P. 2016. A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9: 10-20.
11. de Lucas M, Daviere JM, Rodriguez-Falcon M, Pontin M, Iglesias-Pedraz JM, Lorrain S, Fankhauser C, Blazquez MA, Titarenko E, Prat S. 2008. A molecular framework for light and gibberellin control of cell elongation. Nature 451: 480-484.
12. Dill A, Sun T-P. 2001. Synergistic de-repression of gibberellin signaling by removing RGA and GAI function in Arabidopsis thaliana. Genetics 159: 777-785.
13. Dill A, Thomas SG, Hu J, Steber CM, Sun T-P. 2004. The Arabidopsis F-box protein SLEEPY1 targets GA signaling repressors for GA-induced degradation. Plant Cell 16: 1392-1405
14. Feng S, Martinez C, Gusmaroli G, Wang Y, Zhou J, Wang F, Chen L, Yu L, Iglesias-Pedraz JM, Kircher S, et al. 2008. Coordinated regulation of Arabidopsis thaliana development by light and gibberellins. Nature 451: 475-479.
15. Fridborg I, Kuusk S, Moritz T, Sundberg E. 2001. The Arabidopsis protein SHI represses gibberellin responses in Arabidopsis and barley. Plant Physiol 127: 937-948.
16. Gallego-Bartolome J, Minguet EG, Grau-Enguix F, Abbas M, Locascio A, Thomas SG, Alabadi D, Blazquez MA. 2012. Molecular mechanism for the interaction between gibberellin and brassinosteroid signaling pathways in Arabidopsis. Proc Natl Acad Sci 109: 13446-13451.
17. Gambetta MC, Oktaba K, Muller J. 2009. Essential role of the glycosyltransferase sxc/Ogt in polycomb repression. Science 325: 93-96.
18. Griffiths J, Murase K, Rieu I, Zentella R, Zhang ZL, Powers SJ, Gong F, Phillips AL, Hedden P, Sun T-P, et al. 2006. Genetic characterization and functional analysis of the GID1 gibberellin receptors in Arabidopsis. Plant Cell 18: 3399-3414.
19. Gupta R, Brunak S. 2002. Prediction of glycosylation across the human proteome and the correlation to protein function. Pac Symp Biocomput 7: 310-322.
20. Hanover JA, Krause MW, Love DC. 2010. The hexosamine signaling pathway: O-GlcNAc cycling in feast or famine. Biochim Biophys Acta 1800: 80-95.
21. Hart GW, Slawson C, Ramirez-Correa G, Lagerlof O. 2011. Cross talk between O-GlcNAcylation and phosphorylation: roles in signaling, transcription, and chronic disease. Annu Rev Biochem 80: 825-858.
22. Hartweck LM, Scott CL, Olszewski NE. 2002. Two O-Linked N-acetylglucosamine transferase genes of Arabidopsis thaliana L. Heynh. have overlapping functions necessary for gamete and seed development. Genetics 161: 1279-1291.
23. Hartweck LM, Genger RK, Grey WM, Olszewski NE. 2006. SECRET AGENT and SPINDLY have overlapping roles in the development of Arabidopsis thaliana L. Heyn. J Exp Bot 57: 865-875.
24. Hauvermale AL, Ariizumi T, Steber CM. 2012. Gibberellin signaling: a theme and variations on DELLA repression. Plant Physiol 160: 83-92.
25. Hornitschek P, Lorrain S, Zoete V, Michielin O, Fankhauser C. 2009. Inhibition of the shade avoidance response by formation of non-DNA binding bHLH heterodimers. EMBO J 28: 3893-3902.
26. Hornitschek P, Kohnen MV, Lorrain S, Rougemont J, Ljung K, Lopez-Vidriero I, Franco-Zorrilla JM, Solano R, Trevisan M, Pradervand 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.
27. Hou X, Lee LY, Xia K, Yan Y, Yu H. 2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev Cell 19: 884-894.
28. Hu J, Mitchum MG, Barnaby N, Ayele BT, Ogawa M, Nam E, Lai W-C, Hanada A, Alonso JM, Ecker JR, et al. 2008. Potential sites of bioactive gibberellin production during reproductive growth in Arabidopsis. Plant Cell 20: 320-336.
29. Isono T. 2011. O-GlcNAc-specific antibody CTD110.6 cross-reacts with N-GlcNAc2-modified proteins induced under glucose deprivation. PLoS One 6: e18959.
30. Jacobsen SE, Olszewski NE. 1993. Mutations at the SPINDLY locus of Arabidopsis alter gibberellin signal transduction. Plant Cell 5: 887-896.
31. Jacobsen SE, Binkowski KA, Olszewski NE. 1996. SPINDLY, a tetratricopeptide repeat protein involved in gibberellin signal transduction in Arabidopsis. Proc Natl Acad Sci 93: 9292-9296.
32. Jaillais Y, Chory J. 2010. Unraveling the paradoxes of plant hormone signaling integration. Nat Struct Mol Biol 17: 642-645
33. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4: 363-371.
34. King K, Moritz T, Harberd N. 2001. Gibberellins are not required for normal stem growth in Arabidopsis thaliana in the absence of GAI and RGA. Genetics 159: 767-776.
35. Lazarus MB, Nam Y, Jiang J, Sliz P, Walker S. 2011. Structure of human O-GlcNAc transferase and its complex with a peptide substrate. Nature 469: 564-567.
36. McGinnis KM, Thomas SG, Soule JD, Strader LC, Zale JM, Sun TP, Steber CM. 2003. The Arabidopsis SLEEPY1 gene encodes a putative F-box subunit of an SCF E3 ubiquitin ligase. Plant Cell 15: 1120-1130.
37. Murase K, Hirano Y, Sun T-P, Hakoshima T. 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456: 459-463.
38. Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C, Harmer SL, Maloof JN. 2007. Rhythmic growth explained by coincidence between internal and external cues. Nature 448: 358-361.
39. Oh E, Zhu JY, Bai MY, Arenhart RA, Sun Y, Wang ZY. 2014. Cell elongation is regulated through a central circuit of interacting transcription factors in the Arabidopsis hypocotyl. ELife 3: e03031.
40. Olszewski NE, West CM, Sassi SO, Hartweck LM. 2010. O-GlcNAc protein modification in plants: evolution and function. Biochim Biophys Acta 1800: 49-56.
41. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP. 1997. The Arabidopsis GAI gene defines a signalling pathway that negatively regulates gibberellin responses. Genes Dev 11: 3194-3205.
42. Shafi R, Iyer SP, Ellies LG, O’Donnell N, Marek KW, Chui D, Hart GW, Marth JD. 2000. The O-GlcNAc transferase gene resides on the X chromosome and is essential for embryonic stem cell viability and mouse ontogeny. Proc Natl Acad Sci 97: 5735-5739.
43. Silverstone AL, Mak PYA, Casamitjana Martínez E, Sun T-P. 1997. The new RGA locus encodes a negative regulator of gibberellin response in Arabidopsis thaliana. Genetics 146: 1087-1099.
44. Silverstone AL, Ciampaglio CN, Sun T-P. 1998. The Arabidopsis RGA gene encodes a transcriptional regulator repressing the gibberellin signal transduction pathway. Plant Cell 10: 155-169.
45. Silverstone AL, Jung H-S, Dill A, Kawaide H, Kamiya Y, Sun T-P. 2001. Repressing a repressor: gibberellin-induced rapid reduction of the RGA protein in Arabidopsis. Plant Cell 13: 1555-1566.
46. Silverstone AL, Tseng T-S, Swain S, Dill A, Jeong SY, Olszewski NE, Sun T-P. 2007. Functional analysis of SPINDLY in gibberellin signaling in Arabidopsis. Plant Physiol 143: 987-1000
47. Slawson C, Hart GW. 2011. O-GlcNAc signalling: implications for cancer cell biology. Nat Rev Cancer 11: 678-684
48. Soy J, Leivar P, Gonzalez-Schain N, Sentandreu M, Prat S, Quail PH, Monte E. 2012. Phytochrome-imposed oscillations in PIF3 protein abundance regulate hypocotyl growth under diurnal light/dark conditions in Arabidopsis. Plant J 71: 390-401
49. Sun TP. 2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr Biol 21: R338-R345.
50. Sundaresan V, Springer P, Volpe T, Haward S, Jones JD, Dean C, Ma H, Martienssen R. 1995. Patterns of gene action in plant development revealed by enhancer trap and gene trap transposable elements. Genes Dev 9: 1797-1810.
51. Torii KU, Mitsukawa N, Oosumi T, Matsuura Y, Yokoyama R, Whittier RF, Komeda Y. 1996. The Arabidopsis ERECTA gene encodes a putative receptor protein kinase with extracellular leucine-rich repeats. Plant Cell 8: 735-746.
52. Udeshi ND, Compton PD, Shabanowitz J, Hunt DF, Rose KL. 2008. Methods for analyzing peptides and proteins on a chromatographic timescale by electron-transfer dissociation mass spectrometry. Nat Protoc 3: 1709-1717.
53. Ueguchi-Tanaka M, Ashikari M, Nakajima M, Itoh H, Katoh E, Kobayashi M, Chow TY, Hsing YI, Kitano H, Yamaguchi I, et al. 2005. GIBBERELLIN INSENSITIVE DWARF1 encodes a soluble receptor for gibberellin. Nature 437: 693-698.
54. Vocadlo DJ, Hang HC, Kim EJ, Hanover JA, Bertozzi CR. 2003. A chemical approach for identifying O-GlcNAc-modified proteins in cells. Proc Natl Acad Sci 100: 9116-9121.
55. Xiao J, Xu S, Li C, Xu Y, Xing L, Niu Y, Huan Q, Tang Y, Zhao C, Wagner D, et al. 2014. O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat. Nature Commun 5: 4572.
56. Xu H, Liu Q, Yao T, Fu X. 2014. Shedding light on integrative GA signaling. Curr Opin Plant Biol 21: 89-95.
57. Yang X, Zhang F, Kudlow JE. 2002. Recruitment of O-GlcNAc transferase to promoters by corepressor mSin3A: coupling protein O-GlcNAcylation to transcriptional repression. Cell 110: 69-80.
58. Yang DL, Yao J, Mei CS, Tong XH, Zeng LJ, Li Q, Xiao LT, Sun TP, Li J, Deng XW, et al. 2012. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proc Natl Acad Sci 109: E1192-E1200.
59. Zentella R, Zhang ZL, Park M, Thomas SG, Endo A, Murase K, Fleet CM, Jikumaru Y, Nambara E, Kamiya Y, et al. 2007. Global analysis of DELLA direct targets in early gibberellin signaling in Arabidopsis. Plant Cell 19: 3037-3057.
60. Zhang F, Su K, Yang X, Bowe DB, Paterson AJ, Kudlow JE. 2003. O-GlcNAc modification is an endogenous inhibitor of the proteasome. Cell 115: 715-725.
61. Zhang ZL, Ogawa M, Fleet CM, Zentella R, Hu J, Heo J-O, Lim J, Kamiya Y, Yamaguchi S, Sun T-P. 2011. SCARECROW-LIKE 3 promotes gibberellin signaling by antagonizing DELLA in Arabidopsis. Proc Natl Acad Sci 108: 2160-2165.