Virus-induced gene silencing reveals control of reactive oxygen species accumulation and salt tolerance in tomato by γ-aminobutyric acid metabolic pathway

Virus-induced gene silencing reveals control of reactive oxygen species accumulation and salt tolerance in tomato by γ-aminobutyric acid metabolic pathway
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DOI:
10.1111/pce.12419
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发表时间:
2015-03-01
影响因子:
7.3
通讯作者:
Li, Yinxin
Li, Yinxin
中科院分区:
生物学1区
文献类型:
--
作者:
Bao, Hexigeduleng;Chen, Xianyang;Li, Yinxin

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γ-氨基丁酸(GABA)在许多植物物种中响应于环境胁迫而积累。然而,植物中GABA或其代谢途径(GABA分流)的生理功能在很大程度上仍不清楚。本研究利用病毒诱导的基因沉默技术,对番茄中控制GABA代谢途径三个步骤的基因,包括谷氨酸脱羧酶(SlGADs)、GABA转氨酶(SlGABA-Ts)和琥珀酸半醛脱氢酶(SlSSADH)进行了研究。在200 mm NaCl胁迫下,GABA生物合成基因SlGADs和GABA分解代谢基因SlGABA-Ts的沉默导致活性氧(ROS)的积累增加,同时也增加了对盐的作为盐的敏感性。代谢物的有针对性的定量分析显示,GABA分别在SlGADs-和SlGABA-Ts-沉默的植物中减少和增加,而琥珀酸(GABA代谢的最终产物)在两种沉默的植物中减少。同样,SISSADH沉默的植物,也在GABA降解过程中有缺陷,在正常条件下表现出矮化表型,卷曲的叶片和增强的ROS积累,这表明如先前在拟南芥中报道的琥珀酸半醛催化剂到-羟基丁酸酯的旁路的参与,对盐胁迫不太敏感。这些结果表明,GABA分流参与番茄的耐盐性,可能是通过影响代谢产物的稳态,如琥珀酸和-羟基丁酸和随后的ROS积累在盐胁迫下。氨基丁酸(GABA)在许多植物体内积累,以响应环境胁迫,但植物中GABA的生理功能及其代谢途径(GABA分流)仍不清楚。在本研究中,基于功能丧失的研究,我们的研究结果揭示了GABA分流的功能参与番茄的耐盐性和GABA相关的代谢产物(如琥珀酸和-羟基丁酸)在这些过程中的假定作用。这些结果打开了令人兴奋的前景,进一步调查GABA分流和相关的代谢途径,以适应植物的压力,指出这些途径作为潜在的目标,植物耐逆工程。据我们所知,这项工作是最彻底的研究之一,证明了GABA代谢途径在防御环境应激中的作用。
gamma-Aminobutyric acid (GABA) accumulates in many plant species in response to environmental stress. However, the physiological function of GABA or its metabolic pathway (GABA shunt) in plants remains largely unclear. Here, the genes, including glutamate decarboxylases (SlGADs), GABAtransaminases (SlGABA-Ts) and succinic semialdehyde dehydrogenase (SlSSADH), controlling three steps of the metabolic pathway of GABA, were studied through virus-induced gene silencing approach in tomato. Silencing of SlGADs (GABA biosynthetic genes) and SlGABA-Ts (GABA catabolic genes) led to increased accumulation of reactive oxygen species (ROS) as well as salt sensitivity under 200mm NaCl treatment. Targeted quantitative analysis of metabolites revealed that GABA decreased and increased in the SlGADs- and SlGABA-Ts-silenced plants, respectively, whereas succinate (the final product of GABA metabolism) decreased in both silenced plants. Contrarily, SlSSADH-silenced plants, also defective in GABA degradation process, showed dwarf phenotype, curled leaves and enhanced accumulation of ROS in normal conditions, suggesting the involvement of a bypath for succinic semialdehyde catabolism to -hydroxybutyrate as reported previously in Arabidopsis, were less sensitive to salt stress. These results suggest that GABA shunt is involved in salt tolerance of tomato, probably by affecting the homeostasis of metabolites such as succinate and -hydroxybutyrate and subsequent ROS accumulation under salt stress.-Aminobutyric acid (GABA) accumulates in many plant species in response to environmental stress, but the physiological function of GABA or its metabolic pathway (GABA shunt) in plants remains largely unclear. In the present study, based on loss-of-function studies, our findings revealed the functional involvement of GABA shunt in the salt tolerance of tomato and the putative roles for GABA-related metabolites (such as succinate and -hydroxybutyrate) in these processes. These results open exciting perspectives for further investigations of GABA shunt and associated metabolic pathways to the stress adaptation of plants, pointing to these pathways as potential targets for engineering of plant stress tolerance. To our knowledge, this work represents one of the most thorough studies demonstrating the roles of GABA metabolic pathway in defense against environmental stress.