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Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants

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Abstract

To find if cytosolic glycolysis dynamical metabolism plays a role in mediating respiration homeostasis and its relationship with mitochondrial electron transport chain (miETC) flexibility, we selected two tomato genotypes that differ in chilling tolerance and compared the responses of miETC, cytosolic glycolysis and respiratory homeostasis at 7 °C. Our results showed that the transcripts of both classical and bypass component genes for miETC and glycolysis were comparable for both genotypes when grown at 25 °C. However, there was a rapid global increase in the expression of most respiratory genes in response to chilling at 7 °C for both genotypes. When normally grown plant was set as the control for each genotype, the transcripts of most COX family members, ATP synthase, AOX1b, and UCP are highly up-regulated in chilling-tolerant Zhefen No. 208 plants in contrast to the sensitive Zhefen No. 212 plants. Both genotypes mobilized the energy-saving sucrose synthase pathway for sucrose degradation by cytosolic glycolysis, but this mechanism is evidently more effective in tolerant Zhefen No. 208 plants. Furthermore, only Zhefen No. 208 plants were able to partially switch from low-energy efficiency pathways to ATP conserving pathways to carry out fructose-6-phosphate conversion and pyruvate production. This metabolic flexibility in miETC and cytosolic glycolysis were coupled to higher ATP synthesis and lower ROS accumulation, which may be essential for sustaining the higher leaf respiration and homeostasis of chilling-tolerant plants.

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Abbreviations

AOX:

Alternative oxidase

ATP-PFK:

ATP-dependent phosphofructokinase

CN:

Cyanide

COX:

Cytochrome c oxidase

DAB:

3,3′-diaminobenzidine

Fru-1,6-P2 :

Fructose 1,6-bisphosphate

Fru-6-P:

Fructose-6-phosphate

MDA:

Malonaldehyde

miETC:

Mitochondrial electron transport chain

NBT:

Nitroblue tetrazolium

NDH:

NAD(P)H dehydrogenases

PEP:

Phosphoenolpyruvate

PPi-PFK:

PPi-dependent phosphofructokinase

PPDK:

Pyruvate, orthophosphate dikinase

PK:

Pyruvate kinase

PPi:

Pyrophosphate

ROS:

Reactive oxygen species

SHAM:

Salicylhydroxamic acid

SuSy:

Sucrose synthase

UCP:

Uncoupling protein

UQ:

Ubiquinone

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Acknowledgments

We thank Prof. Gong-Yin Ye and Hong-Wei Yao of Zhejiang University for competent help in ATP content analysis. We thank Dr. Miaoying Tian of Cornell University for her 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 (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, 866 Yuhangtang Road, 310058, Hangzhou, People’s Republic of China

    Kai Shi, Li-Jun Fu, Shuai Zhang, Xin Li, Yang-Wen-Ke Liao, Xiao-Jian Xia, Yan-Hong Zhou, Zhi-Xiang Chen & Jing-Quan Yu

  2. Tangshan Research Institute of Agricultural Science, 063001, Tangshan, People’s Republic of China

    Li-Jun Fu

  3. Zhejiang Academy of Agricultural Sciences, 310021, Hangzhou, People’s Republic of China

    Rong-Qing Wang

  4. 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. Kai Shi
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Correspondence to Kai Shi.

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A contribution to the Special Issue on Evolution and Biogenesis of Chloroplasts and Mitochondria.

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Supplemental Table S1: Primers used for real time RT-PCR assays (DOCX 20 kb)

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Shi, K., Fu, LJ., Zhang, S. et al. Flexible change and cooperation between mitochondrial electron transport and cytosolic glycolysis as the basis for chilling tolerance in tomato plants. Planta 237, 589–601 (2013). https://doi.org/10.1007/s00425-012-1799-3

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