Advances in the Maintenance and Termination of Floral Meristem Regulated by C-type Floral Organ Gene AGAMOUS（AG）

doi:10.13560/j.cnki.biotech.bull.1985.2019-0877

Abstract

Abstract: The maintenance and termination of floral meristems plays key role in the floral organogenesis and metagenesis of plant. Successful floral meristems determinacy ensures the normal reproductive development and life cycle progression of plants. Many studies have shown that AGAMOUS（AG）gene,as a master regulator of both floral organ differentiation and floral determinacy,can coordinate various cell fate decisions in flower development. However,the molecular mechanism of AG involvement in the regulation of plant metagenesis and floral meristem maintenance and termination remains unclear. This paper summarized such research progress and current status of AG gene in regulating the floral meristem maintenance and termination in recent years,with a view to providing a reference for further study of the maintenance and termination of stem cells during floral organ differentiation as well as the molecular regulation between stem cell activity and other developmental processes.

Key words: AGAMOUS（AG）gene, floral meristem maintenance and termination, regulation mechanisms

WEI Ming-ming, ZENG Xia, AN Ze-wei, HU Yan-shi, HUANG Xiao, LI Wei-guo. Advances in the Maintenance and Termination of Floral Meristem Regulated by C-type Floral Organ Gene AGAMOUS（AG）[J]. Biotechnology Bulletin, 2020, 36(1): 135-143.

References

[1] Coen ES, Meyerowitz EM.The war of the whorls:genetic interactions controlling flower development[J]. Nature, 1991, 353(6339):31-37.
[2] Theissen G, Becker A, Rosa AD, et al.A short history of MADS-box genes in plants[J]. Plant Mol Bio, 2000, 42(1):115-149.
[3] Bo L, Li Q, Mao X, et al.Two novel AP2/EREBP transcription factor genes TaPARG have pleiotropic functions on plant architecture and yield-related traits in common wheat[J]. Front Plant Sci, 2016, 7(1191):1-13.
[4] David RS.Evolution and genetic control of the floral ground plan[J]. New Phy, 2018, 220(1):70-86.
[5] Li LY, Fang ZW, Li XF, et al.Isolation and characterization of the C-class MADS-box gene from the distylous pseudo-cereal Fagopyrum esculentum[J]. Plant Bio J, 2017, 60(2):189-198.
[6] Dreni L, Zhang D.Flower development:the evolutionary history and functions of the AGL6 subfamily MADS-box genes[J]. J Exp Bot, 2016, 67(6):1625-1638.
[7] Nakatsuka T, Saito M, Nishihara M.Functional characterization of duplicated B-class MADS-box genes in Japanese gentian[J]. Plant Cell Rep, 2016, 35(4):895-904.
[8] Zeng X, Liu H, Du H, et al.Soybean MADS-box gene GmAGL1 promotes flowering via the photoperiod pathway[J]. BMC Genomics, 2018, 19(51):1-17.
[9] Balanzà V, Martínezfernández I, Sato S, et al.Genetic control of meristem arrest and life span in Arabidopsis by a FRUITFULL-APETALA2 pathway[J]. Nat Commun, 2018, 9(1):565.
[10] Villarino GH, Hu Q, Manrique S, et al.Transcriptomic signature of the SHATTERPROOF2 expression domain reveals the meristematic nature of Arabidopsis gynoecial medial domain[J]. Plant Phy, 2016, 171(1):42-61.
[11] Ferrandiz C, Gu Q, Martienssen R, et al.Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER[J]. Development, 2000, 127(4):725-734.
[12] Pelaz S, Ditta GS, Baumann E, et al.B and C floral organ identity functions require SEPALLATA MADS-box genes[J]. Nature, 2000, 405(6783):200-203.
[13] Nesi N, Debeaujon I, Jond C, et al.The TRANSPARENT TESTA16 locus encodes the ARABIDOPSIS BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat[J]. Plant Cell, 2002, 14(10):2463-2479.
[14] Niu S, Yuan H, Sun X, et al.A transcriptomics investigation into pine reproductive organ development[J]. New Phy, 2016, 209(3):1278-1289.
[15] Ó'Maoiléidigh DS, Graciet E, Wellmer F. Gene networks controlling Arabidopsis thaliana flower development[J]. New Phy, 2014, 201(1):16-30.
[16] Becker A.Tinkering with transcription factor networks for developmental robustness of Ranunculales flowers[J]. Ann Bot, 2016, 117(5):845-858.
[17] Sun B, Ito T.Regulation of floral stem cell terminationin Arabidopsis[J]. Front Plant Sci, 2015, 6:17.
[18] Yamaguchi N, Huang J, Xu Y, et al.Fine-tuning of auxin homeostasis governs the transition from floral stem cell maintenance to gynoecium formation[J]. Nature Comm, 2017, 8(1):1-15.
[19] Guo S, Sun B, Looi LS, et al.Coordination of flower development through epigenetic regulation in two model species:rice and Arabidopsis[J]. Plant Cell Phy, 2015, 56(5):830-842.
[20] Sun B, Xu Y, Ng K, et al.A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem. Genes Dev, 2009, 23, 1791-1804.
[21] Bollier N, Sicard A, Leblond J, et al.At-MINI ZINC FINGER2 and Sl-INHIBITOR OF MERISTEM ACTIVITY, a conserved missing link in the regulation of floral meristem termination in Arabidopsis and tomato[J]. Plant Cell, 2018, 30(1):83-100.
[22] Hawkins C, Liu Z.A model for an early role of auxin in Arabidopsis gynoecium morphogenesis[J]. Front Plant Sci, 2014, 5(327):
1-12.
[23] Marsch-Martinez N, De Folter S.Hormonal control of the development of the gynoecium[J]. Curr Opin Plant Biol, 2016, 12(29):104-114.
[24] Smyth DR, Bowman JL, Meyerowitz EM.Early flower development in Arabidopsis[J]. Plant Cell, 1990, 2(8):755-767.
[25] Heidstra R, Sabatini S.Plant and animal stem cells:similar yet different[J]. Nat Rev Mol Cell Biol, 2014, 15(5):301-312.
[26] Dreni L, Kater MM.MADS reloaded:evolution of the AGAMOUS subfamily genes[J]. New Phytol, 2014, 201:717-732.
[27] Ito T, Ng KH, Lim TS, et al.The homeotic protein AGAMOUS controls late stamen development by regulating a jasmonate biosynthetic gene in Arabidopsis[J]. Plant Cell, 2007, 19(11):3516-3529.
[28] Krizek B A, Prost V, Macias A.AINTEGUMENTA promotes petal identity and acts as a negative regulator of AGAMOUS[J]. The Plant Cell, 2000, 12(8):1357-1366.
[29] Kramer EM, Jaramillo MA, Di Stilio VS.Patterns of gene duplication and functional evolution during the diversification of the agamous subfamily of MADS box genes in angiosperms[J]. Genetics, 2004, 166(2):1011-1023.
[30] Li W, Hu W, Fang C, et al.An AGAMOUS intron-driven cytotoxin leads to flowerless tobacco and produces no detrimental effects on vegetative growth of either tobacco or poplar[J]. Plant Bio J, 2016, 14(12):2276-2287.
[31] Liu X, Kim YJ, Müller R, et al.AGAMOUS terminates floral stem cell maintenance in Arabidopsis by directly repressing wuschel through recruitment of polycomb group proteins[J]. Plant Cell, 2011, 23(10):3654-3670.
[32] Dreni L, Pilatone A, Yun DP, et al.Functional analysis of all AGAMOUS subfamily members in rice reveals their roles in reproductive organ identity determination and meristem determinacy[J]. Plant Cell, 2011, 23(8):2850-2863.
[33] 田亚然, 范天刚, 张钢, 等. 低温引起月季花朵过度重瓣化关键基因的表达及分析[J]. 热带作物学报, 2016, 37(6):1147-1154.
[34] Lu H, Klocko AL, Brunner AM, et al.RNA interference suppression of AGAMOUS and SEEDSTICK alters floral organ identity and impairs floral organ determinacy, ovule differentiation, and seed-hair development in Populus[J]. New Phytol, 2019, 222(2):923-937.
[35] Xu W, Tao J, Chen M, et al.Interactions between FLORAL ORGAN NUMBER4 and floral homeotic genes in regulating rice flower development[J]. J Exp Bot, 2017, 68(3):483-498.
[36] Liu ZX, Xiong HY, Li LY, et al.Functional conservation of an AGAMOUS orthologous gene controlling reproductive organ development in the gymnosperm species Taxus chinensis var. mairei[J]. J Plant Bio, 2018, 61:50-59.
[37] Ó'Maoiléidigh DS, Wuest SE, Rae L, et al. Control of reproductive floral organ identity specification in Arabidopsis by the C function regulator AGAMOUS[J]. Plant Cell, 2013, 25(7):2482-2503.
[38] Liu Y, Zhang D, Ping J, et al.Innovation of a regulatory mechanism modulating semi-determinate stem growth through artificial selection in soybean[J]. PLoS Genetics, 2016, 12(1):e100588.
[39] Mayer K F X, Schoof H, Haecker A, et al. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem[J]. Cell, 1998, 95(6):805-815.
[40] Huang Z, Shi T, Zheng B, et al.APETALA2 antagonizes the transcriptional activity of AGAMOUS in regulating floral stem cells in Arabidopsis thaliana[J]. New Phy, 2017, 215(3):1197-1209.
[41] Lenhard M, Bohnert A, Jürgens G, et al.Termination of stem cell maintenance in Arabidopsis floral meristems by interactions between WUSCHEL and AGAMOUS[J]. Cell, 2001, 105(6):805-814.
[42] Lohmann JU, Hong RL, Hobe M, et al.A molecular link between stem cell regulation and floral patterning in Arabidopsis[J]. Cell, 2001, 105(6):793-803.
[43] Payne T, Johnson SD, Koltunow AM.KNUCKLES(KNU)encodes a C2H2 zinc-finger protein that regulates development of basal pattern elements of the Arabidopsis gynoecium[J]. Development, 2004, 131(15):3737-3749.
[44] Sun B, Xu Y, Ng KH, et al.A timing mechanism for stem cell maintenance and differentiation in the Arabidopsis floral meristem[J]. Genes & Dev, 2009, 23(15):1791-1804.
[45] Sun B, Looi LS, Guo S, et al.Timing mechanism dependent on cell division is invoked by polycomb eviction in plant stem cells[J]. Science, 2014, 343(6170):505-514.
[46] Iwase A, Harashima H, Ikeuchi M, et al.WIND1 promotes shoot regeneration through transcriptional activation of ENHANCER OF SHOOT REGENERATION1 in Arabidopsis[J]. Plant Cell, 2016, 29(1):54-69.
[47] Jásik J, Bokor B, StuchlãKS, et al. Effects of Auxins on PIN-FORMED2(PIN2)dynamics are not mediated by inhibiting PIN2 endocytosis[J]. Plant Phy, 2016, 172(2):1019-1031.
[48] Wang F, Muto A, Velde JVD, et al.Functional analysis of the Arabidopsis TETRASPANIN gene family in plant growth and development[J]. Plant Phys, 2015, 169(3):2200-2214.
[49] Montes AC, Herrera-Ubaldo H, Serwatowska J, et al.Towards a comprehensive and dynamic gynoecium gene regulatory network[J]. Curr Plant Biol, 2015, 3(4):3-12.
[50] Breuilbroyer S, Trehin C, Morel P, et al.Analysis of the Arabidopsis superman allelic series and the interactions with other genes demonstrate developmental robustness and joint specification of male-female boundary, flower meristem termination and carpel compart mentalization[J]. Ann Bot, 2016, 117(5):905-923.
[51] Breuil-Broyer S, Trehin C, Morel P, et al.Analysis of the Arabidopsis superman allelic series and the interactions with other genes demonstrate developmental robustness and joint specification of male-female boundary, flower meristem termination and carpel compartmentalization[J]. Ann Bot, 2016, 117(5):905-923.
[52] SilvaJ, Kim YJ, Xiao D, et al. Cytological analysis of ginseng carpel development[J]. Protoplasma, 2017, 254(5):1909-1922.
[53] Staldal V, Sohlberg JJ, Eklund DM, et al.Auxin can act independently of CRC, LUG, SEU, SPT, STY1 in style development but not apical-basal patterning of the Arabidopsis gynoecium[J]. New Phytol, 2008, 180(4):798-808.
[54] Rong XF, Sang YL, Wang L, et al.Type-B ARRs control carpel regeneration through mediating AGAMOUS expression in Arabidopsis[J]. Plant Cell Phy, 2018, 59(4):756-764.
[55] Xiao J, Jin R, Yu X, et al.Cis and trans determinants of epigenetic silencing by polycomb repressive complex 2 in Arabidopsis[J]. Nature Genetics, 2017, 49(10):1546-1552.
[56] Chanvivattana Y, Bishopp A, Schubert D, et al.Interaction of polycomb-group proteins controlling flowering in Arabidopsis[J]. Development, 2004, 131(21):5263-5276.
[57] Molitor A, Shen WH.The polycomb complex PRC1:composition and function in plants[J]. Journal of Genetics and Genomics, 2013, 40(5):231-238.
[58] Schubert D, Primavesi L, Bishopp A, et al.Silencing by plant Polycomb-group genes requires dispersed trimethylation of histone H3 at lysine 27[J]. EMBO J, 2006, 25(19):4638-4649.
[59] Lodha M, Marco CF, Timmermans MC.The ASYMMETRIC LEAVES complex maintains repression of KNOX homeobox genes via direct recruitment of polycomb-repressive complex2[J]. Genes & Dev, 2013, 27(6):596-601.
[60] Wu HW, Deng S, Xu H, et al.A noncoding RNA transcribed from the AGAMOUS(AG)second intron binds to CURLY LEAF and represses AG expression in leaves[J]. New Phy, 2018, 219(4):1480-1491.
[61] Hu Y, Lai Y, Fan S, et al.Regulation of phytohormone biosynthesis genes by polycomb-mediated histone H3 lysine 27 trimethylation in Arabidopsis[J]. J Plant Sci, 2018, 6(4):117-133.
[62] Liu J, Wang H, Chua NH.Long noncoding RNA transcriptome of plants[J]. Plant Bio J, 2015, 13(3):319-328.
[63] Xu Y, Yamaguchi N, Gan ES, et al.When to stop:an update on molecular mechanisms of floral meristem termination[J]. J Exp Bot, 2019, 70(6):1711-1718.
[64] Lehretz GG, Sonnewald S, Hornyik C, et al.Post-transcriptional regulation of Flowering locus T modulates heat-dependent source-sink development in potato[J]. Current Bio, 2019, 29(10):1614-1624.
[65] Heo JB, Sung S.Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA[J]. Science, 2011, 331(6013):76-79.
[66] Yan W, Chen D, Kaufmann K.Molecular mechanisms of floral organ specification by MADS domain proteins[J]. Curr Opin Plant Biol, 2016, 4(29):154-162.
[67] Simonini S, Deb J, Moubayidin L, et al.A noncanonical auxin-sensing mechanism is required for organ morphogenesis in Arabidopsis[J]. Genes & Dev, 2016, 30(20):2286-2296.
[68] Liu X, Dinh TT, Li D, et al.AUXIN RESPONSE FACTOR 3 integrates the functions of AGAMOUS and APETALA2 in floral meristem determinacy[J]. Plant J, 2014, 80(4):629-641.
[69] Denay G, Chahtane H, Tichtinsky G, et al.A flower is born:an update on Arabidopsis floral meristem formation[J]. Curr Opin Plant Biol, 2017, 9(35):15-22.
[70] Zhang K, Wang R, Zi H, et al.AUXIN RESPONSE FACTOR3 regulates floral meristem determinacy by repressing cytokinin biosynthesis and signaling[J]. The Plant Cell, 2018, 30(2):324-346.
[71] Prunet N, Morel P, Champelovier P, et al.SQUINT promotes stem cell homeostasis and floral meristem termination in Arabidopsis through APETALA2 and CLAVATA signalling[J]. J Exp Bot, 2015, 66(21):6905-6916.
[72] Vaddepalli P, Scholz S, Schneitz K.Pattern formation during early floral development[J]. Curr Opin Genet Dev, 2015, 32:16-23.
[73] Chen DJ, Yan WH, Fu LY, et al.Architecture of gene regulatory networks controlling flower development in Arabidopsis thaliana[J]. Nature Comm, 2018, 9(1):4534.
[74] Zúñiga-Mayo VM, Gómez-Felipe A, Herrera-Ubaldo H, et al.Gynoecium development:networks in Arabidopsis and beyond[J]. J Exp Bot, 2019, 5(70):1447-1460.
[75] Guo S, Sun B, Looi LS, et al.Co-ordination of flower development through epigenetic regulation in two model species:rice and Arabidopsis[J]. Plant & Cell Phy, 2015, 56(5):830-842.
[76] Uemura A, Yamaguchi N, Xu Y, et al.Regulation of floral meristem activity through the interaction of AGAMOUS, SUPERMAN, and CLAVATA3 in Arabidopsis[J]. Plant Rep, 2018, 31(1):89-105.
[77] Berger N, Dubreucq B, Roudier F, et al.Transcriptional regulation of Arabidopsis LEAFY COTYLEDON2 involves RLE, a cis-element that regulates trimethylation of histone H3 at lysine-27[J]. Plant Cell, 2011, 23(11):4065-4078.