Abstract
Floral transition in model plants including Arabidopsis and rice has been studied extensively through molecular genetic approaches. Many genetic factors in different flowering pathways, which depend mainly on photoperiod, vernalization, autonomous and ambient temperature are regulated coordinately to control floral induction. However, for the ornamental plants orchids, the molecular mechanisms underlying the floral transition are still unclear. Recently, genes with potential flowering-related functions have been identified in different orchid species and their functional roles have also been characterized/examined using homologous or heterologous systems. In this review, we summarize the molecular networks of flowering genes and their regulation as revealed in model plants such as Arabidopsis and rice, and also describe the recent discoveries/studies on flowering genes in several commercially representative orchid species providing a perspective on orchid flowering research. In addition, our recent results through transgenic approaches with ectopic expression of Hd3a, a rice florigen gene for the induction of precocious flowering in Phalaenopsis orchids are also discussed.
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References
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. https://doi.org/10.1126/science.1115983
Andres F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639. https://doi.org/10.1038/nrg3291
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. https://doi.org/10.1126/science.1234116
Blanchard MG, Runkle ES (2006) Temperature during the day, but not during the night, controls flowering of Phalaenopsis orchids. J Exp Bot 57:4043–4049. https://doi.org/10.1093/jxb/erl176
Blanchard MG, Runkle ES (2008) Benzyladenine promotes flowering in Doritaenopsis and Phalaenopsis orchids. J Plant Growth Regul 27:141–150. https://doi.org/10.1007/s00344-008-9040-0
Blazquez MA, Green R, Nilsson O, Sussman MR, Weigel D (1998) Gibberellins promote flowering of Arabidopsis by activating the LEAFY promoter. Plant Cell 10:791–800. https://doi.org/10.1105/tpc.10.5.791
Campos KO, Kerbauy GB (2004) Thermoperiodic effect on flowering and endogenous hormonal status in Dendrobium (Orchidaceae). J Plant Physiol 161:1385–1387. https://doi.org/10.1016/j.jplph.2004.07.008
Chen W, Qin Q, Zhang C, Zheng Y, Wang C, Zhou M, Cui Y (2015) DhEFL2, 3 and 4, the three EARLY FLOWERING4-like genes in a Doritaenopsis hybrid regulate floral transition. Plant Cell Rep 34:2027–2041. https://doi.org/10.1007/s00299-015-1848-z
Cheng JZ, Zhou YP, Lv TX, Xie CP, Tian CE (2017) Research progress on the autonomous flowering time pathway in Arabidopsis. Physiol Mol Biol Plants 23:477–485. https://doi.org/10.1007/s12298-017-0458-3
Chin DC, Shen CH, SenthilKumar R, Yeh KW (2014) Prolonged exposure to elevated temperature induces floral transition via up-regulation of cytosolic ascorbate peroxidase 1 and subsequent reduction of the ascorbate redox ratio in Oncidium hybrid orchid. Plant Cell Physiol 55:2164–2176. https://doi.org/10.1093/pcp/pcu146
Chin DC, Hsieh CC, Lin HY, Yeh KW (2016) A low glutathione redox state couples with a decreased ascorbate redox ratio to accelerate flowering in Oncidium orchid. Plant Cell Physiol 57:423–436. https://doi.org/10.1093/pcp/pcv206
Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719. https://doi.org/10.1111/tpj.13461
Choi K, Park C, Lee J, Oh M, Noh B, Lee I (2007) Arabidopsis homologs of components of the SWR1 complex regulate flowering and plant development. Development 134:1931–1941. https://doi.org/10.1242/dev.001891
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. https://doi.org/10.1105/tpc.110.075911
Coupland G (2019) FLOWERING LOCUS C isolation and characterization: two articles that opened many doors. Plant Cell 31:1190–1191. https://doi.org/10.1105/tpc.19.00325
Cozzolino S, Widmer A (2005) Orchid diversity: an evolutionary consequence of deception? Trends Ecol Evol 20:487–494. https://doi.org/10.1016/j.tree.2005.06.004
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. https://doi.org/10.1038/nature06520
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. Plant Cell 19:74–83. https://doi.org/10.1105/tpc.106.048447
Ding L, Wang Y, Yu H (2013) Overexpression of DOSOC1, an ortholog of Arabidopsis SOC1, promotes flowering in the orchid Dendrobium Chao Parya Smile. Plant Cell Physiol 54:595–608. https://doi.org/10.1093/pcp/pct026
Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 18:926–936. https://doi.org/10.1101/gad.1189604
Du A, Tian W, Wei M, Yan W, He H, Zhou D, Huang X, Li S, Ouyang X (2017) The DTH8-Hd1 module mediates day-length-dependent regulation of rice flowering. Mol Plant 10:948–961. https://doi.org/10.1016/j.molp.2017.05.006
Finnegan EJ, Dennis ES (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17:1978–1983. https://doi.org/10.1016/j.cub.2007.10.026
Fornara F, Panigrahi KC, Gissot L, Sauerbrunn N, Ruhl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86. https://doi.org/10.1016/j.devcel.2009.06.015
Goh CJ, Yang AL (1978) Effects of growth regulators and decapitation on flowering of Dendrobium orchid hybrids. Plant Sci Lett 12:278–292
He Y, Doyle MR, Amasino RM (2004) PAF1-complex-mediated histone methylation of FLOWERING LOCUS C chromatin is required for the vernalization-responsive, winter-annual habit in Arabidopsis. Genes Dev 18:2774–2784. https://doi.org/10.1101/gad.1244504
Helliwell CA, Wood CC, Robertson M, James Peacock W, Dennis ES (2006) The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecular-weight protein complex. Plant J 46:183–192. https://doi.org/10.1111/j.1365-313X.2006.02686.x
Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79. https://doi.org/10.1126/science.1197349
Hew CS, Clifford PE (1993) Plant growth regulator and orchid cut-flower industry. Plant Growth Regul 13:231–239
Hou CJ, Yang CH (2009) Functional analysis of FT and TFL1 orthologs from orchid (Oncidium Gower Ramsey) that regulate the vegetative to reproductive transition. Plant Cell Physiol 50:1544–1557. https://doi.org/10.1093/pcp/pcp099
Hsiao YY, Pan ZJ, Hsu CC, Yang YP, Hsu YC, Chuang YC, Shih HH, Chen WH, Tsai WC, Chen HH (2011) Research on orchid biology and biotechnology. Plant Cell Physiol 52:1467–1486. https://doi.org/10.1093/pcp/pcr100
Hsing HX, Lin YJ, Tong CG, Li MJ, Chen YJ, Ko SS (2016) Efficient and heritable transformation of Phalaenopsis orchids. Bot Stud 57:30. https://doi.org/10.1186/s40529-016-0146-6
Hsu HF, Huang CH, Chou LT, Yang CH (2003) Ectopic expression of an orchid (Oncidium Gower Ramsey) AGL6-like gene promotes flowering by activating flowering time genes in Arabidopsis thaliana. Plant Cell Physiol 44:783–794
Hu X, Kong X, Wang C, Ma L, Zhao J, Wei J, Zhang X, Loake GJ, Zhang T, Huang J et al (2014) Proteasome-mediated degradation of FRIGIDA modulates flowering time in Arabidopsis during vernalization. Plant Cell 26:4763–4781. https://doi.org/10.1105/tpc.114.132738
Huang JZ, Lin CP, Cheng TC, Huang YW, Tsai YJ, Cheng SY, Chen YW, Lee CP, Chung WC, Chang BC et al (2016) The genome and transcriptome of Phalaenopsis yield insights into floral organ development and flowering regulation. PeerJ 4:e2017. https://doi.org/10.7717/peerj.2017
Ishikawa R, Aoki M, Kurotani K, Yokoi S, Shinomura T, Takano M, Shimamoto K (2011) Phytochrome B regulates Heading date 1 (Hd1)-mediated expression of rice florigen Hd3a and critical day length in rice. Mol Genet Genom 285:461–470. https://doi.org/10.1007/s00438-011-0621-4
Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG, Imaizumi T (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc Natl Acad Sci USA 109:3582–3587. https://doi.org/10.1073/pnas.1118876109
Jang S, Torti S, Coupland G (2009) Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J 60:614–625. https://doi.org/10.1111/j.1365-313X.2009.03986.x
Jang S (2015) Functional characterization of PhapLEAFY, a FLORICAULA/LEAFY ortholog in Phalaenopsis aphrodite. Plant Cell Physiol 56:2234–2247. https://doi.org/10.1093/pcp/pcv130
Jang S, Choi SC, Li HY, An G, Schmelzer E (2015) Functional characterization of Phalaenopsis aphrodite flowering genes PaFT1 and PaFD. PLoS ONE 10:e0134987. https://doi.org/10.1371/journal.pone.0134987
Jang S, Li HY, Kuo ML (2017) Ectopic expression of Arabidopsis FD and FD PARALOGUE in rice results in dwarfism with size reduction of spikelets. Sci Rep 7:44477. https://doi.org/10.1038/srep44477
Jung JH, Park JH, Lee S, To TK, Kim JM, Seki M, Park CM (2013) The cold signaling attenuator HIGH EXPRESSION OF OSMOTICALLY RESPONSIVE GENE1 activates FLOWERING LOCUS C transcription via chromatin remodeling under short-term cold stress in Arabidopsis. Plant Cell 25:4378–4390. https://doi.org/10.1105/tpc.113.118364
Kim SL, Lee S, Kim HJ, Nam HG, An G (2007) OsMADS51 is a short-day flowering promoter that functions upstream of Ehd1, OsMADS14, and Hd3a. Plant Physiol 145:1484–1494. https://doi.org/10.1104/pp.107.103291pp 107.103291
Kim SK, Yun CH, Lee JH, Jang YH, Park HY, Kim JK (2008) OsCO3, a CONSTANS-LIKE gene, controls flowering by negatively regulating the expression of FT-like genes under SD conditions in rice. Planta 228:355–365. https://doi.org/10.1007/s00425-008-0742-0
Kim W, Park TI, Yoo SJ, Jun AR, Ahn JH (2013) Generation and analysis of a complete mutant set for the Arabidopsis FT/TFL1 family shows specific effects on thermo-sensitive flowering regulation. J Exp Bot 64:1715–1729. https://doi.org/10.1093/jxb/ert036
Koh KW, Lee SH, Chen HK, Chang CY, Chan MT (2018) Phalaenopsis flowering locus VE regulates floral organ maturation. Plant Cell Rep 37:467–482. https://doi.org/10.1007/s00299-017-2243-8
Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774. https://doi.org/10.1242/dev.008631
Koo BH, Yoo SC, Park JW, Kwon CT, Lee BD, An G, Zhang Z, Li J, Li Z, Paek NC (2013) Natural variation in OsPRR37 regulates heading date and contributes to rice cultivation at a wide range of latitudes. Mol Plant 6:1877–1888. https://doi.org/10.1093/mp/sst088
Kostenyuk I, Oh BJ, So IS (1999) Induction of early flowering in Cymbidium niveo-marginatum Mak in vitro. Plant Cell Rep 19:1–5. https://doi.org/10.1007/s002990050701
Kowalik KM, Shimada Y, Flury V, Stadler MB, Batki J, Buhler M (2015) The Paf1 complex represses small-RNA-mediated epigenetic gene silencing. Nature 520:248–252. https://doi.org/10.1038/nature14337
Kubota A, Ito S, Shim JS, Johnson RS, Song YH, Breton G, Goralogia GS, Kwon MS, Laboy Cintron D, Koyama T et al (2017) TCP4-dependent induction of CONSTANS transcription requires GIGANTEA in photoperiodic flowering in Arabidopsis. PLoS Genet 13:e1006856. https://doi.org/10.1371/journal.pgen.1006856
Kumar SV, Lucyshyn D, Jaeger KE, Alos E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245. https://doi.org/10.1038/nature10928
Lazaro A, Valverde F, Pineiro M, Jarillo JA (2012) The Arabidopsis E3 ubiquitin ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24:982–999. https://doi.org/10.1105/tpc.110.081885
Lee J, Lee I (2010) Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot 61:2247–2254. https://doi.org/10.1093/jxb/erq098
Lee JH, Ryu HS, Chung KS, Pose D, Kim S, Schmid M, Ahn JH (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342:628–632. https://doi.org/10.1126/science.1241097
Lee N, Imaizumi T (2018) Uncoupling FT protein transport from its function. Plant Cell Physiol 59:1487–1489. https://doi.org/10.1093/pcp/pcy123
Lee JH, Park CM (2015) Integration of photoperiod and cold temperature signals into flowering genetic pathways in Arabidopsis. Plant Signal Behav 10:e1089373. https://doi.org/10.1080/15592324.2015.1089373
Lee BD, Cha JY, Kim MR, Paek NC, Kim WY (2018) Photoperiod sensing system for timing of flowering in plants. BMB Rep 51:163–164. https://doi.org/10.5483/bmbrep.2018.51.4.052
Lee C, Kim SJ, Jin S, Susila H, Youn G, Nasim Z, Alavilli H, Chung KS, Yoo SJ, Ahn JH (2019) Genetic interactions reveal the antagonistic roles of FT/TSF and TFL1 in the determination of inflorescence meristem identity in Arabidopsis. Plant J 99:452–464. https://doi.org/10.1111/tpj.14335
Li D, Yang C, Li X, Gan Q, Zhao X, Zhu L (2009) Functional characterization of rice OsDof12. Planta 229:1159–1169. https://doi.org/10.1007/s00425-009-0893-7
Li R, Wang A, Sun S, Liang S, Wang X, Ye Q, Li H (2012) Functional characterization of FT and MFT ortholog genes in orchid (Dendrobium nobile Lindl) that regulate the vegetative to reproductive transition in Arabidopsis. Plant Cell Tissue Organ Cult (PCTOC) 111:143–151. https://doi.org/10.1007/s11240-012-0178-x
Li X, Luo J, Yan T, Xiang L, Jin F, Qin D, Sun C, Xie M (2013) Deep sequencing-based analysis of the Cymbidium ensifolium floral transcriptome. PLoS One 8:e85480. https://doi.org/10.1371/journal.pone.0085480
Li DM, Lu FB, Zhu GF, Sun YB, Xu YC, Jiang MD, Liu JW, Wang Z (2014) Identification of warm day and cool night conditions induced flowering-related genes in a Phalaenopsis orchid hybrid by suppression subtractive hybridization. Genet Mol Res 13:7037–7051. https://doi.org/10.4238/2014.February.14.7
Li Z, Jiang D, He Y (2018) FRIGIDA establishes a local chromosomal environment for FLOWERING LOCUS C mRNA production. Nat Plants 4:836–846. https://doi.org/10.1038/s41477-018-0250-6
Lin CS, Hsu CT, Liao DC, Chang WJ, Chou ML, Huang YT, Chen JJ, Ko SS, Chan MT, Shih MC (2016) Transcriptome-wide analysis of the MADS-box gene family in the orchid Erycina pusilla. Plant Biotechnol J 14:284–298. https://doi.org/10.1111/pbi.12383
Lin YJ, Li MJ, Hsing HC, Chen TK, Yang TT, Ko SS (2019) Spike activator 1, encoding a bHLH, mediates axillary bud development and spike initiation in Phalaenopsis aphrodite. Int J Mol Sci 20:5406. https://doi.org/10.3390/ijms20215406
Liu F, Quesada V, Crevillen P, Baurle I, Swiezewski S, Dean C (2007) The Arabidopsis RNA-binding protein FCA requires a lysine-specific demethylase 1 homolog to downregulate FLC. Mol Cell 28:398–407. https://doi.org/10.1016/j.molcel.2007.10.018
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. https://doi.org/10.1126/science.1180278
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 Biol 10:e1001313. https://doi.org/10.1371/journal.pbio.1001313
Liu B, Wei G, Shi J, Jin J, Shen T, Ni T, Shen WH, Yu Y, Dong A (2016) SET DOMAIN GROUP 708, a histone H3 lysine 36-specific methyltransferase, controls flowering time in rice (Oryza sativa). New Phytol 210:577–588. https://doi.org/10.1111/nph.13768
Liu J, Cheng X, Liu P, Li D, Chen T, Gu X, Sun J (2017) MicroRNA319-regulated TCPs interact with FBHs and PFT1 to activate CO transcription and control flowering time in Arabidopsis. PLoS Genet 13:e1006833. https://doi.org/10.1371/journal.pgen.1006833
Liu X, Yang Y, Hu Y, Zhou L, Li Y, Hou X (2018) Temporal-specific interaction of NF-YC and CURLY LEAF during the floral transition regulates flowering. Plant Physiol 177:105–114. https://doi.org/10.1104/pp.18.00296
Lopez RG, Runkle ES, Heins RD, Whitman CM (2003) Temperature and photoperiodic effects on growth and flowering of Zygopetalum redvale ‘Fire Kiss’ orchid. Acta Hort 624:155–162
Lopez RG, Runkle ES (2006) Temperature and photoperiod regulate flowering of potted Miltoniopsis orchids. Hortscience 41:593–597
Luo X, Zhang C, Sun X, Qin Q, Zhou M, Paek KY, Cui Y (2011) Isolation and characterization of a Doritaenopsis hybrid GIGANTEA gene, which possibly involved in inflorescence initiation at low temperatures. Korean J Hortic Sci Technol 29:135–143
Marin-Gonzalez E, Matias-Hernandez L, Aguilar-Jaramillo AE, Lee JH, Ahn JH, Suarez-Lopez P, Pelaz S (2015) SHORT VEGETATIVE PHASE up-regulates TEMPRANILLO2 floral repressor at low ambient temperatures. Plant Physiol 169: 1214–1224. https://doi.org/10.1104/pp. 15.00570
Marquardt S, Raitskin O, Wu Z, Liu F, Sun Q, Dean C (2014) Functional consequences of splicing of the antisense transcript COOLAIR on FLC transcription. Mol Cell 54:156–165. https://doi.org/10.1016/j.molcel.2014.03.026
Mathieu J, Warthmann N, Kuttner F, Schmid M (2007) Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr Biol 17:1055–1060. https://doi.org/10.1016/j.cub.2007.05.009
Moraes TS, Dornelas MC, Martinelli AP (2019) FT/TFL1: calibrating plant architecture. Front Plant Sci 10:97. https://doi.org/10.3389/fpls.2019.00097
Mutasa-Gottgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989. https://doi.org/10.1093/jxb/erp040
Nemoto Y, Nonoue Y, Yano M, Izawa T (2016) Hd1,a CONSTANS ortholog in rice, functions as an Ehd1 repressor through interaction with monocot-specific CCT-domain protein Ghd7. Plant J 86:221–233. https://doi.org/10.1111/tpj.13168
Niwa Y, Ito S, Nakamichi N, Mizoguchi T, Niinuma K, Yamashino T, Mizuno T (2007) Genetic linkages of the circadian clock-associated genes, TOC1, CCA1 and LHY, in the photoperiodic control of flowering time in Arabidopsis thaliana. Plant Cell Physiol 48:925–937. https://doi.org/10.1093/pcp/pcm067
Nohales MA, Kay SA (2019) GIGANTEA gates gibberellin signaling through stabilization of the DELLA proteins in Arabidopsis. Proc Natl Acad Sci USA 116:21893–21899. https://doi.org/10.1073/pnas.1913532116
Oh S, Zhang H, Ludwig P, van Nocker S (2004) A mechanism related to the yeast transcriptional regulator Paf1c is required for expression of the Arabidopsis FLC/MAF MADS box gene family. Plant Cell 16:2940–2953. https://doi.org/10.1105/tpc.104.026062
Ospina-Zapata DA, Madrigal Y, Alzate JF, Pabon-Mora N (2020) Evolution and expression of reproductive transition regulatory genes FT/TFL1 with emphasis in selected neotropical orchids. Front Plant Sci 11:469. https://doi.org/10.3389/fpls.2020.00469
Park SJ, Kim SL, Lee S, Je BI, Piao HL, Park SH, Kim CM, Ryu CH, Park SH, Xuan YH et al (2008) Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J 56:1018–1029. https://doi.org/10.1111/j.1365-313X.2008.03667.x
Peng LT, Shi ZY, Li L, Shen GZ, Zhang JL (2008) Overexpression of transcription factor OsLFL1 delays flowering time in Oryza sativa. J Plant Physiol 165:876–885. https://doi.org/10.1016/j.jplph.2007.07.010
Ponnu J (2020) Molecular mechanisms suppressing COP1/SPA E3 ubiquitin ligase activity in blue light. Physiol Plant 169:418–429. https://doi.org/10.1111/ppl.13103
Questa JI, Song J, Geraldo N, An H, Dean C (2016) Arabidopsis transcriptional repressor VAL1 triggers Polycomb silencing at FLC during vernalization. Science 353:485–488. https://doi.org/10.1126/science.aaf7354
Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z, Yanofsky MF, Coupland G (2000) Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–1616. https://doi.org/10.1126/science.288.5471.1613
Sawa M, Nusinow DA, Kay SA, Imaizumi T (2007) FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–265. https://doi.org/10.1126/science.1146994
Sawettalake N, Bunnag S, Wang Y, Shen L, Yu H (2017) DOAP1 promotes flowering in the orchid Dendrobium Chao Praya Smile. Front Plant Sci 8:400. https://doi.org/10.3389/fpls.2017.00400
Scortecci K, Michaels SD, Amasino RM (2003) Genetic interactions between FLM and other flowering-time genes in Arabidopsis thaliana. Plant Mol Biol 52:915–922
Silvera K, Santiago LS, Cushman JC, Winter K (2009) Crassulacean acid metabolism and epiphytism linked to adaptive radiations in the Orchidaceae. Plant Physiol 149: 1838–1847. https://doi.org/10.1104/pp.108.132555
Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049. https://doi.org/10.1126/science.1219644
Song YH, Kubota A, Kwon MS, Covington MF, Lee N, Taagen ER, Laboy Cintron D, Hwang DY, Akiyama R, Hodge SK et al (2018) Molecular basis of flowering under natural long-day conditions in Arabidopsis. Nat Plants 4:824–835. https://doi.org/10.1038/s41477-018-0253-3
Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120. https://doi.org/10.1038/35074138
Sui P, Shi J, Gao X, Shen WH, Dong A (2013) H3K36 methylation is involved in promoting rice flowering. Mol Plant 6:975–977. https://doi.org/10.1093/mp/sss152
Sun C, Fang J, Zhao T, Xu B, Zhang F, Liu L, Tang J, Zhang G, Deng X, Chen F et al (2012a) The histone methyltransferase SDG724 mediates H3K36me2/3 deposition at MADS50 and RFT1 and promotes flowering in rice. Plant Cell 24:3235–3247. https://doi.org/10.1105/tpc.112.101436
Sun X, Qin Q, Zhang J, Zhang C, Zhou M, Paek KY, Cui Y (2012b) Isolation and characterization of the FVE gene of a Doritaenopsis hybrid involved in the regulation of flowering. Plant Growth Regul 68:77–86. https://doi.org/10.1007/s10725-012-9695-1
Sun C, Chen D, Fang J, Wang P, Deng X, Chu C (2014) Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways. Protein Cell 5:889–898. https://doi.org/10.1007/s13238-014-0068-6
Sung S, Amasino RM (2004) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10. https://doi.org/10.1016/j.pbi.2003.11.010
Thiruvengadam M, Chung I-M, Yang C-H (2012) Overexpression of Oncidium MADS box (OMADS1) gene promotes early flowering in transgenic orchid (Oncidium Gower Ramsey). Acta Physiol Plant 34:1295–1302. https://doi.org/10.1007/s11738-012-0926-x
Tian Y, Zheng H, Zhang F, Wang S, Ji X, Xu C, He Y, Ding Y (2019) PRC2 recruitment and H3K27me3 deposition at FLC require FCA binding of COOLAIR. Sci Adv 5:eaau7246. https://doi.org/10.1126/sciadv.aau7246
Tiwari SB, Shen Y, Chang HC, Hou Y, Harris A, Ma SF, McPartland M, Hymus GJ, Adam L, Marion C et al (2010) The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol 187:57–66. https://doi.org/10.1111/j.1469-8137.2010.03251.x
Tomson BN, Arndt KM (2013) The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochim Biophys Acta 1829:116–126. https://doi.org/10.1016/j.bbagrm.2012.08.011
Truernit E, Sauer N (1995) The promoter of the Arabidopsis thaliana SUC2 sucrose-H + symporter gene directs expression of beta-glucuronidase to the phloem: evidence for phloem loading and unloading by SUC2. Planta 196:564–570. https://doi.org/10.1007/BF00203657
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. https://doi.org/10.1126/science.1091761
Vaz AP, Figueiredo-Ribeiro Rd Rde C, Kerbauy GB (2004) Photoperiod and temperature effects on in vitro growth and flowering of P. pusilla, an epiphytic orchid. Plant Physiol Biochem 42:411–415. https://doi.org/10.1016/j.plaphy.2004.03.008
Wang W-Y, Chen W-S, Chen W-H, Huang L-S, Chang P-S (2002) Influence of abscisic acid on flowering in Phalaenopsis hybrida. Plant Physiol Biochem 40:97–100
Wang W-Y, Chen W-S, Huang K-L, Huang L-S, Chen W-H, Su W-R (2003) The effects of daylength on protein synthesis and flowering in Doritis pulcherrima. Sci Hortic 97:49–56
Wang R, Albani MC, Vincent C, Bergonzi S, Luan M, Bai Y, Kiefer C, Castillo R, Coupland G (2011) Aa TFL1 confers an age-dependent response to vernalization in perennial Arabis alpina. Plant Cell 23:1307–1321. https://doi.org/10.1105/tpc.111.083451
Wang Y, Liu L, Song S, Li Y, Shen L, Yu H (2017) DOFT and DOFTIP1 affect reproductive development in the orchid Dendrobium Chao Praya Smile. J Exp Bot 68:5759–5772. https://doi.org/10.1093/jxb/erx400
Wen Z, Guo W, Li J et al (2017) Comparative Transcriptomic Analysis of Vernalization- and Cytokinin-Induced Floral Transition in Dendrobium nobile. Sci Rep 7:45748. https://doi.org/10.1038/srep45748
Wickland DP, Hanzawa Y (2015) The FLOWERING LOCUS T/TERMINAL FLOWER 1 gene family: functional evolution and molecular mechanisms. Mol Plant 8:983–997. https://doi.org/10.1016/j.molp.2015.01.007
Wu W, Zheng XM, Lu G, Zhong Z, Gao H, Chen L, Wu C, Wang HJ, Wang Q, Zhou K et al (2013) Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc Natl Acad Sci USA 110:2775–2780. https://doi.org/10.1073/pnas.1213962110
Wu Z, Fang X, Zhu D, Dean C (2020) Autonomous pathway: FLOWERING LOCUS C repression through an antisense-mediated chromatin-silencing mechanism. Plant Physiol 182: 27–37. https://doi.org/10.1104/pp. 19.01009
Yamaguchi N, Winter CM, Wu MF, Kanno Y, Yamaguchi A, Seo M, Wagner D (2014) Gibberellin acts positively then negatively to control onset of flower formation in Arabidopsis. Science 344:638–641. https://doi.org/10.1126/science.1250498
Yang J, Lee S, Hang R, Kim SR, Lee YS, Cao X, Amasino R, An G (2013) OsVIL2 functions with PRC2 to induce flowering by repressing OsLFL1 in rice. Plant J 73:566–578. https://doi.org/10.1111/tpj.12057
Yang F, Zhu G, Wei Y et al (2019) Low-temperature-induced changes in the transcriptome reveal a major role of CgSVP genes in regulating flowering of Cymbidium goeringii. BMC Genom 20:53. https://doi.org/10.1186/s12864-019-5425-7
Yoo SK, Chung KS, Kim J, Lee JH, Hong SM, Yoo SJ, Yoo SY, Lee JS, Ahn JH (2005) CONSTANS activates SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 through FLOWERING LOCUS T to promote flowering in Arabidopsis. Plant Physiol 139: 770–778. https://doi.org/10.1104/pp. 105.066928
Yu H, Goh CJ (2000) Differential gene expression during floral transition in an orchid hybrid Dendrobium Madame Thong-In. Plant Cell Report 19:926–931
Yu H, Yang SH, Goh CJ (2000) DOH1, a class 1 knox gene, is required for maintenance of the basic plant architecture and floral transition in orchid. Plant Cell 12:2143–2160
Yu JW, Rubio V, Lee NY, Bai S, Lee SY, Kim SS, Liu L, Zhang Y, Irigoyen ML, Sullivan JA et al (2008) COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability. Mol Cell 32:617–630. https://doi.org/10.1016/j.molcel.2008.09.026
Yuan W, Luo X, Li Z, Yang W, Wang Y, Liu R, Du J, He Y (2016) A cis cold memory element and a trans epigenome reader mediate Polycomb silencing of FLC by vernalization in Arabidopsis. Nat Genet 48:1527–1534. https://doi.org/10.1038/ng.3712
Zhang J-X, Wu K-LW, Tian L-N, Zeng S-J, Duan JD (2011) Cloning and characterization of a novel CONSTANS-like gene from Phalaenopsis hybrida. Acta Physiol Plant 33:409–417. https://doi.org/10.1007/s11738-010-0560-4
Zheng J, Ma Y, Zhang M, Lyu M, Yuan Y, Wu B (2019a) Expression pattern of FT/TFL1 and miR156-targeted SPL genes associated with developmental stages in Dendrobium catenatum. Int J Mol Sci 20:2725. https://doi.org/10.3390/ijms20112725
Zheng T, Sun J, Zhou S, Chen S, Lu J, Cui S, Tian Y, Zhang H, Cai M, Zhu S et al (2019b) Post-transcriptional regulation of Ghd7 protein stability by phytochrome and OsGI in photoperiodic control of flowering in rice. New Phytol 224:306–320. https://doi.org/10.1111/nph.16010
Zuo Z, Liu H, Liu B, Liu X, Lin C (2011) Blue light-dependent interaction of CRY2 with SPA1 regulates COP1 activity and floral initiation in Arabidopsis. Curr Biol 21:841–847. https://doi.org/10.1016/j.cub.2011.03.048
Acknowledgements
The authors are grateful to Miranda Loney for English editing and apologize to all those people whose work was omitted through oversight or space constraints.
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This review paper was financially supported by the National Institute of Horticulture and Herbal Science, RDA, Korea and, in part by the World Vegetable Center Korea Office budget (WKO #10000379) and the long-term strategic donors to the World Vegetable Center: Republic of China (Taiwan), UK aid from the UK government, United States Agency for International Development (USAID), Australian Centre for International Agricultural Research (ACIAR), Germany, Thailand, Philippines, Korea and Japan.
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S.L.W. and S.J. conceived of the presented work. S.L.W. drafted the manuscript and S.J. and S.L.W. revised the manuscript. S.L.W., H.R.A. and S.J. collected the background information. C.G.T. and S.J. performed experiments. All authors read and approved the final manuscript.
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Communicated by So-Young Park, Ph.D.
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Wang, SL., An, H.R., Tong, CG. et al. Flowering and flowering genes: from model plants to orchids. Hortic. Environ. Biotechnol. 62, 135–148 (2021). https://doi.org/10.1007/s13580-020-00309-8
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DOI: https://doi.org/10.1007/s13580-020-00309-8