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M-type thioredoxins are involved in the xanthophyll cycle and proton motive force to alter NPQ under low-light conditions in Arabidopsis

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Abstract

Key message

M-type thioredoxins are required to regulate zeaxanthin epoxidase activity and to maintain the steady-state level of the proton motive force, thereby influencing NPQ properties under low-light conditions in Arabidopsis.

Abstract

Non-photochemical quenching (NPQ) helps protect photosynthetic organisms from photooxidative damage via the non-radiative dissipation of energy as heat. Energy-dependent quenching (qE) is a major constituent of NPQ. However, the mechanism underlying the regulation of qE is not well understood. In this study, we demonstrate that the m-type thioredoxins TRX-m1, TRX-m2, and TRX-m4 (TRX-ms) interact with the xanthophyll cycle enzyme zeaxanthin epoxidase (ZE) and are required for maintaining the redox-dependent stabilization of ZE by regulating its intermolecular disulfide bridges. Reduced ZE activity and accumulated zeaxanthin levels were observed under TRX-ms deficiency. Furthermore, concurrent deficiency of TRX-ms resulted in a significant increase in proton motive force (pmf) and acidification of the thylakoid lumen under low irradiance, perhaps due to the significantly reduced ATP synthase activity under TRX-ms deficiency. The increased pmf, combined with acidification of the thylakoid lumen and the accumulation of zeaxanthin, ultimately contribute to the elevated stable qE in VIGS–TRX-m2m4/m1 plants under low-light conditions. Taken together, these results indicate that TRX-ms are involved in regulating NPQ-dependent photoprotection in Arabidopsis.

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Abbreviations

A:

Antheraxanthin

ATPβ:

β-subunit of ATP synthase complex

BiFC:

Bimolecular fluorescence complementation

DTT:

Dithiothreitol

ΔΨ:

Electric field gradient

ECS:

The electrochromic shift

HPLC:

High performance liquid chromatography

NPQ:

Non-photochemical quenching

NTRC:

NADPH–thioredoxin reductase C

Pmf:

Proton motive force

PSI:

Photosystem I

PSII:

Photosystem II

qE:

Energy-dependent quenching

ROS:

Reactive oxygen species

TRX:

Thioredoxin

V:

Violaxanthin

VIGS:

Tobacco rattle virus-based virus-induced gene silencing

VDE:

Violaxanthin de-epoxidase

Z:

Zeaxanthin

ZE:

Zeaxanthin epoxidase

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Acknowledgements

We thank Bernhard Grimm and Peng Wang (Humboldt-University Berlin, Germany) for technical support and critical reading of the manuscript, Yule Liu (Tsinghua University) for sharing the TRV-based VIGS vectors, Tomas Morosinotto (University of Padova, Italy) for providing us with the VDE antibody, Chuxiong Zhuang and Jing Li (South China Agricultural University) for supporting Dual-PAM 100 analysis, Chunyan Zhang and Yan Yin (Key Laboratory of Photobiology, CAS) for help with the gH + protocol, and Alexander V. Ruban (Queen Mary University of London) for providing us with suggestions for experiments.

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  1. State Key Laboratory of Biocontrol and Collaborative Innovation Center of Genetics and Development, Guangdong Provincial Key Laboratory of Plant Resources, School of Life Sciences, Sun Yat-sen University, 510275, Guangzhou, People’s Republic of China

    Qingen Da, Ting Sun, Menglong Wang, Honglei Jin, Mengshu Li, Dongru Feng, Jinfa Wang, Hong-Bin Wang & Bing Liu

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  1. Qingen Da
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Correspondence to Bing Liu.

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This work was supported by the National Science and Technology Major Project Foundation of China (No. 2016ZX08009003-005-005), the National Natural Science Foundation of China (No. 31,425,003, No. 31,370,297, and No. 31,500,195), and a grant from the International Program for Ph.D. Candidates, Sun Yat-Sen University (No. 52,114,000).

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Communicated by Salim Al-Babili.

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Da, Q., Sun, T., Wang, M. et al. M-type thioredoxins are involved in the xanthophyll cycle and proton motive force to alter NPQ under low-light conditions in Arabidopsis. Plant Cell Rep 37, 279–291 (2018). https://doi.org/10.1007/s00299-017-2229-6

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