Overexpressed β‐cyanoalanine synthase functions with alternative oxidase to improve tobacco resistance to salt stress by alleviating oxidative damage

Yu, Lulu; Liu, Yang; Liu, Cui-Jiao; Feng, Zhaozhong; He, Zhengquan; Xu, Fengming

doi:10.1002/1873-3468.13723

Cited by 11 publications

(11 citation statements)

References 37 publications

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“…The mobile phase consisted of a mixture of acetonitrile and 0.1% trifluoroacetic acid in water (28:72 v/v) and was delivered isocratically at a flow rate of 1 mL/min. The injection volume was 10 µL [ 12 ].…”

Section: Methodsmentioning

confidence: 99%

“…For instance, a study by Machingura et al [ 7 ] demonstrated that the CAS pathway is responsive to water deficit, and the capacity to remove cyanide generated during water deficit may contribute to tolerance to this stress in Arabidopsis. Our previous studies have also shown that enhancing the expression of the CAS enzyme can significantly improve plant tolerance to salt stress in tobacco [ 11 , 12 ]. However, the improvement in plant stress resistance by CAS relies on assistance from the alternative oxidase (AOX) pathway, indicating that the endogenous plant cyanide detoxification system appears to have limited capacity and evolved principally to deal with the relatively small amounts of cyanide produced during metabolism [ 6 , 11 ].…”

Section: Introductionmentioning

confidence: 99%

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The role of cyanoalanine synthase and alternative oxidase in promoting salt stress tolerance in Arabidopsis thaliana

et al. 2023

BMC Plant Biol

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Background Cyanide is a toxic chemical that inhibits cellular respiration. In plants, cyanide can be produced by themselves, especially under stressful conditions. Cyanoalanine synthase (CAS) is a key enzyme involved in plant cyanide detoxification. There are three genes encoding CAS in Arabidopsis thaliana, but the roles of these genes in the plant’s response to stress are less studied. In addition, it is known that alternative oxidase (AOX) mediates cyanide-resistant respiration, but the relationship between CAS and AOX in regulating the plant stress response remains largely unknown. Results Here, the effects of the overexpression or mutation of these three CAS genes on salt stress tolerance were investigated. The results showed that under normal conditions, the overexpression or mutation of the CAS genes had no significant effect on the seed germination and growth of Arabidopsis thaliana compared with wild type (WT). However, under 50, 100, and 200 mM NaCl conditions, the seeds overexpressing CAS genes showed stronger salt stress resistance, i.e., higher germination speed than WT seeds, especially those that overexpressed the CYS-C1 and CYS-D1 genes. In contrast, the seeds with CAS gene mutations exhibited salt sensitivity, and their germination ability and growth were significantly damaged by 100 and 200 mM NaCl. Importantly, this difference in salt stress resistance became more pronounced in CAS-OE, WT, and mutant seeds with increasing salt concentration. The CAS-OE seeds maintained higher respiration rates than the WT and CAS mutant seeds under salt stress conditions. The cyanide contents in CAS mutant seeds were approximately 3 times higher than those in WT seeds and more than 5 times higher than those in CAS-OE seeds. In comparison, plants overexpressing CYS-C1 had the fastest detoxification of cyanide and the best salt tolerance, followed by those overexpressing CYS-D1 and CYS-D2. Furthermore, less hydrogen sulfide (H2S) was observed in CAS-OE seedlings than in WT seedlings under long-term salt stress conditions. Nonetheless, the lack of AOX impaired CAS-OE-mediated plant salt stress resistance, suggesting that CAS and AOX interact to improve salt tolerance is essential. The results also showed that CAS and AOX contributed to the reduction in oxidative damage by helping maintain relatively high levels of antioxidant enzyme activity. Conclusion In summary, the findings of the present study suggest that overexpression of Arabidopsis CAS family genes plays a positive role in salt stress tolerance and highlights the contribution of AOX to CAS-mediated plant salt resistance, mainly by reducing cyanide and H2S toxicity.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The role of cyanoalanine synthase and alternative oxidase in promoting salt stress tolerance in Arabidopsis thaliana

et al. 2023

BMC Plant Biol

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“…The respiration measurement was performed according to the method of Yu et al (2020) . Approximately 50 mg of root tissues were cut into small pieces, and then transferred into air-tight cuvettes containing 20 mM 2-[4-(2-hydroxyethyl)piperazin-1-yl]ethanesulfonic acid (HEPES) and 0.2 mM CaCl 2 with pH 7.2, and oxygen uptake was measured as a decrease of O 2 concentration in the dark using a Clark-type oxygen electrode (Chlorolab2, Hansatech, United Kingdom).…”

Section: Methodsmentioning

confidence: 99%

Alternative Oxidase Inhibition Impairs Tobacco Root Development and Root Hair Formation

Liu

et al. 2021

Front. Plant Sci.

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Alternative oxidase (AOX) is the terminal oxidase of the mitochondrial respiratory electron transport chain in plant cells and is critical for the balance of mitochondrial hemostasis. In this study, the effect of inhibition of AOX with different concentrations of salicylhydroxamic acid (SHAM) on the tobacco root development was investigated. We show here that AOX inhibition significantly impaired the development of the main root and root hair formation of tobacco. The length of the main root of SHAM-treated tobacco was significantly shorter than that of the control, and no root hairs were formed after treatment with a concentration of 1 mM SHAM or more. The transcriptome analysis showed that AOX inhibition by 1 mM SHAM involved in the regulation of gene expression related to root architecture. A total of 5,855 differentially expressed genes (DEGs) were obtained by comparing SHAM-treated roots with control. Of these, the gene expression related to auxin biosynthesis and perception were significantly downregulated by 1 mM SHAM. Similarly, genes related to cell wall loosening, cell cycle, and root meristem growth factor 1 (RGF1) also showed downregulation on SHAM treatment. Moreover, combined with the results of physiological measurements, the transcriptome analysis demonstrated that AOX inhibition resulted in excessive accumulation of reactive oxygen species in roots, which further induced oxidative damage and cell apoptosis. It is worth noting that when indoleacetic acid (20 nM) and dimethylthiourea (10 mM) were added to the medium containing SHAM, the defects of tobacco root development were alleviated, but to a limited extent. Together, these findings indicated that AOX-mediated respiratory pathway plays a crucial role in the tobacco root development, including root hair formation.

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“…More generally, upregulation of AOX enzymes appears to provide beneficial functions during environmental and chemical stress, including cyanide exposure (reviewed by Selinski et al, 2018; Sweetman et al, 2019). For example, AOX has been shown to work synergistically with β‐CAS to withstand oxidative stress in tobacco (Yu et al, 2020), and upregulation of Aox in transgenic cassava can prevent the ROS‐mediated postharvest tissue damage that otherwise occurs in tissues with a high level of cyanide (Zidenga et al, 2012). AOX enzymes could thus potentially operate in multiple ways to mitigate cyanide toxicity within plants.…”

Section: Figurementioning

confidence: 99%

Variable expression of cyanide detoxification and tolerance genes in cyanogenic and acyanogenic white clover (Trifolium repens)

Kuo,

Small,

Olsen

2023

American J of Botany

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Premiseβ‐Cyanoalanine synthase (β‐CAS) and alternative oxidase (AOX) play important roles in the ability of plants to detoxify and tolerate hydrogen cyanide (HCN). These functions are critical for all plants because HCN is produced at low levels during basic metabolic processes, and especially for cyanogenic species, which release high levels of HCN following tissue damage. However, expression of β‐CAS and Aox genes has not been examined in cyanogenic species, nor compared between cyanogenic and acyanogenic genotypes within a species.MethodsWe used a natural polymorphism for cyanogenesis in white clover to examine β‐CAS and Aox gene expression in relation to cyanogenesis‐associated HCN exposure. We identified all β‐CAS and Aox gene copies present in the genome, including members of the Aox1, Aox2a, and Aox2d subfamilies previously reported in legumes. Expression levels were compared between cyanogenic and acyanogenic genotypes and between damaged and undamaged leaf tissue.Resultsβ‐CAS and Aox2a expression was differentially elevated in cyanogenic genotypes, and tissue damage was not required to induce this increased expression. Aox2d, in contrast, appeared to be upregulated as a generalized wounding response.ConclusionsThese findings suggest a heightened constitutive role for HCN detoxification (via elevated β‐CAS expression) and HCN‐toxicity mitigation (via elevated Aox2a expression) in plants that are capable of cyanogenesis. As such, freezing‐induced cyanide autotoxicity is unlikely to be the primary selective factor in the evolution of climate‐associated cyanogenesis clines.

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Overexpressed β‐cyanoalanine synthase functions with alternative oxidase to improve tobacco resistance to salt stress by alleviating oxidative damage

Cited by 11 publications

References 37 publications

The role of cyanoalanine synthase and alternative oxidase in promoting salt stress tolerance in Arabidopsis thaliana

The role of cyanoalanine synthase and alternative oxidase in promoting salt stress tolerance in Arabidopsis thaliana

Alternative Oxidase Inhibition Impairs Tobacco Root Development and Root Hair Formation

Variable expression of cyanide detoxification and tolerance genes in cyanogenic and acyanogenic white clover (Trifolium repens)

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