Photosynthetic inorganic carbon utilization strategies and their ecological adaptability in aquatic plants
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摘要:
水生维管植物经历了从陆生向水生的“回归”演化,这个过程伴随着周围环境的一系列巨大变化,尤其是水体中无机碳环境与陆生生境的差异赋予了水生植物光合无机碳利用策略与陆生植物截然不同的生态学意义。本文综述了以光合作用为核心的水生植物无机碳利用策略的特殊性和多样性,以及研究水生植物无机碳利用策略的意义,并展望了基于水生植物尤其是水鳖科的无机碳利用策略为核心的植物适应机制研究的优势,旨在为水生植物适应机制和适应性进化研究提供新的思考方向。
Abstract:Aquatic vascular plants have undergone an evolutionary transition from terrestrial to aquatic habitats, necessitating substantial adaptations to their surrounding environments. In particular, the different inorganic carbon environments between underwater and terrestrial habitats confer distinct ecological significance to the photosynthetic inorganic carbon utilization strategies of both plant types. This paper elucidates the particularity and diversity of inorganic carbon utilization strategies in aquatic plants and the significance of these studies. In addition, the potential advantages in studying plant adaptation mechanisms based on inorganic carbon utilization strategies in aquatic plants (especially Hydrocharitaceae) is analyzed. Overall, this paper aims to provide a novel perspective for studying the adaptative mechanisms and evolutionary processes of aquatic plants, as well as new directions for research in this field.
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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)。
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 水生植物无机碳利用策略的特殊性和多样性
A:中华水韭(Isoetes sinensis Palmer);B:龙舌草(Ottelia alismoides (L.) Pers.)(照片由付文龙拍摄);C:水筛(Blyxa japonica (Miq.) Maxim.);D:穿叶眼子菜(Potamogeton perfoliatus L.);E:一种轮藻(Chara sp.)(照片由刘洋拍摄);F:眼子菜(Potamogeton distinctus A. Bennett);G:紫萍(Spirodela polyrhiza (L.) Schleid)。轮藻不属于植物,但在无机碳利用时,通常将其视为沉水植物。图中pH极性叶片染色显示眼子菜属植物近轴面被酚酞染成红色(碱性),远轴面无色,表明这类叶片在利用HCO3−过程中形成pH极性。溴麝香草酚蓝染色显示轮藻属在利用HCO3−过程中,细胞呈酸性(黄色)和碱性(蓝色)相间(图片来源于Beilby等[57])。
Figure 1. The distinctiveness and diversity of inorganic carbon utilization strategies in aquatic plants
A: Isoetes sinensis Palmer; B: Ottelia alismoides (L.) Pers. (Photographed by Fu Wenlong); C: Blyxa japonica (Miq.) Maxim.; D: Potamogeton perfoliatus L.; E: Chara sp. (Photographed by Liu Yang); F: Potamogeton distinctus A. Bennett; G: Spirodela polyrhiza (L.) Schleid. Characean algae are not plant, but they are usually regarded as submerged plants in study of inorganic carbon utilization. Under phenolphthalein staining, the adaxial surface of Potamogeton plant leaf is red (alkalinity), while the abaxial surface is colorless, indicating pH polarity of two sides of the same leaf during the process of HCO3− use. Under bromothymol blue staining, the interior of Chara cell exhibits alternating acidity (yellow) and alkalinity (blue) during HCO3−use (The image is from Beilby et al. [57]).
表 1 植物在水生环境中面临的机遇和挑战及水生植物的应对方式(改自Maberly 和 Gontero[14])
Table 1 Opportunities and challenges faced by plants in aquatic environments and how aquatic plants respond (modified from Maberly and Gontero[14])
环境特征
Environmental feature机遇
Opportunity挑战
Challenge水生植物应对方式
Aquatic plant response水分可利用性高 无水分胁迫 藻类竞争 生产力高;表皮细胞包含叶绿体;
叶片薄;分泌化感物质生长介质密度高 支撑性高 水阻力大 机械组织投资减少;茎和叶具有韧性 光照可利用性低 光抑制和光伤害可能低 光合作用和分布深度受限 表皮细胞富含叶绿体 温度变化幅度小 温度胁迫风险小 无 无 O2可利用性低 光呼吸可能低 地下组织器官缺氧 通气组织贯通根茎叶;向地下部位泵氧 无机碳可利用性低 局部生境CO2多;
HCO3−浓度高CO2日变化和年变化
范围极大拓展到局部高CO2生境生长;发展无机碳浓缩机制:HCO3−利用、C4和景天酸代谢(CAM) 养分可利用性高 根、茎、叶均可接触营养元素 藻类竞争 根茎叶均吸收养分;化感作用 表 2 水鳖科植物无机碳利用策略的多样性
Table 2 Diversity of inorganic carbon utilization strategies in Hydrocharitaceae plants
属
Genus种数
No. of speciesHCO3−利用
Bicarbonate use大气CO2
Atmosphere CO2基质CO2
Substrate CO2C4途径
C4 pathwayCAM途径
CAM pathwayAppertiella 1 U U U U U Blyxa[50, 56] 14 N N S N N Elodea[50, 75] 9 Y N U I/N N Enhalus[76] 1 Y N U U U Halophila[77] 17 Y N U N N Hydrilla[78, 73] 1 Y N U I S Hydrocharisa 5 N Y U U U Lagarosiphon[50] 9 Y/N U U U U Najas[50] 39 Y/N N U N N Nechamandra[56, 79] 1 Y N U U S Ottelia[45, 79-81] 23 Y Y U Y/N I/N Stratiotes[82] 1 Y Y U U U Thalassia[77,83,84] 2 Y N U S N Vallisneria[56, 84] 14 Y N Y N S/N 注:Y,具备该途径;N,不具备该途径;S,疑似具备该途径;U,尚未进行测试;I,需要在特殊条件下诱导出该途径;Y/N,在已测试的该属所有物种中,有的物种具有该途径,有的物种不具有该途径;I/N,在已测试的该属所有物种中,有的物种该途径的产生需要诱导,有的物种则不具备该途径;S/N,在已测试的该属所有物种中,有些物种疑似具有该途径,有的物种不具备该途径。a,数据来源于本实验室。 Notes: Y, all plants have this pathway; N, none plant have this pathway; S, the plants are suspected to have this pathway; U, not yet tested; I, this pathway needs to be induced under special conditions; Y/S, among all the tested species from this genus, some have this pathway and some do not; I/N, among all the tested species from this genus, some need to be induced to produce this pathway and some do not have this pathway; S/N, among all the tested species from this genus, some are suspected to have this pathway and some do not have. a, indicates the data are from our lab. -
[1] Les DH,Philbrick CT. Studies of hybridization and chromosome number variation in aquatic angiosperms:evolutionary implications[J]. Aquat Bot,1993,44 (2-3):181−228. doi: 10.1016/0304-3770(93)90071-4
[2] Den Hartog C, Kuo J. Taxonomy and biogeography of seagrasses[M]//Larkum AWD, Orth RJ, Duarte CM, eds. Seagrasse: Biology, Ecology and Conservation. Berlin Heidelberg: Springer, 2006: 1-23.
[3] Cook CD. Aquatic Plant Book[M]. The Hague: SPB Academic Publishing, 1990: 1-7
[4] Les DH,Cleland MA,Waycott M. Phylogenetic studies in Alismatidae,Ⅱ:evolution of marine angiosperms (seagrasses) and hydrophily[J]. Syst Bot,1997,22 (3):443−463. doi: 10.2307/2419820
[5] Friis EM,Pedersen KR,Crane PR. Fossil evidence of water lilies (Nymphaeales) in the Early Cretaceous[J]. Nature,2001,410 (6826):357−360. doi: 10.1038/35066557
[6] Gomez B,Daviero-Gomez V,Coiffard C,Martín-Closas C,Dilcher DL. Montsechia,an ancient aquatic angiosperm[J]. Proc Natl Acad Sci USA,2015,112 (35):10985−10988. doi: 10.1073/pnas.1509241112
[7] Les DH. Water from the rock:ancient aquatic angiosperms flow from the fossil record[J]. Proc Natl Acad Sci USA,2015,112 (35):10825−10826. doi: 10.1073/pnas.1514280112
[8] Philbrick CT,Les DH. Evolution of aquatic angiosperm reproductive systems[J]. BioScience,1996,46 (11):813−826. doi: 10.2307/1312967
[9] Les DH, Tippery NP. In time and with water … the systematics of alismatid monocotyledons[M]//Wilkin P, Mayo SJ, eds. Early Events in Monocot Evolution. Cambridge: Cambridge University Press, 2013: 1-100.
[10] Maberly SC,Spence DHN. Photosynthesis and photorespiration in freshwater organisms:amphibious plants[J]. Aquat Bot,1989,34 (1-3):267−286. doi: 10.1016/0304-3770(89)90059-4
[11] Santamaría L. Why are most aquatic plants widely distributed? Dispersal,clonal growth and small-scale heterogeneity in a stressful environment[J]. Acta Oecol,2002,23 (3):137−154. doi: 10.1016/S1146-609X(02)01146-3
[12] Li W. Environmental opportunities and constraints in the reproduction and dispersal of aquatic plants[J]. Aquat Bot,2014,118:62−70. doi: 10.1016/j.aquabot.2014.07.008
[13] Maberly SC. The fitness of the environments of air and water for photosynthesis,growth,reproduction and dispersal of photoautotrophs:an evolutionary and biogeochemical perspective[J]. Aquat Bot,2014,118:4−13. doi: 10.1016/j.aquabot.2014.06.014
[14] Maberly SC, Gontero B. Trade-offs and synergies in the structural and functional characteristics of leaves photosynthesizing in aquatic environments[M]//Adams Ⅲ WW, Terashima I, eds. The Leaf: A platform for Performing Photosynthesis. Chambrige: Springer, 2018: 307-343.
[15] 沈允钢, 施教耐, 许大全. 动态光合作用[M]. 北京: 科学出版社, 1998: 1-6. [16] Niklaus M,Kelly S. The molecular evolution of C4 photosynthesis:opportunities for understanding and improving the world's most productive plants[J]. J Exp Bot,2019,70 (3):795−804. doi: 10.1093/jxb/ery416
[17] Raven JA,Cockell CS,de La Rocha CL. The evolution of inorganic carbon concentrating mechanisms in photosynthesis[J]. Philos Trans Roy Soc B:Biol Sci,2008,363 (1504):2641−2650. doi: 10.1098/rstb.2008.0020
[18] Sage RF. A portrait of the C4 photosynthetic family on the 50th anniversary of its discovery:species number,evolutionary lineages,and Hall of Fame[J]. J Exp Bot,2016,67 (14):4039−4056. doi: 10.1093/jxb/erw156
[19] Silvera K,Neubig KM,Whitten WM,Williams NH,Winter K,Cushman JC. Evolution along the crassulacean acid metabolism continuum[J]. Funct Plant Biol,2010,37 (11):995−1010. doi: 10.1071/FP10084
[20] Sage RF. Are crassulacean acid metabolism and C4 photosynthesis incompatible?[J]. Funct Plant Biol,2002,29 (6):775−785. doi: 10.1071/PP01217
[21] Winter K, Smith JAC. Crassulacean Acid Metabolism: Biochemistry, Ecophysiology and Evolution[M]. Berlin Heidelberg: Springer, 1996: 19-420.
[22] Sage RF, Monson RK. C4 Plant Biology[M]. San Diego: Academic Press, 1998: 10-375.
[23] Keeley JE,Rundel PW. Evolution of CAM and C4 carbon-concentrating mechanisms[J]. Int J Plant Sci,2003,164 (S3):S55−S77. doi: 10.1086/374192
[24] Griffiths H. Carbon dioxide concentrating mechanisms and the evolution of CAM in vascular epiphytes[M]//Lüttge U, ed. Vascular Plants as Epiphytes: Evolution and Ecophysiology. Berlin Heidelberg: Springer, 1989: 42-86.
[25] Sage RF. Environmental and evolutionary preconditions for the origin and diversification of the C4 photosynthetic syndrome[J]. Plant Biol,2001,3 (3):202−213. doi: 10.1055/s-2001-15206
[26] Hatch MD,Slack CR. Photosynthesis by sugar-cane leaves. A new carboxylation reaction and the pathway of sugar formation[J]. Biochem J,1966,101 (1):103−111. doi: 10.1042/bj1010103
[27] Raghavendra AS, Sage RF. C4 Photosynthesis and Related CO2 Concentrating Mechanisms[M]. Media: Springer, 2011: 161-195.
[28] Cushman JC,Bohnert HJ. CRASSULACEAN ACID METABOLISM:molecular genetics[J]. Annu Rev Plant Physiol Plant Mol Biol,1999,50:305−332. doi: 10.1146/annurev.arplant.50.1.305
[29] Raven JA. Nutrient transport in microalgae[J]. Adv Microb Physiol,1981,21:47−226.
[30] Raven JA,Giordano M,Beardall J. Insights into the evolution of CCMs from comparisons with other resource acquisition and assimilation processes[J]. Physiol Plant,2008,133 (1):4−14. doi: 10.1111/j.1399-3054.2007.01024.x
[31] Sage RF. The evolution of C4 photosynthesis[J]. New Phytol,2004,161 (2):341−370. doi: 10.1111/j.1469-8137.2004.00974.x
[32] Black CC Jr. Photosynthetic carbon fixation in relation to net CO2 uptake[J]. Ann Rev Plant Physiol,1973,24:253−286. doi: 10.1146/annurev.pp.24.060173.001345
[33] Han HE,Felker P. Field validation of water-use efficiency of the CAM plant Opuntia ellisianain south Texas[J]. J Arid Environ,1997,36 (1):133−148. doi: 10.1006/jare.1996.0202
[34] Pearson PN,Palmer MR. Atmospheric carbon dioxide concentrations over the past 60 million years[J]. Nature,2000,406 (6797):695−699. doi: 10.1038/35021000
[35] Maberly SC,Gontero B. Ecological imperatives for aquatic CO2 concentrating mechanisms[J]. J Exp Bot,2017,68 (14):3797−3814. doi: 10.1093/jxb/erx201
[36] Raven JA. Exogenous inorganic carbon sources in plant photosynthesis[J]. Biol Rev,1970,45 (2):167−220. doi: 10.1111/j.1469-185X.1970.tb01629.x
[37] Raven JA,Beardall J. CO2 concentrating mechanisms and environmental change[J]. Aquat Bot,2014,118:24−37. doi: 10.1016/j.aquabot.2014.05.008
[38] Maberly SC,Spence DHN. Photosynthetic inorganic carbon use by freshwater plants[J]. J Ecol,1983,71 (3):705−724. doi: 10.2307/2259587
[39] Cole JJ,Caraco NF,Kling GW,Kratz TK. Carbon dioxide supersaturation in the surface waters of lakes[J]. Science,1994,265 (5178):1568−1570. doi: 10.1126/science.265.5178.1568
[40] Madsen TV,Sand-Jensen K. Photosynthetic carbon assimilation in aquatic macrophytes[J]. Aquat Bot,1991,41 (1-3):5−40. doi: 10.1016/0304-3770(91)90037-6
[41] Maberly SC,Madsen TV. Affinity for CO2 in relation to the ability of freshwater macrophytes to use HCO3−[J]. Funct Ecol,1998,12 (1):99−106. doi: 10.1046/j.1365-2435.1998.00172.x
[42] Maberly SC,Madsen TV. Freshwater angiosperm carbon concentrating mechanisms:processes and patterns[J]. Funct Plant Biol,2002,29 (3):393−405. doi: 10.1071/PP01187
[43] Klavsen SK,Maberly SC. Effect of light and CO2 on inorganic carbon uptake in the invasive aquatic CAM-plant Crassula helmsii[J]. Funct Plant Biol,2010,37 (8):737−747. doi: 10.1071/FP09281
[44] Klavsen SK,Madsen TV,Maberly SC. Crassulacean acid metabolism in the context of other carbon-concentrating mechanisms in freshwater plants:a review[J]. Photosynth Res,2011,109 (1-3):269−279. doi: 10.1007/s11120-011-9630-8
[45] Zhang YZ,Yin LY,Jiang HS,Li W,Gontero B,Maberly SC. Biochemical and biophysical CO2 concentrating mechanisms in two species of freshwater macrophyte within the genus Ottelia (Hydrocharitaceae)[J]. Photosynth Res,2014,121 (2-3):285−297. doi: 10.1007/s11120-013-9950-y
[46] Maberly SC,Stott AW,Gontero B. The differential ability of two species of seagrass to use carbon dioxide and bicarbonate and their modelled response to rising concentrations of inorganic carbon[J]. Front Plant Sci,2022,13:936716. doi: 10.3389/fpls.2022.936716
[47] Wickell D,Kuo LY,Yang HP,Ashok AD,Irisarri I,et al. Underwater CAM photosynthesis elucidated by Isoetes genome
[J]. Nat Commun,2021,12 (1):6348. doi: 10.1038/s41467-021-26644-7 [48] Huang WM,Han SJ,Jiang HS,Gu SP,Li W,et al. External α-carbonic anhydrase and solute carrier 4 are required for bicarbonate uptake in a freshwater angiosperm[J]. J Exp Bot,2020,71 (19):6004−6014. doi: 10.1093/jxb/eraa351
[49] Magnin NC,Cooley BA,Reiskind JB,Bowes G. Regulation and localization of key enzymes during the induction of Kranz-less,C4-type photosynthesis in Hydrilla verticillata[J]. Plant Physiol,1997,115 (4):1681−1689. doi: 10.1104/pp.115.4.1681
[50] Iversen LL,Winkel A,Baastrup-Spohr L,Hinke AB,Alahuhta J,et al. Catchment properties and the photosynthetic trait composition of freshwater plant communities[J]. Science,2019,366 (6467):878−881. doi: 10.1126/science.aay5945
[51] Maberly SC. Photosynthesis by Fontinalis antipyretica[J]. New Phytol,1985,100 (2):127−140. doi: 10.1111/j.1469-8137.1985.tb02765.x
[52] Maberly SC. Photosynthesis by Fontinalis antipyretica. Ⅱ. Assessment of environmental factors limiting photosynthesis and production[J]. New Phytol,1985,100 (2):141−155. doi: 10.1111/j.1469-8137.1985.tb02766.x
[53] Pedersen O,Pulido C,Rich SM,Colmer TD. In situ O2 dynamics in submerged Isoetes australis:varied leaf gas permeability influences underwater photosynthesis and internal O2[J]. J Exp Bot,2011,62 (13):4691−4700. doi: 10.1093/jxb/err193
[54] Casati P,Lara MV,Andreo CS. Induction of a C4-like mechanism of CO2 fixation in Egeria densa,a submersed aquatic species[J]. Plant Physiol,2000,123 (4):1611−1622. doi: 10.1104/pp.123.4.1611
[55] Keeley JE. Isoetes howellii:a submerged aquatic CAM plant?[J]. Am J Bot,1981,68 (3):420−424. doi: 10.1002/j.1537-2197.1981.tb06380.x
[56] Yin LY,Li W,Madsen TV,Maberly SC,Bowes G. Photosynthetic inorganic carbon acquisition in 30 freshwater macrophytes[J]. Aquat Bot,2017,140:48−54. doi: 10.1016/j.aquabot.2016.05.002
[57] Beilby MJ,Bisson MA,Schneider SC. How Characean algae take up needed and excrete unwanted ions: an overview explaining how insights from electrophysiology are useful to understand the ecology of aquatic macrophytes[J]. Aquat Bot,2022,181:103542. doi: 10.1016/j.aquabot.2022.103542
[58] Wang Q. Hydrocharitaceae[M]//Flora of China. Beijing and St. Louis: Science Press and Missouri Botanical Garden Press, 2010: 91-102.
[59] Chen LY,Chen JM,Gituru RW,Wang QF. Generic phylogeny,historical biogeography and character evolution of the cosmopolitan aquatic plant family Hydrocharitaceae[J]. BMC Evol Biol,2012,12:30. doi: 10.1186/1471-2148-12-30
[60] Chen LY,Chen JM,Gituru RW,Wang QF. Eurasian origin of Alismatidae inferred from statistical dispersal-vicariance analysis[J]. Mol Phylogenet Evol,2013,67 (1):38−42. doi: 10.1016/j.ympev.2013.01.001
[61] Olsen JL,Rouzé P,Verhelst B,Lin YC,Bayer T,et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea[J]. Nature,2016,530 (7590):331−335. doi: 10.1038/nature16548
[62] Cook CDK,Urmi-König K. A revision of the genus Egeria (Hydrocharitaceae)[J]. Aquat Bot,1984,19 (1-2):73−96. doi: 10.1016/0304-3770(84)90009-3
[63] Li ZZ,Wu S,Zhou CY,Liu Y,Hu GW,et al. Ottelia fengshanensis,a new bisexual species of Ottelia (Hydrocharitaceae) from southwestern China[J]. PhytoKeys,2019,135:1−10. doi: 10.3897/phytokeys.135.38531
[64] Li ZZ,Liao K,Zou CY,Liu Y,Hu GW,et al. Ottelia guanyangensis (Hydrocharitaceae),a new species from southwestern China[J]. Phytotaxa,2018,361 (3):294−300. doi: 10.11646/phytotaxa.361.3.5
[65] Misra MP. Cytological studies in Ottelia alismoides pers[J]. Cytologia,1974,39 (3):419−427. doi: 10.1508/cytologia.39.419
[66] Krishnappa DG. Cytological studies in some aquatic angiosperms[J]. Proc/Indian Acad Sci,1971,73 (4):179−185.
[67] Chaudhuri JB,Sharma A. Cytological studies on three aquatic members of hydrocharitaceae in relation to their morphological and ecological characteristics[J]. Cytologia,1978,43 (1):1−19. doi: 10.1508/cytologia.43.1
[68] Salvucci ME,Bowes G. Induction of reduced photorespiratory activity in submersed and amphibious aquatic macrophytes[J]. Plant Physiol,1981,67 (2):335−340. doi: 10.1104/pp.67.2.335
[69] Salvucci ME,Bowes G. Ethoxyzolamide repression of the low photorespiration state in two submersed angiosperms[J]. Planta,1983,158 (1):27−34. doi: 10.1007/BF00395399
[70] Shao H,Gontero B,Maberly SC,Jiang HS,Cao Y,et al. Responses of Ottelia alismoides,an aquatic plant with three CCMs,to variable CO2 and light[J]. J Exp Bot,2017,68 (14):3985−3995. doi: 10.1093/jxb/erx064
[71] Pedersen O. Jack of all trades-C4 photosynthesis,CAM and HCO3− use in the same tissue. A commentary on:'Structural basis for C4 photosynthesis without Kranz anatomy in leaves of the submerged freshwater plant Ottelia alismoides'[J]. Ann Bot,2020,125 (6):iv−vi. doi: 10.1093/aob/mcaa034
[72] Han SJ,Maberly SC,Gontero B,Xing ZF,Li W,et al. Structural basis for C4 photosynthesis without Kranz anatomy in leaves of the submerged freshwater plant Ottelia alismoides[J]. Ann Bot,2020,125 (6):869−879. doi: 10.1093/aob/mcaa005
[73] Reiskind JB,Madsen TV,Van Ginkel LC,Bowes G. Evidence that inducible C4-type photosynthesis is a chloroplastic CO2-concentrating mechanism in Hydrilla,a submersed monocot[J]. Plant Cell Environ,1997,20 (2):211−220. doi: 10.1046/j.1365-3040.1997.d01-68.x
[74] Rao SK,Magnin NC,Reiskind JB,Bowes G. Photosynthetic and other phosphoenolpyruvate carboxylase isoforms in the single-cell,facultative C4 system of Hydrilla verticillata[J]. Plant Physiol,2002,130 (2):876−886. doi: 10.1104/pp.008045
[75] Lara MV,Casati P,Andreo CS. CO2-concentrating mechanisms in Egeria densa,a submersed aquatic plant[J]. Physiol Plant,2002,115 (4):487−495. doi: 10.1034/j.1399-3054.2002.1150402.x
[76] Luan WY,Li H,Zhang LT,Liu JG. Enhalus acoroides efficiently alleviate ocean acidification by shifting modes of inorganic carbon uptake and increasing photosynthesis when pH drops[J]. Mar Environ Res,2023,186:105896. doi: 10.1016/j.marenvres.2023.105896
[77] Gavin NM,Durako MJ. Carbon acquisition mechanisms in Halophila johnsonii and Thalassia testudinum[J]. Aquat Bot,2019,152:64−69. doi: 10.1016/j.aquabot.2018.11.001
[78] Holaday AS,Bowes G. C4 acid metabolism and dark CO2 fixation in a submersed aquatic macrophyte (Hydrilla verticillata)[J]. Plant Physiol,1980,65 (2):331−335. doi: 10.1104/pp.65.2.331
[79] Wang SN,Li PP,Liao ZY,Wang WW,Chen T,et al. Adaptation of inorganic carbon utilization strategies in submerged and floating leaves of heteroblastic plant Ottelia cordata[J]. Environ Exp Bot,2022,196:104818. doi: 10.1016/j.envexpbot.2022.104818
[80] Cao Y,Liu Y,Ndirangu L,Li W,Xian L,Jiang HS. The analysis of leaf traits of eight Ottelia populations and their potential ecosystem functions in karst freshwaters in China[J]. Front Plant Sci,2019,9:1938. doi: 10.3389/fpls.2018.01938
[81] Liao ZY,Li PP,Zhou JZ,Li W,Jiang HS. Different photosynthetic inorganic carbon utilization strategies in the heteroblastic leaves of an aquatic plant Ottelia ovalifolia[J]. Front Plant Sci,2023,14:1142848. doi: 10.3389/fpls.2023.1142848
[82] Prins HBA,de Guia MB. Carbon source of the water soldier,Stratiotes aloides L.[J]. Aquat Bot,1986,26:225−234. doi: 10.1016/0304-3770(86)90023-9
[83] Beer S,Waisel Y. Some photosynthetic carbon fixation properties of seagrasses[J]. Aquat Bot,1979,7:129−138. doi: 10.1016/0304-3770(79)90017-2
[84] Benedict CR,Scott JR. Photosynthetic carbon metabolism of a marine grass[J]. Plant Physiol,1976,57 (6):876−880. doi: 10.1104/pp.57.6.876
[85] Von Caemmerer S,Quick WP,Furbank RT. The development of C4 rice:current progress and future challenges[J]. Science,2012,336 (6089):1671−1672. doi: 10.1126/science.1220177
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