ABSCISIC ACID-INSENSITIVE 4 negatively regulates flowering through directly promoting Arabidopsis FLOWERING LOCUS C transcription

Journal of Experimental Botany

Volumn 67, Issue 1, 2016, Pages 195-205

  Shu, Kai ^a,b   Chen, Qian ^a,c   Wu, Yaorong ^a   Liu, Ruijun ^a,c   Zhang, Huawei ^a   Wang, Shengfu ^a   Tang, Sanyuan ^a   Yang, Wenyu ^b   Xie, Qi ^a  

^a INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

^b SICHUAN AGRICULTURAL UNIVERSITY   (China)

^c UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

ABA; ABI4; Chromatin immunoprecipitation; FLC; Flowering; Transcription factor

Indexed keywords

ABI4 PROTEIN, ARABIDOPSIS; ABSCISIC ACID; ARABIDOPSIS PROTEIN; FLF PROTEIN, ARABIDOPSIS; MADS DOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ARABIDOPSIS; FLOWER; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ABSCISIC ACID; ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; MADS DOMAIN PROTEINS; TRANSCRIPTION FACTORS;

EID: 84954490325     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erv459     Document Type: Article

References (60)

1. Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van der Straeten D, Peng JR, Harberd NP. 2006. Integration of plant responses to environmentally activated phytohormonal signals. Science 311, 91-94.
2. Achard P, Herr A, Baulcombe DC, Harberd NP. 2004. Modulation of floral development by a gibberellin-regulated microRNA. Development 131, 3357-3365.
3. Andres F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13, 627-639.
4. Angel A, Song J, Yang H, Questa JI, Dean C, Howard M. 2015. Vernalizing cold is registered digitally at FLC. Proceedings of the National Academy of Sciences, USA 112, 4146-4151.
5. Arenas-Huertero F, Arroyo A, Zhou L, Sheen J, Leon P. 2000. Analysis of Arabidopsis glucose insensitive mutants, gin5 and gin6, reveals a central role of the plant hormone ABA in the regulation of plant vegetative development by sugar. Genes and Development 14, 2085-2096.
6. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C. 2004. Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427, 164-167.
7. Bechtold N, Pelletier G. 1998. In planta Agrobacterium-mediated transformation of adult Arabidopsis thaliana plants by vacuum infiltration. Methods in Molecular Biology 82, 259-266.
8. Berry S, Dean C. 2015. Environmental perception and epigenetic memory: mechanistic insight through FLC. The Plant Journal 83, 133-148
9. Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D. 1998. Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. The Plant Cell 10, 791-800.
10. Boss PK, Bastow RM, Mylne JS, Dean C. 2004. Multiple pathways in the decision to flower: Enabling, promoting, and resetting. The Plant Cell 16, S18-S31.
11. Bossi F, Cordoba E, Dupre P, Mendoza MS, Roman CS, Leon P. 2009. The Arabidopsis ABA-INSENSITIVE (ABI) 4 factor acts as a central transcription activator of the expression of its own gene, and for the induction of ABI5 and SBE2.2 genes during sugar signaling. The Plant Journal 59, 359-374.
12. Choi K, Kim J, Hwang HJ, Kim S, Park C, Kim SY, Lee I. 2011. The FRIGIDA complex activates transcription of FLC, a strong flowering repressor in Arabidopsis, by recruiting chromatin modification factors. The Plant Cell 23, 289-303.
13. Corbesier L, Vincent C, Jang SH, et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033.
14. Craufurd PQ, Wheeler TR. 2009. Climate change and the flowering time of annual crops. Journal of Experimental Botany 60, 2529-2539.
15. Cui F, Liu LJ, Zhao QZ, Zhang ZH, Li QL, Lin BY, Wu YR, Tang SY, Xie Q. 2012. Arabidopsis ubiquitin conjugase UBC32 is an ERAD component that functions in brassinosteroid-mediated salt stress tolerance. The Plant Cell 24, 233-244.
16. Deal RB, Topp CN, McKinney EC, Meagher RB. 2007. Repression of flowering in Arabidopsis requires activation of FLOWERING LOCUS C expression by the histone variant H2A.Z. The Plant Cell 19, 74-83.
17. Dennis ES, Peacock WJ. 2007. Epigenetic regulation of flowering. Current Opinion in Plant Biology 10, 520-527.
18. Domagalska MA, Sarnowska E, Nagy F, Davis SJ. 2010. Genetic analyses of interactions among gibberellin, abscisic acid, and brassinosteroids in the control of flowering time in Arabidopsis thaliana. PLoS One 5, e14012.
19. Finkelstein RR. 1994. Mutations at two new Arabidopsis ABA response loci are similar to the abi3 mutations. The Plant Journal 5, 765-771.
20. Finkelstein RR, Wang ML, Lynch TJ, Rao S, Goodman HM. 1998. The Arabidopsis abscisic acid response locus ABI4 encodes an APETALA2 domain protein. The Plant Cell 10, 1043-1054.
21. Foyer CH, Kerchev PI, Hancock RD. 2012. The ABA-INSENSITIVE-4 (ABI4) transcription factor links redox, hormone and sugar signaling pathways. Plant Signaling and Behavior 7, 276-281.
22. He YH. 2009. Control of the transition to flowering by chromatin modifications. Molecular Plant 2, 554-564.
23. He YH. 2012. Chromatin regulation of flowering. Trends in Plant Science 17, 556-562.
24. Hepworth SR, Valverde F, Ravenscroft D, Mouradov A, Coupland G. 2002. Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. EMBO Journal 21, 4327-4337.
25. Jefferson RA, Kavanagh TA, Bevan MW. 1987. GUS fusions:-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6, 3901-3907.
26. Kerchev PI, Pellny TK, Vivancos PD, Kiddle G, Hedden P, Driscoll S, Vanacker H, Verrier P, Hancock RD, Foyer CH. 2011. The transcription factor ABI4 is required for the ascorbic acid-dependent regulation of growth and regulation of jasmonate-dependent defense signaling pathways in Arabidopsis. The Plant Cell 23, 3319-3334.
27. Kim SY, Michaels SD. 2006. SUPPRESSOR OF FRI 4 encodes a nuclear-localized protein that is required for delayed flowering in winterannual Arabidopsis. Development 133, 4699-4707.
28. Komeda Y. 2004. Genetic regulation of time to flower in Arabidopsis thaliana. Annual Review of Plant Biology 55, 521-535.
29. Kong Y, Chen S, Yang Y, An C. 2013. ABA-insensitive (ABI) 4 and ABI5 synergistically regulate DGAT1 expression in Arabidopsis seedlings under stress. FEBS Letters 587, 3076-3082.
30. Koornneef M, Alonso-Blanco C, Peeters AJ, Soppe W. 1998. Genetic control of flowering time in Arabidopsis. Annual Review of Plant Physiology and Plant Molecular Biology 49, 345-370.
31. Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim IJ, Mittler R, Chory J. 2007. Signals from chloroplasts converge to regulate nuclear gene expression. Science 316, 715-719.
32. Laby RJ, Kincaid MS, Kim D, Gibson SI. 2000. The Arabidopsis sugarinsensitive mutants sis4 and sis5 are defective in abscisic acid synthesis and response. The Plant Journal 23, 587-596.
33. Lang A. 1957. The effect of gibberellin upon flower formation. Proceedings of the National Academy of Sciences, USA 43, 709-717.
34. Liu LJ, Zhang YY, Tang SY, Zhao QZ, Zhang ZH, Zhang HW, Dong L, Guo HS, Xie Q. 2010. An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. The Plant Journal 61, 893-903.
35. Mai YX, Wang L, Yang HQ. 2011. A gain-of-function mutation in IAA7/ AXR2 confers late flowering under short-day light in Arabidopsis. Journal of Integrative Plant Biology 53, 480-492.
36. Matsoukas IG, Massiah AJ, Thomas B. 2013. Starch metabolism and antiflorigenic signals modulate the juvenile-to-adult phase transition in Arabidopsis. Plant, Cell and Environment 36, 1802-1811.
37. Michaels SD. 2009. Flowering time regulation produces much fruit. Current Opinion in Plant Biology 12, 75-80.
38. Michaels SD, Amasino RM. 1999. FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. The Plant Cell 11, 949-956.
39. Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K. 2001. Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiology 127, 252-261.
40. Penfield S, Li Y, Gilday AD, Graham S, Graham IA. 2006. Arabidopsis ABA INSENSITIVE4 regulates lipid mobilization in the embryo and reveals repression of seed germination by the endosperm. The Plant Cell 18, 1887-1899.
41. Reeves W, Lynch T, Mobin R, Finkelstein R. 2011. Direct targets of the transcription factors ABA-insensitive(ABI)4 and ABI5 reveal synergistic action by ABI4 and several bZIP ABA response factors. Plant Molecular Biology 75, 347-363.
42. Riboni M, Galbiati M, Tonelli C, Conti L. 2013. GIGANTEA enables drought escape response via abscisic acid-dependent activation of the florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. Plant Physiology 162, 1706-1719.
43. Searle I, He YH, Turck F, Vincent C, Fornara F, Krober S, Amasino RA, Coupland G. 2006. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes and Development 20, 898-912.
44. Seo M, Hanada A, Kuwahara A, et al. 2006. Regulation of hormone metabolism in Arabidopsis seeds: phytochrome regulation of abscisic acid metabolism and abscisic acid regulation of gibberellin metabolism. The Plant Journal 48, 354-366.
45. Shan H, Chen S, Jiang J, et al. 2012. Heterologous expression of the chrysanthemum R2R3-MYB transcription factor CmMYB2 enhances drought and salinity tolerance, increases hypersensitivity to ABA and delays flowering in Arabidopsis thaliana. Molecular Biotechnology 51, 160-173.
46. Shkolnik-Inbar D, Bar-Zvi D. 2010. ABI4 mediates abscisic acid and cytokinin inhibition of lateral root formation by reducing polar auxin transport in Arabidopsis. The Plant Cell 22, 3560-3573.
47. Shu K, Wu Y, Yang W, Xie Q. 2014. Concurrent deficiency of gibberellins and abscisic acid causes plant male sterility. Journal of Genetics and Genomics 41, 601-604.
48. Shu K, Zhang H, Wang S, Chen M, Wu Y, Tang S, Liu C, Feng Y, Cao X, Xie Q. 2013. ABI4 regulates primary seed dormancy by regulating the biogenesis of abscisic acid and gibberellins in Arabidopsis. PLoS Genetics 9, e1003577.
49. Soderman EM, Brocard IM, Lynch TJ, Finkelstein RR. 2000. Regulation and function of the arabidopsis ABA-insensitive4 gene in seed and abscisic acid response signaling networks. Plant Physiology 124, 1752-1765.
50. Son GH, Park BS, Song JT, Seo HS. 2014. FLC-mediated flowering repression is positively regulated by sumoylation. Journal of Experimental Botany 65, 339-351.
51. Song YH, Ito S, Imaizumi T. 2013. Flowering time regulation: photoperiod-and temperature-sensing in leaves. Trends in Plant Science 18, 575-583.
52. Stalberg K, Ellerstrom M, Josefsson LG, Rask L. 1993 Deletion analysis of a 2S seed storage protein promoter in Brassica napus in transgenic tobacco. Plant Molecular Biology 23, 671-683.
53. Sun XW, Feng PQ, Xu XM, Guo HL, Ma JF, Chi W, Lin RC, Lu CM, Zhang LX. 2011. A chloroplast envelope-bound PHD transcription factor mediates chloroplast signals to the nucleus. Nature Communications 2, 477.
54. Wang YP, Li L, Ye TT, Lu YM, Chen X, Wu Y. 2013. The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. Journal of Experimental Botany 64, 675-684.
55. Wei W, Zhang YQ, Tao JJ, Chen HW, Li QT, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY. 2015. The Alfin-like homeodomain finger protein AL5 suppresses multiple negative factors to confer abiotic stress tolerance in Arabidopsis. The Plant Journal 81, 871-883.
56. Wind JJ, Peviani A, Snel B, Hanson J, Smeekens SC. 2013. ABI4: versatile activator and repressor. Trends in Plant Science 18, 125-132.
57. Yaish MW, El-kereamy A, Zhu T, Beatty PH, Good AG, Bi YM, Rothstein SJ. 2010. The APETALA-2-like transcription factor OsAP2-39 controls key interactions between abscisic acid and gibberellin in rice. PLoS Genetics 6, e1001098.
58. Yamamoto T, Lin HX, Sasaki T, Yano M. 2000. Identification of heading date quantitative trait locus Hd6 and characterization of its epistatic interactions with Hd2 in rice using advanced backcross progeny. Genetics 154, 885-891.
59. Yang Y, Yu XC, Song LF, An CC. 2011. ABI4 activates DGAT1 expression in Arabidopsis seedlings during nitrogen deficiency. Plant Physiology 156, 873-883.
60. Zhou L, Jang JC, Jones TL, Sheen J. 1998. Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucoseinsensitive mutant. Proceedings of the National Academy of Sciences, USA 95, 10294-10299.