PGR5/PGRL1 and NDH Mediate Far-Red Light-Induced Photoprotection in Response to Chilling Stress in Tomato.

Feng Wang,Hengzuo Xiang,Xin Bu,Hongyan Qi,Golam Jalal Ahammed,Xiujie Wang,Tianlai Li,Yanbing Li,Jiarong Yan,Yufeng Liu,Mingfang Qi,Jiazhi Lu

doi:10.3389/fpls.2020.00669

Abstract

Plants experience low ambient temperature and low red to far-red ratios (L-R/FR) of light due to vegetative shading and longer twilight durations in cool seasons. Low temperature induce photoinhibition through inactivation of the photosynthetic apparatus, however, the role of light quality on photoprotection during cold stress remains poorly understood. Here, we report that L-R/FR significantly prevents the overreduction of the entire intersystem electron transfer chain and the limitation of photosystem I (PSI) acceptor side, eventually alleviating the cold-induced photoinhibition. During cold stress, L-R/FR activated cyclic electron flow (CEF), enhanced protonation of PSII subunit S (PsbS) and de-epoxidation state of the xanthophyll cycle, and promoted energy-dependent quenching (qE) component of non-photochemical quenching (NPQ), enzyme activity of Foyer-Halliwell-Asada cycle and D1 proteins accumulation. However, L-R/FR –induced photoprotection pathways were compromised in tomato PROTON GRADIENT REGULATION5 (PGR5) and PGR5-LIKE PHOTOSYNTHETIC PHENOTYPE1A (PGRL1A) co-silenced plants and NADH DEHYDROGENASE-LIKE COMPLEX M (NDHM) -silenced plants during cold stress. Our results demonstrate that both PGR5/PGRL1- and NDH-dependent CEF mediate L-R/FR –induced cold tolerance by enhancing the thermal dissipation and the repair of photodamaged PSII, thereby mitigating the overreduction of electron carriers and the accumulation of reactive oxygen species. The study indicates that there is an anterograde link between photoreception and photoprotection in tomato plants during cold stress.

Highlights

Photosynthesis is the most important biosynthetic process on earth, which converts light energy into chemical energy that drives the food chain
We found that exposure to cold stress resulted in an increased of reactive oxygen species (ROS) and MDA, low red to far-red ratios (L-R/FR) alleviated the accumulation of ROS and MDA in tomato under cold stress
The chloroplasts contained large amounts of osmiophilic lipid droplets, which were big and round as well as presented in great numbers, in plants under high red to far-red light ratios (H-R/FR) conditions during cold stress. These results suggest that L-R/FR alleviates the damage of the membrane and chloroplast ultrastructure in tomato plants via decreasing the levels of ROS and MDA during cold stress

Summary

Introduction

Photosynthesis is the most important biosynthetic process on earth, which converts light energy into chemical energy that drives the food chain. Thylakoid luminal acidification slows the plastoquinol oxidation at the Cyt b6f complex to prevent excess electron flow toward PSI. This phenomenon is called photosynthetic control (Tikhonov et al, 1981). Photosynthetic control depends on the balance between proton release in the lumen and the “consumption” of these protons by ATP-synthase, and it is an important process for the regulation of photosynthetic LET. When the ATP/NADPH ratio (1.29) in LET does not satisfy the requirement of that (1.5) for CO2 assimilation (Allen, 2002; Shikanai, 2007; Hahn et al, 2018), cyclic electron flow (CEF) around PSI, which delivers electrons from ferredoxin (Fd) to PQ to form pH without accumulation of NADPH, is driven to balance the production of ATP with NADPH for CO2 fixation (Yamori and Shikanai, 2016)

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