Research progress on mechanisms of plant adaptation to flooding stress
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摘要:
涝渍胁迫是农业生产中的主要非生物逆境之一。涝渍胁迫包括渍害和涝害，通过低氧胁迫、离子毒害、能量短缺等方面抑制植物的生长发育。为了适应涝渍环境，植物在不同生态条件下形成了多样且复杂的响应和适应机制。本文综述了涝渍胁迫对植物的危害，植物适应涝渍胁迫的形态多样性与主要分子响应机制，讨论了提高植物耐涝渍性的遗传途径，以期为深入研究植物抗涝渍胁迫机制和培育抗涝渍作物提供理论指导。
Abstract:Flooding stress constitutes a major abiotic challenge in agricultural production. Flooding stress, including waterlogging and submergence, inhibits plant growth and development through hypoxia, ion toxicity, and energy deficits. As such, plants have evolved various adaptive responses and mechanisms to counter flooding stress under diverse ecological conditions. This review discusses the detrimental effects of flooding stress on plants, as well as the morphological diversity and molecular mechanisms associated with plant adaptation to flooding stress. The genetic strategies for improving plant resistance to flooding stress are also discussed. This review aims to provide guidance for future research into the mechanisms of plant resistance to flooding stress and flooding stress-resistant crop breeding.
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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]。
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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 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]。
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图 2 高等植物温度途径及菊花中响应温度变化的同源基因红线代表在菊花中涉及的研究。Figure 2. Temperature pathway of higher plants and temperature-responsive homologous genes in ChrysanthemumRed line represents research involving Chrysanthemums.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 植物响应和适应涝渍胁迫的调控网络
涝渍胁迫诱导植物体内产生乙烯、低氧、NO、能量短缺和ROS等信号，以帮助植物适应胁迫下的生长。不同背景颜色表示不同的信号响应通路。涝渍胁迫导致淹水组织迅速积累乙烯，乙烯积累导致乙烯受体和乙烯负调节器CRT1（Constitutive triple response 1）复合物失去对乙烯正调节器EIN2（Ethylene-insensitive 2）的抑制作用，从而诱导转录因子EIN3（Ethylene-insensitive 3）和EIL（EIN3-LIKE）的积累，进而促进下游靶基因的表达。涝渍引起缺氧状态导致有氧呼吸受到抑制，从而导致淹水组织能量供应不足。Ca2 + -CBL（Calcineurin B-like protein）-CIPK15（Calcineurin B-like protein-interacting protein kinase 15）-SnRK1（Suc-non-fermenting 1-related protein kinase 1）模块以及OsTPP7（Trehalose-6-phosphate phosphatase 7）等参与能量感知和低能源状态下糖类利用效率，增加在涝渍胁迫下的能量供应，从而促进植物在涝渍胁迫下的生长。同时，植物能感知缺氧信号，在生理和分子水平产生适应性响应。正常生长状态下，Ⅶ亚族乙烯响应因子（Ethylene response factor Ⅶ，ERF-Ⅶ）蛋白与ACBPs（Acyl-CoA-binding proteins）在质膜上紧密结合，涝渍胁迫发生时蛋白转移到细胞核中行使转录因子功能，促进下游靶基因的表达。同时，涝渍缺氧状态会抑制NERP（N-end rule pathway）蛋白降解反应，从而提高ERF-Ⅶs蛋白的稳定性，进一步促进其行使转录激活功能。拟南芥中MPK3/MPK6、SR1（Submergence resistant 1）、WRKY12、WRKY33参与到了ERF-Ⅶs对靶基因的转录激活过程中。低氧条件下，线粒体电子传递链上生成NO，通过对蛋白质翻译后修饰，例如调节ERF-Ⅶs的稳定性，参与涝渍胁迫响应。而拟南芥中ERF-Ⅶs能够诱导血红蛋白编码基因HB1（Hemoglobin 1）的表达，促进植物对胞内NO的清除，维持NO的稳态。低浓度的活性氧（ROS）作为信号分子参与胁迫响应，可以通过叶绿体和线粒体中的电子传递链以非酶促的方式产生或者通过RBOHs（Respiratory burst oxidase homolog proteins）以酶促的方式产生。植物体内通过ROS清除酶系统（超氧化物歧化酶（SOD）、抗坏血酸过氧化物酶（APX）、过氧化氢酶（CAT）、谷胱甘肽过氧化物酶（GSH-Px）等）和非酶抗氧化剂（抗坏血酸（AsA）、谷胱甘肽（GSH）、褪黑素（Meltonin）等）能对过多的ROS进行清除。多种调控机制构成复杂的调控网络，促进植物响应和适应涝渍胁迫。
Figure 1. Regulatory network of plant responses and adaptations to flooding stress
Flooding stress induces ethylene production, hypoxia, NO, energy shortage, and ROS in plants to promote growth under flooding stress. Different background colors indicate different signal response pathways. Flooding stress causes the rapid accumulation of ethylene in flooded tissues, resulting in ethylene receptor and ethylene negative regulator CRT1 (Ethylene insensitive 2) complexes to lose their inhibitory effects on ethylene positive regulator EIN2 (Ethylene insensitive 2). Accumulation of transcription factors EIN3 (Ethyleninsensitive 3) and EIL (EIN3-like) by EIN2 promotes the expression of downstream target genes. Hypoxic state of flooding suppresses aerobic respiration, leading to insufficient energy supply to flooded tissues. Ca2 + -CBL (Calcineurin B-like protein)-CIPK15 (Calcineurin B-like protein-interacting protein kinase 15)-SnRK1 (Suc-non-fermenting 1-related protein kinase 1) module and OsTPP7 (Trehalose-6-phosphate phosphatase 7) participate in energy perception and sugar utilization efficiency under low energy states and increase energy supply under flooding stress, thus promoting plant growth under flooding stress. At the same time, plants can sense hypoxic signals and produce adaptive responses at the physiological and molecular levels. Under normal growth conditions, the ethylene response factor Ⅶ (ERF-Ⅶ) protein closely binds to acyl-CoA-binding proteins (ACBPs) on the plasma membrane. Under flooding stress, ERF-Ⅶs are transferred to the nucleus to promote the expression of downstream target genes. At the same time, hypoxia inhibits NERP (N-end rule pathway) protein degradation, thereby improving ERF-Ⅶs protein stability and further promoting its transcriptional activation function. MPK3/MPK6, SR1 (Submergence resistant 1), WRKY12, and WRKY33 in Arabidopsis thaliana are involved in the transcriptional activation of target genes by ERF-Ⅶs. Under hypoxic conditions, NO is produced on the electron transport chain of mitochondria and is involved in the flooding stress response through post-translational modifications to proteins, such as regulating ERF-Ⅶs stability. ERF-Ⅶs can induce hemoglobin coding gene HB1 (Hemoglobin 1) expression, promote intracellular NO clearance, and maintain NO homeostasis in A. thaliana. Low-concentration ROS participate in the stress response as signaling molecules, produced in a non-enzymatic manner via electron transport chain in chloroplasts and mitochondria or enzymatically via respiratory burst homolog proteins (RBOHs). In plants, excessive ROS can be removed by excessive oxygen removal enzymes (superoxide dismutase (SOD), ascorbate peroxidase (APX), catalase (CAT), and glutathione peroxidase (GSH-PX)) and non-enzymatic antioxidants (ascorbate (AsA), glutathione (GSH), and melatonin (Melatonin)). These various regulatory mechanisms constitute a complex regulatory network that promotes plant response and adaptation to flooding stress.
表 1 已验证的植物响应和适应涝渍胁迫的基因
Table 1 Verified genes involved in response and adaptation to flooding stress in plants
基因
Gene物种
Species植株生长适应性表型
Growth adaptive phenotype参考文献
ReferenceSUB1 水稻 Oryza sativa 株高 [37] SK1、SK2 水稻 总节间伸长长度 [38] SnRK1、CIPK15 水稻 株高 [73] OsTPP7 水稻 胚芽鞘长度 [39] LGF1 水稻 最小气室厚度/水下净光合作用 [44] SD1（OsGA20ox2） 水稻 总节间长度 [90] OsCBL10 水稻 胚芽鞘长度 [40] OsGF14h、OsVP1；OsHOX3、OsGA20ox1 水稻 存活率/胚芽鞘长度 [41] OsUGT75A、OsJAZ6；OsJAZ7、OsABI3 水稻 胚芽鞘长度 [42] LSD1、EDS1、PAD4 拟南芥 Arabidopsis thaliana 通气组织形成 [24] RAP2.2 拟南芥 存活率/鲜重 [91] HRE1、HRE2、PRT6；ATE1、ATE2 拟南芥 存活指数/萌发率 [57] RAP2.12 拟南芥 存活率/干重 [58] ACBP3 拟南芥 存活率/干重 [92] GDH2 拟南芥 存活率/损伤指数 [93] SnRK1 拟南芥 坏死叶面积百分比 [87] MYC2、LOX2-S、AOS；JAR1、COI1、VTC1、GSH1 拟南芥 存活率/干重 [79] eIFiso4G1、SnRK1 拟南芥 存活率 [76] RBOHD、ORE1、SAG113 拟南芥 新叶形成速度/失水率/叶绿素含量 [85] ACBP1、ACBP2、LACS2、FAD3 拟南芥 存活率/叶绿素含量 [94] SR1、WRKY33 拟南芥 存活率/干重 [62] WRKY12 拟南芥 存活率/干重 [61] TaERFⅦ.1 小麦 Triticum aestivum 存活率/叶绿素含量/粒重 [59] EREB180 玉米 Zea mays 茎鲜重/根长/不定根数 [60] CmERF5、CmRAP2.3 菊 Chrysanthemum morifolium 叶片黄化率/恢复率 [82] 
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