趙晶晶，周濃，曹鳴宇

非生物脅迫下植物體內(nèi)丙酮醛代謝的研究進展

趙晶晶1，周濃1，曹鳴宇2

1重慶三峽學院生物與食品工程學院，重慶 404000；2黑龍江八一農(nóng)墾大學理學院，黑龍江大慶 163319

由于植物固著生長，其無法通過移動來逃避逆境，故非生物脅迫（如極端溫度、鹽脅迫、干旱或光脅迫等）會伴隨著植物的整個生長發(fā)育過程，嚴重脅迫植物的分布、生長、品質(zhì)和產(chǎn)量，甚至生存。植物只能通過改變自身形態(tài)結(jié)構(gòu)以及生理生化反應來適應環(huán)境，或者通過釋放化學物質(zhì)來影響周邊其他植物的生長發(fā)育，以改變微環(huán)境，使環(huán)境向著更適合自己生長的方向發(fā)展。丙酮醛（methylglyoxal，MG）又稱之為甲基乙二醛，作為植物體內(nèi)正常的生理代謝產(chǎn)物可由多條途徑產(chǎn)生，其最主要的來源是糖酵解途徑，如糖酵解中間體二羥丙酮磷酸和甘油醛3-磷酸去除磷酸基。而植物體內(nèi)MG的分解主要靠乙二醛酶系統(tǒng)，包括乙二醛酶I、乙二醛酶II以及還原型谷胱甘肽，MG經(jīng)乙二醛酶降解后形成D-乳酸。在正常生長條件下，植物體內(nèi)的MG含量維持在較低水平，而當植物遭受非生物脅迫時，其含量會迅速升高；植物體內(nèi)的MG含量過高會破壞植物細胞的增殖和生存，控制細胞的氧化還原狀態(tài)以及其他許多方面的新陳代謝過程，最終導致生物大分子蛋白質(zhì)、DNA、RNA、脂質(zhì)和生物膜的破壞。因此，MG現(xiàn)在被認為是植物非生物脅迫耐受性的潛在生化標志物，并受到科學界的廣泛關注。該文結(jié)合最新的研究進展，對非生物脅迫下植物體內(nèi)丙酮醛合成及降解機制予以綜述。

非生物脅迫；丙酮醛；乙二醛酶

0 引言

植物由于固著性不能自行移動，決定了其不能像動物一樣躲避逆境的威脅，因此經(jīng)常暴露于一種或多種非生物脅迫下。非生物脅迫和植物之間的相互作用是復雜的，可以引起植物的多種形態(tài)、生理、生物化學和分子變化，如當植物處于非生物脅迫時，體內(nèi)會產(chǎn)生大量的有害物質(zhì)（如活性氧、活性氮和丙二醛等），破壞細胞膜結(jié)構(gòu)，產(chǎn)生脂質(zhì)過氧化反應，致使細胞生理功能受損，最終使細胞死亡[1]。前人對于活性氧（ROS）[1-3]和活性氮[4-5]的產(chǎn)生和清除機制研究已經(jīng)十分深入，而關于非生物脅迫對植物體內(nèi)丙酮醛（methylglyoxal，MG）產(chǎn)生及清除機制的研究報道較少[6]，故筆者著重且詳細地介紹了非生物脅迫下植物體內(nèi)丙酮醛的代謝過程。

丙酮醛又稱之為甲基乙二醛、2-氧代丙醛或α-氧代醛，常溫下MG是一種黃色黏稠狀液體，具有特殊的刺激性氣味，其分子式為CH3COCHO，由其結(jié)構(gòu)式可知（圖1），MG具有酮基和醛基2個功能基團，因此MG在生物體內(nèi)既可以被氧化也可以被還原，一般情況下，醛基比酮基更具反應性[7]。目前，國內(nèi)外測定MG含量的常用方法主要有高效液相分析法[8-9]、氣相色譜法[10]和化學滴定法[11]等。

圖1 丙酮醛結(jié)構(gòu)式

1 植物體內(nèi)丙酮醛的形成過程

MG作為一種小分子的高活性二羰基復合物，廣泛存在于植物體內(nèi)的各種組織和細胞中，包括胞質(zhì)溶膠、葉綠體和線粒體等，其產(chǎn)生的具體比率和位點取決于細胞或組織類型、植物器官以及整個植株的生理狀態(tài)[12]。20世紀30年代中期Meyerhof和Lohmann首次報道了MG合成反應，但由于合成的MG僅僅是一種實驗產(chǎn)物而被忽略[13]，直至1993年Richard發(fā)現(xiàn)了從三糖磷酸鹽中形成MG的機制，首次確定了這種反應的生理學意義[14]。

如圖2所示，植物體內(nèi)的MG可來源于多條代謝通路，如氨基酸代謝、蛋白質(zhì)代謝和糖酵解等過程[12,15-16]。其中，糖酵解途徑是MG形成的最主要來源，由植物光合作用中間體三磷酸甘油醛（glyceraldehyde- 3-phosphate，G3P）和磷酸二羥丙酮（dihydroxyacetone phosphate，DHAP）裂解產(chǎn)生[17-18]，這一形成途徑既有非酶促反應也有酶促反應，如丙糖磷酸異構(gòu)酶（TPI）催化G3P和DHAP的水解產(chǎn)物去磷酸化后形成MG屬于酶促反應過程[19-20]。植物體內(nèi)的MG也可以由蛋白質(zhì)和氨基酸代謝過程產(chǎn)生，如糖基化蛋白質(zhì)的降解以及蘇氨酸代謝過程中氨基丙酮的氧化均會形成MG[21]。

2 植物體內(nèi)丙酮醛的降解過程

植物體內(nèi)可以分解MG的酶主要有乙二醛酶（glyoxalase，Gly）、丙酮醛脫氫酶、醛酮還原酶、甘油脫氫酶以及D-乳酸脫氫酶（圖3），此5種酶構(gòu)成了5條分解代謝途徑，即（1）依賴于還原型谷胱甘肽（GSH）的乙二醛酶Ⅰ（也稱之為S-D-乳糖基谷胱甘肽裂解酶，glyoxalase I，GlyI）和乙二醛酶Ⅱ（也稱之為S-2-羥酰基谷胱甘肽水解酶，glyoxalase II，GlyII）[12,16,18]；（2）不依賴于谷胱甘肽的乙二醛酶Ⅲ（glyoxalase III，GlyIII）[22]；（3）依賴于NADPH的丙酮醛還原酶；（4）依賴于NADPH的醛酮還原酶和甘油脫氫酶；（5）丙酮醛脫氫酶[22]。其中，依賴于GSH的GlyⅠ和GlyⅡ是MG降解的主要途徑，MG能夠與GSH經(jīng)非酶促反應自發(fā)形成半縮醛后與GlyⅠ的2個活性位點結(jié)合，在Gly I的催化作用下轉(zhuǎn)化成S-D-乳糖基谷胱甘肽（S-D-lactoylglutathione，SLG），而細胞內(nèi)SLG含量的增加不利于DNA的生物合成[23-24]；繼而在Gly II的作用下SLG被水解成D-乳酸[15,23-24]，當細胞內(nèi)的D-乳酸含量超過正常范圍之后，其對細胞會產(chǎn)生毒害作用，故需D-乳酸脫氫酶進行及時分解生成丙酮酸，最后通過乙酰輔酶A催化進入三羧酸（TCA）循環(huán)（圖2），與此同時重新生成的GSH進入Gly I催化的第一步反應中被循環(huán)利用[12,15]。

在植物細胞中，Gly途徑存在于細胞質(zhì)和細胞器中，在植物的葉綠體和線粒體中發(fā)現(xiàn)高水平的乙二醛酶活性，Gly I被認為是MG分解過程中的關鍵酶，其活性程度會直接影響MG濃度的高低[25]。Ghosh等[26]在植物中檢測到一種新型乙二醛酶—Gly III，其發(fā)現(xiàn)為植物體內(nèi)MG分解提供了更短的途徑。常規(guī)的乙二醛酶（Gly I和Gly II）在GSH的幫助下將MG轉(zhuǎn)化為D-乳酸，而Gly III含有DJ-1/PfpI結(jié)構(gòu)域，能夠在一步不可逆反應中將MG轉(zhuǎn)化為D-乳酸，而不需要GSH（圖3），在單子葉植物、雙子葉植物、石松類植物、裸子植物和苔蘚植物中均檢測到Gly III的存在[26]。

除了乙二醛酶系統(tǒng)外，其他幾種途徑也有利于植物體內(nèi)MG的分解。依賴于NADPH的丙酮醛還原酶可以直接將MG還原成乳醛。依賴于NADPH的醛酮還原酶（Aldo-keto reductases，AKRs）和甘油脫氫酶可將MG還原成相應的醇[27-28]。最后一條途徑是丙酮醛脫氫酶催化MG形成丙酮酸。在正常生理條件下，Gly系統(tǒng)是植物中最有效的MG分解系統(tǒng)[26]，并且該途徑對于非生物脅迫下植物來說非常重要。

3 非生物脅迫下植物體內(nèi)丙酮醛代謝

3.1 非生物脅迫下丙酮醛的含量變化

在正常生理條件下，植物中MG保持低水平（30—75 μmol·L-1）[18]，如水稻中的濃度約為2 μmol·g-1鮮重[12]。然而當植物受到非生物脅迫時，MG含量可以瞬間升高（表1），據(jù)不完全統(tǒng)計，與各自的對照組相比，鹽脅迫可使綠豆幼苗葉片內(nèi)的MG含量升高74%—109%[29-30]，玉米幼苗葉片內(nèi)的MG含量可以升高2.41—2.36倍[31]；重金屬脅迫導致綠豆葉片內(nèi)MG含量升高了86%—132%[32-33]，水稻幼苗葉片內(nèi)的MG含量較對照升高了22%—84%[34-37]，豌豆幼苗葉片內(nèi)MG含量較對照增加了20%—32%[38]；堿脅迫導致玉米幼苗葉片內(nèi)MG含量增加了27%—56%[39]；干旱脅迫導致綠豆幼苗葉片內(nèi)的MG含量較對照增加了90%—107%[40]；高溫脅迫導致綠豆幼苗葉片內(nèi)的MG含量較對照增加了66%—91%[41]。雖有部分參考文獻中尚未檢測出MG含量[42-51]，但多數(shù)參考文獻的研究結(jié)果表明，植物體內(nèi)MG含量的增加是植物對各種非生物脅迫的常見反應，并且隨著脅迫程度的增加以及脅迫時間的延長，植物葉片內(nèi)的MG含量逐漸升高[29-41,52-54]。

圖2 植物體內(nèi)丙酮醛形成過程

圖3 植物體內(nèi)丙酮醛降解過程

3.2 非生物脅迫下丙酮醛對植株的危害

非生物脅迫導致植物體內(nèi)活性氧類物質(zhì)（ROS）含量迅速升高已是不爭的事實[1-3]。那么非生物脅迫下，植物體內(nèi)MG與ROS之間又有怎樣的關系呢？Kaur等[55]報道，非生物脅迫導致植物細胞中MG含量升高時，會直接加快ROS的生成，或間接促進高級糖基化終產(chǎn)物（AGEs）的積累而使ROS含量增加。Maeta等[56]認為ROS產(chǎn)生的增加可能與MG積累有關，一方面非生物脅迫下MG積累會降低GSH含量，破壞氧化應激下植物體內(nèi)的抗氧化酶功能而間接導致ROS產(chǎn)量增加；另一方面MG可以作為希爾氧化劑（Hill oxidant）起催化作用，使光系統(tǒng)I（PSI）中的O2成為超氧陰離子（），而的產(chǎn)生是有害的，可能導致細胞成分的氧化損傷[57]。0.5—10 mmol·L-1的MG噴施于煙草植株會導致其體內(nèi)抗氧化酶（谷胱甘肽-S-轉(zhuǎn)移酶和抗壞血酸過氧化物酶）的活性降低，致使植株發(fā)生氧化應激反應[58-59]。此外，Saito等[57]也證明了MG在光合作用中可以誘導葉綠體產(chǎn)生。

當植物體內(nèi)MG含量超過最適濃度時，MG對植物細胞產(chǎn)生高度毒性，抑制細胞增殖[12]，在缺乏足夠的保護機制情況下，MG易與DNA、RNA和蛋白質(zhì)等大分子反應并修飾大分子，從而形成AGEs[12,55,60]，例如MG的醛基可與植物體內(nèi)蛋白質(zhì)的氨基之間發(fā)生非酶性糖基化反應，形成一系列具有高度異質(zhì)性和高度活性的終產(chǎn)物，從而導致蛋白質(zhì)功能失活和/或降解以及無法修復的代謝功能障礙和細胞死亡[61]。MG與DNA的脫氧鳥苷殘基以及精氨酸的胍基反應形成AGEs，這些AGEs會破壞植物體內(nèi)的抗氧化防御系統(tǒng)[18]，Thornalley等[23]認為MG衍生的修飾既可以與DNA和/或RNA進行直接的相互作用，也可以通過修飾參與多種生物途徑的蛋白質(zhì)活性實現(xiàn)間接作用。

此外，脅迫誘導的MG作為毒性分子起作用，抑制不同的發(fā)育過程，包括種子萌發(fā)[18,62]、根生長[63]和光合作用[57,64-65]等，如Mano等[64]發(fā)現(xiàn)，MG對菠菜葉綠體的光合作用具有毒性，缺少TPI質(zhì)體同種型的突變體中，MG的積累會延緩菠菜的生長發(fā)育，增加萎黃癥的發(fā)生[65]。此外，Saito等[57]還發(fā)現(xiàn)，向葉綠體中添加MG可刺激類囊體膜中的光合電子傳遞，誘導葉綠體中的產(chǎn)生，從而抑制植物的光合作用。鹽脅迫導致煙草葉片內(nèi)MG的積累會抑制其種子萌發(fā)和幼苗的生長[18]；Hoque等[62]發(fā)現(xiàn)低于0.1mmol·L-1的MG溶液對擬南芥種子萌發(fā)沒有影響，但卻會降低根的伸長率，培養(yǎng)擬南芥的MS培養(yǎng)基補充1 mmol·L-1的MG會對根系生長產(chǎn)生不利的影響[63,66]，并存在劑量依賴性，隨MG濃度的增加其抑制效果明顯增強，當培養(yǎng)基中的MG濃度超過1 mmol·L-1后，隨培養(yǎng)時間的延長幼苗逐漸褪綠出現(xiàn)白化現(xiàn)象。

3.3 非生物脅迫下乙二醛酶系統(tǒng)的變化

乙二醛酶途徑的存在可以限制非生物脅迫下細胞內(nèi)MG的積累，來抵抗MG過度產(chǎn)生的不利影響。大量研究發(fā)現(xiàn)，低水平的MG作為重要的信號分子，通過傳播和放大細胞信號進而促進植物對非生物脅迫生長的適應性，還參與調(diào)節(jié)多種事件，例如細胞增殖和存活、控制細胞的氧化還原狀態(tài)以及一般代謝和細胞穩(wěn)態(tài)等許多其他方面[12,18,55]。為了使MG真正起特定信號分子的作用，必須存在一種機制來檢測其在細胞中的含量變化情況，這可以通過MG介導的蛋白質(zhì)中半胱氨酸殘基的可逆修飾來實現(xiàn)[60]，這種氧化還原調(diào)節(jié)反過來還可以改變蛋白質(zhì)構(gòu)象，從而觸發(fā)細胞反應[12]。MAPKs是植物體內(nèi)響應各種環(huán)境脅迫的信號分子，Kaur等[12]認為MAPKs級聯(lián)途徑能夠?qū)⒍喾N脅迫信號逐級放大、傳遞給靶蛋白，這可能是植物對MG脅迫耐受性的原因。通過施用不同濃度MG處理水稻幼苗發(fā)現(xiàn)，隨著MG濃度的增加，幼苗的根長和株高受到抑制，當濃度高于10 mmol·L-1時抑制效果顯著。Kaur等[12]為了深入了解MG反應的分子基礎，使用GeneChip微陣列研究發(fā)現(xiàn)，MG可以作為一個信號分子，誘導信號轉(zhuǎn)導基因和轉(zhuǎn)錄因子的表達，后者參與調(diào)節(jié)各種細胞過程，如代謝、運輸、防御反應和蛋白質(zhì)降解等。利用計算機分析，Kaur等[12]在MG響應基因的上游區(qū)域中鑒定了保守基序作為MG響應元件（MGRE）并提供了推定的MGRE序列（CTXXCTC和GGCGGCGX）。此外，Cho等[67]還發(fā)現(xiàn)MG可以誘導參與代謝信號傳導的基因表達，如SnRK1型激酶，該基因編碼一種能量傳感器蛋白，該蛋白可以在消耗植物體內(nèi)的能量時調(diào)節(jié)基因的表達。MG影響應激反應信號網(wǎng)絡的能力凸顯了MG在植物脅迫反應中的重要性。因此，MG和乙二醛酶現(xiàn)在被認為是評估植物非生物脅迫耐受性的潛在生物化學標記，并且正受到科學界的關注。

表1 非生物脅迫對植物體內(nèi)丙酮醛含量和乙二醛酶系統(tǒng)的影響

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表示未檢測到MG

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

乙二醛酶系統(tǒng)涉及各種細胞功能，但是該系統(tǒng)參與植物非生物脅迫反應，提高植物對非生物脅迫耐受性被認為是其最重要的作用[12]。非生物脅迫下，乙二醛酶系統(tǒng)可以減少MG的積累以及促進GSH的再生，GSH含量的增加以及GSH/GSSG比值的升高可以保護植物免受氧化應激，因為GSH可以直接或間接地促進各種抗氧化酶的活性，如谷胱甘肽過氧化物酶（GPX）、谷胱甘肽S-轉(zhuǎn)移酶（GST）、抗壞血酸過氧化酶（APX）等。許多研究表明，非生物脅迫下植物中抗氧化劑和乙二醛酶系統(tǒng)之間存在密切聯(lián)系，這表明乙二醛酶系統(tǒng)對ROS解毒的間接影響[18,43,68]。

各物種轉(zhuǎn)錄組和蛋白質(zhì)組學的研究分析提高了我們對非生物脅迫下乙二醛酶系統(tǒng)的認識和理解[69-71]，已經(jīng)從各種植物中克隆了乙二醛酶基因（和）并進行了詳細的表征描述。非生物脅迫下，植物體內(nèi)的和基因表達量明顯上調(diào)，和基因的超表達促進了Gly I和Gly II酶活性的增強（表2），進而提高了植物對非生物脅迫的耐受性[70]。乙二醛酶基因超表達的轉(zhuǎn)基因植物在非生物脅迫下具有較低的MG和ROS水平，因為它們具有更好的GSH穩(wěn)態(tài)，并保留了更強的抗氧化酶功能。

表2 轉(zhuǎn)基因植物中乙二醛酶基因的過表達提高了植物的非生物脅迫耐受性

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

非生物脅迫會伴隨著植物的整個生長發(fā)育過程，嚴重威脅到了植物的分布、生長、品質(zhì)和產(chǎn)量，甚至生存。最近對丙酮醛（MG）代謝的研究已經(jīng)揭示了MG與植物非生物脅迫反應和耐受性有關的許多重要功能。非生物脅迫下，植物體內(nèi)MG的過度積累是不可避免，但MG可以刺激不同脅迫保護途徑的組分，被認為是植物對非生物脅迫的適應過程。乙二醛酶途徑通過清除MG賦予了植物對多種非生物脅迫的耐受性，因此，MG水平和乙二醛酶途徑與植物的非生物脅迫耐受性密切相關，在今后研究植物非生物脅迫耐受性方面，應該更加注重MG的代謝情況。

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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

國家自然科學基金（31571613）、黑龍江省農(nóng)墾總局重點科研計劃（HKKY190602）

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

（責任編輯 楊鑫浩）