Respiratory Response of Arabidopsis thaliana Plants with NPQ1 Suppression to High Light: Some Aspects of the Functional Interaction of Chloroplasts and Mitochondria

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Abstract

The energy-dissipating systems (EDS) of a photosynthetic cell — the violaxanthin cycle (VXC) in chloroplasts and the alternative respiratory pathway (AP) in mitochondria — are involved in protecting against excess light energy. The mechanisms of functional interaction of EDS are poorly understood. The aim was to study the effect of high light on respiration and AP activity in Arabidopsis thaliana plants with suppression of NPQ1 encoding the VXC enzyme — violaxanthine de-epoxidase. Four-week-old plants of npq1 line and Columbia-0 wild type line (Col-0) grown at 90 mmol/(m2 s) were exposed to high light, 400 mmol/(m2 s), for 8 hours. Under stress conditions, the npq1 line showed significantly lower values of non-photochemical quenching of chlorophyll fluorescence and the level of de-epoxidation compared to the wild-type line (Col-0), which indicated the absence of zeaxanthin-dependent protection of the photosynthetic apparatus. The plants of the mutant line reacted to high light by increasing respiration due to activation of both alternative and cytochrome pathways. At the same time, the part of AP from total respiration in the npq1 line was consistently high and amounted to about 50%, regardless of the light conditions. Activation of AP and accumulation of the alternative oxidase (AOX) protein were obviously facilitated by increased expression of most AOX genes, the level of transcripts of which was higher under control conditions (0 h), but decreased by the end of the experiment. At the same time, the amount of mRNA of the most stress-inducible AOX1a gene was the lowest among all AOX genes. It is assumed that in the npq1 line the signaling pathway supported by the transcriptional factor of MYB4, a negative regulator of phenylpropanoid synthesis, is weakened. This could be the reason for the low expression of AOX1a, which contains a large number of MYB4-binding sites in the promoter, and an increased content of anthocyanins in leaves compared to Col-0. Unlike Col-0 plants, the npq1 line was characterized by half the activity of superoxide dismutase (SOD), with a predominance of Fe-SOD localized mainly in chloroplasts. However, based on the content of superoxide anion radical and hydrogen peroxide, plants of the npq1 line showed a higher level of oxidative reactions in high-light conditions compared with the wild type line. The data obtained showed a reduced ability of plants with suppression of the genes of two key components of energy-dissipating systems (NPQ1 and AOX1a) to withstand stress. The results indicate the mutual regulation of the EDS of mitochondria and chloroplasts to protect against photooxidation, the importance of AOX in the modulation of respiratory function, and the existence of fast adaptive metabolic rearrangements that provide plant viability under stressful conditions.

About the authors

E. V Garmash

Institute of Biology Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Email: garmash@ib.komisc.ru
Syktyvkar, Russian Federation

K. V Yadrikhinskiy

Institute of Biology Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Syktyvkar, Russian Federation

M. A Shelyakin

Institute of Biology Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Syktyvkar, Russian Federation

E. S Belykh

Institute of Biology Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Syktyvkar, Russian Federation

E. V Silina

Institute of Biology Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Syktyvkar, Russian Federation

R. V Malyshev

Institute of Biology Komi Science Centre of the Ural Branch of the Russian Academy of Sciences

Syktyvkar, Russian Federation

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