Research progress on the genetic regulatory mechanism of flowering in Chrysanthemum
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摘要:
开花是植物发育过程中一个关键的质变过程,是植物从营养生长向生殖生长阶段的转变。对于观赏植物来说,开花的早晚决定了其市场应用和经济价值。植物开花受到内外信号的复杂调控,基于模式植物拟南芥(Arabidopsis thaliana (L.) Heynh)的研究,目前已经阐明了6条主要的开花调控途径,这些途径彼此独立又互相交叉,形成复杂的遗传调控网络。菊花(Chrysanthemum × morifolium Ramat)作为起源于中国的世界名花,是世界花卉市场的重要一员,但因其是典型的短日照植物,不仅增加了生产中开花期调控成本,也限制了菊花的应用范围。本文以高等植物开花遗传调控网络为基础,综述了菊花开花遗传调控机制的研究进展,以期为菊花开花时间改良育种工作提供理论指导,同时也为解析高等植物开花机制提供新见解。
Abstract:Flowering represents a critical transition in plant development, shifting from the vegetative to reproductive growth stages. In ornamental plants, the timing of flowering significantly impacts marketability and economic value. Plant flowering is regulated by complex internal and external signals. Studies on the model plant Arabidopsis thaliana have identified six primary pathways related to flowering regulation. These independent but intersecting pathways form a complex genetic regulatory network. Chrysanthemum × morifolium, a famous flower originating from China, holds a considerable share of the world flower market. However, its typical short-day flowering requirements not only increase production costs but also limit its application scope. Based on the flowering regulatory networks of higher plants, this review discusses current research progress on the genetic regulatory mechanisms underlying chrysanthemum flowering, thus providing theoretical guidance for the breeding and improvement of flowering time, as well as new insights into the flowering mechanisms of higher plants.
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Keywords:
- Chrysanthemum × morifolium /
- Flowering /
- Environmental factors /
- Genetic regulation
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开花是高等植物生命周期中一个关键的质变过程,涉及植物从营养生长阶段到生殖生长阶段的转换,在植物的繁衍和生态适应过程中发挥着重要作用。经过数代科学家们的探索,克隆得到不同物种中诱导开花的关键调控基因,尤其是模式植物拟南芥(Arabidopsis thaliana (L.) Heynh)的研究,揭示了植物中复杂的开花调控网络[1]。作为关键的农艺性状之一,开花早晚直接影响作物的高产稳产、品质和区域分布,对于观赏植物而言,适宜的开花时间也决定了其自身观赏价值向产业价值的转化。因此,研究观赏植物开花遗传调控机制不仅为植物开花研究提供新的资料,对于筛选早花新品种满足市场需求也具有实际意义。
菊花(Chrysanthemum × morifolium Ramat)是起源于中国的世界名花,具有3 000多年的栽培历史,品种繁多,以奇特的姿态、绚丽的色彩深受人们喜爱[2]。随着菊花作为切花、盆花等被广泛应用,其栽培品种和应用数量在世界切花市场中占据首位[3]。近年来,我国花卉产业迅猛发展,2012年中国花卉生产总面积达1 120 300 hm2,其中菊花的种植面积达7 184.75 hm2,年销售额达到10亿元人民币[4];随着我国花卉种植面积的逐渐突破[5],我国花卉产品质量和产品规格类型也愈加得到国际市场的认可[6],菊花的种植面积和年销售额也逐渐上涨。菊花作为集深厚文化内涵和丰富经济价值于一体的世界名花,其全球产值和产量均位居前列,加大国内菊花产业化发展仍是亟待开展的工作。
作为典型的短日照植物,大多菊花品种的开花时间都集中在秋季或立冬前后,其生长过程中需经过一段时间的短日照诱导才能开花,这就大大限制了菊花的应用范围,尤其在特定节假日春节、五一等用花。为满足周年生产用花需求,除了利用传统杂交育种方式选育早花新品种外[7-9],生产中还常利用遮光、补光、调控氮肥用量等方式促进开花提前,但夏季遮光容易因温度过高导致花芽分化滞后,冬季补光和加温设备也导致生产成本增加,而盲目追施氮肥导致植株贪青晚熟,开花延迟,肥效资源浪费等[10-12]。探究菊花开花特性和开花机制,不仅为实际生产中科学栽培提供理论指导,同时也为分子育种定向培育适时开花品种奠定基础。因此,本文以高等植物开花机制研究进展为基础,综述了菊花开花遗传调控机制和关键开花基因的研究进展,以期为开展菊花早花育种工作提供理论依据。
1. 高等植物开花遗传调控网络
自1904年Klebs提出C/N比学说至今一个世纪以来,人们对高等植物开花机理进行了大量研究探索。高等植物开花时间的调控是一个复杂的过程,它往往是由外部环境信号和内部信号协同调控完成的,外部环境信号主要包括温度(高温、低温)、光照(光强、光质和光周期),内部信号主要包括激素(以赤霉素为主)、植物的年龄和碳水化合物的积累[13, 14]。这些调控途径并不是孤立的,各种信号途径彼此交织,最终通过整合基因实现对开花阶段转变的调控,达到对开花的精准控制[15, 16]。
当前,通过对模式植物开花机制的研究已明确了6条主要的开花途径:光周期途径(Photoperiod pathway)、春化途径(Vernalization pathway)、自主途径(Autonomous pathway)、赤霉素途径(Gibberellin pathway)、年龄途径(Age pathway)和环境温度途径(Ambient temperature pathway),其中春化途径和环境温度途径又可统称为温度途径[13, 14]。除此之外,研究发现海藻糖合成相关基因TPS1(TREHALOSE-6-PHOS- PHATE SYNTHASE 1)在开花中也起到了重要作用,海藻糖-6-磷酸(T6P)作为植物体内内源糖含量的指标性糖类,能通过调控叶片和茎尖中关键成花整合子的表达来传递成花转变的信号[17, 18]。部分miRNA(MicroRNA)也被分离并鉴定到参与开花诱导和花发育过程,在开花决定及花发育进程中发挥重要作用[19]。研究还发现压力条件,如热、盐和紫外线均可以促进开花,矿物质营养也被报道能影响开花[20-23]。这些信号途径既彼此独立又相互联系,最终形成一个复杂的高等植物开花调控网络,启动植物开花进程。
2. 菊花响应环境因素开花的类型
植物的开花是协调外界环境因素和自身内源信号的共同结果,对外界环境因素的不同需求导致了不同物种之间开花时间和开花方式的差异性。植物只有准确地感受内外信号,在最合适的时间激活体内与促花反应相关的生理代谢过程,启动开花进程才能将植物适合度收益最大化,不适宜的开花时间对于植物的发育、繁衍和进化将带来严重的不利影响[24-26]。过早开花使植物开花时间与传粉环境不匹配,导致植物不能顺利完成传粉从而繁殖失败[25],过晚开花则会错过资源利用最佳时间,不能在生长季结束前完成繁殖行为,也会使其相对于早花物种来说处于竞争弱势环境中,不利于资源利用[27]。
菊花品种繁多,不同种类及品种开花对外界的光照、温度等条件的需求不同,开花类型也存在极大差异。按照对光照的响应类型,菊花可以分为两大类:必须经过短日照诱导才能开花的光周期品种系列,即典型的短日照植物;无需经历短日照诱导可自然开花的非光周期品种系列,即非短日照植物。菊花按照自然花期可分为春菊(4月下旬-5月下旬)、夏菊(5月下旬-8月)、夏秋菊(8-9月)、秋菊(10月下旬-11月下旬)、寒菊(12上旬-次年2月)、四季菊(四季开花)[28],春菊、夏菊和四季菊均属于无严格短日照需求的日中性类型,秋菊和寒菊属于短日照诱导开花的短日照类型[29]。除光照外,温度的影响也极为重要,夏菊在10 ℃左右被诱导花芽分化,夏秋菊和秋菊在15 ℃以上被诱导花芽分化,寒菊在高温下被诱导花芽分化。此外,研究发现部分菊花品种在外源施用赤霉素后开花时间明显提前,并且在适宜的氮素栽培环境下生长速率加快,开花时间也明显提前[30-33]。
所有菊花开花期类型中,以秋菊类型品种最多,夏菊、寒菊的数量较少[29]。秋菊的开花需要在长日照条件下积累足够的营养生长量达到成花感受态,再接受短日照诱导才能开花。受长日照条件限制,部分秋菊品种在春夏季节均无法正常开花。研究表明,光周期主要通过红光(Pr)和远红光(Pfr)之间的相互转化实现植物开花阶段体内的生理代谢转变过程[34]。菊花进入短日照条件后,随着Pfr/Pr逐渐降低至临界值,会激活与促花反应相关的激素代谢途径,在激素的协同作用下形成开花刺激物传递到茎尖分生组织,从而诱发一系列生理代谢过程启动花芽分化进程[35, 36]。光照时长不同也会导致菊花生长呈现差异,虽然长日照延迟开花,短日照诱导开花提前,但过分缩短日照会导致菊花生长不良,花卉品质下降,只有在充足的光照条件下植株根系发育良好,地上部分生长量提高,开花品质才能提升[37-40]。
3. 菊花开花途径和开花关键基因的研究
3.1 光周期途径
植物响应日照长度成花的现象即为光周期现象。光周期信号对植物开花的调控可分为3个部分:光信号的输入、昼夜节律钟和信号的输出途径[41](图1)。叶片中的光受体能特异识别光信号,并与信号蛋白互作,将信号传递给昼夜节律钟,通过输出途径将信号传输给成花基因CO(CONSTANS),进而诱导下游FT(FLOWERING LOCUS T)和TSF(TWIN SISTER OF FT)表达[42-44]。FT蛋白转运至茎端分生组织后, 与FD(FLOWERING LOCUS D)形成蛋白复合物, 激活SOC1(SUPPRESSOR OF OVEREXPRESSION OF CO 1)、AP1(APETALA1)、FUL(FRUITFULL)等基因的表达,AP1又以正反馈调节的方式激活LFY(LEAFY),最终诱导开花。近期研究还发现CO和染色质重塑因子PKL(PICKLE)存在遗传和蛋白水平的互作,PKL对于光周期调控FT染色质的激活和抑制状态转变具有必需性[45];PcG(Polycomb group)蛋白介导的对FT的表观抑制可阻止提早开花,TrxG(Trithorax group)蛋白又能拮抗这种转录抑制作用,维持FT的特异且适当表达[46]。
图 1 拟南芥中以光周期途径为主的开花途径和菊花中响应光周期的同源基因红线代表在菊花中涉及的研究(参考网站:https://www.wikipathways.org/index.php/Pathway:WP622)。Figure 1. Flowering pathway dominated by photoperiodic pathway in Arabidopsis thaliana and photoperiod-responsive homologous genes in ChrysanthemumRed line represents research involving Chrysanthemum (Photoperiodic pathway available online: https://www.wikipathways.org/index.php/Pathway: WP2312).光周期是影响菊花开花的重要因素之一,尤其是对于大部分秋菊品种而言。近些年来,随着人们对光周期影响菊花开花作用机制研究的逐渐深入,越来越多参与调控菊花开花的光周期途径基因被鉴定(图1)。不同菊花品种响应光照的临界日长不同,其光周期的诱导效应也存在差异。前人研究提出红光对菊花开花具有抑制作用,而蓝光促进成花[47, 48]。但是Nissim-Levi等[49]的研究发现蓝光对3个菊花品种的开花存在抑制作用,抑制效率取决于照明持续时间。菊花的短日照诱导过程被持续性或间歇性的光照中断后,开花进程也会被抑制。进一步研究发现,光受体基因ClCRYs(Cryptochromes)能响应短日照诱导甘菊(C. lavandulifolium (Fisch. ex Trautv.) M)开花,过表达ClCRY1a、ClCRY1b和ClCRY2后甘菊开花提前[50, 51];甘菊和毛华菊(C. vestitum (Hemsl.) Stapf)中PHYA(Phytochrome)和PHYB均能响应短日照诱导表达,且过表达ClPHYB后拟南芥开花延迟[34]。PRR(Pseudo-response regulator)在植物的生物钟中发挥重要作用,对菊花中鉴定到的4个PRRs成员(CmPRR2、CmPRR7、CmPRR37和CmPRR73)进行分析,发现CmPRRs在不同光周期处理下均可在一程度上保持昼夜节律振荡特征,可能调控了菊花的开花过程[52]。而通过比对野菊(C. indicum L.)中分离的CO基因,发现CiCO与甘菊、黄花蒿(Artemisia annua L.)中CO同源性极高,短日照环境能诱导CiCO的表达并提前野菊开花时间[53]。
目前在菊花中共发现3个FT-like基因,其中CmFTL1和CmFTL3分别在长日照和短日照条件下作为开花调控因子,CmFTL2在光不敏感菊花品种‘优香’中被发现响应光周期变化和外源蔗糖供应[54-56]。在野菊中也鉴定到两个FT-like基因,CiCO能特异地结合CiFTL1启动子,不能结合到CiFTL2启动子上,CO/FT开花调控模块在野菊中被保留[57]。在甘野菊(C. seticuspe (Maxim.) Hand.-Mazz. f. boreale (Makino) H. Ohashi & Yonek)中鉴定的FTL3和AFT(ANTI-FLORIGENIC FT/TFL1 FAMILY PROTEIN)基因分别能被短日照和非短日照条件诱导,将LHY/CCA1-like(LATE ELONGATED HYPOCOTYL/CIRCADIAN CLOCK ASSOCIATED 1-like)与SRDX(Short transcriptional repressor domain)基因融合后在甘野菊中组成性表达,导致植株开花阶段转变对光周期不敏感,并影响CsFTL3 和 CsAFT的表达[54, 55, 58]。过表达CsGI(GIGANTEA)后,甘野菊需要较长的黑暗期来维持较低的CsAFT水平,从而延长了开花临界夜长,CsGI通过形成光诱导CsAFT的闸门,在光周期开花控制中发挥重要作用[59]。其他相关基因是否调控菊花响应光周期成花尚未见报道。
3.2 温度途径
植物可以通过复杂的感觉系统感知外界环境的温度变化,并根据温度变化优化它们的生长发育进程[60]。植物响应低温诱导开花的作用称为春化作用[61],作为一种程序化的生理过程,长时间的低温暴露下能够使植物具备开花的能力(图2)。FLC(FLOWERING LOCUS C)和FRI(FRIGIDA)基因是春化途径上调控开花的关键因子,FLC能够编码一种MADS-box(MCM1-AGAMOUSDEFICIENS-SRF-box)蛋白, 直接结合到FT、FD和SOC1基因位点抑制其转录。在小麦(Triticum aestivum L.)等谷物中鉴定到了VRN1(VERNALIZATION 1)、VRN2和VRN3 3个响应低温春化作用的关键基因[62]。研究还发现长链非编码RNA(IncRNAs)在春化作用中也起到了重要的作用[63, 64],O-GlcNAc修饰和磷酸化修饰动态也参与调控春化作用,介导小麦的开花过程[65]。
除了低温影响植物开花,环境中微小的温度变化也会对植物开花产生影响,且不同物种之间差异显著[66]。研究发现,环境温度升高至27 ℃条件下可诱导拟南芥FT表达,组蛋白变体H2A.Z会从FT启动子中脱离,解除对FT的抑制作用,同时转录因子PIF4(Phytochrome interacting factor 4)积累并激活FT转录,促使拟南芥在非诱导性短日照条件下提前开花[21, 67-69](图2)。FLM(FLOW-ERING LOCUS M)作为FLC分支成员,转录了两种不同剪切体:FLM-β和FLM-δ,两类剪切体均受环境温度的调控[70]。非编码RNA(non-coding RNAs,ncRNAs)、miRNAs和长链非编码 RNA(Long non-coding RNAs,lncRNAs)也被证实能参与环境温度介导的植物开花调控[71, 72],染色质重塑因子、组蛋白修饰酶和EC复合体(Evening complex)在环境温度介导的植物开花进程发挥了重要作用[69, 73-77]。
近些年来,随着国内外对于菊花花卉资源的迫切需求和经济价值的提升,探索除光照的外部温度环境调控开花的作用机制也已经取得一定进展(图2)。菊花在度过炎热的夏季时,当夜间温度 ≥ 26 ℃后日间的温度也会偏高,夜间高温会延迟菊花的花芽分化并导致开花异常甚至败育,因此通过有效利用控制夜间温度的措施可以提高菊花的开花质量和开花品质[78]。菊花所在的环境温度升高(>20 ℃)后,FTL3的表达被抑制,因而导致开花延迟[79, 80]。植物对外界温度环境的热敏感性已经被证明在一天中波动,像受生物钟调节一样,菊花的热敏感性同样受光暗转换的内部时钟控制,随着向黑暗的过渡菊花的热敏感度不会立即提高,而是随着暗夜时期而逐渐增强,在暗夜结束时菊花的热敏感度能达到最大值,该现象与光周期的变化无关[80, 81]。
当菊花处在较低的环境温度下同样会导致开花延迟[82],对于夏季开花的品种来说,有类似于春化植物的特性,其开花受低温诱导,能在长日照条件下完成成花转变[83]。分离的拟南芥CRAP2(CRT/DRE-binding factor 3)基因在菊花中表达后,能诱导SOC1和FTL3表达,在夜间温度低于15 ℃的短日照条件下促使菊花开花提前[82]。与拟南芥中FLC的作用机制不同,菊花中FLC同源基因CmMAF2(MADS AFFECTING FLOWERING 2)在感受低温期间被迅速诱导表达,进而抑制赤霉素合成酶基因GA20ox1表达,温度回暖后CmMAF2的表达被抑制,从而解除了对GA20ox1基因的抑制作用,促进菊花生长和开花[83]。长时间低温环境暴露下,内部形成的抑制开花状态(“冷记忆”)也会使菊花即使进入春季也不会立马开花。短日照条件能诱导甘野菊中CsFTL3 表达并开花,但在感受长时间的低温环境后CsFTL3 的表达被抑制了,开花诱导被阻碍,这也是决定大多数菊花秋季开花的因素之一[84]。此外,菊花中也鉴定到了拟南芥功能同源基因,ClMAD1(Mitotic arrest deficiency 1)能与ClSUF4(Suppressor of FRIGIDA 4)发生互作,从而在温度变化期间调节甘菊FLC1基因介导的开花过程[85]。
3.3 赤霉素途径
植物激素赤霉素(Gibberellins,GA)能诱导个别长日照植物开花,外源喷施赤霉素可部分替代冷依赖植物的低温处理[86]。阻断了内源赤霉素生物合成则植物开花延迟[87]。GID1(GIBBERELLIN INSENSITIVE DWARF1)是拟南芥中的赤霉素受体蛋白,与GA结合后通过调控DELLA蛋白活性影响开花。迄今为止,在拟南芥基因组中共鉴定到5个DELLA蛋白[88]。近期研究还发现DELLA蛋白能与光周期调控的F-box蛋白FKF1(FLAVIN-BINDING KELCH REPEAT F-BOX 1)构成FKF1-DELLA,反馈调控环介导光周期途径和GA途径协同调节植物开花[89]。而miRNA也能通过赤霉素途径调控植物开花,miRNA159通过调控赤霉素途径中一类MYB转录因子抑制LFY的表达,该机制与GA-DELLA-SPL9(SQUAMOSA PROMOTER BINDING PROTEIN-LIKE 9)途径相互独立[90, 91]。
菊花的开花进程主要发生在短日照条件下,但其从营养生长向生殖生长的转变过程涉及了众多因素,其中就包括植物激素的影响。外源施用GA后,菊花品种‘Pink Champagne’能在无诱导的长日照条件下开花,尤其是结合细胞分裂素BA(N6-Benzyladenine)共施后开花效果更佳,二者协同促进菊花开花[92]。盆栽小菊在外源施用GA3后提前5 d开花,花期延长了7 d[30]。在对不同光周期条件下的菊花‘神马’突变体材料进行测序分析后,发现昼夜节律钟基因和CmFTL3基因在短日照条件下上调表达,诱导开花进程;GA通路相关基因GA20ox (Gibberellin 20-oxidase)和GID1(Gibberellin receptor)在长日照条件下的突变体材料中上调表达,GA2ox和 GAI (GA-INSENSITIVE)下调表达,表明光周期途径是短日照条件下调控菊花开花的主要通路,GA途径仅起到了辅助作用,而进入长日照环境后GA途径是调控菊花开花的主要通路[93]。研究发现,低温和GA处理都能促进短日植物的开花,不同栽培菊花中开花需求特性存在差异,需要GA诱导的同时也需要低温才能开花,而不需要GA的则没有低温需求[86]。近期在菊花的研究中还鉴定到R2R3型MYB转录因子CmMYB2能通过赤霉素途径调控开花,过表达CmMYB2后开花提前,CmMYB2能与抑制赤霉素合成的CmBBX24直接互作,调控菊花开花[94, 95];夏菊中CmMAF2基因在低温下被诱导表达后进一步抑制赤霉素合成酶基因GA20ox1的表达和GAs的合成,而在温度升高后CmMAF2的表达下调,GA20ox1基因的抑制作用被解除,GAs开始合成,菊花快速生长并开花[83]。
3.4 年龄途径和自主途径
年龄途径和自主途径是独立于外源信号刺激和内源激素信号的开花途径[14, 16]。目前在植物中鉴定到的年龄调控途径主要包括2条:miR156-SPLs和JMJ18(JUMONJI DOMAIN-CONTAINING PROTEIN 18)-FLC/MAFs。研究表明,miR156及miR172分别作为开花抑制因子和促进因子起作用[96-98]。JMJ18也作为一类自身年龄的衡量因子调控植物开花[99]。FLC作为调控开花的关键基因,在自主途径上分离得到的基因主要通过调节FLC的染色质或对其mRNA进行修饰而影响开花。自主途径基因的编码蛋白可以归为两大类:参与染色质重塑以及影响RNA加工。其中FLD(FLOWERING LOCUS D)、FVE(FLOWERING LOCUS VE)和REF6(RELATIVE OF EARLY FLOWERING 6)已被鉴定参与染色质重塑,而FCA(FLOWERING CONTROL LOCAL A)、FPA(FLOWERING TIME CONTROL PROTEIN FPA)、FY(FLOWERING TIME CONTROL PROTEIN FY)、FLK(FLOWERING LOCUS KH DOMAIN)编码RNA结合蛋白。
鉴于菊花的短日开花特性,目前对菊花的开花研究主要集中在光周期通路上,然而在进入成花感受态之前,菊花必须经过一定时间的营养生长才能接受开花诱导向生殖生长阶段过渡,这一过程涉及了植物中除光周期途径外的其他开花途径。目前在菊花中共分离鉴定了12个SPLs(SBP-like)基因,其中确定了两对分别在菊花和拟南芥中的直系同源基因,6个CmSPLs包含了miR156目标位点,5个CmSPLs是miR157的靶基因,这些结果对于菊花中CmSPLs基因家族成员的功能解析也奠定了基础[100]。对菊花中CmSPL4.1、CmSPL5.1、CmSPL6和CmSPL13基因功能做进一步分析,发现4个基因在菊花中的组织特异性表达模式存在差异,超表达后均能使拟南芥开花提前,下游基因AP1、FUL、SOC1、FT、LFY的表达均显著上升,开花抑制子FLC的表达量下调[101]。菊花的核因子(Nuclear factor Y , NF-Y)家族成员CmNF-YB8沉默后,菊花中SPLs家族基因SPL3、SPL5和SPL9均表达上调,CmNF-YB8能与年龄途径上miR156的启动子直接结合调控菊花的开花早晚,无论长短日照条件,沉默转基因植株均能提前开花[102, 103]。同时还发现NF-YA2 和 NF-YC3蛋白能与 NF-YB8 蛋白互作,明确了NF-YA2\NF-YB8\NF-YC3 蛋白复合体在年龄途径中的作用[102, 104]。这些研究结果不仅为阐明菊花的开花作用机制提供了新的见解,同时也为菊花花期改良分子育种提供了基因储备。
3.5 菊花中其他开花关键基因的研究
随着人们对菊花开花机制探究的逐渐深入,越来越多参与调控菊花开花过程的关键基因被鉴定。研究发现,菊花中MADS-box基因 CmSVP的第2个LXLXLX基序(LRLGLP)能与CmTPL1-2(TOPLESS-2)互作,CmTPL1-2又进一步结合在CmFTL3启动子上的CArG 元件抑制其表达,CmSVP-CmTPL1-2 转录复合物是SVP作为开花抑制因子发挥作用的先决条件,进一步降低CmFTL3 的转录活性[105]。此外,BBX19(B-box 19)作为一种在植物中鉴定的新型生物钟调节器,BBX19-PRRs蛋白复合体能直接在昼夜节律钟的转录调节中起作用,BBX19与CO互作抑制FT及下游基因的转录水平,是植物光周期途径上重要的开花调节基因[106-108]。而在夏菊‘优香’中发现B-box家族成员CmBBX8在调控日中性菊花的开花进程中发挥了重要作用,CmRCD1 (RADICAL-INDUCED CELL DEATH 1)能与CmBBX8互作并抑制CmBBX8的转录活性,干扰其对CmFTL1的调控作用,导致开花延迟[109, 110];该家族另外两个成员CmBBX29、CmBBX13也被鉴定介导了开花延迟现象[111, 112]。
除了研究最多的赤霉素对菊花开花的影响,其他内源激素在菊花开花上的作用机制也取得了新进展。乙烯能延迟短日照菊花的开花时间,在菊花品种‘SeiMarine’中突变乙烯受体基因mDG-ERS1(etr1-4)后,不仅降低了植株对乙烯的敏感性,同时突变体植株比野生型开花提前,下游FT同源基因表达增强,其中CmFTL3基因表达增强与菊花开花提前和乙烯敏感性降低相关[113]。乙烯反应元件结合蛋白(Ethylene‐responsive element-binding protein,ERF)转录因子CmERF110能与菊花中FLK同源基因CmFLK 相互作用,通过调控生物钟促进菊花开花提前[114]。茉莉酸(Jasmonic acid,JA)信号通路上的重要组分TIFY家族基因JAZs广泛参与植物的生长发育过程[115],而JA信号路径的负调节因子CmJAZ1-like基因参与调控了菊花‘神马’的开花进程,超表达Jas结构域缺失的CmJAZ1-like基因后菊花开花延迟,下游开花基因FT、SOC1和FUL表达呈现差异[116]。这些关键基因功能的鉴定为分子育种改良菊花开花提供了重要的基因资源。
4. 展望
在历经了一百多年的研究后,高等植物的开花调控网络逐渐清晰,尤其是针对模式植物的开花遗传调控网络研究,但仍然存在很多未解的谜团和具有争议的问题。菊花作为全球最重要的观赏植物种类之一,在菊花的商品生产中,因营养生长周期长,往往需要通过人工补光和遮光进行精确开花调控,这就极大地增加了生产成本。因此,创制营养生长期短、光周期不敏感的种质资源对菊花的推广应用及节能生产具有重要意义[102, 104]。作为遗传背景复杂的六倍体物种,菊花开花调控机制仍然存在很大的研究空白,挖掘关键开花相关基因,利用分子育种手段改良菊花花期并筛选早花品种仍需加快脚步。虽然目前市场上已经培育出了一部分日中性品种,但这远远不能满足市场对菊花周年产业化生产的需求。
随着组学时代的迅猛发展,各种生物技术层出不穷,尤其是RNA-seq测序技术、单细胞测序技术、分子标记等,这些技术的快速发展为现代分子生物学的发展提供了有力的技术支撑。未来,针对高等植物包括菊花的开花机制应开展更加全面深入的研究。首先是对新基因的功能鉴定,这对于了解植物开花多样性的分子机制,以及定向育种均具有重要意义。如在菊花中鉴定关于乙烯和茉莉酸激素相关基因在开花中的作用[114, 116],对于未来基于激素途径定向改良菊花花期,以及生产中通过激素应用精准调控菊花开花都具有极大的应用前景。其次,调控植物开花因素应开展多方面的研究,如各类营养物质在植物开花中的作用机制等。植物在生长发育过程中需要矿质营养的供应,尤其是大量元素氮的施用,生产中常通过加大氮肥施用量加速植株营养生长,但往往因施用过量导致植株徒长,开花延迟。氮在开花中的重要性已被无数园艺学家验证[117-120],然而氮究竟通过何种通路调控菊花开花却还始终是一个谜。对氮素在菊花开花中的作用机制解析,对于生产中精准施肥调控开花提供科学的理论指导。随着现代生物学技术的快速发展,以及当代人们对观赏植物需求的逐渐上涨,如何全面解析观赏植物开花调控机制,定向培育并改良开花还需要进一步探究。
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图 1 拟南芥中以光周期途径为主的开花途径和菊花中响应光周期的同源基因
红线代表在菊花中涉及的研究(参考网站:https://www.wikipathways.org/index.php/Pathway:WP622)。
Figure 1. Flowering pathway dominated by photoperiodic pathway in Arabidopsis thaliana and photoperiod-responsive homologous genes in Chrysanthemum
Red line represents research involving Chrysanthemum (Photoperiodic pathway available online: https://www.wikipathways.org/index.php/Pathway: WP2312).
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[1] 舒黄英,郝园园,蔡庆泽,王振,朱国鹏,等. 模式植物拟南芥开花时间分子调控研究进展[J]. 植物科学学报,2017,35(4):603−608. doi: 10.11913/PSJ.2095-0837.2017.40603 Shu HY,Hao YY,Cai QZ,Wang Z,Zhu GP,et al. Recent research progress on the molecular regulation of flowering time in Arabidopsis thaliana[J]. Plant Science Journal,2017,35 (4):603−608. doi: 10.11913/PSJ.2095-0837.2017.40603
[2] 张秋玲,刘海鹏,高康,孔德元,戴思兰. 盆栽菊花反季节开花调控技术研究[J]. 黑龙江农业科学,2021(9):62−67. Zhang QL,Liu HP,Gao K,Kong DY,Dai SL. Research on anti-seasonal flowering control technology of potted chrysanthemum[J]. Heilongjiang Agricultural Sciences,2021 (9):62−67.
[3] 陈俊愉, 程绪珂. 富贵神仙品(中国花经节编)[M]//王明明. 大匠之门5. 南宁: 广西美术出版社, 2015: 1-100. [4] 谯德惠. 花卉产销实现平稳增长——2012年全国花卉统计数据分析[J]. 中国花卉园艺,2013(15):26−31. [5] 李小青. 我国花卉出口贸易的现状、问题及对策[J]. 中国市场,2022(29):75−78. doi: 10.13939/j.cnki.zgsc.2022.29.075 [6] 张引潮. 坚定信心锚定花卉业高质量发展——在2022全国花卉产销形势分析会上的讲话[J]. 中国花卉园艺,2022(4):10−15. doi: 10.3969/j.issn.1009-8496.2022.4.zghhyy202204003 [7] 尚嘉琪. 地被菊花期改良育种技术研究[D]. 晋中: 山西农业大学, 2017: 1-10. [8] 古晓红,李方舟,张海生,杨婷婷,王军. 大豆常规杂交育种和生物分子育种的优劣对比[J]. 种子科技,2020,38(17):29−30. doi: 10.3969/j.issn.1005-2690.2020.17.013 [9] 雒新艳,张俊丽,张二海. 盆栽小菊育种研究进展[J]. 山东林业科技,2021,51(1):81−86. doi: 10.3969/j.issn.1002-2724.2021.01.019 Luo XY,Zhang JL,Zhang EH. Research progress on potted chrysanthemum breeding[J]. Journal of Shandong Forestry Science and Technology,2021,51 (1):81−86. doi: 10.3969/j.issn.1002-2724.2021.01.019
[10] 赵小刚. 日中性小菊新品种选育及小菊开花期遗传分析[D]. 北京: 北京林业大学, 2019: 1-10. [11] 蒋志敏,王威,储成才. 植物氮高效利用研究进展和展望[J]. 生命科学,2018,30(10):1060−1071. doi: 10.13376/j.cbls/2018128 Jiang ZM,Wang W,Chu CC. Towards understanding of nitrogen use efficiency in plants[J]. Chinese Bulletin of Life Sciences,2018,30 (10):1060−1071. doi: 10.13376/j.cbls/2018128
[12] Gojon A. Nitrogen nutrition in plants:rapid progress and new challenges[J]. J Exp Bot,2017,68 (10):2457−2462. doi: 10.1093/jxb/erx171
[13] Srikanth A,Schmid M. Regulation of flowering time:all roads lead to Rome[J]. Cell Mol Life Sci,2011,68 (12):2013−2037. doi: 10.1007/s00018-011-0673-y
[14] Blümel M,Dally N,Jung C. Flowering time regulation in crops:what did we learn from Arabidopsis?[J]. Curr Opin Biotechnol,2015,32:121−129. doi: 10.1016/j.copbio.2014.11.023
[15] 孙昌辉,邓晓建,方军,储成才. 高等植物开花诱导研究进展[J]. 遗传,2007,29(10):1182−1190. doi: 10.3321/j.issn:0253-9772.2007.10.005 Sun CH,Deng XJ,Fang J,Chu CC. An overview of flowering transition in higher plants[J]. Hereditas (Beijing)
,2007,29 (10):1182−1190. doi: 10.3321/j.issn:0253-9772.2007.10.005 [16] 张艺能,周玉萍,陈琼华,黄小玲,田长恩. 拟南芥开花时间调控的分子基础[J]. 植物学报,2014,49(4):469−482. doi: 10.3724/SP.J.1259.2014.00469 Zhang YN,Zhou YP,Chen QH,Huang XL,Tian CE. Molecular basis of flowering time regulation in Arabidopsis[J]. Chinese Bulletin of Botany,2014,49 (4):469−482. doi: 10.3724/SP.J.1259.2014.00469
[17] Komeda Y. Genetic regulation of time to flower in Arabidopsis thaliana[J]. Annu Rev Plant Biol,2004,55:521−535. doi: 10.1146/annurev.arplant.55.031903.141644
[18] Wahl V,Ponnu J,Schlereth A,Arrivault S,Langenecker T,et al. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana[J]. Science,2013,339 (6120):704−707. doi: 10.1126/science.1230406
[19] Teotia S,Tang GL. To bloom or not to bloom:role of MicroRNAs in plant flowering[J]. Mol Plant,2015,8 (3):359−377. doi: 10.1016/j.molp.2014.12.018
[20] Achard P,Cheng H,de Grauwe L,Decat J,Schoutteten H,et al. Integration of plant responses to environmentally activated phytohormonal signals[J]. Science,2006,311 (5757):91−94. doi: 10.1126/science.1118642
[21] Balasubramanian S,Sureshkumar S,Lempe J,Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature[J]. PLoS Genetics,2006,2 (7):e106. doi: 10.1371/journal.pgen.0020106
[22] Martínez C,Pons E,Prats G,León J. Salicylic acid regulates flowering time and links defence responses and reproductive development[J]. Plant J,2004,37 (2):209−217. doi: 10.1046/j.1365-313X.2003.01954.x
[23] Vidal EA,Moyano TC,Canales J,Gutiérrez RA. Nitrogen control of developmental phase transitions in Arabidopsis thaliana[J]. J Exp Bot,2014,65 (19):5611−5618. doi: 10.1093/jxb/eru326
[24] Kitamoto N,Ueno S,Takenaka A,Tsumura Y,Washitani I,Ohsawa R. Effect of flowering phenology on pollen flow distance and the consequences for spatial genetic structure within a population of Primula sieboldii (Primulaceae)[J]. Am J Bot,2006,93 (2):226−233. doi: 10.3732/ajb.93.2.226
[25] Elzinga JA,Atlan A,Biere A,Gigord L,Weis AE,Bernasconi G. Time after time:flowering phenology and biotic interactions[J]. Trends Ecol Evol,2007,22 (8):432−439. doi: 10.1016/j.tree.2007.05.006
[26] Lemoine NP,Doublet D,Salminen JP,Burkepile DE,Parker JD. Responses of plant phenology,growth,defense,and reproduction to interactive effects of warming and insect herbivory[J]. Ecology,2017,98 (7):1817−1828. doi: 10.1002/ecy.1855
[27] Vermeulen PJ. On selection for flowering time plasticity in response to density[J]. New Phytol,2015,205 (1):429−439. doi: 10.1111/nph.12984
[28] 万亚楠. 菊花的花期调控方法初探[J]. 现代园艺,2013(20):50−51. doi: 10.3969/j.issn.1006-4958.2013.20.035 [29] 张树林, 戴思兰. 中国菊花全书[M]. 北京: 中国林业出版社, 2013: 1-100. [30] 陈洪国,马容明. GA3对菊花开花和花瓣某些生理生化指标的影响[J]. 安徽农业科学,2006,34(6):1050−1051. doi: 10.3969/j.issn.0517-6611.2006.06.005 Chen HG,Ma RM. Effects of GA3 on the flowering and some physiological indexes of chrysanthemum[J]. Journal of Anhui Agricultural Sciences,2006,34 (6):1050−1051. doi: 10.3969/j.issn.0517-6611.2006.06.005
[31] 刘敏,丁江南,王飞翔,于晓英. 叶面喷施赤霉素对瓜叶菊生长与开花的影响[J]. 天津农业科学,2010,16(6):36−38. doi: 10.3969/j.issn.1006-6500.2010.06.014 Liu M,Ding JN,Wang FX,Yu XY. Effects of gibberellins treatment on growth and flowering of Senecio × hybridus[J]. Tianjin Agricultural Sciences,2010,16 (6):36−38. doi: 10.3969/j.issn.1006-6500.2010.06.014
[32] 张秋玲,杨秀珍,戴思兰,张倩,罗虹,张伯晗. 不同氮磷钾水平对毛华菊生长发育的影响[J]. 山东农业大学学报(自然科学版),2020,51(4):611−616. doi: 10.3969/j.issn.1000-2324.2020.04.005 Zhang QL,Yang XZ,Dai SL,Zhang Q,Luo H,Zhang BH. Effect of different N,P,K proportions on the development of Chrysanthemum vestitum[J]. Journal of Shandong Agricultural University (Natural Science Edition)
,2020,51 (4):611−616. doi: 10.3969/j.issn.1000-2324.2020.04.005 [33] 张秋玲,杨秀珍,戴思兰,邱丹丹,董南希,李清清. 不同氮水平下毛华菊形态性状的差异分析[J]. 中国农业大学学报,2020,25(5):70−77. doi: 10.11841/j.issn.1007-4333.2020.05.07 Zhang QL,Yang XZ,Dai SL,Qiu DD,Dong NX,Li QQ. Difference analysis of morphological traits of Chrysanthemum vestitum under different nitrogen levels[J]. Journal of China Agricultural University,2020,25 (5):70−77. doi: 10.11841/j.issn.1007-4333.2020.05.07
[34] 马朝峰. 甘菊和毛华菊PHYA和PHYB同源基因表达分析及ClPHYB功能验证[D]. 北京: 北京林业大学, 2019: 1-10. [35] 王富刚,张静,张雄. 光敏色素与植物的光形态建成[J]. 基因组学与应用生物学,2017,36(8):3167−3171. doi: 10.13417/j.gab.036.003167 Wang FG,Zhang J,Zhang X. Phytochromes and plant photomorphogenesis[J]. Genomics and Applied Biology,2017,36 (8):3167−3171. doi: 10.13417/j.gab.036.003167
[36] 王君杰,田翔,秦慧彬,王海岗,曹晓宁,等. 光周期对糜子生长发育及叶片内源激素的调控效应[J]. 中国农业科学,2021,54(2):286−295. doi: 10.3864/j.issn.0578-1752.2021.02.005 Wang JJ,Tian X,Qin HB,Wang HG,Cao XN,et al. Regulation effects of photoperiod on growth and leaf endogenous hormones in broomcorn millet[J]. Scientia Agricultura Sinica,2021,54 (2):286−295. doi: 10.3864/j.issn.0578-1752.2021.02.005
[37] 贺玉利. 菊花矮化及提前开花栽培技术[J]. 北方园艺,2003(3):80. doi: 10.3969/j.issn.1001-0009.2003.03.055 [38] 姜贝贝,房伟民,陈发棣,赵宏波,顾俊杰. 植株营养生长天数对切花菊花芽分化与品质的影响[J]. 中国农业科学,2008,41(6):1755−1760. doi: 10.3864/j.issn.0578-1752.2008.06.024 Jiang BB,Fang WM,Chen FD,Zhao HB,Gu JJ. Effect of vegetative growth days on flower bud differentiation and quality of cut chrysanthemum[J]. Scientia Agricultura Sinica,2008,41 (6):1755−1760. doi: 10.3864/j.issn.0578-1752.2008.06.024
[39] 陆思宇,杨再强,杨立,张源达,郑涵. 不同光周期对菊花生长发育及内源激素的影响[J]. 华北农学报,2021,36(6):106−115. doi: 10.7668/hbnxb.20192386 Lu SY,Yang ZQ,Yang L,Zhang YD,Zheng H. Effects of different photoperiods on the growth and development process and endogenous hormones of chrysanthemum[J]. Acta Agriculturae Boreali-Sinica,2021,36 (6):106−115. doi: 10.7668/hbnxb.20192386
[40] 陆思宇. 光周期对‘红面’菊花生长发育的影响机理[D]. 南京: 南京信息工程大学, 2022: 1-10. [41] Hsu PY,Harmer SL. Wheels within wheels:the plant circadian system[J]. Trends Plant Sci,2014,19 (4):240−249. doi: 10.1016/j.tplants.2013.11.007
[42] Yu JW,Rubio V,Lee NY,Bai SL,Lee SY,et al. COP1 and ELF3 control circadian function and photoperiodic flowering by regulating GI stability[J]. Molecular Cell,2008,32 (5):617−630. doi: 10.1016/j.molcel.2008.09.026
[43] Song YH,Shim JS,Kinmonth-Schultz HA,Imaizumi T. Photoperiodic flowering:time measurement mechanisms in leaves[J]. Annu Rev Plant Biol,2015,66:441−464. doi: 10.1146/annurev-arplant-043014-115555
[44] Shim JS,Kubota A,Imaizumi T. Circadian clock and photoperiodic flowering in Arabidopsis:CONSTANS is a hub for signal integration[J]. Plant Physiol,2017,173 (1):5−15. doi: 10.1104/pp.16.01327
[45] Jing YJ,Guo Q,Lin RC. The chromatin-remodeling factor PICKLE antagonizes polycomb repression of FT to promote flowering[J]. Plant Physiol,2019,181 (2):656−668. doi: 10.1104/pp.19.00596
[46] Jing YJ,Guo Q,Zha P,Lin RC. The chromatin‐remodelling factor PICKLE interacts with CONSTANS to promote flowering in Arabidopsis[J]. Plant Cell Environ,2019,42 (8):2495−2507. doi: 10.1111/pce.13557
[47] Kadman-Zahavi A,Yahel H. Phytochrome effects in night-break illuminations on flowering of Chrysanthemum[J]. Physiol Plant,1971,25 (1):90−93. doi: 10.1111/j.1399-3054.1971.tb01094.x
[48] Jeong SW,Park S,Jin JS,Seo ON,Kim GS,et al. Influences of four different light-emitting diode lights on flowering and polyphenol variations in the leaves of chrysanthemum (Chrysanthemum morifolium)[J]. J Agric Food Chem,2012,60 (39):9793−9800. doi: 10.1021/jf302272x
[49] Nissim-Levi A,Kitron M,Nishri Y,Ovadia R,Forer I,et al. Effects of blue and red LED lights on growth and flowering of Chrysanthemum morifolium[J]. Sci Hortic,2019,254:77−83. doi: 10.1016/j.scienta.2019.04.080
[50] Yang LW,Wen XH,Fu JX,Dai SL. ClCRY2 facilitates floral transition in Chrysanthemum lavandulifolium by affecting the transcription of circadian clock-related genes under short-day photoperiods[J]. Hortic Res,2018,5:58. doi: 10.1038/s41438-018-0063-9
[51] Yang LW,Fu JX,Qi S,Hong Y,Huang H,Dai SL. Molecular cloning and function analysis of ClCRY1a and ClCRY1b,two genes in Chrysanthemum lavandulifolium that play vital roles in promoting floral transition[J]. Gene,2017,617:32−43. doi: 10.1016/j.gene.2017.02.020
[52] Wang SJ,Zhang CL,Zhao J,Li RH,Lv JH. Expression analysis of four pseudo-response regulator (PRR) genes in Chrysanthemum morifolium under different photoperiods[J]. PeerJ,2019,7:e6420. doi: 10.7717/peerj.6420
[53] 陈丹丹,邹庆军,郭巧生,汪涛. 短日照处理对野菊CO基因表达量的影响[J]. 中国中药杂志,2019,44(4):648−653. doi: 10.19540/j.cnki.cjcmm.2019.0014 Chen DD,Zou QJ,Guo QS,Wang T. Effect of short-day treatment on expression of CO gene in Chrysanthemum indicum[J]. China Journal of Chinese Materia Medica,2019,44 (4):648−653. doi: 10.19540/j.cnki.cjcmm.2019.0014
[54] Oda A,Narumi T,Li TP,Kando T,Higuchi Y,et al. CsFTL3,a chrysanthemum FLOWERING LOCUS T-like gene,is a key regulator of photoperiodic flowering in chrysanthemums[J]. J Exp Bot,2012,63 (3):1461−1477. doi: 10.1093/jxb/err387
[55] Higuchi Y,Narumi T,Oda A,Nakano Y,Sumitomo K,et al. The gated induction system of a systemic floral inhibitor,antiflorigen,determines obligate short-day flowering in chrysanthemums[J]. Proc Natl Acad Sci USA,2013,110 (42):17137−17142. doi: 10.1073/pnas.1307617110
[56] Sun J,Wang H,Ren LP,Chen SM,Chen FD,et al. CmFTL2 is involved in the photoperiod- and sucrose-mediated control of flowering time in chrysanthemum[J]. Hortic Res,2017,4:17001. doi: 10.1038/hortres.2017.1
[57] Zuo L,Wang T,Guo Q,Yang F,Zou Q,et al. Conserved CO-FT module regulating flowering time in Chrysanthemum indicum L.[J]. Russ J Plant Physiol,2021,68 (6):1018−1028. doi: 10.1134/S102144372106025X
[58] Oda A,Higuchi Y,Hisamatsu T. Photoperiod-insensitive floral transition in chrysanthemum induced by constitutive expression of chimeric repressor CsLHY-SRDX[J]. Plant Sci,2017,259:86−93. doi: 10.1016/j.plantsci.2017.03.007
[59] Oda A,Higuchi Y,Hisamatsu T. Constitutive expression of CsGI alters critical night length for flowering by changing the photo-sensitive phase of anti-florigen induction in chrysanthemum[J]. Plant Sci,2020,293:110417. doi: 10.1016/j.plantsci.2020.110417
[60] 赵航, 梁丽, 张淑欣. 温度调控植物开花的研究进展[J/OL]. 分子植物育种, 2022. https: //kns.cnki.net/kcms/detail/46.1068.S.20220420.1718.020.html. Zhao H, Liang L, Zhang SX. Research progress on temperature-regulated of plant flowering[J]. Molecular Plant Breeding, 2022. https: //kns.cnki.net/kcms/detail/46.1068.S.20220420.1718.020.html.
[61] Laurie DA. Comparative genetics of flowering time[J]. Plant Mol Biol,1997,35 (1-2):167−177.
[62] Trevaskis B,Hemming MN,Dennis ES,Peacock WJ. The molecular basis of vernalization-induced flowering in cereals[J]. Trends Plant Sci,2007,12 (8):352−357. doi: 10.1016/j.tplants.2007.06.010
[63] Bouché F,Woods DP,Amasino RM. Winter memory throughout the plant kingdom:different paths to flowering[J]. Plant Physiol,2017,173 (1):27−35. doi: 10.1104/pp.16.01322
[64] Kim DH,Sung S. Vernalization-triggered intragenic chromatin loop formation by long noncoding RNAs[J]. Dev Cell,2017,40 (3):302−312.e4. doi: 10.1016/j.devcel.2016.12.021
[65] Xu SJ,Xiao J,Yin F,Guo XY,Xing LJ,et al. The protein modifications of O-GlcNAcylation and phosphorylation mediate vernalization response for flowering in winter wheat[J]. Plant Physiol,2019,180 (3):1436−1449. doi: 10.1104/pp.19.00081
[66] Lutz U,Nussbaumer T,Spannagl M,Diener J,Mayer KF,Schwechheimer C. Natural haplotypes of FLM non-coding sequences fine-tune flowering time in ambient spring temperatures in Arabidopsis[J]. eLife,2017,6:e22114. doi: 10.7554/eLife.22114
[67] Kumar SV,Lucyshyn D,Jaeger KE,Alós E,Alvey E,et al. Transcription factor PIF4 controls the thermosensory activation of flowering[J]. Nature,2012,484 (7393):242−245. doi: 10.1038/nature10928
[68] Song YH,Ito S,Imaizumi T. Flowering time regulation:photoperiod- and temperature-sensing in leaves[J]. Trends Plant Sci,2013,18 (10):575−583. doi: 10.1016/j.tplants.2013.05.003
[69] Jin SY,Ahn JH. Regulation of flowering time by ambient temperature:repressing the repressors and activating the activators[J]. New Phytol,2021,230 (3):938−942. doi: 10.1111/nph.17217
[70] Posé D,Verhage L,Ott F,Yant L,Mathieu J,et al. Temperature-dependent regulation of flowering by antagonistic FLM variants[J]. Nature,2013,503 (7476):414−417. doi: 10.1038/nature12633
[71] Kim JJ,Lee JH,Kim W,Jung HS,Huijser P,Ahn JH. The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis[J]. Plant Physiol,2012,159 (1):461−478. doi: 10.1104/pp.111.192369
[72] Jung JH,Seo PJ,Ahn JH,Park CM. Arabidopsis RNA-binding protein FCA regulates MicroRNA172 processing in thermosensory flowering[J]. J Biol Chem,2012,287 (19):16007−16016. doi: 10.1074/jbc.M111.337485
[73] Kumar SV,Wigge PA. H2A. Z-containing nucleosomes mediate the thermosensory response in Arabidopsis[J]. Cell,2010,140 (1):136−147. doi: 10.1016/j.cell.2009.11.006
[74] Zheng SZ,Hu HM,Ren HM,Yang ZL,Qiu Q,et al. The Arabidopsis H3K27me3 demethylase JUMONJI 13 is a temperature and photoperiod dependent flowering repressor[J]. Nat Commun,2019,10 (1):1303. doi: 10.1038/s41467-019-09310-x
[75] Huang H,Nusinow DA. Into the evening:complex interactions in the Arabidopsis circadian clock[J]. Trends Genet,2016,32 (10):674−686. doi: 10.1016/j.tig.2016.08.002
[76] Ezer D,Jung JH,Lan H,Biswas S,Gregoire L,et al. The evening complex coordinates environmental and endogenous signals in Arabidopsis[J]. Nat Plants,2017,3 (7):17087. doi: 10.1038/nplants.2017.87
[77] Zhao H,Xu D,Tian T,Kong FY,Lin K,et al. Molecular and functional dissection of EARLY-FLOWERING 3 (ELF3) and ELF4 in Arabidopsis[J]. Plant Sci,2021,303:110786. doi: 10.1016/j.plantsci.2020.110786
[78] Cho AR,Kim YJ. Night temperature determines flowering time and quality of Chrysanthemum morifolium during a high day temperature[J]. J Hortic Sci Biotechnol,2021,96 (2):239−248. doi: 10.1080/14620316.2020.1834460
[79] Cockshull KE,Kofranek AM. High night temperatures delay flowering,produce abnormal flowers and retard stem growth of cut-flower chrysanthemums[J]. Sci Hortic,1994,56 (3):217−234. doi: 10.1016/0304-4238(94)90004-3
[80] Nakano Y,Higuchi Y,Sumitomo K,Oda A,Hisamatsu T,Naro N. Delay of flowering by high temperature in chrysanthemum:heat-sensitive time-of-day and heat effects on CsFTL3 and CsAFT gene expression[J]. J Hortic Sci Biotechnol,2015,90 (2):143−149. doi: 10.1080/14620316.2015.11513165
[81] Nakano Y,Takase T,Sumitomo K,Suzuki S,Tsuda-Kawamura K,Hisamatsu T. Delay of flowering at high temperature in chrysanthemum:duration of darkness and transitions in lighting determine daily peak heat sensitivity[J]. Hortic J,2020,89 (5):602−608. doi: 10.2503/hortj.UTD-192
[82] Luo C,Liu H,Ren JN,Chen DL,Cheng X,et al. Cold-inducible expression of an Arabidopsis thaliana AP2 transcription factor gene,AtCRAP2,promotes flowering under unsuitable low-temperatures in chrysanthemum[J]. Plant Physiol Biochem,2020,146:220−230. doi: 10.1016/j.plaphy.2019.11.022
[83] Lyu J,Aiwaili P,Gu ZY,Xu YJ,Zhang YH,et al. Chrysanthemum MAF2 regulates flowering by repressing gibberellin biosynthesis in response to low temperature[J]. Plant J,2022,112 (5):1159−1175. doi: 10.1111/tpj.16002
[84] Sumitomo K,Nakano Y,Hisamatsu T,Oda A,Narumi-Kawasaki T,et al. Delayed flowering due to ‘cold memory’ is regulated by suppression of FLOWERING LOCUS T-like 3 gene in chrysanthemums[J]. J Hortic Sci Biotechnol,2023,98 (3):334−341. doi: 10.1080/14620316.2022.2136112
[85] Zhang XY,Zhang P,Wang G,Bao ZL,Ma FF. Chrysanthemum lavandulifolium homolog ClMAD1 modulates the floral transition during temperature shift[J]. Environ Exp Bot,2022,194:104720. doi: 10.1016/j.envexpbot.2021.104720
[86] Sumitomo K,Li TP,Hisamatsu T. Gibberellin promotes flowering of chrysanthemum by upregulating CmFL,a chrysanthemum FLORICAULA/LEAFY homologous gene[J]. Plant Sci,2009,176 (5):643−649. doi: 10.1016/j.plantsci.2009.02.003
[87] Wilson RN,Heckman JW,Somerville CR. Gibberellin is required for flowering in Arabidopsis thaliana under short days[J]. Plant Physiol,1992,100 (1):403−408. doi: 10.1104/pp.100.1.403
[88] Murase K,Hirano Y,Sun TP,Hakoshima T. Gibberellin-induced DELLA recognition by the gibberellin receptor GID1[J]. Nature,2008,456 (7221):459−463. doi: 10.1038/nature07519
[89] Yan JD,Li XM,Zeng BJ,Zhong M,Yang JX,et al. FKF1 F‐box protein promotes flowering in part by negatively regulating DELLA protein stability under long‐day photoperiod in Arabidopsis[J]. J Integr Plant Biol,2020,62 (11):1717−1740. doi: 10.1111/jipb.12971
[90] Achard P,Herr A,Baulcombe DC,Harberd NP. Modulation of floral development by a gibberellin-regulated microRNA[J]. Development,2004,131 (14):3357−3365. doi: 10.1242/dev.01206
[91] Allen RS,Li JY,Stahle MI,Dubroué A,Gubler F,Millar AA. Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family[J]. Proc Natl Acad Sci USA,2007,104 (41):16371−16376. doi: 10.1073/pnas.0707653104
[92] Pharis RP. Flowering of Chrysanthemum under non-inductive long days by gibberellins and N6-benzyladenine[J]. Planta,1972,105 (3):205−212. doi: 10.1007/BF00385392
[93] Dong B,Deng Y,Wang HB,Gao R,Stephen GU,et al. Gibberellic acid signaling is required to induce flowering of chrysanthemums grown under both short and long days[J]. Int J Mol Sci,2017,18 (6):1259. doi: 10.3390/ijms18061259
[94] Yang YJ,Ma C,Xu YJ,Wei Q,Imtiaz M,et al. A zinc finger protein regulates flowering time and abiotic stress tolerance in chrysanthemum by modulating gibberellin biosynthesis[J]. Plant Cell,2014,26 (5):2038−2054. doi: 10.1105/tpc.114.124867
[95] Zhu L,Guan YX,Liu YN,Zhang ZH,Jaffar MA,et al. Regulation of flowering time in chrysanthemum by the R2R3 MYB transcription factor CmMYB2 is associated with changes in gibberellin metabolism[J]. Hortic Res,2020,7 (1):96. doi: 10.1038/s41438-020-0317-1
[96] Wu G,Park MY,Conway SR,Wang JW,Weigel D,Poethig RS. The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis[J]. Cell,2009,138 (4):750−759. doi: 10.1016/j.cell.2009.06.031
[97] Wang JW,Czech B,Weigel D. miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana[J]. Cell,2009,138 (4):738−749. doi: 10.1016/j.cell.2009.06.014
[98] Fornara F,Coupland G. Plant phase transitions make a SPLash[J]. Cell,2009,138 (4):625−627. doi: 10.1016/j.cell.2009.08.011
[99] Yang HC,Han ZF,Cao Y,Fan D,Li H,et al. A companion cell–dominant and developmentally regulated H3K4 demethylase controls flowering time in Arabidopsis via the repression of FLC expression[J]. PLoS Genet,2012,8 (4):e1002664. doi: 10.1371/journal.pgen.1002664
[100] Song AP,Gao TW,Wu D,Xin JJ,Chen SM,et al. Transcriptome-wide identification and expression analysis of chrysanthemum SBP-like transcription factors[J]. Plant Physiol Biochem,2016,102:10−16. doi: 10.1016/j.plaphy.2016.02.009
[101] 朱文静. 菊花转录因子CmSPL4. 1/5. 1/6/13的克隆与功能鉴定[D]. 南京: 南京农业大学, 2020: 1-10. [102] 魏倩. 菊花核因子NF-YB调节开花时间和干旱胁迫耐性的机理分析[D]. 北京: 中国农业大学, 2015: 1-10. [103] Wei Q,Ma C,Xu YJ,Wang TL,Chen YY,et al. Control of chrysanthemum flowering through integration with an aging pathway[J]. Nat Commun,2017,8 (1):829. doi: 10.1038/s41467-017-00812-0
[104] 马超. 菊花成花调控机制: 第三届全国植物开花·衰老与采后生物学大会论文摘要集[C]. 杭州: 中国植物生理与植物分子生物学学会, 2019. [105] Jiang JF, Zhang ZX, Hu Q, Zhu YQ, Gao Z, et al. The flowering repressor SVP recruits the TOPLESS co-repressor to control flowering in chrysanthemum and Arabidopsis[J/OL]. BioRxiv, 2021. doi: 10.1101/2021.11.23.469726.
[106] Wang CQ,Guthrie C,Sarmast MK,Dehesh K. BBX19 interacts with CONSTANS to repress FLOWERING LOCUS T transcription,defining a flowering time checkpoint in Arabidopsis[J]. Plant Cell,2014,26 (9):3589−3602. doi: 10.1105/tpc.114.130252
[107] Yuan L,Yu YJ,Liu MM,Song Y,Li HM,et al. BBX19 fine-tunes the circadian rhythm by interacting with PSEUDO-RESPONSE REGULATOR proteins to facilitate their repressive effect on morning-phased clock genes[J]. Plant Cell,2021,33 (8):2602−2617. doi: 10.1093/plcell/koab133
[108] Zhang T. Tick-tock:BBX19 functions as a novel regulator of the circadian clock[J]. Plant Cell,2021,33 (8):2511−2512. doi: 10.1093/plcell/koab142
[109] Wang LJ,Sun J,Ren LP,Zhou M,Han XY,et al. CmBBX8 accelerates flowering by targeting CmFTL1 directly in summer chrysanthemum[J]. Plant Biotechnol J,2020,18 (7):1562−1572. doi: 10.1111/pbi.13322
[110] Wang LJ,Cheng H,Wang Q,Si CN,Yang YM,et al. CmRCD1 represses flowering by directly interacting with CmBBX8 in summer chrysanthemum[J]. Hortic Res,2021,8:79. doi: 10.1038/s41438-021-00516-z
[111] Chen H,Huang F,Liu YN,Cheng PL,Guan ZY,et al. Constitutive expression of chrysanthemum CmBBX29 delays flowering time in transgenic Arabidopsis[J]. Can J Plant Sci,2020,100 (1):86−94. doi: 10.1139/cjps-2018-0154
[112] Ping Q,Cheng PL,Huang F,Ren LP,Cheng H,et al. The heterologous expression in Arabidopsis thaliana of a chrysanthemum gene encoding the BBX family transcription factor CmBBX13 delays flowering[J]. Plant Physiol Biochem,2019,144:480−487. doi: 10.1016/j.plaphy.2019.10.019
[113] Morita S,Murakoshi Y,Hojo A,Chisaka K,Harada T,Satoh S. Early flowering and increased expression of a FLOWERING LOCUS T-like gene in chrysanthemum transformed with a mutated ethylene receptor gene mDG-ERS1(etr1-4)[J]. J Plant Biol,2012,55 (5):398−405. doi: 10.1007/s12374-012-0109-8
[114] Huang YY,Xing XJ,Tang Y,Jin JY,Ding L,et al. An ethylene‐responsive transcription factor and a flowering locus KH domain homologue jointly modulate photoperiodic flowering in chrysanthemum[J]. Plant Cell Environ,2022,45 (5):1442−1456. doi: 10.1111/pce.14261
[115] Gomi K. Jasmonic acid:an essential plant hormone[J]. Int J Mol Sci,2020,21 (4):1261. doi: 10.3390/ijms21041261
[116] Guan YX,Ding L,Jiang JF,Shentu YY,Zhao WQ,et al. Overexpression of the CmJAZ1-like gene delays flowering in Chrysanthemum morifolium[J]. Hortic Res,2021,8:87. doi: 10.1038/s41438-021-00525-y
[117] Yuan S,Zhang ZW,Zheng C,Zhao ZY,Wang Y,et al. Arabidopsis cryptochrome 1 functions in nitrogen regulation of flowering[J]. Proc Natl Acad Sci USA,2016,113 (27):7661−7666. doi: 10.1073/pnas.1602004113
[118] Lin YL,Tsay YF. Influence of differing nitrate and nitrogen availability on flowering control in Arabidopsis[J]. J Exp Bot,2017,68 (10):2603−2609. doi: 10.1093/jxb/erx053
[119] Sanagi M,Aoyama S,Kubo A,Lu Y,Sato Y,et al. Low nitrogen conditions accelerate flowering by modulating the phosphorylation state of FLOWERING BHLH 4 in Arabidopsis[J]. Proc Natl Acad Sci USA,2021,118 (19):e2022942118. doi: 10.1073/pnas.2022942118
[120] Zhang SN,Zhang YY,Li KN,Yan M,Zhang JF,et al. Nitrogen mediates flowering time and nitrogen use efficiency via floral regulators in rice[J]. Curr Biol,2021,31 (4):671−683.e5. doi: 10.1016/j.cub.2020.10.095
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