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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全球气候变化使得涝渍胁迫的发生变得更加频繁和不可预测。陆生植物普遍对涝渍比较敏感，涝渍胁迫会造成植物生物多样性的下降以及作物的产量损失等。植物生长环境中过多的水取代了植物根系和地上环境中的气体空间，这种状态称之为涝渍（Flooding）。土壤中水分取代气体空间而限制植物气体交换的状态称之为渍水（Waterlogging），而植株的部分或者全部地上组织被水淹没的状态称之为淹水（Submergence）[1, 2]。渍水时，植物根系的生长和功能受到直接影响；而淹水时，植株地上部分的光合和呼吸等功能也受到抑制。造成涝渍胁迫的原因主要包括短时间内的极端降水、排水不畅以及土壤结构粘重等因素[3]。涝渍胁迫影响到全球大约10%耕地的作物生产，对成熟期种子产量能造成15% ~ 80%的损失[2]。因此，分析涝渍胁迫对植物生长发育的危害，解析植物响应和适应涝渍胁迫的生理变化和分子机制，将为提高植物的耐涝渍性提供理论依据，对作物的耐涝渍性遗传改良具有重要的指导意义。
1. 涝渍胁迫对植物的危害
1.1 涝渍胁迫对生理代谢的影响
涝渍胁迫发生时，淹水组织与环境中的气体交换受阻，淹水环境中的O2被植物和微生物迅速消耗后，微生物在缺氧条件下利用硝酸盐、锰的氧化物、铁的硫酸盐等物质作为呼吸作用中的替代电子受体，从而导致淹水环境中可溶性Mn2 + 和Fe2 + 以及H2S等植物毒素大量积累[4, 5]。同时，淹水环境中根际Fe2 + 积累以及硝态氮（NO3−）被还原为氨态氮（NH4 + ）等情况，使得根际土壤微环境的pH值显著下降，导致植物阴阳离子摄入失衡，从而影响根系的生理功能[5, 6]。此外，pH值下降导致酚类脂肪酸和挥发性脂肪酸由解离状态转变为非解离状态，进一步对植物产生毒害[7, 8]。植物在淹水缺氧状态下，糖酵解和乙醇发酵代替了线粒体介导的氧化磷酸化的高产能方式[9]。淹水组织中的发酵供能方式，导致根中能源物质被迅速消耗，并产生乙醛等有毒物质，从而导致根系能量状态、细胞结构和功能均受到影响[10]。另外，水通道蛋白受涝渍缺氧的影响，对水分的吸收与运输功能也受到抑制[11]。
1.2 涝渍胁迫对形态和生长发育的影响
长时间淹水不仅会严重抑制根系功能并导致根系孔隙度增加、生根率下降以及根系腐烂等情况发生，地下部分对水分和营养元素吸收等功能受损还间接地导致了地上部分功能的改变，包括气孔关闭、叶绿素降解、细胞结构损伤等，从而抑制了叶片的气体交换和光合效率，严重降低了植株能源物质的供应[12, 13]。光合组织中高O2含量和低CO2含量的状态，促进植株增强光呼吸作用对能源物质的消耗，进一步阻碍了光合同化产物的积累[12, 14]。涝渍胁迫持续的时间越长，植物受到的影响越严重，持续的涝渍胁迫会导致萌发率降低、株高降低、根系受损、叶片生长减慢、植株早衰、开花提前等，最终会导致成熟期的产量损失甚至植株死亡[2, 15, 16]。由此可见，涝渍胁迫会造成植株遭受低氧、离子毒害、能量短缺等情况，从多个方面影响植物的生长发育。
2. 植物适应涝渍胁迫的形态多样性
2.1 通气组织
根和茎中气体的低阻力导管称之为通气组织，能促进根尖与植株非淹没区之间的气体交换[17]。孔隙度高的根系，保证了根尖足够的O2含量，能促进根系向离茎基部更远的地方生长[18]。湿地和水生植物普遍能够形成初级通气组织，初级通气组织主要包括溶生型和裂生型两种[19]。根系皮层细胞或茎的薄壁细胞死亡并溶解形成溶生型通气组织，根系皮层细胞分化和/或扩张促进相邻细胞簇分离而形成裂生型通气组织[19, 20]。此外，植物中还存在膨胀型通气组织，主要通过细胞的分裂和增大发育而成[21]。同时，多种植物经涝渍胁迫诱导后可以形成通气程度更高的次级通气组织，而次级通气组织通过供氧量增加、耗氧细胞数量减少双重方式改善根尖供氧状态。水稻（Oryza sativa L.）、大麦（Hordeum vulgare L.）等植物受涝渍胁迫诱导形成溶生型的次级通气组织[22, 23]；在大豆（Glycine max (L.) Merr.）和拟南芥（Arabidopsis thaliana (L.) Heynh.）中，则形成裂生型的次级通气组织[24, 25]。因此，初级和次级通气组织均能够改善根系中氧的平衡状态[26]。
2.2 不定根
植株根系受损严重时，涝渍胁迫还能诱导不定根通过分生组织从头诱导或者根原基产生。新生的不定根更接近空气环境，能缩短对根尖的供氧距离，替代原有根系受损的水分、养分吸收功能，还能对植株产生支撑作用[25]。在水稻基部茎节上，通过乙烯和活性氧（Reactive oxygen species，ROS）协同作用，能诱导根原基形成不定根[27]。在沼生酸模（Rumex palustris Sm.）和番茄（Solanum lycopersicum L.）中，乙烯与生长素协同作用，通过分生组织诱导不定根的形成[28, 29]。
2.3 径向氧扩散屏障
根系中的O2一部分被根细胞消耗，另一部分直接被扩散到土壤中而损失。因此，植物在适应涝渍环境时，还能形成根系的径向氧扩散（Radial oxygen loss，ROL）屏障结构，减少根系O2向土壤环境的扩散，加大了O2径向扩散的物理阻力，延长了O2扩散到根尖的强度和深度[30, 31]。根系形成ROL屏障后，导致扩散到根系内皮层和外皮层的O2含量减少，表明其对根系中O2的损失具有强大的抑制作用[32]。此外，ROL屏障在不妨碍营养物质吸收的情况下，还可以减少对植物毒素（如Fe2 + ）的吸收，从而维持根系的生理功能[33, 34]。同时，研究表明，ROL屏障在较长的根系中更容易诱导产生，而提前在有氧环境中适应过的根系，在逆境下能迅速诱导ROL屏障的产生[35]。细胞壁中的木栓质和木质素被认为参与到了ROL屏障的形成过程中[18]，研究表明，水稻中调控木栓质生物合成的基因受涝渍胁迫上调表达，而木质素生物合成基因的表达则不受影响[36]。
2.4 其他适应性形态
此外，淹水胁迫发生时，植株地上组织还能产生其他的形态学适应性变化。淹水条件下，水稻会出现茎秆节间迅速伸长逃离胁迫（逃逸策略）或者植株停止生长保存能量（静止策略）的两种不同响应策略[37, 38]。水稻在淹水条件下萌发时，能通过促进胚芽鞘的生长，使萌发种子迅速脱离胁迫环境[39-42]。此外，水稻叶片蜡质能促进叶表面与水面之间形成气室（Gas film）微环境，在叶片和气室之间能进行一定水平的气体交换，维持叶片在淹水环境中的光合作用和有氧呼吸[43, 44]。拟南芥和沼生酸模中，涝渍胁迫诱导叶柄伸长，同时叶片出现偏下性生长情况，使植株生长挺拔，从而促进植株逃离胁迫环境[45-47]。涝渍发生时，不同植物会选择不同的形态适应策略来应对胁迫，而植物应对不同程度的胁迫采取的响应和适应的策略也不尽相同。
3. 植物响应和适应涝渍胁迫的生理变化和分子机制
3.1 乙烯的响应与信号转导
在淹水条件下，乙烯大量积累，不易受其他环境因素的影响，因此是植物响应涝渍胁迫的关键因子。在正常条件下，气态的乙烯在植物体内产生后会迅速扩散到环境中，从而保证体内低水平状态；而乙烯在水中低溶解度的特性，导致当涝渍胁迫发生时，内源乙烯难以排除体外而积累，在1 h内迅速达到生理饱和状态[48]。在涝渍低氧条件下，乙烯合成通路被激活，从而促进乙烯的主动积累[49-51]。乙烯的生物合成始于甲硫氨酸在S-腺苷甲硫氨酸合成酶（S-adenosylmethionine synthase，SAMS）催化下合成S-腺苷甲硫氨酸（S-adenosylmethionine，SAM），随后1-氨基环丙烷-1-羧酸合酶（1-aminocyclopropane-1-carboxylate synthase，ACS）继续催化SAM生产1-氨基环丙烷-1-羧酸（1-aminocyclopropane-1-carboxylate，ACC），然后ACC氧化酶（ACC oxidase，ACO）在氧的参与下将ACC氧化为乙烯。
此外，低氧或淹水会诱导乙烯受体基因的表达[23]。在拟南芥中，内质网膜和高尔基体膜上的5个受体家族蛋白能感知乙烯信号的变化[52]。拟南芥乙烯信号转导的主要过程如下：在乙烯缺乏的情况下，乙烯受体与下游的乙烯负调节器CTR1（Constitutive triple response 1）互作，抑制信号的传递；体内乙烯积累后，大量乙烯在铜辅因子参与下与受体蛋白结合，导致CTR1与受体复合体的构象发生改变，从而使下游的EIN2（Ethylene-insensitive 2）能够与复合体的激酶结构域互作，诱导编码转录因子EIN3（Ethylene-insensitive 3）和EIL（EIN3-LIKE）的基因表达；EIN3和EIL（EIN3-LIKE）随后促进下游另一类转录因子—乙烯响应因子（Ethylene response factor，ERF）的积累，从而进一步激活下游靶基因表达，以促进植株对胁迫的响应和适应[52, 53]。乙烯在淹水后迅速积累，且不易受其他环境条件影响，使得乙烯成为响应淹水胁迫可靠和及时的信号分子。
3.2 O2的响应和信号转导
在淹水条件下，水分阻隔了根系与土壤孔隙之间的气体交换，加之微生物和植物根系活动导致的O2消耗，导致植株迅速进入缺氧状态[54, 55]。同时，根系的圆柱形结构限制其与根围环境的气体交换速度，因此导致根系活动容易受缺氧的影响[48]。另外，淹水组织的孔隙度、形态结构和气体扩散距离都极大地影响了根系供氧状态[30]。拟南芥淹水时，根系在15 min内迅速进入缺氧状态，而水稻由于通气组织发达，根系在淹水环境中依然能够正常生长[9]。
根系的呼吸作用和微生物活动会引起局部CO2浓度的升高，导致胞内pH值和关键酶的活性发生变化，从而调控根系响应低O2信号[56]。同时，在拟南芥中解析了直接感应O2的机制，该通路主要通过NERP（N-end rule pathway）蛋白降解途径调控乙烯响应因子Ⅶ亚族（Ethylene response factor Ⅶ，ERF-Ⅶ）蛋白的稳定性来感知胞内氧含量的变化[45]。在正常氧含量条件下，ERF-Ⅶ转录因子被NERP途径降解或者在质膜上与酰基辅酶A结合蛋白（Acyl-CoA-binding proteins，ACBPs）结合而不能入核行使功能；而在低氧条件下，NEPR蛋白降解通路对ERF-Ⅶ转录因子的降解作用被抑制，ERF-Ⅶ转录因子被从膜上释放出来，随后进入细胞核触发下游靶基因的起始转录，介导了植物对低氧的响应[57, 58]。拟南芥中有5个ERF-Ⅶs，分别为HRE1（Hypoxia responsive 1）、HRE2（Hypoxia responsive 2）、RAP2.2（Related to AP2 2）、RAP2.3（Related to AP2 3）和RAP2.12（Related to AP2 12），从水稻中克隆的淹水响应相关基因SUB1s（submergence1s）和SKs（snorkels）编码的也属于ERF-Ⅶ转录因子[37, 38, 57, 58]。研究表明，小麦（Triticum aestivum L.）和玉米（Zea mays L.）中的ERF-Ⅶ也参与了O2感应[59, 60]。在拟南芥的研究中发现，WRKY33和WRKY12在该信号途径中能协同作用以转录激活RAP2.2，而RAP2.2在胁迫后中能够对WRKY33进行反馈调控[61]。E3泛素连接酶SR1（Submergence resistant 1）介导的蛋白降解在正常情况下能部分降解WRKY33，而在低氧状态下WRKY33被MPK3/MPK6（Mitogen-activated protein kinase 3/ mitogen-activated protein kinase 6）磷酸化后能够诱导RAP2.2的表达，在复氧后磷酸化的WRKY33则被SR1迅速且彻底地降解[62]。另外，有研究发现，乙烯、赤霉素（Gibberellic acid，GA）、活性氧等信号也参与到ERF-Ⅶ介导的响应中[38, 63, 64]。以上研究结果表明，淹水引起的缺氧会对被淹没的组织造成严重的能量和碳水化合物短缺，ERF-Ⅶ作为信号分子诱导植株在生理和分子水平上的适应。
3.3 一氧化氮（NO）的响应和循环
NO是植物响应环境刺激的高活性信号分子，多种逆境均能诱导内源NO含量迅速且大范围的变化[65, 66]。研究表明，低氧胁迫时，在根系过渡区产生大量的NO，促进根系适应低氧环境[67]。通过化学方法阻断NO在缺氧下的合成后，严重抑制了根尖的存活率，说明NO在维持缺氧条件下根尖的正常生长中起作用[67, 68]。此外，NO与乙烯协同作用，诱导拟南芥在涝渍胁迫下的叶片偏下性生长[46]。
植物淹水缺氧时，硝酸还原酶（Nitrate reductase，NR）的磷酸化水平下降导致其催化活性增强，促进植物体内亚硝酸盐的积累，从而致使根系过渡区和分生区NO爆发[67]。在植物线粒体电子传递链上，NR催化NO3−还原成NO2−，随后与NR互作的蛋白ARC（Amidoxime reducing component）进一步将NO2−催化成NO[3]。高浓度的NO对植物具有毒害作用，因此在NO信号转导结束后，植物大量诱导血红蛋白（Hemoglobin，Hb）进行解毒[69]。Hb通过消耗NAD(P)H的催化反应将NO氧化为NO3−，NO3−在胞质中再次被NR催化生成NO2−，生成的NO2−再次在线粒体电子传递链上还原成NO，在植物体内形成NO3−-NO的循环[23, 69, 70]。缺氧诱导生成的NO导致线粒体上产生ROS，同时还促进Ca2 + 的释放，从而进行信号转导[23]。另外，NO还可以通过对蛋白质翻译后的修饰，例如调节ERF-Ⅶ的稳定性，参与到响应涝渍胁迫的信号转导中，而ERF-Ⅶ则能够诱导血红蛋白编码基因HB1（hemoglobin 1）的表达，从而促进植物对胞内NO的清除[48]。因此，尽管对NO响应涝渍胁迫的动态过程的解析还不够深入，但已有的研究表明NO响应和循环是植株在涝渍缺氧条件下保持能量状态和适应的关键策略。
3.4 能量代谢方式的转变与调控
涝渍条件下的缺氧状态导致淹水组织由氧化磷酸化的高产能方式转变为糖酵解和发酵的低产能方式[56]。涝渍低氧状态下，线粒体电子传递链中最终电子受体O2的可用性降低，迅速降低了细胞的ATP/ADP比值，此时细胞激活糖酵解和发酵途径以维持ATP的合成以及再生NAD + 来保证胁迫下部分的能量供应[23]。然而，糖酵解途径中，1 mol的己糖分解仅能生成2 mol的ATP，长时间的涝渍胁迫下植株依然会有能量危机的风险。为应对长期的涝渍胁迫，植物还会诱导淀粉酶将淀粉分解为葡萄糖，促进能源物质的动员[71]。另一方面，糖酵解中蔗糖的利用方式发生了转变，植株加强双向的UDP依赖的蔗糖合酶（Bidirectional UDP-dependent sucrose synthase，SUS）途径，抑制单向的蔗糖转化酶（Unidirectional invertase，INV）途径[23]。在缺氧条件下，SUS途径比INV途径能量转化效率更高，INV途径相关基因的表达受到抑制，而SUS途径的基因被激活表达[23, 72]。在缺氧条件下，糖酵解的代谢终产物丙酮酸通过丙酮酸脱羧酶（Pyruvate decarboxylase，PDC）转化成乙醛，而乙醛被乙醇脱氢酶（Alcohol dehydrogenase，ADH）分解成乙醇并生成NAD + ，再次为糖酵解提供底物[9, 71]。
碳水化合物含量和ATP供应的减少会促发植株对能源物质的调动，大量研究表明淹水胁迫下主要通过SnRK1（Suc-nonfermenting1-related protein kinase 1）为核心模块介导的能源物质动员途径，感知能量短缺信号，增加植物在涝渍胁迫下的能量供应[73-75]。在能源物质短缺时，SnRK1一方面促进能源物质分解代谢以维持低氧环境的能源供应，另一方面抑制雷帕霉素靶蛋白（Target of rapamycin，TOR）激酶信号转导，从而防止植物过度生长导致的能源消耗[45]。拟南芥中，SnRK1提高了碳饥饿中的碳源利用效率，促进碳水化合物和氨基酸分解代谢、加速老叶衰老[75]，SnRK1磷酸化翻译起始因子eIFiso4Gs，促进靶基因的表达，从而提高植株对淹水胁迫的耐受性[76]。水稻厌氧萌发时，OsTPP7（Trehalose-6-phosphate phosphatase 7）作为能量感知的核心原件，通过6-磷酸海藻糖代谢感知能量短缺信号和调控糖类利用效率，从而促进水稻在无氧环境中的胚芽鞘伸长[39]。水稻种子中，CIPK15（Calcineurin B-like protein-interacting protein kinase 15）能促进SnRK1的表达，加快淀粉的分解供能速度，从而促进胚芽鞘的伸长生长[73]，而6-磷酸葡萄糖和/或6-磷酸海藻糖则负调控SnRK1信号介导的能源物质动员[74]。耐淹水稻萌发时，Ca2 + 结合蛋白OsCBL10（Calcineurin B-like protein 10）间接促进CIPK15蛋白的积累，增加淀粉酶活性，从而维持胚芽鞘生长以应对淹水环境[40]。以上研究结果表明，植物对糖类物质和能量信号感知的调节是响应涝渍胁迫的重要组成部分。
3.5 活性氧（ROS）的生成与清除
ROS是O2在各种代谢途径中还原而形成的一系列高活性氧化物的总称，包括超氧阴离子、单线氧、过氧化氢和羟基自由基，主要通过非酶促和酶促的方式产生[48]。非酶促方式主要发生在线粒体和叶绿体的电子传递链上，O2接收电子后，被部分还原形成超氧化物及其他活性更强的ROS[77]。而在过氧化物酶体、细胞壁、质膜和外质体等细胞器和细胞组分中可以通过酶促方式生成ROS[78]。在淹水缺氧的条件下，以及淹水结束后的复氧阶段，均会导致大量ROS的积累[48, 79]。
低浓度的ROS能作为信号分子参与胁迫响应，但过多的ROS不能及时清除将会破坏生物膜并导致生理生化代谢过程紊乱，最终引起根系腐烂和叶片萎蔫等植株损伤[80]。ROS清除酶系统包括超氧化物歧化酶（Superoxide dismutase，SOD）、抗坏血酸过氧化物酶（Ascorbate peroxidase，APX）、过氧化氢酶（Catalase，CAT）、谷胱甘肽过氧化物酶（Glutathione peroxidase，GPX）等，是ROS清除的主要途径[81]。在渍水条件下，柑橘（Citrus reticulata Blanco）和菊花（Chrysanthemum morifolium Ramat.）叶片中的SOD、APX和CAT活性均高于对照水平[80, 82]。此外，植株可以通过抗坏血酸（Ascorbate，AsA）和谷胱甘肽（Glutathione，GSH）循环，以非酶促方式进行ROS清除[83]。在淹水后的复氧阶段，水稻幼苗中的AsA和GSH含量会迅速上升[84]。拟南芥在淹水5 d时的AsA含量比处理前显著上升，而AsA和GSH含量在复氧阶段均显著高于对照组[85]。研究发现，拟南芥叶片中内源茉莉酸类似物（Jasmonates，JAs）含量在复氧阶段迅速升高，诱导了转录因子MYC2的积累，随后MYC2激活VTCs（Vitamin C defectives）和GSHs（Glutathione synthetases）的表达，合成AsA和GSH，从而参与到AsA-GSH循环介导的ROS清除过程中，最终提高植物在复氧阶段的耐受性[79]。此外，其他小分子抗氧化剂也能参与植物体内ROS的清除，例如褪黑素就能够清除各种ROS。在苹果（Malus pumila Mill.）中，外施褪黑素降低了ROS对植物的生理损害，从而提高了其耐渍性[86]。可见，ROS的生成与清除受到严格调控，对响应和适应涝渍胁迫至关重要。
3.6 不同响应通路之间的信号交叉
植物为了应对涝渍胁迫带来的生理改变，一方面通过改变代谢方式来维持部分能量供应，调整内部生理状态，以适应涝渍低氧环境；另一方面诱导植株形成适应性形态变化，以逃离胁迫环境。在适应涝渍胁迫的过程中，植物产生了多种响应与适应机制，不同的响应通路之间存在繁复的信号交叉，从而协同调控植物对涝渍胁迫的响应（图1）。
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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 stressFlooding 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.涝渍胁迫发生时，植物淹水组织中O2的迅速消耗是最直接、最重要的变化。O2的缺乏导致植株能量代谢方式由有氧呼吸高效供能转变为糖酵解和发酵的低效供能，同时植物体内和环境中产生大量的有毒物质，这种变化导致了植株遭受能量短缺和生理毒害等情况[3, 58]。在适应缺氧导致的能量供应不足中，植株一方面主要通过依赖于SnRK1的响应通路来动员能源物质、提高糖类物质的可用性，从而维持植株在涝渍胁迫下的生长，增加植物对涝渍胁迫的耐受性[39, 73]；另一方面，提高光合同化效率以提供涝渍胁迫下生长所需的能源物质，例如，水稻LGF1促进叶片合成表面蜡质，促进水稻在淹水时形成气室微环境来部分维持水下的光合同化作用，提高植物涝渍胁迫下的存活率[44]；另外，转录因子ERF-Ⅶ还能调控靶基因的表达来改变糖酵解和发酵的效率，从而提高涝渍胁迫下的能量利用效率[48]。
生理适应过程中，缺氧会抑制NERP蛋白降解过程，提高胞内ERF-Ⅶ蛋白的稳定性，从而感知和适应低氧胁迫[3]。缺氧时，线粒体电子传递链上生成的亚硝酸盐会造成NO爆发，通过对蛋白质翻译后修饰，例如调节ERF-Ⅶ的稳定性，参与涝渍响应[23, 48]。此外，乙烯、GA、ROS等信号也参与ERF-Ⅶs介导的响应通路中，最终导致茎或叶柄伸长、叶片衰老[38, 63, 64]。同时，涝渍胁迫下，在线粒体和叶绿体中产生的ROS，能作为信号分子参与响应涝渍胁迫信号转导，然而过多的ROS会造成生物膜的氧化损伤，并导致代谢过程紊乱[80]。植株过高的ROS水平可以通过抗氧化酶、抗氧化小分子以及乙烯响应基因来清除[82]。
生长适应中，乙烯与其他信号协同作用共同调控多种形态适应性的形成，提高淹水组织O2的可用性，从而提高对涝渍胁迫的抗性[87]。例如，乙烯和NO共同参与拟南芥叶片偏下性生长的调控[46]；乙烯和ROS共同介导拟南芥溶生型通气组织的形成[24]；乙烯响应通路中的CsEIN3间接诱导ROS信号的产生，从而促进黄瓜（Cucumis sativus L.）渍害下的不定根形成[88]；水稻淹水组织中，乙烯调控根原基机械信号的产生，而ROS诱导表皮细胞程序性死亡，二者协同作用，共同调控不定根的形成[27]。不同物种对涝渍胁迫的形态适应性各不相同，其具体的形成机制还有待进一步解析。
4. 植物提高耐涝渍性的遗传途径
植物对涝渍胁迫的耐受性和形态学适应性的形成归根结底受基因的调控[89]。因此，与涝渍胁迫相关的遗传位点和基因是改良作物耐涝渍性的重要遗传资源（表1）。渍水能诱导大麦野生种形成发达的通气组织，通过渍水敏感的普通大麦‘Franklin’与耐渍的野生大麦‘TAM407227’构建的定位群体，在4H染色体定位到一个调控通气组织形成的主效数量性状位点（Quantitative trait locus，QTL），该位点的导入提高了栽培大麦的耐渍性[22]。黄瓜属于不耐渍物种，耐渍品系‘Zaoer-N’来源的基因CsARN6.1能促进根系形成不定根，将该基因导入普通黄瓜品种中能显著提高其耐渍性[88]。在缺氧状态下能诱导产生紧密的ROL屏障是玉米近缘种尼加拉瓜大刍草（Zea nicaraguensis Iltis & B. F. Benz）具有强耐渍性的重要因素，通过远缘杂交将尼加拉瓜大刍草染色体片段在玉米中形成渗入系（ILs），能诱导玉米在渍害下形成ROL屏障[31]。此外，通过基因渗入，将深水稻品种‘C9285’来源的水稻绿色革命基因SD1导入普通水稻品种‘T56’（‘台中56’）背景中，提高了‘T56’在淹水胁迫下节间伸长的能力[90]。在研究水稻苗期对淹水胁迫的反应中发现，地方品种‘FR13’A在淹水胁迫下能抑制地上部分的生长，促进植株耐受2周的淹水胁迫，在胁迫结束后迅速恢复生长[37]，该品种来源的SUB1A基因对其耐淹性的形成起决定作用，通过标记辅助回交将该基因渗入粳稻和籼稻，显著提高了其耐淹性，目前已经育成多个品种在南亚和东南亚洪水易发区进行推广种植[89]。
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] 此外，其他涝渍胁迫相关基因在作物抗涝渍胁迫的遗传改良中也具有很大的应用潜力。在淹水情况下，过表达LGF1基因能促进叶片表皮蜡质的合成，使水稻叶片与水面之间形成气室，形成微环境下的气体交换，从而提高水稻的耐淹性[44]。而水稻淹水萌发中，幼苗胚芽鞘的迅速生长能促进植株逃离胁迫环境得以存活，过表达CIPK15、SnRK1、OsTPP7、OsGF14h等基因，能提高低能源状态下糖类利用效率或者平衡激素响应，从而促进水稻淹水萌发中的胚芽鞘的生长[39, 41, 73]。小麦中，耐渍材料中编码ERF-Ⅶ转录因子的基因TaERFⅦ.1，受渍水诱导上调表达，过表达该基因提高了小麦的苗期存活率和成熟期产量[60]。玉米中，EREB180基因编码一个ERF-Ⅶ转录因子，过表达该基因显著提高了玉米长期渍水下的存活率[60]。菊中过表达CmERF5与CmRAP2.3均能抑制植株ROS水平，从而提高其耐渍性[82]。此外，从模式植物拟南芥中鉴定到的相关基因，也可以为作物耐涝渍性的遗传改良提供遗传信息。
5. 展望
涝渍胁迫是植物生长和农业生产中最重要的非生物逆境之一。涝渍胁迫发生时，植物进化出了复杂多样的调控机制，从分子响应到形态适应等多层面应对不利环境。国内外学者从涝渍胁迫对植物的生长影响、植物适应涝渍胁迫的形态多样性、植株对胁迫的生理和分子响应、重要QTL定位和基因的克隆与利用等多个角度进行了比较深入和全面的研究。在农业生产中，大面积种植的农作物普遍适应了比较温和的土壤环境，对涝渍胁迫的耐受性较弱，在特定环境中生长的品种、野生种和近缘种中存在大量优异的耐渍种质可以进行利用。此外，解析不同物种、不同生态条件下的涝渍胁迫调控机制，可以针对性地为不同作物进行耐渍性遗传改良提供理论依据。
然而，涝渍胁迫作为包含低氧、离子毒害、能量短缺等应激响应的复合型非生物逆境，存在复杂的信号交叉和物种特异性，调控机制的研究中还有许多问题亟待解决。植物涝渍胁迫遗传基础和分子机制解析中，有待解决的重要问题包括：（1）植物如何分辨短期和长期涝渍胁迫，在分子和生理水平应对两种类型的涝渍胁迫有何差异；（2）自然界中，涝渍胁迫常与弱光胁迫、盐胁迫、温度胁迫等并发，植物如何响应和耐受并发的多种胁迫；（3）植物如何通过核心转录因子ERF-Ⅶ的激活和终止对涝渍胁迫进行时空特异性的精准调控；（4）涝渍胁迫如何对植物花期提前和早衰进行调控；（5）不同激素如何协调植物在涝渍胁迫下的生长和适应性；（6）植物在不同发育阶段对涝渍胁迫的响应中，有哪些共通和特异的遗传基础和分子机制。相信随着相关研究深度和广度的加大，将为我们呈现出更完整和清晰的植物涝渍调控网络，更好地为认识植物与环境互作和培育抗涝渍作物提供理论指导。
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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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[1] Sasidharan R,Bailey-Serres J,Ashikari M,Atwell BJ,Colmer TD,et al. Community recommendations on terminology and procedures used in flooding and low oxygen stress research[J]. New Phytol,2017,214 (4):1403−1407. doi: 10.1111/nph.14519
[2] Setter TL,Waters I. Review of prospects for germplasm improvement for waterlogging tolerance in wheat,barley and oats[J]. Plant Soil,2003,253 (1):1−34. doi: 10.1023/A:1024573305997
[3] Fukao T,Barrera-Figueroa BE,Juntawong P,Peña-Castro JM. Submergence and waterlogging stress in plants:a review highlighting research opportunities and understudied aspects[J]. Front Plant Sci,2019,10:340. doi: 10.3389/fpls.2019.00340
[4] Marschner H. Mechanisms of adaptation of plants to acid soils[J]. Plant Soil,1991,134 (1):1−20. doi: 10.1007/BF00010712
[5] Kirk G. The Biogeochemistry of Submerged Soils[M]. Chichester: Wiley, 2004: 17-44.
[6] Shabala S. Physiological and cellular aspects of phytotoxicity tolerance in plants:The role of membrane transporters and implications for crop breeding for waterlogging tolerance[J]. New Phytol,2011,190 (2):289−298. doi: 10.1111/j.1469-8137.2010.03575.x
[7] Drew MC,Lynch JM. Soil anaerobiosis,microorganism,and root function[J]. Ann Rev Phytopathol,1980,18:37−66. doi: 10.1146/annurev.py.18.090180.000345
[8] Armstrong J,Armstrong W. Rice and Phragmites:effects of organic acids on growth,root permeability,and radial oxygen loss to the rhizosphere[J]. Am J Bot,2001,88 (8):1359−1370. doi: 10.2307/3558443
[9] Gibbs J,Greenway H. Review:mechanisms of anoxia tolerance in plants. I. Growth,survival and anaerobic catabolism[J]. Funct Plant Biol,2003,30 (1):1−47. doi: 10.1071/PP98095
[10] Sasidharan R,Voesenek LACJ. Ethylene-mediated acclimations to flooding stress[J]. Plant Physiol,2015,169 (1):3−12. doi: 10.1104/pp.15.00387
[11] Colmer TD,Greenway H. Ion transport in seminal and adventitious roots of cereals during O2 deficiency[J]. J Exp Bot,2010,62 (1):39−57.
[12] Mommer L,Visser EJW. Underwater photosynthesis in flooded terrestrial plants:a matter of leaf plasticity[J]. Ann Bot,2005,96 (4):581−589. doi: 10.1093/aob/mci212
[13] Peng YJ,Zhou ZX,Tong RG,Hu XY,Du KB. Anatomy and ultrastructure adaptations to soil flooding of two full-sib poplar clones differing in flood-tolerance[J]. Flora,2017,233:90−98. doi: 10.1016/j.flora.2017.05.014
[14] Mommer L,Pons TL,Wolters-Arts M,Venema JH,Visser EJW. Submergence-induced morphological,anatomical,and biochemical responses in a terrestrial species affect gas diffusion resistance and photosynthetic performance[J]. Plant Physiol,2005,139 (1):497−508. doi: 10.1104/pp.105.064725
[15] Zhou WJ,Lin XQ. Effects of waterlogging at different growth stages on physiological characteristics and seed yield of winter rape (Brassica napus L. )[J]. Field Crops Res,1995,44 (2-3):103−110. doi: 10.1016/0378-4290(95)00075-5
[16] Ren BZ,Zhang JW,Dong ST,Liu P,Zhao B. Effects of waterlogging on leaf mesophyll cell ultrastructure and photosynthetic characteristics of summer maize[J]. PLoS One,2016,11 (9):e0161424. doi: 10.1371/journal.pone.0161424
[17] Jackson MB,Armstrong W. Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence[J]. Plant Biol,1999,1 (3):274−287. doi: 10.1111/j.1438-8677.1999.tb00253.x
[18] Yamauchi T,Colmer TD,Pedersen O,Nakazono M. Regulation of root traits for internal aeration and tolerance to soil waterlogging-flooding stress[J]. Plant Physiol,2018,176 (2):1118−1130. doi: 10.1104/pp.17.01157
[19] Takahashi H, Yamauchi T, Colmer TD, Nakazono M. Aerenchyma formation in plants[M]//Van Dongen JT, Licausi F, eds. Low-Oxygen Stress in Plants: Oxygen Sensing and Adaptive Responses to Hypoxia. Vienna: Springer, 2014: 247-265.
[20] Seago JL Jr,Marsh LC,Stevens K J,Soukup A,Votrubova O,et al. A re-examination of the root cortex in wetland flowering plants with respect to aerenchyma[J]. Ann Bot,2005,96 (4):565−579. doi: 10.1093/aob/mci211
[21] Saika H,Okamoto M,Miyoshi K,Kushiro T,Shinoda S,et al. Ethylene promotes submergence-induced expression of OsABA8ox1,a gene that encodes ABA 8′-hydroxylase in rice[J]. Plant Cell Physiol,2007,48 (2):287−298.
[22] Nishiuchi S,Yamauchi T,Takahashi H,Kotula L,Nakazono M. Mechanisms for coping with submergence and waterlogging in rice[J]. Rice,2012,5 (1):2. doi: 10.1186/1939-8433-5-2
[23] Zhang XC,Fan Y,Shabala S,Koutoulis A,Shabala L,et al. A new major-effect QTL for waterlogging tolerance in wild barley (H. spontaneum)[J]. Theor Appl Genet,2017,130 (8):1559−1568. doi: 10.1007/s00122-017-2910-8
[24] Bailey-Serres J,Voesenek LACJ. Flooding stress:a cclimations and genetic diversity[J]. Annu Rev Plant Biol,2008,59:313−339. doi: 10.1146/annurev.arplant.59.032607.092752
[25] Mühlenbock P,Plaszczyca M,Plaszczyca M,Mellerowicz E,Karpinski S. Lysigenous aerenchyma formation in Arabidopsis is controlled by LESION SIMULATING DISEASE1[J]. Plant Cell,2007,19 (11):3819−3830. doi: 10.1105/tpc.106.048843
[26] Sauter M. Root responses to flooding[J]. Curr Opin Plant Biol,2013,16 (3):282−286. doi: 10.1016/j.pbi.2013.03.013
[27] Steffens B,Kovalev A,Gorb SN,Sauter M. Emerging roots alter epidermal cell fate through mechanical and reactive oxygen species signaling[J]. Plant Cell,2012,24 (8):3296−3306. doi: 10.1105/tpc.112.101790
[28] Visser E,Cohen JD,Barendse G,Blom C,Voesenek L. An ethylene-mediated increase in sensitivity to auxin induces adventitious root formation in flooded Rumex palustris Sm[J]. Plant Physiol,1996,112 (4):1687−1692. doi: 10.1104/pp.112.4.1687
[29] Vidoz ML,Loreti E,Mensuali A,Alpi A,Perata P. Hormonal interplay during adventitious root formation in flooded tomato plants[J]. Plant J,2010,63 (4):551−562. doi: 10.1111/j.1365-313X.2010.04262.x
[30] Colmer TD. Long-distance transport of gases in plants:a perspective on internal aeration and radial oxygen loss from roots[J]. Plant,Cell Environ,2003,26 (1):17−36.
[31] Watanabe K,Takahashi H,Sato S,Nishiuchi S,Omori F,et al. A major locus involved in the formation of the radial oxygen loss barrier in adventitious roots of teosinte Zea nicaraguensis is located on the short-arm of chromosome 3[J]. Plant Cell Environ,2017,40 (2):304−316. doi: 10.1111/pce.12849
[32] Armstrong W,Cousins D,Armstrong J,Turner DW,Beckett PM. Oxygen distribution in wetland plant roots and permeability barriers to gas-exchange with the rhizosphere:a microelectrode and modelling study with Phragmites australis[J]. Ann Bot,2000,86 (3):687−703. doi: 10.1006/anbo.2000.1236
[33] Armstrong J,Armstrong W. Rice:sulfide-induced barriers to root radial oxygen loss,Fe2 + and water uptake,and lateral root emergence[J]. Ann Bot,2005,96 (4):625−638. doi: 10.1093/aob/mci215
[34] Kotula L,Ranathunge K,Schreiber L,Steudle E. Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L. ) grown in aerated or deoxygenated solution[J]. J Exp Bot,2009,60 (7):2155−2167. doi: 10.1093/jxb/erp089
[35] Shiono K,Ogawa S,Yamazaki S,Isoda H,Fujimura T,et al. Contrasting dynamics of radial O2-loss barrier induction and aerenchyma formation in rice roots of two lengths[J]. Ann Bot,2011,107 (1):89−99. doi: 10.1093/aob/mcq221
[36] Shiono K,Yamauchi T,Yamazaki S,Mohanty B,Malik AI,et al. Microarray analysis of laser-microdissected tissues indicates the biosynthesis of suberin in the outer part of roots during formation of a barrier to radial oxygen loss in rice (Oryza sativa)[J]. J Exp Bot,2014,65 (17):4795−4806. doi: 10.1093/jxb/eru235
[37] Xu KN,Xu X,Fukao T,Canlas P,Maghirang-Rodriguez R,et al. Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice[J]. Nature,2006,442 (7103):705−708. doi: 10.1038/nature04920
[38] Hattori Y,Nagai K,Furukawa S,Song XJ,Kawano R,et al. The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water[J]. Nature,2009,460 (7258):1026−1030. doi: 10.1038/nature08258
[39] Kretzschmar T,Pelayo MAF,Trijatmiko KR,Gabunada LFM,Alam R,et al. A trehalose-6-phosphate phosphatase enhances anaerobic germination tolerance in rice[J]. Nat Plants,2015,1 (9):15124. doi: 10.1038/nplants.2015.124
[40] Ye NH,Wang FZ,Shi L,Chen MX,Cao YY,et al. Natural variation in the promoter of rice calcineurin B-like protein10 (OsCBL10) affects flooding tolerance during seed germination among rice subspecies[J]. Plant J,2018,94 (4):612−625. doi: 10.1111/tpj.13881
[41] Sun J,Zhang GC,Cui ZB,Kong XM,Yu XY,et al. Regain flood adaptation in rice through a 14-3-3 protein OsGF14h[J]. Nat Commun,2022,13 (1):5664. doi: 10.1038/s41467-022-33320-x
[42] He YQ,Sun S,Zhao J,Huang ZB,Peng LL,et al. UDP-glucosyltransferase OsUGT75A promotes submergence tolerance during rice seed germination[J]. Nat Commun,2023,14 (1):2296. doi: 10.1038/s41467-023-38085-5
[43] Verboven P,Pedersen O,Ho QT,Nicolai BM,Colmer TD. The mechanism of improved aeration due to gas films on leaves of submerged rice[J]. Plant,Cell Environ,2014,37 (10):2433−2452.
[44] Kurokawa Y,Nagai K,Huan PD,Shimazaki K,Qu HQ,et al. Rice leaf hydrophobicity and gas films are conferred by a wax synthesis gene (LGF1) and contribute to flood tolerance[J]. New Phytol,2018,218 (4):1558−1569. doi: 10.1111/nph.15070
[45] Bailey-Serres J,Lee SC,Brinton E. Waterproofing crops:effective flooding survival strategies[J]. Plant Physiol,2012,160 (4):1698−1709. doi: 10.1104/pp.112.208173
[46] Hebelstrup KH,van Zanten M,Mandon J,Voesenek LACJ,Harren FJM,et al. Haemoglobin modulates NO emission and hyponasty under hypoxia-related stress in Arabidopsis thaliana[J]. J Exp Bot,2012,63 (15):5581−5591. doi: 10.1093/jxb/ers210
[47] Colmer TD,Voesenek LACJ. Flooding tolerance:Suites of plant traits in variable environments[J]. Funct Plant Biol,2009,36 (8):665−681. doi: 10.1071/FP09144
[48] Sasidharan R,Hartman S,Liu ZG,Martopawiro S,Sajeev N,et al. Signal dynamics and interactions during flooding stress[J]. Plant Physiol,2018,176 (2):1106−1117. doi: 10.1104/pp.17.01232
[49] Van der Straeten D,Zhou ZY,Prinsen E,van Onckelen HA,van Montagu MC. A comparative molecular-physiological study of submergence response in lowland and deepwater rice[J]. Plant Physiol,2001,125 (2):955−968. doi: 10.1104/pp.125.2.955
[50] Lee SC,Mustroph A,Sasidharan R,Vashisht D,Pedersen O,et al. Molecular characterization of the submergence response of the Arabidopsis thaliana ecotype Columbia[J]. New Phytol,2011,190 (2):457−471. doi: 10.1111/j.1469-8137.2010.03590.x
[51] Van Veen H,Mustroph A,Barding GA,Vergeer-van Eijk M,Welschen-Evertman RAM,et al. Two Rumex species from contrasting hydrological niches regulate flooding tolerance through distinct mechanisms[J]. Plant Cell,2013,25 (11):4691−4707. doi: 10.1105/tpc.113.119016
[52] Kendrick MD,Chang CR. Ethylene signaling:new levels of complexity and regulation[J]. Curr Opin Plant Biol,2008,11 (5):479−485. doi: 10.1016/j.pbi.2008.06.011
[53] Stepanova AN,Alonso JM. Ethylene signaling and response:where different regulatory modules meet[J]. Curr Opin Plant Biol,2009,12 (5):548−555. doi: 10.1016/j.pbi.2009.07.009
[54] Blom CWPM,Voesenek LACJ. Flooding:the survival strategies of plants[J]. Trends Ecol Evol,1996,11 (7):290−295. doi: 10.1016/0169-5347(96)10034-3
[55] Panozzo A,Dal Cortivo C,Ferrari M,Vicelli B,Varotto S,Vamerali T. Morphological changes and expressions of AOX1A,CYP81D8,and putative PFP genes in a large set of commercial maize hybrids under extreme waterlogging[J]. Front Plant Sci,2019,10:62. doi: 10.3389/fpls.2019.00062
[56] Greenway H,Armstrong W,Colmer TD. Conditions leading to high CO2 (>5 kPa) in waterlogged-flooded soils and possible effects on root growth and metabolism[J]. Ann Bot,2006,98 (1):9−32. doi: 10.1093/aob/mcl076
[57] Gibbs DJ,Lee SC,Md Isa N,Gramuglia S,Fukao T,et al. Homeostatic response to hypoxia is regulated by the N-end rule pathway in plants[J]. Nature,2011,479 (7373):415−418. doi: 10.1038/nature10534
[58] Licausi F,Kosmacz M,Weits DA,Giuntoli B,Giorgi FM,et al. Oxygen sensing in plants is mediated by an N-end rule pathway for protein destabilization[J]. Nature,2011,479 (7373):419−422. doi: 10.1038/nature10536
[59] Wei XN,Xu HJ,Rong W,Ye XG,Zhang ZY. Constitutive expression of a stabilized transcription factor group Ⅶ ethylene response factor enhances waterlogging tolerance in wheat without penalizing grain yield[J]. Plant,Cell Environ,2019,42 (5):1471−1485.
[60] Yu F,Liang K,Fang T,Zhao HL,Han XS,et al. A group Ⅶ ethylene response factor gene,ZmEREB180,coordinates waterlogging tolerance in maize seedlings[J]. Plant Biotechnol J,2019,17 (12):2286−2298. doi: 10.1111/pbi.13140
[61] Tang H,Bi H,Liu B,Lou SL,Song Y,et al. WRKY33 interacts with WRKY12 protein to up-regulate RAP2.2 during submergence induced hypoxia response in Arabidopsis thaliana[J]. New Phytol,2021,229 (1):106−125. doi: 10.1111/nph.17020
[62] Liu B,Jiang YZ,Tang H,Tong SF,Lou SL,et al. The ubiquitin E3 ligase SR1 modulates the submergence response by degrading phosphorylated WRKY33 in Arabidopsis[J]. Plant Cell,2021,33 (5):1771−1789. doi: 10.1093/plcell/koab062
[63] Schmitz AJ,Folsom JJ,Jikamaru Y,Ronald P,Walia H. SUB1A-mediated submergence tolerance response in rice involves differential regulation of the brassinosteroid pathway[J]. New Phytol,2013,198 (4):1060−1070. doi: 10.1111/nph.12202
[64] Xie ZL,Nolan TM,Jiang H,Yin YH. AP2/ERF transcription factor regulatory networks in hormone and abiotic stress responses in Arabidopsis[J]. Front Plant Sci,2019,10:228. doi: 10.3389/fpls.2019.00228
[65] Uchida A,Jagendorf AT,Hibino T,Takabe T,Takabe T. Effects of hydrogen peroxide and nitric oxide on both salt and heat stress tolerance in rice[J]. Plant Sci,2002,163 (3):515−523. doi: 10.1016/S0168-9452(02)00159-0
[66] Laspina NV,Groppa MD,Tomaro ML,Benavides MP. Nitric oxide protects sunflower leaves against Cd-induced oxidative stress[J]. Plant Sci,2005,169 (2):323−330. doi: 10.1016/j.plantsci.2005.02.007
[67] Mugnai S,Azzarello E,Baluška F,Mancuso S. Local root apex hypoxia induces NO-mediated hypoxic acclimation of the entire root[J]. Plant Cell Physiol,2012,53 (5):912−920. doi: 10.1093/pcp/pcs034
[68] Peng RY,Bian ZY,Zhou LN,Cheng W,Hai N,et al. Hydrogen sulfide enhances nitric oxide-induced tolerance of hypoxia in maize (Zea mays L. )[J]. Plant Cell Rep,2016,35 (11):2325−2340. doi: 10.1007/s00299-016-2037-4
[69] Dordas C,Rivoal J,Hill RD. Plant haemoglobins,nitric oxide and hypoxic stress[J]. Ann Bot,2003,91 (2):173−178. doi: 10.1093/aob/mcf115
[70] Planchet E,Jagadis Gupta K,Sonoda M,Kaiser WM. Nitric oxide emission from tobacco leaves and cell suspensions:rate limiting factors and evidence for the involvement of mitochondrial electron transport[J]. Plant J,2005,41 (5):732−743. doi: 10.1111/j.1365-313X.2005.02335.x
[71] Drew MC. Oxygen deficiency and root metabolism:injury and acclimation under hypoxia and anoxia[J]. Annu Rev Plant Biol,1997,48:223−250. doi: 10.1146/annurev.arplant.48.1.223
[72] Bologa KL,Fernie AR,Leisse A,Ehlers Loureiro M,Geigenberger P. A bypass of sucrose synthase leads to low internal oxygen and impaired metabolic performance in growing potato tubers[J]. Plant Physiol,2003,132 (4):2058−2072. doi: 10.1104/pp.103.022236
[73] Lee KW,Chen PW,Lu CA,Chen S,Ho THD,et al. Coordinated responses to oxygen and sugar deficiency allow rice seedlings to tolerate flooding[J]. Sci Signal,2009,2 (91):ra61.
[74] Baena-González E. Energy signaling in the regulation of gene expression during stress[J]. Mol Plant,2010,3 (2):300−313. doi: 10.1093/mp/ssp113
[75] Cho YH,Hong JW,Kim EC,Yoo SD. Regulatory functions of SnRK1 in stress-responsive gene expression and in plant growth and development[J]. Plant Physiol,2012,158 (4):1955−1964. doi: 10.1104/pp.111.189829
[76] Cho HY,Lu MYJ,Shih MC. The SnRK1-eIFiso4G1 signaling relay regulates the translation of specific mRNAs in Arabidopsis under submergence[J]. New Phytol,2019,222 (1):366−381. doi: 10.1111/nph.15589
[77] Møller IM. Plant mitochondria and oxidative stress:electron transport,NADPH turnover,and metabolism of reactive oxygen species[J]. Annu Rev Plant Biol,2001,52:561−591. doi: 10.1146/annurev.arplant.52.1.561
[78] Mignolet-Spruyt L,Xu EJ,Idänheimo N,Hoeberichts FA,Mühlenbock P,et al. Spreading the news:Subcellular and organellar reactive oxygen species production and signalling[J]. J Exp Bot,2016,67 (13):3831−3844. doi: 10.1093/jxb/erw080
[79] Yuan LB,Dai YS,Xie LJ,Yu LJ,Zhou Y,et al. Jasmonate regulates plant responses to postsubmergence reoxygenation through transcriptional activation of antioxidant synthesis[J]. Plant Physiol,2017,173 (3):1864−1880. doi: 10.1104/pp.16.01803
[80] Hossain Z,López-Climent MF,Arbona V,Pérez-Clemente RM,Gómez-Cadenas A. Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage[J]. J Plant Physiol,2009,166 (13):1391−1404. doi: 10.1016/j.jplph.2009.02.012
[81] Steffens B,Steffen-Heins A,Sauter M. Reactive oxygen species mediate growth and death in submerged plants[J]. Front Plant Sci,2013,4:179.
[82] Li CW,Su JS,Zhao N,Lou L,Ou XL,et al. CmERF5-CmRAP2.3 transcriptional cascade positively regulates waterlogging tolerance in Chrysanthemum morifolium[J]. Plant Biotechnol J,2023,21 (2):270−282. doi: 10.1111/pbi.13940
[83] Foyer CH,Noctor G. Ascorbate and glutathione:the heart of the redox hub[J]. Plant Physiol,2011,155 (1):2−18. doi: 10.1104/pp.110.167569
[84] Ushimaru T,Shibasaka M,Tsuji H. Development of the O2−-detoxification system during adaptation to air of submerged rice seedlings[J]. Plant Cell Physiol,1992,33 (8):1065−1071.
[85] Yeung E,van Veen H,Vashisht D,Sobral Paiva AL,Hummel M,et al. A stress recovery signaling network for enhanced flooding tolerance in Arabidopsis thaliana[J]. Proc Natl Acad Sci USA,2018,115 (26):E6085−E6094.
[86] Zheng XD,Zhou JZ,Tan DX,Wang N,Wang L,et al. Melatonin improves waterlogging tolerance of Malus baccata (Linn. ) Borkh. Seedlings by maintaining aerobic respiration,photosynthesis and ROS migration[J]. Front Plant Sci,2017,8:483.
[87] Cho HY,Wen TN,Wang YT,Shih MC. Quantitative phosphoproteomics of protein kinase SnRK1 regulated protein phosphorylation in Arabidopsis under submergence[J]. J Exp Bot,2016,67 (9):2745−2760. doi: 10.1093/jxb/erw107
[88] Xu XW,Ji J,Xu Q,Qi XH,Weng YQ,Chen XH. The major-effect quantitative trait locus CsARN6.1 encodes an AAA ATPase domain-containing protein that is associated with waterlogging stress tolerance by promoting adventitious root formation[J]. Plant J,2018,93 (5):917−930. doi: 10.1111/tpj.13819
[89] Mackill DJ,Ismail AM,Singh US,Labios RV,Paris TR. Development and rapid adoption of submergence-tolerant (Sub1) rice varieties[J]. Adv Agron,2012,115:299−352.
[90] Kuroha T,Nagai K,Gamuyao R,Wang DR,Furuta T,et al. Ethylene-gibberellin signaling underlies adaptation of rice to periodic flooding[J]. Science,2018,361 (6398):181−186. doi: 10.1126/science.aat1577
[91] Hinz M,Wilson IW,Yang J,Buerstenbinder K,Llewellyn D,et al. Arabidopsis RAP2.2:an ethylene response transcription factor that is important for hypoxia survival[J]. Plant Physiol,2010,153 (2):757−772. doi: 10.1104/pp.110.155077
[92] Xie LJ,Yu LJ,Chen QF,Wang FZ,Huang L,et al. Arabidopsis acyl-CoA-binding protein ACBP3 participates in plant response to hypoxia by modulating very-long-chain fatty acid metabolism[J]. Plant J,2015,81 (1):53−67. doi: 10.1111/tpj.12692
[93] Tsai KJ,Lin CY,Ting CY,Shih MC. Ethylene-regulated glutamate dehydrogenase fine-tunes metabolism during anoxia-reoxygenation[J]. Plant Physiol,2016,172 (3):1548−1562. doi: 10.1104/pp.16.00985
[94] Zhou Y,Tan WJ,Xie LJ,Qi H,Yang YC,et al. Polyunsaturated linolenoyl-CoA modulates ERF-Ⅶ-mediated hypoxia signaling in Arabidopsis[J]. J Integr Plant Biol,2020,62 (3):330−348. doi: 10.1111/jipb.12875
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