Research Progress of Flowering Gene Regulatory Networks in Arabidopsis thaliana

doi:10.13560/j.cnki.biotech.bull.1985.2014.12.001

Abstract

Abstract: Flowering is one of the most important phase changes during the vegetative to reproductive growth in the life cycle of higher plants. And in recent years, flowering regulation has become a hot research in plant molecular biology. In current study, the gene regulatory network controlling flowering in Arabidopsis thaliana has grown up to a intricate web of crosstalk, feedback, and redundancy, bound tightly with other developmental processes by “process integrators”. The paper only briefly contextualizes the genetic pathways involved in regulating flowering, and focuses on the integration of signals at the shoot apical meristem(SAM), the spatial-temporal regulation of flower development, and finally functions that floral-related genes have in processes other than flowering time or flower development in A. thaliana. Also we discuss about the prospects of future research works, according to the present research status．

Key words: Flowering gene regulatory networks, Flowering integrators, Integration of signals, Flower development, Spatial-temporal regulation

Li Jing, Gu Huiying, Wang Zhimin, Tang Qinglin, Song Ming. Research Progress of Flowering Gene Regulatory Networks in Arabidopsis thaliana[J]. Biotechnology Bulletin, 2014, 0(12): 1-8.

References

[1] Niu W, Lu ZJ, Zhong M, et al. Diverse transcription factor binding features revealed by genome-wide ChIP-seq in C. elegans[J]. Genome Research, 2011, 21: 245-254.
[2] Redestig H, Weicht D, Selbig J, Hannah MA. Transcription factor target prediction using multiple short expression time series from Arabidopsis thaliana[J]. BMC Bioinformatics, 2007, 8: 454.
[3] Srikanth A, Schmid M. Regulation of flowering time: all roads lead to Rome[J]. Cell Mol Life Sci, 2011, 68: 2013-2037.
[4] Michaels SD. Flowering time regulation produces much fruit[J]. Curr Opin Plant Biol, 2009, 12: 75-80.
[5] Putterill J, Laurie R, Macknight R. It’s time to flower: the genetic control of flowering time[J]. Bioessays, 2004, 26(4)：363-373.
[6] Corbesier L, Vincent C, Jang S, et al. FT protein movement contribu-tes to long-distance signaling in floral induction of Arabidopsis[J]. Science, 2007, 316: 1030-1033.
[7] Jaeger KE, Wigge PA. FT protein acts as a long-range signal in Arabidopsis[J]. Curr Biol, 2007, 17: 1050-1054.
[8] Lifschitz E, Eviatar T, Rozman A, et al. The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli[J]. PANS, 2006, 103 (16)：6398-6403.
[9] Imaizumi T, Kay SA. Photoperiodic control of flowering: not only by coincidence[J]. Trends in Plant Science, 2006, 11(11)：550-558.
[10] Abe M, Kobayashi Y, Yamamoto S, et al. FD, a bZIP protein medi-ating signals from the floral pathway integrator FT at the shoot apex [J]. Science, 2005, 309: 1052-1056.
[11] Wigge PA, Kim MC, Jaeger KE, et al. Integration of spatial and temporal information during floral induction in Arabidopsis[J]. Science, 2005, 309: 1056-1059.
[12] Kardailsky I, Shukla VK, Ahn JH, et al. Activation tagging of the floral inducer FT[J]. Science, 1999, 286: 1962-1965.
[13] Blazquez MA, Weigel D. Integration of floral inductive signals in Arabidopsis[J]. Nature, 2000, 404(6780)：889-892.
[14] Blazquez MA, Soowal LN, Lee I, Weigel D. LEAFY expression and flower initiation in Arabidopsis[J]. Development, 1997, 124(19)：3835-3844.
[15] Michaels SD, Himelblau E, Kim SY, et al. Integration of flowering signals in winter-annual Arabidopsis[J]. Plant Physiol, 2005, 137(1)：149-156.
[16] Moon J, Lee H, Kim M, Lee I. Analysis of flowering pathway integrators in Arabidopsis[J]. Plant Cell Physiol, 2005, 46: 292299.
[17] Samach A, Onouchi H, Gold SE, et al. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis[J]. Science, 2000, 288: 1613-1616.
[18] Yoo SK, Chung KS, Kim J, et al. CONSTANS activates SUPPRES-SOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWE-RING LOCUS T to promote flowering in Arabidopsis[J]. Plant Physiol 2005, 139: 770-778.
[19] Borner R, Kampmann G, Chandler J, et al. MADS domain gene involved in the transition to flowering in Arabidopsis[J]. Plant J, 2000, 24: 591-599.
[20] Lee H, Suh SS, Park E, et al.The AGAMOUS-LIKE 20 MADS do-main protein integrates floral inductive pathways in Arabidopsis [J]. Genes Dev, 2000, 14: 2366-2376.
[21] Lee J, Lee I. Regulation and function of SOC1, a flowering pathway integrator[J]. J Exp Bot, 2010, 61: 2247-2254.
[22] Liu C, Zhou J, Bracha-Drori K, et al. Specification of Arabidopsis floral meristem identity by repression of flowering time genes[J]. Development, 2007, 134: 1901-1910.
[23] Melzer S, Lens F, Gennen J, et al. Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana[J]. Nat Genet, 2008, 40: 1489-1492.
[24] Liu C, Xi W, Shen L, et al. Regulation of floral patterning by flowering time genes[J]. Dev Cell, 2009, 16: 711-722.
[25] Lee JH, Yoo SJ, Park SH, et al. Role of SVP in the control of flowering time by ambient temperature in Arabidopsis[J]. Genes Dev, 2007, 21(4)：397-402.
[26] Li D. A repressor complex governs the integration of flowering signals in Arabidopsis[J]. Dev Cell, 2008, 15: 110-120.
[27] 刘建武, 孙成华, 刘宁. 花器官决定的ABC模型和四因子模型[J]. 植物学通报, 2004, 3: 346-351.
[28] Theissen G, Becker A, Rosa AD, et al. A short history of MADS-box genes in plants[J]. Plant Mol Biol, 2000, 42: 115-149.
[29] Theissen G. Development of floral organ identity: stories from the MADS house[J]. Curr Opin Plant Biol, 2001, 4: 75-85.
[30] Ratcliffe OJ, Bradley DJ, Coen ES. Separation of shoot and floral identity in Arabidopsis[J]. Development, 1999, 126: 11091120.
[31] Liljegren SJ, Gustafson-Brown C, Pinyopich A, et al. Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate[J]. Plant Cell, 1999, 11: 1007-1018.
[32] Theissen G, Saedler H. Plant biology Floral quartets[J]. Nature, 2001, 409: 469-471.
[33] Krizek BA, Fletcher JC. Molecular mechanisms of flower develop-ment: an armchair guide[J]. Nat Rev Genet, 2005, 6: 688-698.
[34] Benlloch R, Berbel A, Serrano-Mislata A, Madueno F. Floral initiation and in florescence architecture: a comparative view[J]. Annals Bot, 2007, 100: 659-676.
[35] Lee J, Oh M, Park H, Lee I. SOC1 translocated to the nucleus by interaction with AGL24 directly regulates LEAFY[J]. Plant J, 2008, 55: 832-843.
[36] Yamaguchi A, Wu MF, Yang L, et al. The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1[J]. Dev Cell, 2009, 17: 268-278.
[37] Gocal GF, Sheldon CC, Gubler F, et al. GAMYB-like genes, flowering, and gibberellin signaling in Arabidopsis[J]. Plant Physiol, 2001, 127: 1682-1693.
[38] Kanrar S, Bhattacharya M, Arthur B, et al. Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis[J]. Plant J, 2008, 54: 924-937.
[39] Smith HMS, Ung N, Lal S, Courtier J. Specification of reproductive meristems requires the combined function of SHOOT MERISTEM-LESS and floral integrators FLOWERING LOCUS T and FD during Arabidopsis inflorescence development[J]. J Exp Bot, 2011, 62: 583-593.
[40] Wang JW, Czech B, Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana[J]. Cell, 2009, 138: 738-749.
[41] Smyth DR, Bowman JL, Meyerowitz EM. Early flower development in Arabidopsis[J]. Plant Cell, 1990, 2: 755-767.
[42] Yu H, Ito T, Wellmer F, Meyerowitz EM. Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development[J]. Nat Genet, 2004, 36: 157-161.
[43] Li B, Carey M, Workman JL. The role of chromatin during transcription[J]. Cell, 2007, 128: 707-719.
[44] Gregis V, Sessa A, Dorca-Fornell C, Kater M. The Arabidopsis floral meristem identity genes AP1, AGL24 and SVP directly repress class B and C floral homeotic genes[J]. Plant J, 2009, 60: 626-637.
[45] Kaufmann K, Wellmer F, Muino JM, et al. Orchestration of floral initiation by APETALA1[J]. Science, 2010, 328: 85-89.
[46] Moyroud E, Minguet EG, Ott F, et al. Prediction of regulatory interactions from genome sequences using a biophysical model for the Arabidopsis LEAFY transcription factor[J]. Plant Cell, 2011, 23: 1293-1306.
[47] Kaufmann K, Muino JM, Jauregui R, et al. Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower[J]. PLoS Biol, 2009, 7: e1000090.
[48] Folter S, Immink RGH, Kieffer M, et al. Comprehensive interaction map of the Arabidopsis MADS Box transcription factors[J]. Plant Cell, 2005, 17: 1424-1433.
[49] Sridhar VV, Surendrarao A, Liu Z. APETALA1: SEPALLATA3 interact with SEUSS to mediate transcription repression during flower development[J]. Development, 2006, 133: 3159-3166.
[50] Gustafson-Brown C, Savidge B, Yanofsky MF. Regulation of the Arabidopsis floral homeotic gene APETALA1[J]. Cell, 1994, 76: 131-143.
[51] Bomblies K, Dagenais N, Weigel D. Redundant enhancers mediate transcriptional repression of AGAMOUS by APETALA2[J]. Dev Biol, 1999, 216: 260-264.
[52] Yant L, Mathieu J, Dinh TT, et al. Orchestration of the floral transi-tion and floral development in Arabidopsis by the bifunctional transcription factor APETALA2[J]. Plant Cell, 2010, 22: 21562170.
[53] Aukerman MJ, Sakai H. Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes[J]. Plant Cell, 2003, 15: 2730-2741.
[54] Chen X. A microRNA as a translational repressor of APETALA2 in Arabidopsis flower development[J]. Science, 2004, 303: 2022-2025.
[55] Schwab R, Palatnik JF, Riester M, et al. Specific effects of microRNAs on the plant transcriptome[J]. Dev Cell, 2005, 8: 517-527.
[56] Wollmann H, Mica E, Todesco M, et al. On reconciling the interactions between APETALA2, miR172 and AGAMOUS with the ABC model of flower development[J]. Development, 2010, 137: 3633-3642.
[57] Grigorova B, Mara C, Hollender C, et al. LEUNIG and SEUSS co-repressors regulate miR172 expression in Arabidopsis flowers[J]. Development, 2011, 138: 2451-2456.
[58] Lee H, Yoo SJ, Lee JH, et al. Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis[J]. Nucleic Acids Res, 2010, 38: 3081-3093.
[59] Mathieu, J, Yant, LJ, Murdter, F, et al. Repression of flowering by the miR172 target SMZ[J]. PLoS Biol, 2009, 7: e1000148.
[60] Ahn JH, Miller D, Winter VJ, et al. A divergent external loop confers antagonistic activity on floral regulators FT and TFL1[J]. EMBO J, 2006, 25: 605-614.
[61] Searle I, He YH, Turck F, et al. The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis[J]. Gene Dev, 2006, 20: 898-912.
[62] Willmann MR, Poethig RS. The effect of the floral repressor FLC on the timing and progression of vegetative phase change in Arabidopsis[J]. Development, 2011, 138: 677-685.
[63] Chiang GCK, Barua D, Kramer EM, et al. Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thalia-na[J]. Proc Natl Acad Sci USA, 2009, 106: 11661-11666.
[64] Swiezewski S, Liu F, Magusin A, Dean C. Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target[J]. Nature, 2009, 462: 799-802.
[65] Heo JB, Sung S. Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA[J]. Science, 2011, 331: 76-79.
[66] Crevillen P, Dean C. Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context[J]. Curr Opin Plant Biol, 2011, 14: 38-44.
[67] Winter CM, Austin RS, Blanvillain-Baufume S, et al. LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response[J]. Dev Cell, 2011, 20: 430-443.
[68] Deal RB, Henikoff S. A simple method for gene expression and chromatin profiling of individual cell types within a tissue[J]. Dev Cell, 2010, 18: 1030-1040.