2022, Vol. 46
文章信息
- 卢科宇, 裴炎沼, 何晴, 周斌. 2022.
- LU Ke-yu, PEI Yan-zhao, HE Qing, ZHOU Bin. 2022.
- 海草抗氧化系统及其对逆境胁迫的响应特征
- Research progress on the antioxidant system of seagrass and its response to stress
- 海洋科学, 46(8): 171-185
- Marina Sciences, 46(8): 171-185.
- http://dx.doi.org/10.11759/hykx20211221002
-
文章历史
- 收稿日期：2021-12-21
- 修回日期：2022-05-19
2. 青岛海洋科学与技术试点国家实验室, 山东 青岛 266237
2. Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China
海草是地球上唯一能够完全在海水中生活的被子植物, 起源于陆生高等植物, 经演化而适应海洋环境[1-3], 具有重要的进化地位[4]。海草经历了海洋-陆地-海洋的演化进程, 具有区别于陆生高等植物和大型海洋藻类的独特生理特征。鳗草(Zostera marina)和牟氏鳗草(Zostera muelleri)全基因组测序结果揭示了海草基因组具有区别于陆生高等植物的诸多特性, 如细胞壁组分基因变化、气孔基因缺失、萜类物质合成与乙烯信号转导基因缺失、紫外线防护与远红外线感受基因缺失、抗氧化系统基因收缩等, 提示海草具有不同于陆生高等植物的特殊逆境响应机制[5-6]。
植物抗氧化系统兼具响应逆境胁迫和调控活性氧信号传导的双重功能, 对其进行研究有助于全面理解植物的逆境响应过程和机制。绿色植物进行有氧代谢时产生的副产物活性氧(reactive oxygen species, ROS), 包括超氧阴离子(O2·–)、过氧化氢(H2O2)、单态氧(1O2)和羟基自由基(·OH), 能够对植物体产生氧化损伤[7-9], 而植物也进化出了精细的抗氧化机制清除活性氧[9-10]。正常情况下, 植物体内的抗氧化系统能够及时清除过量ROS[9-11]; 在逆境胁迫下, 植物体内ROS生成速度加快, 抗氧化系统清除能力相对不足, ROS的动态平衡被打破而导致累积。累积的ROS在造成氧化应激和产生氧化伤害的同时, 也参与多种信息传递过程, 激活植物抗逆响应机制[9-17]。对于不同的逆境胁迫, 植物生成ROS的位点与种类存在差异, 而抗氧化系统本身的响应方式、程度和组分也有所区别[7, 9, 15]。
近年来, 对陆生高等植物和藻类抗氧化系统及其逆境响应已经开展了较多研究[8, 18-19], 并取得了系统性的成果[20-24]。与陆生高等植物相比, 海草由陆地到海洋的进化历程使其在适应过程中产生了独特的生理特点和抗逆机制。同时, 海草能够提供众多生态系统服务, 具有重要的生态价值[25-29]。其独特性与重要性促使人们对海草这一重要植物类群的抗氧化系统及其逆境响应机制进行深入研究。
1 海草抗氧化系统的组成及其基因分类海草抗氧化系统包括酶促和非酶促清除系统[30], 主要包括抗氧化酶类、非酶抗氧化物以及由二者共同组成的一些循环系统如: 抗坏血酸-谷胱甘肽循环、谷胱甘肽过氧化物酶循环、过氧化氢酶循环以及硫氧还蛋白还原酶系统和甲硫氨酸亚砜还原酶系统等[10, 30](图 1)。主要抗氧化酶有超氧化物歧化酶(superoxide dismutase, SOD)、过氧化氢酶(catalase, CAT)、抗坏血酸过氧化物酶(ascorbate peroxidase, APX)和谷胱甘肽过氧化物酶(glutathione peroxidase, GPX)等。非酶抗氧化物包括β-胡萝卜素、维生素A、α-生育酚(维生素E)、抗坏血酸(维生素C)、谷胱甘肽、黄酮类化合物, 以及某些渗透调节物质, 如脯氨酸、甘露醇等[31-32]。目前对于海草抗氧化系统的研究多集中于主要酶促反应, 对于上游转录因子和基因的研究较少。
 |
| 图 1 海草抗氧化系统组成图[7-10, 13, 24, 30, 33-37] Fig. 1 Schematic of the main antioxidant system in seagrass[7-10, 13, 24, 30, 33-37] 注: O2·–: 超氧阴离子; H2O2: 过氧化氢; 1O2: 单态氧; ·OH: 羟基自由基; SOD: 超氧化物歧化酶; APX: 抗坏血酸过氧化物酶; GPX: 谷胱甘肽过氧化物酶; CAT: 过氧化氢酶; AsA, s: 抗坏血酸; GSH: 谷胱甘肽; (M)DHA: (单)脱氢抗坏血酸; GSSG: 氧化型谷胱甘肽; (M)DHAR: (单)脱氢抗坏血酸还原酶; GR: 谷胱甘肽还原酶; PUFA: 多不饱和脂肪酸; Met: 甲硫氨酸; MetO: 甲硫氨酸亚砜; MSR: 甲硫氨酸亚砜还原酶; 2-Cys Prx: 2-半胱氨酸过氧化物还蛋白; NTRC: NADPH依赖的硫氧还蛋白还原酶C; FTR: 铁氧还蛋白依赖的硫氧还蛋白还原酶。亮色箭头代表氧化过程, 相应暗色箭头代表还原过程, 红色方框表示ROS, 红色箭头表示ROS的清除路径; AsA和GSH是参与酶促抗氧化系统的两种重要非酶抗氧化物。 |
SOD、CAT、APX和GPX等关键酶是海草体内应对逆境胁迫的重要防卫系统(图 1)。SOD作为抗氧化系统中的第一道防线, 将难以直接清除的O2·–歧化为H2O2, CAT、APX和GPX则将H2O2转化为H2O(图 1)[7, 9, 33-37]。其中APX通过催化抗坏血酸(ascorbic acid, AsA)与H2O2的反应参与到抗坏血酸-谷胱甘肽循环中, 其氧化产物单脱氢抗坏血酸(monodehydroascorbic acid, MDHA)与脱氢抗坏血酸(dehydroascorbic acid, DHA)能够通过相应的单脱氢抗坏血酸还原酶(MDHAR)和脱氢抗坏血酸还原酶(DHAR)还原为AsA, 从而维持这一重要非酶抗氧化物的浓度[7, 9, 13, 35]。而另一种重要的非酶抗氧化物谷胱甘肽(GSH)作为还原剂参加了DHA的还原反应。类似地, GPX催化GSH清除H2O2产生的氧化态谷胱甘肽(GSSG)也能通过谷胱甘肽还原酶(GR)再生GSH。这两种主要非酶抗氧化物除了通过酶促反应清除H2O2外, 还能够参与清除其他三种ROS[7-10, 24, 38-39]。重要的抗氧化酶还包括谷胱甘肽S-转移酶(glutathione S-transferase, GST)和过氧化物酶(peroxidase, POD)等[34, 37, 40-42]。
另外, 硫氧还蛋白/硫氧还蛋白还原酶系统和甲硫氨酸亚砜/甲硫氨酸亚砜还原酶系统也是植物体内应对氧化胁迫的重要途径(图 1)[43]。在逆境胁迫下产生的过量ROS除了对肽主链造成一般的氧化损伤外, 一些含硫氨基酸侧链的功能和结构也可能会在氧化应激过程中被特定的修饰所改变。如甲硫氨酸(Met)和半胱氨酸(Cys)其侧链中含有一个硫原子, 是最容易被氧化的氨基酸[44]。Met和Cys的氧化损伤可分别由甲硫氨酸亚砜还原酶(methionine sulfoxide reductase, MSR)系统和硫氧还蛋白还原酶(thioredoxin reductase, TrxR)系统修复, ROS则在蛋白质修复的过程中被清除。其中Met被过量ROS和H2O2氧化形成的甲硫氨酸亚砜(MetO)可以通过MSR还原为Met[45-47]。因此MetO的形成是氧化损伤的标志之一, 该损伤可由MSRs控制或逆转[44]; 而TrxR系统是由一系列蛋白质组成: 硫氧还蛋白(Trx)、过氧化物氧还蛋白(Prx)和硫氧还蛋白还原酶(TrxR)。这些蛋白与还原性烟酰胺腺嘌呤二核苷酸磷酸(NADPH)相互作用, 作为辅因子清除H2O2或其他ROS[48-49]。
单态氧和羟基自由基的清除主要依靠非酶抗氧化物(图 1)。除GSH和AsA外, 还包括类胡萝卜素、生育酚、黄酮类化合物和脯氨酸等。这些非酶抗氧化物都能够清除单态氧, 多酚类化合物和脯氨酸还能够参与清除羟基自由基[7-10, 14, 50-51]。其中生育酚还能参与清除超氧化物, 并通过GSH和AsA的作用再生, 表明抗氧化物之间存在协作关系[7-8, 10, 13, 24, 52]。由于抗氧化系统的各个组分能够清除的活性氧种类存在差异, 而且存在的位点也有区别(例如生育酚、类胡萝卜素和CAT的主要存在位点分别在细胞膜、叶绿体和过氧化物酶体), 所以除了浓度以外, 各组分之间比例的变化也将影响活性氧的清除效果以及海草整体上对逆境胁迫的响应[9, 14, 53]。总体而言, 抗氧化物基因的过表达能够提高抗逆性, 且多种抗氧化酶基因同时过表达能够起到相互协同的作用[10]。
控制海草抗氧化系统关键酶和非酶抗氧化物基因的上游核转录因子调控过程也是氧化应激的重要控制环节, 影响抗氧化系统相关基因的转录。在正常生理状态下这些转录因子在胞质内与各自的抑制蛋白结合为复合体而呈现非活性状态。当受到胁迫时, 复合体会被氧化剂等物质激活而解离, 转录因子被转移入核内诱导含有特异启动子(如抗氧化元件antioxidant response element, ARE)的基因转录, 调控氧化应激。这些信号通路主要有Nrf2-Keap1信号通路、NF-кB信号通路等, 但在海草等水生高等植物中研究较少[54-61]。
其中核因子E2相关因子2(Nrf2)是抗氧化系统的关键调节因子。Nrf2-Keap1信号通路主要由转录因子NF-E2相关因子2(Nrf2)及其伴侣分子Keap1组成。Nrf2/Keap1系统通过与抗氧化反应元件(ARE)相互作用, 调控一系列解毒酶和抗氧化酶基因的表达来维持机体氧化还原的平衡状态[54]。例如Nrf2控制谷胱甘肽生物合成的限速步骤也控制谷胱甘肽过氧化物酶2和还原酶1的表达, 从而影响抗坏血酸-谷胱甘肽循环[62]; Nrf2也能影响控制胞质硫氧还蛋白1(TXN1)[63]、硫氧还蛋白还原酶1(TXNRD1)[64-67]和硫氧还蛋白1(SRXN1)[68]的表达, 并且调控体内产生NADPH的各个途径, 从而对抗氧化系统进行调控[69-72]。在非应激条件下, Keap1是E3泛素连接酶复合物的氧化还原调控底物接头, 其结合Nrf2形成Nrf2-Keap1复合物, 从而抑制Nrf2的活性并持续引导NRF2降解以确保Nrf2以较低浓度存在, 并将Nrf2限制在细胞质中[55-57]。当细胞暴露于氧化胁迫时, Keap1上的高活性半胱氨酸基团被过量ROS氧化使其构象产生变化, Keap1被亲电子分子修饰后, 阻止其靶向蛋白Nrf2的降解, 复合体释放Nrf2并将其转运到细胞核中, 从而使Nrf2在氧化胁迫下在细胞核中快速积累, 诱导含有抗氧化元件ARE的基因转录[58-60]。拥有ARE的基因编码形成合作酶网络, Nrf2可通过转录网络调控抗氧化系统以应对外界胁迫[61]。
目前在基因水平对海草抗氧化系统的研究相对较少。由于仅有鳗草和牟氏鳗草完成了全基因组测序, 因此本文以北半球代表性海草鳗草为代表, 根据鳗草全基因组测序结果等研究成果, 对鳗草抗氧化酶基因进行了分类注释。根据抗氧化酶参与ROS清除的不同作用, 将相关酶分为3类进行注释, 分别为: 直接清除ROS的抗氧化酶(表 1)、参与清除ROS的蛋白和酶(表 2)、催化抗氧化剂再生的酶(表 3)[6]。
| 相关酶及涉及的反应过程 | 基因名称 | 基因代码 |
| Superoxide dismutase(SOD) | ZMFeSOD | Zosma106g00140 |
| O2–+ O2–+2H+→ H2O2+O2 | ZMFeSOD | Zosma1306g00070 |
| ZMCu/ZnSOD | Zosma72g00490 | |
| ZMCu/ZnSOD | Zosma5g01030 | |
| ZMCu/ZnSOD | Zosma16g01180 | |
| ZMMnSOD | Zosma270g00070 | |
| ZMSOD | Zosma6583g00010 | |
| ZMSOD | Zosma12595g00010 | |
| ZMSOD | Zosma12509g00010 | |
| ZMSOD | Zosma10604g00020 | |
| Ascorbate peroxidase(APX) | ZMAPX | Zosma21g01150 |
| 2Asc+ H2O2→2MDA+2H2O | ZMAPX | Zosma230g00360 |
| ZMAPX1 | Zosma123g00790 | |
| ZML-APX3 | Zosma1g02970 | |
| ZML-APX6 | Zosma4g01780 | |
| ZMStromal-APX | Zosma182g00510 | |
| Catalase(CAT) | ZMCAT | Zosma11924g00010 |
| 2H2O2→2H2O+O2 | ZMCAT | Zosma9250g00010 |
| ZMCAT | Zosma228g00030 | |
| Glutathione peroxidase(GPx) | ZMGPx1 | Zosma180g00060 |
| H2O2+2GSH→2 H2O+GSSG | ZMGPx5 | Zosma44g01480 |
| ZMGPx | Zosma533g00130 | |
| ZMGPx | Zosma269g00080 | |
| ZMGPx | Zosma41g01010 | |
| Peroxiredoxin(PrxR) | ZMPrxR | Zosma12201g00010 |
| 2P-SH+H2O2→P-S-S-P+2H2O | ZMPrxR | Zosma12323g00010 |
| ZMPrxR | Zosma12946g00010 | |
| ZMPrxR | Zosma13231g00010 | |
| ZMPrxR | Zosma161g00470 | |
| ZMPrxR | Zosma1861g00010 | |
| ZMPrxR | Zosma2227g00010 | |
| ZMPrxR | Zosma6632g00010 | |
| ZMPrxR-2F | Zosma16g01570 | |
| ZMPrxR Q | Zosma176g00240 | |
| ZM1-Cys PrxR | Zosma44g00080 | |
| ZM1-Cys PrxR | Zosma44g00090 | |
| ZM2-Cys PrxR | Zosma2g03310 |
| 相关酶及涉及的反应过程 | 基因名称 | 基因代码 |
| Ferritin | ZMFerritin | Zosma105g00360 |
| Fe+P→P-Fe | ZMFerritin | Zosma105g00430 |
| ZMFerritin | Zosma175g00320 | |
| Blue Copper Protein | ZM Blue copper protein | Zosma75g00400 |
| Cu+P→P-Cu | ||
| Alternative Oxidase(AOX) | ZMAOX1 | Zosma120g00200 |
| 2e- +H++O2→H2O | ||
| Thioredoxin(Trx) | ZMTrx | Zosma10352g00020 |
| P-S-S-P→P-SH | ZMTrx | Zosma110g00370 |
| ZMTrx | Zosma125g00410 | |
| ZMTrx | Zosma194g00220 | |
| ZMTrx | Zosma42g00310 | |
| ZMTrx family | Zosma161g00120 | |
| ZMTrx h1 | Zosma4g00450 | |
| ZMTrx H-type | Zosma74g00380 | |
| ZMTrx H-type 1 | Zosma632g00030 | |
| ZTrx M3 | Zosma41g01280 | |
| ZMTrx O1 | Zosma189g00190 | |
| ZMTrx Y | Zosma373g00110 | |
| ZMTrx-like HCF164 | Zosma49g00620 | |
| ZMTrx-like 1-1 | Zosma53g00120 | |
| ZMTrx-like 3 | Zosma330g00090 | |
| ZMTrx-like 4B | Zosma125g00410 | |
| ZMTrx-like AAED1 | Zosma207g00240 | |
| ZMm-typeTrx1 | Zosma15g01700 |
| 相关酶及涉及的反应过程 | 基因名称 | 基因代码 |
| Monodehydroascorbate Reductase(MDHAR) | ZMMDHAR | Zosma1159g00010 |
| MDA+NAD(P)H+H+→ASC+NAD(P)– | ZMMDHAR | Zosma153g00080 |
| Dehydroascorbate Reductase(DHAR) | ZMDHAR | Zosma64g00760 |
| DHA+2GSH→ASC+GSSG | ZMDHAR | Zosma243g00090 |
| ZMDHAR | Zosma3g01440 | |
| Glutathione Reductase (GR) | ZMGR | Zosma206g00070 |
| GSSG+NAD(P)H→2GSH+NAD(P) | ZMGR1 | Zosma82g00060 |
| Glutaredoxin (GLR) | ZMGLR | Zosma175g00390 |
| DHASc+2GSH→ASC+GSSG | ZMGLR | Zosma1861g00010 |
| ZMGLR | Zosma6177g00030 | |
| ZMGLR | Zosma8720g00010 | |
| ZMGLR family | Zosma8g00210 | |
| ZMGLR family | Zosma27g00500 | |
| ZMGLR family | Zosma315g00080 | |
| ZMGLR family | Zosma400g00060 | |
| ZMGLR family | Zosma400g00070 | |
| ZMGLR family | Zosma400g00080 | |
| ZMGLR family | Zosma64g00630 |
全球变暖导致的高温胁迫是海草面临的主要环境问题之一。高温胁迫能够影响海草的光合作用与呼吸进程, 影响其生长和代谢平衡, 并导致海草体内ROS过量生成和累积而引起氧化损伤[73-78]。具体表现为在高温胁迫下海草的光合酶系统受到损伤, 最终呼吸作用会大于光合作用, 导致消耗的O2增加以及ROS的生成增加, 并且海水温度升高可以直接抑制海草体内抗氧化酶(如GST)的活性, 从而削弱抗氧化系统清除ROS的能力。因此, 过量的ROS在植物体内累积, 能够影响正常的生理过程, 造成氧化损伤[79-80]。鳗草、大洋波喜荡草(Posidonia oceanica)、小丝粉草(Cymodocea nodosa)、泰来草(Thalassia hemprichii)等均通过增加抗氧化酶的含量或提高抗氧化酶的活性来应对高温胁迫, 但参与响应的抗氧化酶种类、响应程度和速度等受到海草种类、生境、胁迫强度与持续时间等诸多因素的影响。大多数情况下, SOD作为抗氧化系统的第一道防线在清除ROS过程中具有重要作用, 比如高温胁迫能够诱导大洋波喜荡草、小丝粉草、泰来草SOD基因表达量显著上调以应对ROS的累积, 避免氧化损伤[34, 74, 80]; 鳗草的SOD基因会在非极端高温诱导时上调表达, 并在一段时间内保持其过表达状态, 同时保持较高的光合能力[81-84]。一定范围内的高温胁迫能够通过激活SOD活性而不是提高基因表达程度来提高活性氧清除能力, 而在极端高温下(≥25 ℃)SOD酶活性急剧下降, 使抗氧化系统的高温胁迫响应能力急剧下降[77, 83]。相对于其他抗氧化酶组分活性受到抑制而逐渐降低、自由基清除能力变弱, SOD的重要性还体现在能够在连续多次的高温胁迫过程中始终保持有效响应[34, 77]。其他种类的抗氧化酶也在海草响应高温胁迫中发挥重要作用, 比如高温能够诱导泰来草和诺氏鳗草CAT和GST基因表达量增高[80, 85], 鳗草中这两种酶的活性也有显著升高[78, 84]。海草抗氧化系统的其他组分对高温胁迫的响应相对于上述几种主要抗氧化酶具有较高的可变性[34], 这种可变性与物种和生境的相关性较高, 总体而言高纬度物种和深水生态型的适应程度低, 其抗氧化系统响应速度慢、强度低, 除主要抗氧化酶外需要更多的抗氧化系统组分参与响应, 且高温胁迫后的恢复较慢[34, 81, 86-87]。可见, 包括温度升高在内的气候变化能够影响海草抗氧化能力等生理过程, 进而改变海草的分布与种群结构[76]; 而基于气候驯化的生态适应对于海草应对高温胁迫具有重要意义。
2.2 对重金属胁迫的响应重金属是影响海草的主要胁迫因素之一[88-92]。重金属的过量累积能够对海草产生严重的生理伤害, 包括抑制生长、降低光合速率等, 同时也能诱导海草体内ROS的过量生成而产生氧化损伤[93-100]。抗氧化系统对于重金属的敏感性可能是由于重金属离子能通过与抗氧化酶的巯基蛋白结合来破坏其结构[94, 98-99], 或是在高浓度下造成严重的细胞损伤, 使与抗氧化系统相关的代谢循环受损而导致整个抗氧化系统的崩溃[94]。海草抗氧化系统对重金属胁迫的响应特征与重金属的种类和浓度有关, 如抗氧化酶基因的表达程度与重金属浓度在一定限度内呈正相关[37, 40, 42]。海草对Cu2+胁迫非常敏感, 在短时间、低浓度的Cu2+胁迫下, 海草能够上调抗氧化酶(GPX、CAT、SOD、GR、APX和GST)和抗氧化剂(GSH)的基因表达来清除额外生成的ROS; 而在长时间或高浓度的Cu2+胁迫下, 抗氧化系统组分的基因表达受到抑制, ROS得不到及时清除而导致氧化损伤[37, 41, 93-94, 100-101]。但是对牟氏鳗草的研究表明, 在低浓度Cu2+胁迫下并不响应的POD与GST基因随着Cu2+浓度的升高而出现过表达[98]。
对于其他重金属(Fe、Mn、Zn、Cd、Cr、Pb、Hg、Ni)而言, 即使在较高浓度下, 海草抗氧化系统的相关组分也能通过基因上调表达来提高ROS清除能力[41, 46]。其中, 海草对Cd2+的耐受能力最强, 例如大洋波喜荡草只有受到高浓度Cd2+胁迫时才需要提高GST的活性[102]; 鳗草在Cu2+胁迫下会增加GSH的生成量来协助清除ROS, 而即使暴露于高浓度的Cd2+胁迫下, GSH基因的表达也没有显著升高[93]。Greco等认为Cu2+与Cd2+在海草体内的累积是竞争性的, 因此低浓度Cd2+的存在甚至可能会减轻Cu2+对海草的氧化损伤[93]。此外, 乙酰胆碱酯酶(AchE)对重金属也具有高敏感性, 因而被认为通过基因上调表达参与了对重金属胁迫的响应, 并与SOD共同组成第一道防线[42]。
对于纳米金属颗粒胁迫的响应研究主要集中于纳米银微粒, 实验证明其在极低含量下也能导致海草体内ROS过量生成, 而不同种类的海草对其响应程度存在差异。小丝粉草能够通过提高SOD和APX等主要抗氧化酶的活性, 有效防止氧化损伤[103]; 而长萼喜盐草(Halophila stipulacea)只能通过增加SOD的生成来应对氧化胁迫且APX的活性受到抑制, 因此并不能避免脂质过氧化[104-105]。与之相似的, 氧化锌微粒也能导致氧化应激, 引起海草抗氧化系统的响应变化, 但其作用机制尚不明确[106]。
在一定的重金属浓度范围内, 抗氧化系统的活性随着重金属浓度升高而提升, 但这并不一定代表其能够有效地清除额外生成的ROS, 保护植物组织免受氧化损伤。例如, 大洋波喜荡草随着Hg2+胁迫强度的提高不断增加GST和CAT的生成量, 而代表脂质过氧化程度的丙二醛(MDA)含量也在增加, 其在高浓度Hg2+胁迫下通过植物螯合物才能有效降低氧化损伤的程度[44]。不同抗氧化酶对不同重金属的响应程度也不同, 例如日本鳗草SOD的含量及活性在Cd2+胁迫下不发生明显变化, CAT则对Pb2+胁迫无显著响应[37]; 泰来草在受到Zn2+、Cu2+、Cd2+胁迫时, SOD基因的表达受到显著抑制, 而POD则一直保持过表达状态[100]。迄今为止, 重金属对海草抗氧化系统的影响研究仍限于单一重金属对单一海草物种的胁迫和响应, 对多种重金属协同效应的研究较少, 且普遍缺少胁迫的分子机制研究。
2.3 对光胁迫的响应光是海草生产力、分布和丰度的重要决定因素。海草的光合速率低于陆生植物, 具有较低的光补偿点与光饱和点, 可以保证在水下弱光环境中正常生长, 是海草对弱光环境的适应[107-109]。但在近岸海域中, 由于悬浮颗粒增加、附生植物或浮游藻类过度生长而导致的光散射和/或光衰减增加, 可能会进一步削弱海草的可利用光照, 导致海草光合产能不足, 从而影响海草生长繁育[110]。弱光胁迫对海草的影响可能涉及更多的光适应基因, 对抗氧化系统影响较小。长期弱光胁迫使大洋波喜荡草光合作用碳反应关键调节酶Rubisco的基因表达下调, 参与碳水化合物裂解的酶和蛋白水解酶表达上调, 而抗氧化系统CAT、SOD和APX三种抗氧化酶的合成减少, 但未呈现受胁迫状态[110-113]。
相比于光照不足, 海草对强光胁迫更加敏感, 而抗氧化系统作为光保护机制的重要部分, 对海草响应强光胁迫至关重要。生长在潮间带和浅水环境中的海草经常在一天中的部分时间暴露在过饱和光强下, 甚至直接暴露于阳光直晒之下, 这可能会导致强光胁迫。由于海草的光饱和点较低不能充分利用光能, 过剩的光能会导致ROS产生, 破坏海草体内的代谢平衡, 产生光抑制[114]。在强光胁迫下, 海草的光适应相关基因(Rubisco酶、铁氧还蛋白、叶绿素结合蛋白)和光保护相关基因(抗氧化酶、叶黄素循环相关基因、生育酚的生物合成)上调, 表明了抗氧化系统作为防御机制被激活[115]。持续强光胁迫能够激活牟氏鳗草和大洋波喜荡草AsA-GSH循环, 表现为APX、GPX、MDHAR等抗氧化酶和相关基因上调表达, 并显著提高AsA和GSH的合成相关的酶与蛋白的表达量; 同时CAT、POX、GST、生育酚和类黄酮化合物的合成量增加[110, 115]。大洋波喜荡草在强光胁迫下并没有产生光损伤或氧化损伤, 说明抗氧化系统能够起到有效的保护作用[110]。与之不同的是, 卵叶喜盐草(Halophila ovalis)与泰来草作为典型的热带海草, 在强光胁迫下一般不会显著增加ROS生成量或抗氧化系统的活跃程度, 体现了其对热带强光环境的适应性[116]。深水生态型与浅水生态型大洋波喜荡草之间存在的抗逆基因差异, 也说明其对于光胁迫具备足够的适应能力[110]。在不同纬度及深度环境下, 不同生态型海草的抗氧化系统均对光胁迫表现出适应特征, 表明了海草抗氧化系统能够应对光强变化产生的胁迫。
2.4 对其他环境因子胁迫的响应除上述的主要逆境胁迫外, 海草抗氧化系统还会响应其他环境胁迫, 包括附生生物、高盐度、海洋酸化、缺氧及硫化物等。
1) 对附生生物胁迫的响应。有关海草抗氧化系统对附生生物响应的研究主要局限于大洋波喜荡草。附生生物一般附着在海草叶片表面上, 能够导致光照衰减, 降低光合作用, 但是不会导致氧化胁迫。附生生物一般通过直接创伤导致海草体内产生过量ROS, 引起海草体内APX、GPX、CAT、SOD、DHAR和GSH等多种抗氧化组分活性或含量的增加, 抗氧化系统总体清除能力显著提升; 但现有研究认为这种清除能力的提升不足以应对ROS的快速产生和过量累积, 导致氧化胁迫产生, 表现为MDA含量显著增加[115, 117]。不同海草物种对附生生物的响应可能存在差异, 因此需要更多相关研究来完善认识。
2) 对盐胁迫的响应。海草在高或低盐度胁迫下均能激活其抗氧化系统的大部分组分, 包括非酶抗氧化物和与AsA-GSH循环相关的抗氧化酶, 然而由于SOD和CAT这两种主要抗氧化酶的活性受到抑制, 海草还是会受到一定程度的氧化损伤[118-119]。在陆生植物中, 高盐胁迫诱导的氧化应激会导致植物卡尔文循环消耗的NADPH和光合作用固定的CO2减少而影响ASA-GSH循环, 电子可能从PSI转移至O2而形成O2–, 并引发链式反应[120-122]。对海草而言, 在高盐胁迫下其线粒体和叶绿体的相对面积随盐度的增加而增加, 总光合受到抑制, 净光合作用减少[123-124], 表明高盐度胁迫导致了海草光合器官损伤。在光、盐度与营养盐联合胁迫下, 光胁迫成为主导因素。强光胁迫能够促进SOD和POD等抗氧化酶活性提高以应对氧化胁迫[124]。我们推测海草与陆生植物的抗氧化系统具有相同的盐胁迫响应机制, 如黄秋葵(Abelmoschus esculentus)、水稻(Oryza sativa)、大豆植株在盐胁迫下能够诱导CAT、POD等主要抗氧化酶活性增强[121, 125-126]。此外, 有研究表明植物可以通过一种非典型的双特异性蛋白酪氨酸磷酸酶ATPFA- DSP3(DSP3)调节蛋白质磷酸化介导植物抗氧化系统对盐胁迫的响应[127]。
3) 对缺氧及硫化物胁迫的响应。全球变暖及富营养化引起的缺氧现象正成为海洋生态系统的重要威胁[128-130]。缺氧胁迫会显著降低海草的光合作用, 并影响海草的碳/氮代谢, 而海草抗氧化系统在缺氧胁迫下也会被激活以应对ROS产生的危害, 如鳗草在缺氧胁迫下显著上调编码CAT、SOD、POD、GST、MDHAR等抗氧化系统相关酶的基因[128]。缺氧不仅对海草有直接影响, 还会引起硫化物对海草的入侵。海草一般生长在高度还原性的沉积物中, 沉积物中的有机质经过厌氧代谢产生的硫化物在低氧环境下会侵入海草内部, 进而破坏海草的分生组织并抑制海草的光合作用[131]。而目前海草对硫化物胁迫响应的分子机制研究较少, 关于海草抗氧化系统如何应对硫化物胁迫尚不清晰。
4) 对海洋酸化的响应。对海草抗氧化系统而言, 海水中CO2含量(pCO2)升高导致的海洋酸化并非逆境胁迫, 反而能够在一定程度上缓解海草的氧化压力。高pCO2驯化(一般需要持续数月)能够使海草稳态下抗氧化酶和抗氧化物(SOD、CAT、APX、GR和GSH)活性降低, 表明抗氧化系统在相对不活跃的情况下也能有效地阻止氧化损伤, 表明了海草的高pCO2偏好; 而未驯化的海草在低pCO2下抗氧化酶和抗氧化物表达量短期内提高, 在高pCO2下表达下降, 但下降趋势不明显[132]。相关研究一般利用海洋火山口这一自然实验室, 但是其导致的温度变化和排放的其他气体带来了大量的干扰, 例如Lauritano等用同种同源的海草在不同火山口进行培养实验却得出了截然不同的结果[133]; 而Ravaglioli等在证明火山口高不确定性的同时, 还表明营养盐的浓度会显著影响海草抗氧化系统对pCO2变化的响应[134]。由于pH的改变还会影响海草附生生物群落[135], 因此在气候变化及海洋酸化的背景下, 揭示海草抗氧化系统的响应情况需要更多深入全面的研究。
3 展望1) 海草抗氧化系统组分在逆境胁迫下的协同变化和多层次关联分析: 目前对海草抗氧化系统响应逆境胁迫的研究关注于主要抗氧化酶的变化, 往往忽视非酶抗氧化物和参与AsA-GSH循环的其他抗氧化酶。抗氧化系统是复杂的多酶多剂系统, 不同组分之间存在响应差异, 某一种或某几种组分的变化不能全面反映抗氧化系统的总体状态。应当结合基因组、转录组、蛋白质组等多个研究层次的成果, 将抗氧化酶活性变化与基因表达变化关联分析, 综合分析逆境胁迫下抗氧化系统的响应特征及机制, 这是全面开展海草抗逆生理机制研究的重要基础。
2) 不同海草物种抗氧化系统对逆境胁迫的响应差异: 海草抗氧化系统对逆境胁迫的响应存在显著的种间差异, 需要将海草种间差异响应特征与关键差异基因相关联, 进而基于差异基因的功能阐明抗氧化系统响应存在种间差异的原因, 这是揭示海草逆境胁迫耐受性种间差异机制的重要前提。
3) 多个胁迫因子联合作用下海草抗氧化系统的响应特征与机制: 海草抗氧化系统的逆境胁迫响应研究仍局限于少数胁迫因子, 与海草面对的复杂实际环境相距甚远, 需要开展多个胁迫因子联合作用下海草抗氧化系统的响应特征与机制研究, 这是全面分析复杂环境条件下海草逆境响应机制的基础。
| [1] |
黄小平, 江志坚, 范航清, 等. 中国海草的"藻"名更改[J]. 海洋与湖沼, 2016, 47(1): 290-294. HUANG Xiaoping, JIANG Zhijian, FAN Hangqing, et al. The nomenclature of the "algae" name of seagrasses in China[J]. Oceanologia et Limnologia Sinica, 2016, 47(1): 290-294. |
| [2] |
黄小平, 江志坚, 张景平, 等. 全球海草的中文命名[J]. 海洋学报, 2018, 40(4): 127-133. HUANG Xiaoping, JIANG Zhijian, ZHANG Jingping, et al. The Chinese nomenclature of the global seagrasses[J]. Haiyang Xuebao, 2018, 40(4): 127-133. DOI:10.3969/j.issn.0253-4193.2018.04.012 |
| [3] |
林鹏. 海洋高等植物生态学[M]. 北京: 科学出版社, 2006. LIN Peng. Marine higher plant ecology[M]. Beijing: Science Press, 2006. |
| [4] |
ORTH R J, CARRUTHERS T J B, DENNISON W C, et al. A global crisis for seagrass ecosystems[J]. Bioscience, 2006, 56: 987-996. DOI:10.1641/0006-3568(2006)56[987:AGCFSE]2.0.CO;2 |
| [5] |
LEE H T, GOLICZ A A, BAYER P E, et al. The Ge1nome of a southern hemisphere seagrass species (Zostera muelleri)[J]. Plant Physiology, 2016, 172: 272-283. DOI:10.1104/pp.16.00868 |
| [6] |
OLSEN J L, ROUZÉ P, VERHELST B, et al. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea[J]. Nature, 2016, 530: 331-335. DOI:10.1038/nature16548 |
| [7] |
KAUSHIK D, ARYADEEP R. Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants[J]. Frontiers in Environmental Science, 2014, 2: 53-66. |
| [8] |
LESSER M P. Oxidative stress in marine environments: biochemistry and physiological ecology[J]. Annual Review of Physiology, 2006, 68(1): 253-278. DOI:10.1146/annurev.physiol.68.040104.110001 |
| [9] |
APEL K, HIRT H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction[J]. Annual Review of Plant Biology, 2004, 55(1): 373-399. DOI:10.1146/annurev.arplant.55.031903.141701 |
| [10] |
PALLAVI S, BHUSHAN J A, SHANKER D R, et al. Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions[J]. Journal of Botany, 2012, 217037. |
| [11] |
FOYER C H, NOCTOR G. Redox homeostasis and antioxidant signaling: a metabolic interface between stress perception and physiological responses[J]. Plant Cell, 2005, 17: 1866-1875. DOI:10.1105/tpc.105.033589 |
| [12] |
KRESLAVSKI V D, LOS D A, ALLAKHVERDIEV S I, et al. Signaling role of reactive oxygen species in plants under stress[J]. Russian Journal of Plant Physiology, 2012, 59(2): 141-154. DOI:10.1134/S1021443712020057 |
| [13] |
ALSCHER R G, DONAHUE J L, CRAMER C L. Reactive oxygen species and antioxidants: relationships in green cells[J]. Physiologia Plantarum, 1997, 100(2): 224-233. DOI:10.1111/j.1399-3054.1997.tb04778.x |
| [14] |
MITTLER R. Oxidative stress, antioxidants and stress tolerance[J]. Trends in Plant Science, 2002, 7(9): 405-410. DOI:10.1016/S1360-1385(02)02312-9 |
| [15] |
DAT J, VANDENABEELE S, VRANOVA E, et al. Dual action of the active oxygen species during plant stress responses[J]. Cellular and Molecular Life Sciences, 2000, 57(5): 779-795. DOI:10.1007/s000180050041 |
| [16] |
GONG Z Z, XIONG L M, SHI H Z, et al. Plant abiotic stress response and nutrient use efficiency[J]. Science China: Life sciences, 2020, 63(5): 635-674. DOI:10.1007/s11427-020-1683-x |
| [17] |
MITTLER R, VANDERAUWERA S, GOLLERY M, et al. Reactive oxygen gene network of plants[J]. Trends in Plant Science, 2004, 9(10): 490-498. DOI:10.1016/j.tplants.2004.08.009 |
| [18] |
LIVINGSTONE D R. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms[J]. Marine Pollution Bulletin, 2001, 42(8): 656-666. DOI:10.1016/S0025-326X(01)00060-1 |
| [19] |
REGOLI F, GIULIANI M E. Oxidative pathways of chemical toxicity and oxidative stress biomarkers in marine organisms[J]. Marine Environmental Research, 2014, 93: 106-117. DOI:10.1016/j.marenvres.2013.07.006 |
| [20] |
DRING M J. Stress resistance and disease resistance in seaweeds: the role of reactive oxygen metabolism[J]. Advances in Botanical Research, 2005, 43(5): 175-207. |
| [21] |
COLLÉN J, DAVISON I R. Stress tolerance and reactive oxygen metabolism in the intertidal red seaweeds Mastocarpus stellatus and Chondrus crispus[J]. Plant, Cell and Environment, 2010, 22(9): 1143-1151. |
| [22] |
DAVISON I R, PEARSON G A. Stress tolerance in intertidal seaweeds[J]. Journal of Phycology, 1996, 32: 197-211. DOI:10.1111/j.0022-3646.1996.00197.x |
| [23] |
PINTO E, SIGAUD-KUTNER T C S, LEITAO M A S, et al. Heavy metal-induced oxidative stress in algae[J]. Journal of Phycology, 2003, 39(6): 1008-1018. DOI:10.1111/j.0022-3646.2003.02-193.x |
| [24] |
ZHANG R F, TANG D S, LIU F. Alage antioxidant system and its influence on stress[J]. Environmental Science and Management, 2011, 36: 21-25. |
| [25] |
HEMMINGA M A, DUARTE C M. Seagrass ecology[M]. Cambridge: Cambridge University Press, 2000.
|
| [26] |
ALOTAIBI N M, KENYON E J, COOK K J, et al. Low genotypic diversity and long-term ecological decline in a spatially structured seagrass population[J]. Scientific Reports, 2019, 9(1): 18387. DOI:10.1038/s41598-019-54828-1 |
| [27] |
COSTANZ R, D'ARGE R, GROOT R D, et al. The value of the world's ecosystem services and natural capital[J]. Ecological Economics, 1997, 25(1): 3-15. |
| [28] |
BARBIER E B, HACKER S D, KENNEDY C, et al. The value of estuarine and coastal ecosystem services[J]. Ecological Monographs, 2011, 81: 169-193. DOI:10.1890/10-1510.1 |
| [29] |
DUFFY J E. Biodiversity and the functioning of seagrass ecosystems[J]. Marine Ecology Progress Series, 2006, 311: 233-250. DOI:10.3354/meps311233 |
| [30] |
尹永强, 胡建斌, 邓明军. 植物叶片抗氧化系统及其对逆境胁迫的响应研究进展[J]. 中国农学通报, 2007, 23(1): 105-110. YIN Yongqiang, HU Jjianbin, DENG Mingjun. Latest development of antioxidant system and responses to stress in plant leaves[J]. Chinese Agricultural Science Bulletin, 2007, 23(1): 105-110. DOI:10.3969/j.issn.1000-6850.2007.01.025 |
| [31] |
薛鑫, 张芊, 吴金霞. 植物体内活性氧的研究及其在植物抗逆方面的应用[J]. 生物技术通报, 2013(10): 6-11. XUE Xin, ZHANG Qian, WU Jinxia. Research of reactive oxygen species in plants and its application on stress tolerance[J]. Biotechnology Bulletin, 2013(10): 6-11. DOI:10.13560/j.cnki.biotech.bull.1985.2013.10.033 |
| [32] |
杨舒贻, 陈晓阳, 惠文凯, 等. 逆境胁迫下植物抗氧化酶系统响应研究进展[J]. 福建农林大学学报(自然科学版), 2016, 45(5): 481-489. YANG Shuyi, CHEN Xiaoyang, HUI Wenkai, et al. Progress in responses of antioxidant enzyme systems in plant to environmental stresses[J]. Journal of Fujian Agriculture and Forestry University (Nature Science Edition), 2016, 45(5): 481-489. DOI:10.13323/j.cnki.j.fafu(nat.sci.).2016.05.001 |
| [33] |
FRIDOVICH I. Superoxide anion radical (O2·–), superoxide dismutases, and related matters[J]. Journal of Biological Chemistry, 1997, 272(30): 18515-18517. DOI:10.1074/jbc.272.30.18515 |
| [34] |
TUTAR O, MARIN-GUIRAO L, RUIZ J M, et al. Antioxidant response to heat stress in seagrasses. A gene expression study[J]. Marine Environmental Research, 2017, 132: 94-102. DOI:10.1016/j.marenvres.2017.10.011 |
| [35] |
FOYER C H, NOCTOR G. Ascorbate and glutathione: the heart of the redox hub[J]. Plant Physiology, 2011, 155(1): 2-18. DOI:10.1104/pp.110.167569 |
| [36] |
ZANG Yu, CHEN Jun, LI Ruoxi, et al. Genome-wide analysis of the superoxide dismutase (SOD) gene family in Zostera marina and expression profile analysis under temperature stress[J]. PeerJ, 2020, 8(4): e9063. DOI:10.7717/peerj.9063 |
| [37] |
LIN H, SUN T, ZHOU Y, et al. Anti-oxidative feedback and biomarkers in the intertidal seagrass Zostera japonica induced by exposure to copper, lead and cadmium[J]. Marine Pollution Bulletin, 2016, 109(1): 325-333. DOI:10.1016/j.marpolbul.2016.05.062 |
| [38] |
JACOB S, DIETZ K J. Systematic analysis of superoxide‐dependent signaling in plant cells: usefulness and specificity of methyl viologen application[C]//HIRT H. Plant stress biology: from genomics to systems biology. Weinheim, Germany: Wiley‐VCH Verlag GmbH & Co. KGaA, 2009, 10: 179-196.
|
| [39] |
SMIRNOFF N. Ascorbate biosynthesis and function in photoprotection[J]. Philosophical Transactions of The Royal Society B Biological Sciences, 2000, 355(1402): 1455-1464. DOI:10.1098/rstb.2000.0706 |
| [40] |
FERRAT L, ROMÉO M, GNASSIA-BARELLI M, et al. Effects of mercury on antioxidant mechanisms in the marine phanerogam Posidonia oceanica[J]. Diseases of Aquatic Organisms, 2002, 50(2): 157. |
| [41] |
BERTINI L, FOCARACCI F, PROIETTI S, et al. Physiological response of Posidonia oceanica to heavy metal pollution along the Tyrrhenian coast[J]. Functional Plant Biology, 2019, 46(10): 933-941. DOI:10.1071/FP18303 |
| [42] |
ALJAHDALI M O, ALHASSAN A B. Heavy metal accumulation and anti-oxidative feedback as a biomarker in seagrass Cymodocea serrulata[J]. Sustainability, 2020, 12(7): 2841. DOI:10.3390/su12072841 |
| [43] |
VOGT W. Oxidation of methionyl residues in proteins: tools, targets, and reversal[J]. Free Radical Biology and Medicine, 1995, 18(1): 93-105. DOI:10.1016/0891-5849(94)00158-G |
| [44] |
CHATELAIN E, SATOUR P, LAUGIER E, et al. Evidence for participation of the methionine sulfoxide reductase repair system in plant seed longevity[J]. Proceedings of the National Academy of Sciences, USA, 2013, 110(9): 3633-3638. DOI:10.1073/pnas.1220589110 |
| [45] |
ABRAMS W R, WEINBAUM G, WEISSBACH L, et al. Enzymatic reduction of oxidized alpha-1-proteinase inhibitor restores biological activity[J]. Proceedings of the National Academy of Sciences of the United States of America, 1981, 78(12): 7483-7486. DOI:10.1073/pnas.78.12.7483 |
| [46] |
MOSKOVITZ J, RAHMAN M, STRASSMAN J, et al. Escherichia coli peptide methionine sulfoxide reductase gene: regulation of expression and role in protecting against oxidative damage[J]. Journal of Bacteriology, 1995, 177(3): 502-507. DOI:10.1128/jb.177.3.502-507.1995 |
| [47] |
SADANANDOM A, PIFFANELLI P, KNOTT T, et al. Identification of a peptide methionine sulphoxide reductase gene in an oleosin promoter from Brassica napus[J]. Plant Journal for Cell & Molecular Biology, 2010, 10(2): 235-242. |
| [48] |
DIETZ K J, JACOB S, OELZA M L, et al. The function of peroxiredoxins in plant organelle redox metabolism[J]. Journal of Experimental Botany, 2006, 57(8): 1697-1709. DOI:10.1093/jxb/erj160 |
| [49] |
PANNALA V R, DASH R K. Mechanistic characterization of the thioredoxin system in the removal of hydrogen peroxide[J]. Free Radical Biology and Medicine, 2015, 78(1): 42-55. |
| [50] |
MØLLER I M, JENSEN P E, HASSON A. Oxidative modifications to cellular components in plants[J]. Annual Review of Plant Biology, 2007, 58: 459-481. DOI:10.1146/annurev.arplant.58.032806.103946 |
| [51] |
ASADA K. Production and scavenging of reactive oxygen species in chloroplasts and their functions[J]. Plant Physiology, 2006, 141(2): 391-396. DOI:10.1104/pp.106.082040 |
| [52] |
FRYER M J. The antioxidant effects of thylakoid Vitamin E (α-tocopherol)[J]. Plant Cell and Environment, 2010, 15(4): 381-392. |
| [53] |
CREISSEN G. Elevated glutathione biosynthetic capacity in the chloroplasts of transgenic tobacco plants paradoxically causes increased oxidative stress[J]. The Plant Cell, 1999, 11(7): 1277-1292. DOI:10.1105/tpc.11.7.1277 |
| [54] |
覃思, 侯德兴. 植物化学物质的生物功能及其在家畜中的应用研究——以Nrf2/Keap1系统为目标[J]. Engineering, 2017, 3(5): 351-381. QIN Si, HOU Dexing. The biofunctions of phytochemicals and their applications in farm animals: the Nrf2/ Keap1 system as a target[J]. Engineering, 2017, 3(5): 351-381. |
| [55] |
CUADRADO A, ROJO A I, WELLS G, et al. Therapeutic targeting of the NRF2 and KEAP1 partnership in chronic diseases[J]. Nature Reviews Drug Discovery, 2019, 18(4): 295-317. DOI:10.1038/s41573-018-0008-x |
| [56] |
KOBAYASHI A, KANG M I, OKAWA H, et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-Based E3 ligase to regulate proteasomal degradation of Nrf2[J]. Molecular and Cellular Biology, 2004, 24(16): 7130-7139. DOI:10.1128/MCB.24.16.7130-7139.2004 |
| [57] |
ZHANG D D, LO S C, CROSS J V, et al. Keap1 is a redox-regulated substrate adaptor protein for a Cul3- dependent ubiquitin ligase complex[J]. Molecular and Cellular Biology, 2004, 24(24): 10941-10953. DOI:10.1128/MCB.24.24.10941-10953.2004 |
| [58] |
ITOH K, CHIBA T, TAKAHASHI S, et al. An Nrf2/ small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements[J]. Biochemical and Biophysical Research Communications, 1997, 236(2): 313-322. DOI:10.1006/bbrc.1997.6943 |
| [59] |
CUADRADO A, MANDA G, HASSAN A, et al. Transcription factor NRF2 as a therapeutic target for chronic diseases: A systems medicine approach[J]. Pharma cological Reviews, 2018, 70(2): 348-383. |
| [60] |
MASAYUKI Y, KENSLER T W, HOZUMI M. The KEAP1-NRF2 system: a thiol-based sensor-effector apparatus for maintaining redox homeostasis[J]. Physio logical Reviews, 2018, 98(3): 1169-1203. |
| [61] |
HAYES J D, DINKOVA-KOSTOVA A T. The Nrf2 regulatory network provides an interface between redox and intermediary metabolism[J]. Trends in Biochemical Sciences, 2014, 39(4): 199-218. DOI:10.1016/j.tibs.2014.02.002 |
| [62] |
HIGGINS L G, KELLEHER M O, EGGLESTON I M, et al. Transcription factor Nrf2 mediates an adaptive response to sulforaphane that protects fibroblasts in vitro against the cytotoxic effects of electrophiles, peroxides and redox-cycling agents[J]. Toxicology and App lied Pharmacology, 2009, 237(3): 267-280. DOI:10.1016/j.taap.2009.03.005 |
| [63] |
HAWKES H, KARLENIUS T C, TONISSEN K F. Regulation of the human thioredoxin gene promoter and its key substrates: a study of functional and putative regulatory elements[J]. Biochimica et Biophysica Acta (BBA) - General Subjects, 2014, 1840(1): 303-314. DOI:10.1016/j.bbagen.2013.09.013 |
| [64] |
KENNETH M L A, MICHAEL M M, PLUMMER S M, et al. Characterization of the cancer chemopreventive NRF2-dependent gene battery in human keratinocytes: demonstration that the KEAP1–NRF2 pathway, and not the BACH1–NRF2 pathway, controls cytoprotection against electrophiles as well as redox-cycling compoun[J]. Carcinogenesis, 2009, 30(9): 1571-1580. DOI:10.1093/carcin/bgp176 |
| [65] |
DEEPTI M, ELODIE P C, ANJU S, et al. Global mapping of binding sites for Nrf2 identifies novel targets in cell survival response through ChIP-Seq profiling and network analysis[J]. Nucleic Acids Research, 2010, 38(17): 5718-5734. DOI:10.1093/nar/gkq212 |
| [66] |
AGYEMAN A S, CHAERKADY R, SHAW P G, et al. Transcriptomic and proteomic profiling of KEAP1 disrupted and sulforaphane-treated human breast epithelial cells reveals common expression profiles[J]. Breast Can cer Research and Treatment, 2012, 132(1): 175-187. DOI:10.1007/s10549-011-1536-9 |
| [67] |
ABBAS K, BRETON J, PLANSON A G, et al. Nitric oxide activates an Nrf2/sulfiredoxin antioxidant pathway in macrophages[J]. Free Radical Biology and Medicine, 2011, 51(1): 107-114. DOI:10.1016/j.freeradbiomed.2011.03.039 |
| [68] |
JEONG W, BAE S H, TOLEDANO M B, et al. Role of sulfiredoxin as a regulator of peroxiredoxin function and regulation of its expression[J]. Free Radical Biology and Medicine, 2012, 53(3): 447-456. DOI:10.1016/j.freeradbiomed.2012.05.020 |
| [69] |
THIMMULAPPA R K, MAI K H, SRISUMA S, et al. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray[J]. Cancer Research, 2002, 62(62): 5196-5203. |
| [70] |
LEE J M, CALKINS M J, CHAN K, et al. Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis[J]. Journal of Biological Chemistry, 2003, 278(14): 12029-12038. DOI:10.1074/jbc.M211558200 |
| [71] |
WU K C, CUI J Y, KLAASSEN C D. Beneficial role of Nrf2 in regulating NADPH generation and consumption[J]. Toxicological Sciences, 2011, 123(2): 590-600. DOI:10.1093/toxsci/kfr183 |
| [72] |
MITSUISHI Y, TAGUCHI K, KAWATANI Y, et al. Nrf2 redirects glucose and glutamine into anabolic pathways in metabolic reprogramming[J]. Cancer Cell, 2012, 22(1): 66-79. DOI:10.1016/j.ccr.2012.05.016 |
| [73] |
MARÍN-GUIRAO L, RUIZ J M, DATTOLO E, et al. Physiological and molecular evidence of differential short-term heat tolerance in Mediterranean seagrasses[J]. Scientific Reports, 2016, 6(1): 28615. DOI:10.1038/srep28615 |
| [74] |
MARÍN-GUIRAO L, ENTRAMBASAGUAS L, DATTOLO E, et al. Molecular mechanisms behind the physiological resistance to intense transient warming in an iconic marine plant[J]. Frontiers in Plant Science, 2017, 8(8): 1142-1157. |
| [75] |
LEE K S, SANG R P, KIM Y K. Effects of irradiance, temperature, and nutrients on growth dynamics of seagrasses: A review[J]. Journal of Experimental Marine Biology and Ecology, 2007, 350(1): 144-175. |
| [76] |
SHORT F T, NECKLES H A. The effects of global climate change on seagrasses[J]. Aquatic Botany, 1999, 63(3/4): 169-196. |
| [77] |
LIU J, TANG X X, WANG Y, et al. A Zostera marina manganese superoxide dismutase gene involved in the responses to temperature stress[J]. Gene, 2016, 575(2): 718-724. DOI:10.1016/j.gene.2015.09.050 |
| [78] |
YAN W J, LIU J, SENG S, et al. Cloning, characterization and expression analysis of a microsomal glutathione S-transferase gene from the seagrass Zostera marina[J]. Acta Oceanologica Sinica, 2019, 38(10): 115-119. |
| [79] |
AN M I, CHOI C Y. Activity of antioxidant enzymes and physiological responses in ark shell, Scapharca broughtonii, exposed to thermal and osmotic stress: effects on hemolymph and biochemical parameters[J]. Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology, 2010, 155(1): 34-42. DOI:10.1016/j.cbpb.2009.09.008 |
| [80] |
RAKHMAD P, HARIYANTO S, SRI Y, et al. Gene expression of antioxidant enzymes and heat shock proteins in tropical seagrass Thalassia hemprichii under heat stress[J]. Taiwania, 2019, 64(2): 117-123. |
| [81] |
WINTERS G, NELLE P, FRICKE B, et al. Effects of a simulated heat wave on photophysiology and gene expression of high- and low-latitude populations of Zostera marina[J]. Marine Ecology Progress, 2011, 435: 83-95. DOI:10.3354/meps09213 |
| [82] |
GUPTA A S, HEINEN J L, HOLADAY A S, et al. Increased resistance to oxidative stress in transgenic plants that overexpress chloroplastic Cu/Zn superoxide dismutase[J]. Proceedings of the National Academy of Sciences, 1993, 90(4): 1629-1633. DOI:10.1073/pnas.90.4.1629 |
| [83] |
ZANG Y, CHEN J, LI R X, et al. Genome-wide analysis of the superoxide dismutase (SOD) gene family in Zostera marina and expression profile analysis under temperature stress[J]. PeerJ, 2020, 8(4): e9063. |
| [84] |
ZANG Y, LIU J, TANG X X, et al. Description of a Zostera marina catalase gene involved in responses to temperature stress[J]. PeerJ, 2018, 6(3): e4532. |
| [85] |
MASSA S I, PEARSON G A, AIRES T, et al. Expressed sequence tags from heat-shocked seagrass Zostera noltii (Hornemann) from its southern distribution range[J]. Marine Genomics, 2011, 4(3): 181-188. DOI:10.1016/j.margen.2011.04.003 |
| [86] |
FRANSSEN S U, GU J, BERGMANN N, et al. Transcriptomic resilience to global warming in the seagrass Zostera marina, a marine foundation species[J]. Proceedings of the National Academy of Sciences of the United States of America, 2011, 108(48): 19276-19281. DOI:10.1073/pnas.1107680108 |
| [87] |
BERGMANN N, WINTERS G, RAUCH G, et al. Population-specificity of heat stress gene induction in northern and southern eelgrass Zostera marina populations under simulated global warming[J]. Molecular Ecology, 2010, 19(14): 2870-2883. DOI:10.1111/j.1365-294X.2010.04731.x |
| [88] |
SHORT T F, POLIDORO B, LIVINGSTONE S R, et al. Extinction risk assessment of the world's seagrass species[J]. Biological Conservation, 2011, 144(7): 1961-1971. DOI:10.1016/j.biocon.2011.04.010 |
| [89] |
WAYCOTT M, DUARTE C M, CARRUTHERS T J B, et al. Accelerating loss of seagrasses across the globe threatens coastal ecosystems[J]. Proceedings of the National Academy of Sciences of the United States of America, 2009, 106: 12377-12381. DOI:10.1073/pnas.0905620106 |
| [90] |
BONANNO G, RACCUIA S A. Comparative assessment of trace element accumulation and bioindication in seagrasses Posidonia oceanica, Cymodocea nodosa and Halophila stipulacea[J]. Marine Pollution Bulletin, 2018, 131: 260-266. DOI:10.1016/j.marpolbul.2018.04.039 |
| [91] |
COELHO F J R C, SANTOS A L, COIMBRA J, et al. Interactive effects of global climate change and pollution on marine microbes: the way ahead[J]. Ecology and Evolution, 2013, 3(6): 1808-1818. DOI:10.1002/ece3.565 |
| [92] |
SHORT F T, WYLLIE-ECHEVERRIA S. Natural and human-induced disturbance of seagrasses[J]. Environmental Conservation, 1996, 23(1): 17-27. DOI:10.1017/S0376892900038212 |
| [93] |
GRECO M, SAEZ C A, CONTRERAS R A, et al. Cadmium and/or copper excess induce interdependent metal accumulation, DNA methylation, induction of metal chelators and antioxidant defences in the seagrass Zostera marina[J]. Chemosphere, 2019, 224: 111-119. DOI:10.1016/j.chemosphere.2019.02.123 |
| [94] |
BUAPET P, MOHAMMADI N S, PERNICE M, et al. Excess copper promotes photoinhibition and modulates the expression of antioxidant-related genes in Zostera muelleri[J]. Aquatic Toxicology, 2019, 207: 91-100. DOI:10.1016/j.aquatox.2018.12.005 |
| [95] |
LLAGOSTERA I, CERVANTES D, SANMARTÍ N, et al. Effects of copper exposure on photosynthesis and growth of the seagrass Cymodocea nodosa: an experimental a[ssessment[J]. Bulletin of Environmental Contamination and Toxicology, 2016, 97(3): 374-379. DOI:10.1007/s00128-016-1863-y |
| [96] |
ZHAO J S, ZHANG Q, LIU J, et al. Effects of copper enrichment on survival, growth and photosynthetic pigment of seedlings and young plants of the eelgrass Zostera marina[J]. Marine Biology Research, 2016, 12(7): 695-705. DOI:10.1080/17451000.2016.1189083 |
| [97] |
Macinnis-Ng C M O, Ralph P J. Towards a more ecologically relevant assessment of the impact of heavy metals on the photosynthesis of the seagrass, Zostera capricorni[J]. Marine Pollution Bulletin, 2002, 45: 100-106. DOI:10.1016/S0025-326X(01)00300-9 |
| [98] |
MOHAMMADI N S, BUAPET P, PERNICE M, et al. Transcriptome profiling analysis of the seagrass, Zostera muelleri under copper stress[J]. Marine Pollution Bulletin, 2019, 149: 110556. DOI:10.1016/j.marpolbul.2019.110556 |
| [99] |
YRUELA I. Copper in plants: acquisition, transport and interactions[J]. Functional Plant Biology, 2009, 36(5): 409-430. DOI:10.1071/FP08288 |
| [100] |
ZHENG J, GU X Q, ZHANG T J, et al. Phytotoxic effects of Cu, Cd and Zn on the seagrass Thalassia hemprichii and metal accumulation in plants growing in Xincun Bay, Hainan, China[J]. Ecotoxicology, 2018, 27: 517-526. DOI:10.1007/s10646-018-1924-6 |
| [101] |
LI L, HUANG X P, BORTHAKUR D, et al. Photosynthetic activity and antioxidative response of seagrass Thalassia hemprichii to trace metal stress[J]. Acta Oceanologica Sinica, 2012, 31: 98-108. |
| [102] |
HAMOUTENE D, ROMEO M, GNASSIA M, et al. 1996. Cadmium effects on oxidative metabolism in a marine seagrass: Posidonia oceanica[J]. Bulletin of Environmental Contamination and Toxicology, 1996, 56: 327-334. DOI:10.1007/s001289900048 |
| [103] |
MYLONA Z, PANTERIS E, MOUSTAKAS M, et al. Physiological, structural and ultrastructural impacts of silver nanoparticles on the seagrass Cymodocea nodosa[J]. Chemosphere, 2020, 248: 126066. DOI:10.1016/j.chemosphere.2020.126066 |
| [104] |
MYLONA Z, PANTERIS E, KEVREKIDIS T, et al. Silver nanoparticle toxicity effect on the seagrass Halophila stipulacea[J]. Ecotoxicology and Environmental Safety, 2020, 189: 109925. DOI:10.1016/j.ecoenv.2019.109925 |
| [105] |
NAVARRO E, BAUN A, BEHRA R, et al. Environmental behavior and ecotoxicity of engineered nanoparticles to algae, plants, and fungi[J]. Ecotoxicology, 2008, 17(5): 372-386. DOI:10.1007/s10646-008-0214-0 |
| [106] |
MALEA P, CHARITONIDOU K, SPERDOULI I, et al. Zinc Uptake, Photosynthetic efficiency and oxidative stress in the seagrass Cymodocea nodosa exposed to ZnO Nanoparticles[J]. Materials, 2019, 12(13): 2101. DOI:10.3390/ma12132101 |
| [107] |
ERFTEMEIJER P, OSINGA R, MARS A E. Primary production of seagrass beds in South Sulawesi (Indonesia): a comparison of habitats, methods and species[J]. Aquatic Botany, 1993, 46(1): 67-90. DOI:10.1016/0304-3770(93)90065-5 |
| [108] |
EDWARD D A. Physiological aspects of primary production in seagrasses[J]. Aquatic Botany, 1979, 7(2): 139-150. |
| [109] |
KENWORTHY W J, FONSECA M S. Light requirements of seagrasses Halodule wrightii and Syringodium filiforme derived from the relationship between diffuse light attenuation and maximum depth distribution[J]. Estuaries, 1996, 19(3): 740-750. DOI:10.2307/1352533 |
| [110] |
MANOJ K, PADULA M P, DAVEY P, et al. Proteome analysis reveals extensive light stress-response reprogramming in the seagrass Zostera muelleri (Alismatales, Zosteraceae) metabolism[J]. Frontiers in Plant Science, 2016, 7: 2023. |
| [111] |
MAZZUCA S, SPADAFORA A, FILADORO D, et al. Seagrass light acclimation: 2-DE protein analysis in Posidonia leaves grown in chronic low light conditions[J]. Journal of Experimental Marine Biology and Ecology, 2009, 374(2): 113-122. DOI:10.1016/j.jembe.2009.04.010 |
| [112] |
SALO T, REUSCH T B H, BOSTROEM C. Genotype-specific responses to light stress in eelgrass Zostera marina, a marine foundation plant[J]. Marine Eco logy Progress, 2015, 519: 129-140. DOI:10.3354/meps11083 |
| [113] |
COSTA M M, BARROTE I, SILVA J, et al. Epiphytes modulate Posidonia Oceanica photosynthetic production, energetic balance, antioxidant mechanisms, and oxidative damage[J]. Frontiers in Marine Science, 2015, 2(58): 111. |
| [114] |
柳杰, 张沛东, 郭栋, 等. 环境因子对海草生长及光合生理影响的研究进展[J]. 水产科学, 2012, 31(2): 119-124. LIU Jie, ZHANG Peidong, GUO Dong, et al. Research advancement in effects of environmental factors on growth and photosynthetic physiology of sea weed[J]. Fisheries Science, 2012, 31(2): 119-124. DOI:10.3969/j.issn.1003-1111.2012.02.013 |
| [115] |
DATTOLO E, RUOCCO M, BRUNET C, et al. Response of the seagrass Posidonia oceanica to different light environments: insights from a combined molecular and photo-physiological study[J]. Marine Environmental Research, 2014, 101: 225-236. DOI:10.1016/j.marenvres.2014.07.010 |
| [116] |
PHANDEE S, BUAPET P. Photosynthetic and antioxidant responses of the tropical intertidal seagrasses Halophila ovalis and Thalassia hemprichii to moderate and high irradiances[J]. Botanica Marina, 2018, 61(3): 247-256. DOI:10.1515/bot-2017-0084 |
| [117] |
SUREDA A, BOX A, TERRADOS J, et al. Antioxidant response of the seagrass Posidonia oceanica when epiphytized by the invasive macroalgae Lophocladia lallemandii[J]. Marine Environmental Research, 2008, 66(3): 359-363. DOI:10.1016/j.marenvres.2008.05.009 |
| [118] |
CAPÓ X, TEJADA S, FERRIOL P, et al. Hypersaline water from desalinization plants causes oxidative damage in Posidonia oceanica meadows[J]. Science of The Total Environment, 2020, 736: 139601. DOI:10.1016/j.scitotenv.2020.139601 |
| [119] |
JIANG Z J, HUANG X P, ZHANG J P. Effect of nitrate enrichment and salinity reduction on the seagrass Thalassia hemprichii previously grown in low light[J]. Journal of Experimental Marine Biology and Ecology, 2013, 443: 114-122. DOI:10.1016/j.jembe.2013.02.034 |
| [120] |
HSU S Y, KAO C H. Differential effect of sorbitol and polyethylene glycol on antioxidant enzymes in rice leaves[J]. Plant Growth Regulation, 2003, 39(1): 83-90. DOI:10.1023/A:1021830926902 |
| [121] |
ASHRAF M A, ASMA H F, IQBAL M. Exogenous menadione sodium bisulfite mitigates specific ion toxicity and oxidative damage in salinity-stressed okra (Abelmoschus esculentus Moench)[J]. Acta Physiologiae Plantarum, 2019, 41(12): 1-12. |
| [122] |
PARIHAR P, SINGH S, SINGH R, et al. Effect of salinity stress on plants and its tolerance strategies: a review[J]. Environmental Science and Pollution Research, 2015, 22(6): 4056-4075. DOI:10.1007/s11356-014-3739-1 |
| [123] |
IYER V, BARNABAS A D. Effects of varying salinity on leaves of Zostera capensis Setchell. I. Ultrastructural changes[J]. Aquatic Botany, 1993, 46(2): 141-153. DOI:10.1016/0304-3770(93)90042-U |
| [124] |
SANDOVAL-GIL J M, MARIN-GUIRAO L, RUIZ J M. The effect of salinity increase on the photosynthesis, growth and survival of the Mediterranean seagrass Cymodocea nodosa[J]. Estuarine Coastal and Shelf Science, 2012, 115: 260-271. DOI:10.1016/j.ecss.2012.09.008 |
| [125] |
JAN M, ANWAR-UL-HAQ M, SHAH A N, et al. Modulation in growth, gas exchange, and antioxidant activities of salt-stressed rice (Oryza sativa L.) genotypes by zinc fertilization[J]. Arabian Journal of Geosciences, 2019, 12(24): 775. DOI:10.1007/s12517-019-4939-2 |
| [126] |
KHAN M A, ASAF S, KHAN A L, et al. Alleviation of salt stress response in soybean plants with the endophytic bacterial isolate Curtobacterium sp. SAK1[J]. Annals of Microbiology, 2019, 69(8): 797-808. DOI:10.1007/s13213-019-01470-x |
| [127] |
XIN J, LI C L, NING K I, et al. AtPFA-DSP3, an atypical dual﹕pecificity protein tyrosine phosphatase, affects salt stress response by modulating MPK3 and MPK6 activity[J]. Plant Cell and Environment, 2021, 44: 1534-1548. DOI:10.1111/pce.14002 |
| [128] |
ZHANG Y, ZHAO P, YUE S, et al. New insights into physiological effects of anoxia under darkness on the iconic seagrass Zostera marina based on a combined analysis of transcriptomics and metabolomics[J]. Science of The Total Environment, 2021, 768: 144717. DOI:10.1016/j.scitotenv.2020.144717 |
| [129] |
HOWARTH R W. Coastal nitrogen pollution: A review of sources and trends globally and regionally[J]. Har mful Algae, 2009, 8(1): 14-20. |
| [130] |
HARDISON A K, CANUEL E A, ANDERSON I C, et al. Fate of macroalgae in benthic systems: Carbon and nitrogen cycling within the microbial community[J]. Marine Ecology Progress, 2010, 413: 41-55. |
| [131] |
张玉, 赵鹏, 张晓梅, 等. 硫化物胁迫对海草影响的研究进展[J]. 海洋科学, 2020, 44(11): 123-131. ZHANG Yu, ZHAO Peng, ZHANG Xiaomei, et al. A review of the effects of sulfide stress on seagrass[J]. Marine Sciences, 2020, 44(11): 123-131. |
| [132] |
OLIVÉ I, SILVA J, LAURITANO C, et al. Linking gene expression to productivity to unravel long- and short- term responses of seagrasses exposed to CO2 in volcanic vents[J]. Scientific Reports, 2017, 7: 42278. DOI:10.1038/srep42278 |
| [133] |
LAURITANO C, RUOCCO M, DATTOLO E, et al. Response of key stress-related genes of the seagrass Posidonia oceanica in the vicinity of submarine volcanic vents[J]. Biogeosciences, 2015, 12(13): 4185-4194. DOI:10.5194/bg-12-4185-2015 |
| [134] |
RAVAGLIOLI C, LAURITANO C, BUIA M C, et al. Nutrient loading fosters seagrass productivity under ocean acidification[J]. Scientific Reports, 2017, 7(1): 13732. DOI:10.1038/s41598-017-14075-8 |
| [135] |
CAMPBELL J E, FOURQUREAN J W. Ocean acidification outweighs nutrient effects in structuring seagrass epiphyte communities[J]. Journal of Ecology, 2014, 102: 730-737. DOI:10.1111/1365-2745.12233 |