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The reduction of reactive oxygen species formation by mitochondrial alternative respiration in tomato basal defense against TMV infection

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Abstract

The role of mitochondrial alternative oxidase (AOX) and the relationship between systemic AOX induction, ROS formation, and systemic plant basal defense to Tobacco mosaic virus (TMV) were investigated in tomato plants. The results showed that TMV inoculation significantly increased the level of AOX gene transcripts, ubiquinone reduction levels, pyruvate content, and cyanide-resistant respiration (CN-resistant R) in upper, un-inoculated leaves. Pretreatment with potassium cyanide (KCN, a cytochrome pathway inhibitor) greatly increased CN-resistant R and reduced reactive oxygen species (ROS) formation, while application of salicylhydroxamic acid (SHAM, an AOX inhibitor) blocked the AOX activity and enhanced the production of ROS in the plants. Furthermore, TMV systemic infection was enhanced by SHAM and reduced by KCN pretreatment, as compared with the un-pretreated TMV counterpart. In addition, KCN application significantly diminished TMV-induced increase in antioxidant enzyme activities and dehydroascorbate/total ascorbate pool, while an opposite change was observed with SHAM-pretreated plants. These results suggest that the systemic induction of the mitochondrial AOX pathway plays a critical role in the reduction of ROS to enhance basal defenses. Additional antioxidant systems were also coordinately regulated in the maintenance of the cellular redox homeostasis.

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Abbreviations

AOX:

Alternative oxidase

APX:

Ascorbate peroxidase

AsA:

Ascorbate

A sat :

Light saturated rate of the CO2 assimilation

CAT:

Catalase

CN-resistant R:

Cyanide-resistant respiration

CP:

Coat protein

DAB:

3,3′-diaminobenzidine

DHA:

Dehydroascorbate

dpi:

Days post-inoculation

GLDH:

l-galactono-1,4-lactone dehydrogenase

GPOD:

Guaiacol peroxidase

KCN:

Potassium cyanide

NBT:

Nitroblue tetrazolium

NO:

Nitric oxide

ROS:

Reactive oxygen species

SHAM:

Salicylhydroxamic acid

SOD:

Superoxide dismutase

TMV:

Tobacco mosaic virus

UQ:

Ubiquinone

UQH2:

Ubiquinol

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Acknowledgments

We thank Prof. Zhixiang Chen of Purdue University for his critical reading of the manuscript. This work was supported by the National Basic Research Program of China (2009CB119000), the National Natural Science Foundation of China (30800763 and 31071832), the National Key Technology R&D Program of China (2011BAD12B04) and the Fundamental Research Funds for the Central Universities.

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Authors and Affiliations

  1. Department of Horticulture, Zijingang Campus, Zhejiang University, Yuhangtang Road 866, 310058, Hangzhou, People’s Republic of China

    Yang-Wen-Ke Liao, Kai Shi, Li-Jun Fu, Shuai Zhang, Xin Li, Yu-Ping Jiang, Yan-Hong Zhou, Xiao-Jian Xia, Wu-Sheng Liang & Jing-Quan Yu

  2. The Institute of Crop and Nuclear Technology Utilization, Zhejiang Academy of Agricultural Sciences, 310021, Hangzhou, People’s Republic of China

    De-Kun Dong

  3. Key Laboratory of Horticultural Plants Growth, Development and Quality Improvement, Agricultural Ministry of China, Yuhangtang Road 866, 310058, Hangzhou, People’s Republic of China

    Jing-Quan Yu

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  1. Yang-Wen-Ke Liao
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Liao, YWK., Shi, K., Fu, LJ. et al. The reduction of reactive oxygen species formation by mitochondrial alternative respiration in tomato basal defense against TMV infection. Planta 235, 225–238 (2012). https://doi.org/10.1007/s00425-011-1483-z

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