非生物胁迫下植物体内丙酮醛代谢的研究进展

赵晶晶，周浓，曹鸣宇

非生物胁迫下植物体内丙酮醛代谢的研究进展

赵晶晶1，周浓1，曹鸣宇2

1重庆三峡学院生物与食品工程学院，重庆 404000；2黑龙江八一农垦大学理学院，黑龙江大庆 163319

由于植物固着生长，其无法通过移动来逃避逆境，故非生物胁迫（如极端温度、盐胁迫、干旱或光胁迫等）会伴随着植物的整个生长发育过程，严重胁迫植物的分布、生长、品质和产量，甚至生存。植物只能通过改变自身形态结构以及生理生化反应来适应环境，或者通过释放化学物质来影响周边其他植物的生长发育，以改变微环境，使环境向着更适合自己生长的方向发展。丙酮醛（methylglyoxal，MG）又称之为甲基乙二醛，作为植物体内正常的生理代谢产物可由多条途径产生，其最主要的来源是糖酵解途径，如糖酵解中间体二羟丙酮磷酸和甘油醛3-磷酸去除磷酸基。而植物体内MG的分解主要靠乙二醛酶系统，包括乙二醛酶I、乙二醛酶II以及还原型谷胱甘肽，MG经乙二醛酶降解后形成D-乳酸。在正常生长条件下，植物体内的MG含量维持在较低水平，而当植物遭受非生物胁迫时，其含量会迅速升高；植物体内的MG含量过高会破坏植物细胞的增殖和生存，控制细胞的氧化还原状态以及其他许多方面的新陈代谢过程，最终导致生物大分子蛋白质、DNA、RNA、脂质和生物膜的破坏。因此，MG现在被认为是植物非生物胁迫耐受性的潜在生化标志物，并受到科学界的广泛关注。该文结合最新的研究进展，对非生物胁迫下植物体内丙酮醛合成及降解机制予以综述。

非生物胁迫；丙酮醛；乙二醛酶

0 引言

植物由于固着性不能自行移动，决定了其不能像动物一样躲避逆境的威胁，因此经常暴露于一种或多种非生物胁迫下。非生物胁迫和植物之间的相互作用是复杂的，可以引起植物的多种形态、生理、生物化学和分子变化，如当植物处于非生物胁迫时，体内会产生大量的有害物质（如活性氧、活性氮和丙二醛等），破坏细胞膜结构，产生脂质过氧化反应，致使细胞生理功能受损，最终使细胞死亡[1]。前人对于活性氧（ROS）[1-3]和活性氮[4-5]的产生和清除机制研究已经十分深入，而关于非生物胁迫对植物体内丙酮醛（methylglyoxal，MG）产生及清除机制的研究报道较少[6]，故笔者着重且详细地介绍了非生物胁迫下植物体内丙酮醛的代谢过程。

丙酮醛又称之为甲基乙二醛、2-氧代丙醛或α-氧代醛，常温下MG是一种黄色黏稠状液体，具有特殊的刺激性气味，其分子式为CH3COCHO，由其结构式可知（图1），MG具有酮基和醛基2个功能基团，因此MG在生物体内既可以被氧化也可以被还原，一般情况下，醛基比酮基更具反应性[7]。目前，国内外测定MG含量的常用方法主要有高效液相分析法[8-9]、气相色谱法[10]和化学滴定法[11]等。

图1 丙酮醛结构式

1 植物体内丙酮醛的形成过程

MG作为一种小分子的高活性二羰基复合物，广泛存在于植物体内的各种组织和细胞中，包括胞质溶胶、叶绿体和线粒体等，其产生的具体比率和位点取决于细胞或组织类型、植物器官以及整个植株的生理状态[12]。20世纪30年代中期Meyerhof和Lohmann首次报道了MG合成反应，但由于合成的MG仅仅是一种实验产物而被忽略[13]，直至1993年Richard发现了从三糖磷酸盐中形成MG的机制，首次确定了这种反应的生理学意义[14]。

如图2所示，植物体内的MG可来源于多条代谢通路，如氨基酸代谢、蛋白质代谢和糖酵解等过程[12,15-16]。其中，糖酵解途径是MG形成的最主要来源，由植物光合作用中间体三磷酸甘油醛（glyceraldehyde- 3-phosphate，G3P）和磷酸二羟丙酮（dihydroxyacetone phosphate，DHAP）裂解产生[17-18]，这一形成途径既有非酶促反应也有酶促反应，如丙糖磷酸异构酶（TPI）催化G3P和DHAP的水解产物去磷酸化后形成MG属于酶促反应过程[19-20]。植物体内的MG也可以由蛋白质和氨基酸代谢过程产生，如糖基化蛋白质的降解以及苏氨酸代谢过程中氨基丙酮的氧化均会形成MG[21]。

2 植物体内丙酮醛的降解过程

植物体内可以分解MG的酶主要有乙二醛酶（glyoxalase，Gly）、丙酮醛脱氢酶、醛酮还原酶、甘油脱氢酶以及D-乳酸脱氢酶（图3），此5种酶构成了5条分解代谢途径，即（1）依赖于还原型谷胱甘肽（GSH）的乙二醛酶Ⅰ（也称之为S-D-乳糖基谷胱甘肽裂解酶，glyoxalase I，GlyI）和乙二醛酶Ⅱ（也称之为S-2-羟酰基谷胱甘肽水解酶，glyoxalase II，GlyII）[12,16,18]；（2）不依赖于谷胱甘肽的乙二醛酶Ⅲ（glyoxalase III，GlyIII）[22]；（3）依赖于NADPH的丙酮醛还原酶；（4）依赖于NADPH的醛酮还原酶和甘油脱氢酶；（5）丙酮醛脱氢酶[22]。其中，依赖于GSH的GlyⅠ和GlyⅡ是MG降解的主要途径，MG能够与GSH经非酶促反应自发形成半缩醛后与GlyⅠ的2个活性位点结合，在Gly I的催化作用下转化成S-D-乳糖基谷胱甘肽（S-D-lactoylglutathione，SLG），而细胞内SLG含量的增加不利于DNA的生物合成[23-24]；继而在Gly II的作用下SLG被水解成D-乳酸[15,23-24]，当细胞内的D-乳酸含量超过正常范围之后，其对细胞会产生毒害作用，故需D-乳酸脱氢酶进行及时分解生成丙酮酸，最后通过乙酰辅酶A催化进入三羧酸（TCA）循环（图2），与此同时重新生成的GSH进入Gly I催化的第一步反应中被循环利用[12,15]。

在植物细胞中，Gly途径存在于细胞质和细胞器中，在植物的叶绿体和线粒体中发现高水平的乙二醛酶活性，Gly I被认为是MG分解过程中的关键酶，其活性程度会直接影响MG浓度的高低[25]。Ghosh等[26]在植物中检测到一种新型乙二醛酶—Gly III，其发现为植物体内MG分解提供了更短的途径。常规的乙二醛酶（Gly I和Gly II）在GSH的帮助下将MG转化为D-乳酸，而Gly III含有DJ-1/PfpI结构域，能够在一步不可逆反应中将MG转化为D-乳酸，而不需要GSH（图3），在单子叶植物、双子叶植物、石松类植物、裸子植物和苔藓植物中均检测到Gly III的存在[26]。

除了乙二醛酶系统外，其他几种途径也有利于植物体内MG的分解。依赖于NADPH的丙酮醛还原酶可以直接将MG还原成乳醛。依赖于NADPH的醛酮还原酶（Aldo-keto reductases，AKRs）和甘油脱氢酶可将MG还原成相应的醇[27-28]。最后一条途径是丙酮醛脱氢酶催化MG形成丙酮酸。在正常生理条件下，Gly系统是植物中最有效的MG分解系统[26]，并且该途径对于非生物胁迫下植物来说非常重要。

3 非生物胁迫下植物体内丙酮醛代谢

3.1 非生物胁迫下丙酮醛的含量变化

在正常生理条件下，植物中MG保持低水平（30—75 μmol·L-1）[18]，如水稻中的浓度约为2 μmol·g-1鲜重[12]。然而当植物受到非生物胁迫时，MG含量可以瞬间升高（表1），据不完全统计，与各自的对照组相比，盐胁迫可使绿豆幼苗叶片内的MG含量升高74%—109%[29-30]，玉米幼苗叶片内的MG含量可以升高2.41—2.36倍[31]；重金属胁迫导致绿豆叶片内MG含量升高了86%—132%[32-33]，水稻幼苗叶片内的MG含量较对照升高了22%—84%[34-37]，豌豆幼苗叶片内MG含量较对照增加了20%—32%[38]；碱胁迫导致玉米幼苗叶片内MG含量增加了27%—56%[39]；干旱胁迫导致绿豆幼苗叶片内的MG含量较对照增加了90%—107%[40]；高温胁迫导致绿豆幼苗叶片内的MG含量较对照增加了66%—91%[41]。虽有部分参考文献中尚未检测出MG含量[42-51]，但多数参考文献的研究结果表明，植物体内MG含量的增加是植物对各种非生物胁迫的常见反应，并且随着胁迫程度的增加以及胁迫时间的延长，植物叶片内的MG含量逐渐升高[29-41,52-54]。

图2 植物体内丙酮醛形成过程

图3 植物体内丙酮醛降解过程

3.2 非生物胁迫下丙酮醛对植株的危害

非生物胁迫导致植物体内活性氧类物质（ROS）含量迅速升高已是不争的事实[1-3]。那么非生物胁迫下，植物体内MG与ROS之间又有怎样的关系呢？Kaur等[55]报道，非生物胁迫导致植物细胞中MG含量升高时，会直接加快ROS的生成，或间接促进高级糖基化终产物（AGEs）的积累而使ROS含量增加。Maeta等[56]认为ROS产生的增加可能与MG积累有关，一方面非生物胁迫下MG积累会降低GSH含量，破坏氧化应激下植物体内的抗氧化酶功能而间接导致ROS产量增加；另一方面MG可以作为希尔氧化剂（Hill oxidant）起催化作用，使光系统I（PSI）中的O2成为超氧阴离子（），而的产生是有害的，可能导致细胞成分的氧化损伤[57]。0.5—10 mmol·L-1的MG喷施于烟草植株会导致其体内抗氧化酶（谷胱甘肽-S-转移酶和抗坏血酸过氧化物酶）的活性降低，致使植株发生氧化应激反应[58-59]。此外，Saito等[57]也证明了MG在光合作用中可以诱导叶绿体产生。

当植物体内MG含量超过最适浓度时，MG对植物细胞产生高度毒性，抑制细胞增殖[12]，在缺乏足够的保护机制情况下，MG易与DNA、RNA和蛋白质等大分子反应并修饰大分子，从而形成AGEs[12,55,60]，例如MG的醛基可与植物体内蛋白质的氨基之间发生非酶性糖基化反应，形成一系列具有高度异质性和高度活性的终产物，从而导致蛋白质功能失活和/或降解以及无法修复的代谢功能障碍和细胞死亡[61]。MG与DNA的脱氧鸟苷残基以及精氨酸的胍基反应形成AGEs，这些AGEs会破坏植物体内的抗氧化防御系统[18]，Thornalley等[23]认为MG衍生的修饰既可以与DNA和/或RNA进行直接的相互作用，也可以通过修饰参与多种生物途径的蛋白质活性实现间接作用。

此外，胁迫诱导的MG作为毒性分子起作用，抑制不同的发育过程，包括种子萌发[18,62]、根生长[63]和光合作用[57,64-65]等，如Mano等[64]发现，MG对菠菜叶绿体的光合作用具有毒性，缺少TPI质体同种型的突变体中，MG的积累会延缓菠菜的生长发育，增加萎黄症的发生[65]。此外，Saito等[57]还发现，向叶绿体中添加MG可刺激类囊体膜中的光合电子传递，诱导叶绿体中的产生，从而抑制植物的光合作用。盐胁迫导致烟草叶片内MG的积累会抑制其种子萌发和幼苗的生长[18]；Hoque等[62]发现低于0.1mmol·L-1的MG溶液对拟南芥种子萌发没有影响，但却会降低根的伸长率，培养拟南芥的MS培养基补充1 mmol·L-1的MG会对根系生长产生不利的影响[63,66]，并存在剂量依赖性，随MG浓度的增加其抑制效果明显增强，当培养基中的MG浓度超过1 mmol·L-1后，随培养时间的延长幼苗逐渐褪绿出现白化现象。

3.3 非生物胁迫下乙二醛酶系统的变化

乙二醛酶途径的存在可以限制非生物胁迫下细胞内MG的积累，来抵抗MG过度产生的不利影响。大量研究发现，低水平的MG作为重要的信号分子，通过传播和放大细胞信号进而促进植物对非生物胁迫生长的适应性，还参与调节多种事件，例如细胞增殖和存活、控制细胞的氧化还原状态以及一般代谢和细胞稳态等许多其他方面[12,18,55]。为了使MG真正起特定信号分子的作用，必须存在一种机制来检测其在细胞中的含量变化情况，这可以通过MG介导的蛋白质中半胱氨酸残基的可逆修饰来实现[60]，这种氧化还原调节反过来还可以改变蛋白质构象，从而触发细胞反应[12]。MAPKs是植物体内响应各种环境胁迫的信号分子，Kaur等[12]认为MAPKs级联途径能够将多种胁迫信号逐级放大、传递给靶蛋白，这可能是植物对MG胁迫耐受性的原因。通过施用不同浓度MG处理水稻幼苗发现，随着MG浓度的增加，幼苗的根长和株高受到抑制，当浓度高于10 mmol·L-1时抑制效果显著。Kaur等[12]为了深入了解MG反应的分子基础，使用GeneChip微阵列研究发现，MG可以作为一个信号分子，诱导信号转导基因和转录因子的表达，后者参与调节各种细胞过程，如代谢、运输、防御反应和蛋白质降解等。利用计算机分析，Kaur等[12]在MG响应基因的上游区域中鉴定了保守基序作为MG响应元件（MGRE）并提供了推定的MGRE序列（CTXXCTC和GGCGGCGX）。此外，Cho等[67]还发现MG可以诱导参与代谢信号传导的基因表达，如SnRK1型激酶，该基因编码一种能量传感器蛋白，该蛋白可以在消耗植物体内的能量时调节基因的表达。MG影响应激反应信号网络的能力凸显了MG在植物胁迫反应中的重要性。因此，MG和乙二醛酶现在被认为是评估植物非生物胁迫耐受性的潜在生物化学标记，并且正受到科学界的关注。

表1 非生物胁迫对植物体内丙酮醛含量和乙二醛酶系统的影响

Gly I表示乙二醛酶I；Gly II表示乙二醛酶II；↑表示含量或酶活性升高；↓表示酶活性降低；ND表示未检测到MG

Gly I, glyoxalase I; Gly II, glyoxalase II; ↑, increased; ↓, decreased; ND, not determined

乙二醛酶系统涉及各种细胞功能，但是该系统参与植物非生物胁迫反应，提高植物对非生物胁迫耐受性被认为是其最重要的作用[12]。非生物胁迫下，乙二醛酶系统可以减少MG的积累以及促进GSH的再生，GSH含量的增加以及GSH/GSSG比值的升高可以保护植物免受氧化应激，因为GSH可以直接或间接地促进各种抗氧化酶的活性，如谷胱甘肽过氧化物酶（GPX）、谷胱甘肽S-转移酶（GST）、抗坏血酸过氧化酶（APX）等。许多研究表明，非生物胁迫下植物中抗氧化剂和乙二醛酶系统之间存在密切联系，这表明乙二醛酶系统对ROS解毒的间接影响[18,43,68]。

各物种转录组和蛋白质组学的研究分析提高了我们对非生物胁迫下乙二醛酶系统的认识和理解[69-71]，已经从各种植物中克隆了乙二醛酶基因（和）并进行了详细的表征描述。非生物胁迫下，植物体内的和基因表达量明显上调，和基因的超表达促进了Gly I和Gly II酶活性的增强（表2），进而提高了植物对非生物胁迫的耐受性[70]。乙二醛酶基因超表达的转基因植物在非生物胁迫下具有较低的MG和ROS水平，因为它们具有更好的GSH稳态，并保留了更强的抗氧化酶功能。

表2 转基因植物中乙二醛酶基因的过表达提高了植物的非生物胁迫耐受性

表示乙二醛酶I的基因；表示乙二醛酶II的基因

is the gene for glyoxalase I;is the gene for glyoxalase II

4 展望

非生物胁迫会伴随着植物的整个生长发育过程，严重威胁到了植物的分布、生长、品质和产量，甚至生存。最近对丙酮醛（MG）代谢的研究已经揭示了MG与植物非生物胁迫反应和耐受性有关的许多重要功能。非生物胁迫下，植物体内MG的过度积累是不可避免，但MG可以刺激不同胁迫保护途径的组分，被认为是植物对非生物胁迫的适应过程。乙二醛酶途径通过清除MG赋予了植物对多种非生物胁迫的耐受性，因此，MG水平和乙二醛酶途径与植物的非生物胁迫耐受性密切相关，在今后研究植物非生物胁迫耐受性方面，应该更加注重MG的代谢情况。

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Advance on the Methylglyoxal Metabolism in Plants under Abiotic Stress

ZHAO JingJing1, ZHOU Nong1, CAO MingYu2

1College of Biological and Food Engineering, Chongqing Three Gorges University, Chongqing 404000;2College of Science, Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang

Because plants grow steadily, they cannot escape adversity by moving. Most of plants live in environments where they are constantly exposed to one or combinations of various abiotic stressors, such as extreme temperatures, salinity, drought, and excessive light, which can severely limit plant distribution, growth and development, quality, yield and even survival. Plants can only adapt to the environment by changing their morphological structure and physiological and biochemical reactions, or by releasing chemical substances to affect the growth and development of other surrounding plants, so as to change the microenvironment and make the environment more suitable for their growth. Methylglyoxal (MG) as a normal physiological metabolites, is formed from various metabolic pathways in plants, among them the glycolysis pathway provides the most important source, including elimination of phosphate groups from glycolysis intermediates dihydroxyacetone phosphate and glyceraldehyde 3-phosphate. MG is mostly detoxified by the combined actions of the enzymes glyoxalase I and glyoxalase II that together with glutathione make up the glyoxalase system, and it converts to D-lactate finally. Under normal growth conditions, basal levels of MG remain low in plants; However, when plants are exposed to abiotic stress, MG can be accumulated to much higher levels. Stress-induced MG, as a toxic molecule, inhibited different developmental processes, including seed germination, photosynthesis and root growth, destroyed cell proliferation and survival, controlled of the redox status of cells, and many other aspects of general metabolism. The increase of MG content eventually leads to the destruction of biological macromolecule proteins, DNA, RNA, lipids and biological membranes. Thus, MG is now considered as a potential biochemical marker for plant abiotic stress tolerance, and is receiving considerable attention by the scientific community. The aim of this review was to summarize the mechanisms of MG in plants under abiotic stress. In this review, the recent findings regarding MG synthesis and degradation metabolism in plants under abiotic stress was summarized.

abiotic stress; methylglyoxal; glyoxalase

10.3864/j.issn.0578-1752.2021.08.005

2020-06-30；

2020-08-17

国家自然科学基金（31571613）、黑龙江省农垦总局重点科研计划（HKKY190602）

赵晶晶，E-mail：nl140828@163.com。通信作者周浓，E-mail：erhaizn@126.com

（责任编辑 杨鑫浩）