Regulation of flowering time by the miR156-mediated age pathway

Journal of Experimental Botany

Volumn 65, Issue 17, 2014, Pages 4723-4730

  Wang, Jia Wei ^a  

^a INSTITUTE OF PLANT PHYSIOLOGY AND ECOLOGY   (China)

Author keywords

Age; Flowering time; MicroRNA

Indexed keywords

MICRORNA;

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

ARABIDOPSIS; FLOWERS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MICRORNAS;

EID: 84907384889     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/eru246     Document Type: Review

References (102)

1. Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T. 2005. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309, 1052-1056.
2. Amasino RM, Michaels SD. 2010. The timing of flowering. Plant Physiology 154, 516-520.
3. An H, Roussot C, Suarez-Lopez P et al. 2004. CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131, 3615-3626.
4. Andres F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nature Reviews Genetics 13, 627-639.
5. Aukerman MJ, Sakai H. 2003. Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15, 2730-2741.
6. Bäurle I, Dean C. 2006. The timing of developmental transitions in plants. Cell 125, 655-664.
7. Bartel DP. 2009. MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
8. Bergonzi S, Albani MC, Ver Loren van Themaat E, Nordstrom KJ, Wang R, Schneeberger K, Moerland PD, Coupland G. 2013. Mechanisms of age-dependent response to winter temperature in perennial flowering of Arabis alpina. Science 340, 1094-1097.
9. Bhogale S, Mahajan AS, Natarajan B, Rajabhoj M, Thulasiram HV, Banerjee AK. 2014. MicroRNA156: A potential graft-transmissible microRNA that modulates plant architecture and tuberization in Solanum tuberosum ssp. andigena. Plant Physiology 164, 1011-1027.
10. Brodersen P, Sakvarelidze-Achard L, Bruun-Rasmussen M, Dunoyer P, Yamamoto YY, Sieburth L, Voinnet O. 2008. Widespread translational inhibition by plant miRNAs and siRNAs. Science 320, 1185-1190.
11. Cardon G, Hohmann S, Klein J, Nettesheim K, Saedler H, Huijser P. 1999. Molecular characterisation of the Arabidopsis SBP-box genes. Gene 237, 91-104.
12. Causier B, Ashworth M, Guo W, Davies B. 2012. The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiology 158, 423-438.
13. Chen X. 2004. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development. Science 303, 2022-2025.
14. 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. Plant Cell 23, 289-303.
15. Chuck G, Cigan AM, Saeteurn K, Hake S. 2007. The heterochronic maize mutant Corngrass1 results from overexpression of a tandem microRNA. Nature Genetics 39, 544-549.
16. Chuck GS, Tobias C, Sun L, Kraemer F, Li C, Dibble D, Arora R, Bragg JN, Vogel JP, Singh S, Simmons BA, Pauly M, Hake S. 2011. Overexpression of the maize Corngrass1 microRNA prevents flowering, improves digestibility, and increases starch content of switchgrass. Proceedings of the National Academy of Sciences, USA 108, 17550-17555.
17. Corbesier L, Vincent C, Jang S et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316, 1030-1033.
18. Crevillen P, Sonmez C, Wu Z, Dean C. 2013. A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. The EMBO Journal 32, 140-148.
19. Dill A, Jung HS, Sun TP. 2001. The DELLA motif is essential for gibberellin-induced degradation of RGA. Proceedings of the National Academy of Sciences, USA 98, 14162-14167.
20. Eviatar-Ribak T, Shalit-Kaneh A, Chappell-Maor L, Amsellem Z, Eshed Y, Lifschitz E. 2013. A cytokinin-activating enzyme promotes tuber formation in tomato. Current Biology 23, 1057-1064.
21. Fowler S, Lee K, Onouchi H, Samach A, Richardson K, Morris B, Coupland G, Putterill J. 1999. GIGANTEA: a circadian clock-controlled gene that regulates photoperiodic flowering in Arabidopsis and encodes a protein with several possible membrane-spanning domains. The EMBO Journal 18, 4679-4688.
22. Galvao VC, Horrer D, Kuttner F, Schmid M. 2012. Spatial control of flowering by DELLA proteins in Arabidopsis thaliana. Development 139, 4072-4082.
23. Gandikota M, Birkenbihl RP, Hohmann S, Cardon GH, Saedler H, Huijser P. 2007. The miRNA156/157 recognition element in the 3' UTR of the Arabidopsis SBP box gene SPL3 prevents early flowering by translational inhibition in seedlings. The Plant Journal 49, 683-693.
24. Harberd NP. 2003. Botany. Relieving DELLA restraint. Science 299, 1853-1854.
25. He Y, Michaels SD, Amasino RM. 2003. Regulation of flowering time by histone acetylation in Arabidopsis. Science 302, 1751-1754.
26. Heo JB, Sung S. 2011. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331, 76-79.
27. Huijser P, Schmid M. 2011. The control of developmental phase transitions in plants. Development 138, 4117-4129.
28. Jaeger KE, Wigge PA. 2007. FT protein acts as a long-range signal in Arabidopsis. Current Biology 17, 1050-1054.
29. Jang S, Marchal V, Panigrahi KC, Wenkel S, Soppe W, Deng XW, Valverde F, Coupland G. 2008. Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. The EMBO Journal 27, 1277-1288.
30. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C. 2000. Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344-347.
31. Jung JH, Ju Y, Seo PJ, Lee JH, Park CM. 2011a. The SOC1-SPL module integrates photoperiod and gibberellic acid signals to control flowering time in Arabidopsis. The Plant Journal 69, 577-588.
32. Jung JH, Seo PJ, Kang SK, Park CM. 2011b. miR172 signals are incorporated into the miR156 signaling pathway at the SPL3/4/5 genes in Arabidopsis developmental transitions. Plant Molecular Biology 76, 35-45.
33. Jung JH, Seo YH, Seo PJ, Reyes JL, Yun J, Chua NH, Park CM. 2007. The GIGANTEA-regulated microRNA172 mediates photoperiodic flowering independent of CONSTANS in Arabidopsis. Plant Cell 19, 2736-2748.
34. Kobayashi Y, Weigel D. 2007. Move on up, it's time for change- mobile signals controlling photoperiod-dependent flowering. Genes and Development 21, 2371-2384.
35. Lal S, Pacis LB, Smith HM. 2011. Regulation of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes/microRNA156 module by the homeodomain proteins PENNYWISE and POUND-FOOLISH in Arabidopsis. Molecular Plant 4, 1123-1132.
36. Lee J, Lee I. 2010. Regulation and function of SOC1, a flowering pathway integrator. Journal of Experimental Botany 61, 2247-2254.
37. Li S, Liu L, Zhuang X et al. 2013. MicroRNAs inhibit the translation of target mRNAs on the endoplasmic reticulum in Arabidopsis. Cell 153, 562-574.
38. Lim MH, Kim J, Kim YS, Chung KS, Seo YH, Lee I, Kim J, Hong CB, Kim HJ, Park CM. 2004. A new Arabidopsis gene, FLK, encodes an RNA binding protein with K homology motifs and regulates flowering time via FLOWERING LOCUS C. Plant Cell 16, 731-740.
39. Lin MK, Belanger H, Lee YJ et al. 2007. FLOWERING LOCUS T protein may act as the long-distance florigenic signal in the cucurbits. Plant Cell 19, 1488-1506.
40. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C. 2010. Targeted 3' processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327, 94-97.
41. Liu L, Liu C, Hou X, Xi W, Shen L, Tao Z, Wang Y, Yu H. 2012. FTIP1 is an essential regulator required for florigen transport. PLoS Biology 10, e1001313.
42. Liu LJ, Zhang YC, Li QH, Sang Y, Mao J, Lian HL, Wang L, Yang HQ. 2008. COP1-mediated ubiquitination of CONSTANS is implicated in cryptochrome regulation of flowering in Arabidopsis. Plant Cell 20, 292-306.
43. Llave C, Xie Z, Kasschau KD, Carrington JC. 2002. Cleavage of Scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053-2056.
44. Long JA, Ohno C, Smith ZR, Meyerowitz EM. 2006. TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312, 1520-1523.
45. Macknight R, Bancroft I, Page T et al. 1997. FCA, a gene controlling flowering time in Arabidopsis, encodes a protein containing RNA-binding domains. Cell 89, 737-745.
46. Manzano D, Marquardt S, Jones AM, Baurle I, Liu F, Dean C. 2009. Altered interactions within FY/AtCPSF complexes required for Arabidopsis FCA-mediated chromatin silencing. Proceedings of the National Academy of Sciences, USA 106, 8772-8777.
47. Mathieu J, Warthmann N, Kuttner F, Schmid M. 2007. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Current Biology 17, 1055-1060.
48. Mathieu J, Yant LJ, Murdter F, Kuttner F, Schmid M. 2009. Repression of flowering by the miR172 target SMZ. PLoS Biology 7, e1000148.
49. Mockler TC, Yu X, Shalitin D et al. 2004. Regulation of flowering time in Arabidopsis by K homology domain proteins. Proceedings of the National Academy of Sciences, USA 101, 12759-12764.
50. Moon J, Suh SS, Lee H, Choi KR, Hong CB, Paek NC, Kim SG, Lee I. 2003. The SOC1 MADS-box gene integrates vernalization and gibberellin signals for flowering in Arabidopsis. The Plant Journal 35, 613-623.
51. Murase K, Hirano Y, Sun TP, Hakoshima T. 2008. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1. Nature 456, 459-463.
52. Park DH, Somers DE, Kim YS, Choy YH, Lim HK, Soh MS, Kim HJ, Kay SA, Nam HG. 1999. Control of circadian rhythms and photoperiodic flowering by the Arabidopsis GIGANTEA gene. Science 285, 1579-1582.
53. Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP. 1997. The Arabidopsis GAI gene defines a signaling pathway that negatively regulates gibberellin responses. Genes and Development 11, 3194-3205.
54. Poethig RS. 2003. Phase change and the regulation of developmental timing in plants. Science 301, 334-336.
55. Poethig RS. 2013. Vegetative phase change and shoot maturation in plants. Current Topics in Developmental Biology 105, 125-152.
56. Porri A, Torti S, Romera-Branchat M, Coupland G. 2012. Spatially distinct regulatory roles for gibberellins in the promotion of flowering of Arabidopsis under long photoperiods. Development 139, 2198-2209.
57. Proveniers M. 2013. Sugars speed up the circle of life. elife 2, e00625.
58. Putterill J, Robson F, Lee K, Simon R, Coupland G. 1995. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80, 847-857.
59. Reinhart BJ, Weinstein EG, Rhoades MW, Bartel B, Bartel DP. 2002. MicroRNAs in plants. Genes and Development 16, 1616-1626.
60. Rhoades MW, Reinhart BJ, Lim LP, Burge CB, Bartel B, Bartel DP. 2002. Prediction of plant microRNA targets. Cell 110, 513-520.
61. Richter R, Bastakis E, Schwechheimer C. 2013. Cross-repressive interactions between SOC1 and the GATAs GNC and GNL/CGA1 in the control of greening, cold tolerance, and flowering time in Arabidopsis. Plant Physiology 162, 1992-2004.
62. Richter R, Behringer C, Muller IK, Schwechheimer C. 2010. The GATA-type transcription factors GNC and GNL/CGA1 repress gibberellin signaling downstream from DELLA proteins and PHYTOCHROMEINTERACTING FACTORS. Genes and Development 24, 2093-2104.
63. Rosa S, De Lucia F, Mylne JS, Zhu D, Ohmido N, Pendle A, Kato N, Shaw P, Dean C. 2013. Physical clustering of FLC alleles during Polycomb-mediated epigenetic silencing in vernalization. Genes and Development 27, 1845-1850.
64. Schmid M, Uhlenhaut NH, Godard F, Demar M, Bressan R, Weigel D, Lohmann JU. 2003. Dissection of floral induction pathways using global expression analysis. Development 130, 6001-6012.
65. Schomburg FM, Patton DA, Meinke DW, Amasino RM. 2001. FPA, a gene involved in floral induction in Arabidopsis, encodes a protein containing RNA-recognition motifs. Plant Cell 13, 1427-1436.
66. Schwab R, Palatnik JF, Riester M, Schommer C, Schmid M, Weigel D. 2005. Specific effects of microRNAs on the plant transcriptome. Developmental Cell 8, 517-527.
67. Schwarz S, Grande AV, Bujdoso N, Saedler H, Huijser P. 2008. The microRNA regulated SBP-box genes SPL9 and SPL15 control shoot maturation in Arabidopsis. Plant Molecular Biology 67, 183-195.
68. Schwechheimer C, Willige BC. 2009. Shedding light on gibberellic acid signalling. Current Opinion in Plant Biology 12, 57-62.
69. Searle I, He Y, 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.
70. Simpson GG, Dijkwel PP, Quesada V, Henderson I, Dean C. 2003. FY is an RNA 3' end-processing factor that interacts with FCA to control the Arabidopsis floral transition. Cell 113, 777-787.
71. Song J, Angel A, Howard M, Dean C. 2012. Vernalization-a coldinduced epigenetic switch. Journal of Cell Science 125, 3723-3731.
72. Song J, Irwin J, Dean C. 2013. Remembering the prolonged cold of winter. Current Biology 23, R807-811.
73. Srikanth A, Schmid M. 2011. Regulation of flowering time: all roads lead to Rome. Cellular and Molecular Life Sciences 68, 2013-2037.
74. Sun Q, Csorba T, Skourti-Stathaki K, Proudfoot NJ, Dean C. 2013. R-loop stabilization represses antisense transcription at the Arabidopsis FLC locus. Science 340, 619-621.
75. Torti S, Fornara F, Vincent C, Andres F, Nordstrom K, Gobel U, Knoll D, Schoof H, Coupland G. 2012. Analysis of the Arabidopsis shoot meristem transcriptome during floral transition identifies distinct regulatory patterns and a leucine-rich repeat protein that promotes flowering. Plant Cell 24, 444-462.
76. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. 2004. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303, 1003-1006.
77. van Dijken AJ, Schluepmann H, Smeekens SC. 2004. Arabidopsis trehalose-6-phosphate synthase 1 is essential for normal vegetative growth and transition to flowering. Plant Physiology 135, 969-977.
78. Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M. 2013. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339, 704-707.
79. Wang JW, Czech B, Weigel D. 2009a. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138, 738-749.
80. Wang JW, Park MY, Wang LJ, Koo Y, Chen XY, Weigel D, Poethig RS. 2011a. miRNA control of vegetative phase change in trees. PLoS Genetics 7, e1002012.
81. Wang JW, Schwab R, Czech B, Mica E, Weigel D. 2008. Dual effects of miR156-targeted SPL genes and CYP78A5/KLUH on plastochron length and organ size in Arabidopsis thaliana. Plant Cell 20, 1231-1243.
82. Wang R, Albani MC, Vincent C, Bergonzi S, Luan M, Bai Y, Kiefer C, Castillo R, Coupland G. 2011b. Aa TFL1 confers an age-dependent response to vernalization in perennial Arabis alpina. Plant Cell 23, 1307-1321.
83. Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC. 2009b. PEP1 regulates perennial flowering in Arabis alpina. Nature 459, 423-427.
84. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309, 1056-1059.
85. Wilson RN, Heckman JW, Somerville CR. 1992. Gibberellin is required for flowering in Arabidopsis thaliana under short days. Plant Physiology 100, 403-408.
86. Wu G, Park MY, Conway SR, Wang JW, Weigel D, Poethig RS. 2009. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138, 750-759.
87. Wu G, Poethig RS. 2006. Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133, 3539-3547.
88. Xie K, Shen J, Hou X, Yao J, Li X, Xiao J, Xiong L. 2012. Gradual increase of miR156 regulates temporal expression changes of numerous genes during leaf development in rice. Plant Physiology 158, 1382-1394.
89. Xie K, Wu C, Xiong L. 2006. Genomic organization, differential expression, and interaction of SQUAMOSA promoter-binding-like transcription factors and microRNA156 in rice. Plant Physiology 142, 280-293.
90. Xing S, Salinas M, Hohmann S, Berndtgen R, Huijser P. 2010. miR156-targeted and nontargeted SBP-box transcription factors act in concert to secure male fertility in Arabidopsis. Plant Cell 22, 3935-3950.
91. Yamaguchi A, Abe M. 2012. Regulation of reproductive development by non-coding RNA in Arabidopsis: to flower or not to flower. Journal of Plant Research 125, 693-704.
92. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D. 2009. The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Developmental Cell 17, 268-278.
93. Yang L, Conway SR, Poethig RS. 2011. Vegetative phase change is mediated by a leaf-derived signal that represses the transcription of miR156. Development 138, 245-249.
94. Yang L, Xu M, Koo Y, He J, Poethig RS. 2013. Sugar promotes vegetative phase change in Arabidopsis thaliana by repressing the expression of MIR156A and MIR156C. elife 2, e00260.
95. Yanovsky MJ, Kay SA. 2002. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419, 308-312.
96. Yant L, Mathieu J, Dinh TT, Ott F, Lanz C, Wollmann H, Chen X, Schmid M. 2010. Orchestration of the floral transition and floral development in Arabidopsis by the bifunctional transcription factor APETALA2. Plant Cell 22, 2156-2170.
97. Yoshikawa T, Ozawa S, Sentoku N, Itoh J, Nagato Y, Yokoi S. 2013. Change of shoot architecture during juvenile-to-adult phase transition in soybean. Planta 238, 229-237.
98. Yu S, Cao L, Zhou CM, Zhang TQ, Lian H, Sun Y, Wu JQ, Huang JR, Wang GD, Wang JW. 2013. Sugar is an endogenous cue for juvenile-toadult phase transition in plants. elife 2, e00269.
99. Yu S, Galvao VC, Zhang YC, Horrer D, Zhang TQ, Hao YH, Feng YQ, Wang S, Schmid M, Wang JW. 2012. Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. Plant Cell 24, 3320-3332.
100. Zhou CM, Wang JW. 2013. Regulation of flowering time by microRNAs. Journal of Genetics and Genomics 40, 211-215.
101. Zhou CM, Zhang TQ, Wang X, Yu S, Lian H, Tang H, Feng ZY, Zozomova-Lihova J, Wang JW. 2013. Molecular basis of agedependent vernalization in Cardamine flexuosa. Science 340, 1097-1100.
102. Zografos BR, Sung S. 2012. Vernalization-mediated chromatin changes. Journal of Experimental Botany 63, 4343-4348.