Abstract

Photosynthesis is an essential pathway providing the chemical energy and reducing equivalents that sustain higher plant metabolism. It relies on sunlight, which is an inconstant source of energy that fluctuates in both intensity and spectrum. The fine and rapid tuning of the photosynthetic apparatus is essential to cope with changing light conditions and increase plant fitness. Recently PROTON GRADIENT REGULATION 6 (PGR6-ABC1K1), an atypical plastoglobule-associated kinase, was shown to regulate a new mechanism of light response by controlling the homeostasis of photoactive plastoquinone (PQ). PQ is a crucial electron carrier existing as a free neutral lipid in the photosynthetic thylakoid membrane. Perturbed homeostasis of PQ impairs photosynthesis and plant acclimation to high light. Here we show that a homologous kinase, ABC1K3, which like PGR6-ABC1K1 is associated with plastoglobules, also contributes to the homeostasis of the photoactive PQ pool. Contrary to PGR6-ABC1K1, ABC1K3 disfavors PQ availability for photosynthetic electron transport. In fact, in the abc1k1/abc1k3 double mutant the pgr6(abc1k1) the photosynthetic defect seen in the abc1k1 mutant is mitigated. However, the PQ concentration in the photoactive pool of the double mutant is comparable to that of abc1k1 mutant. An increase of the PQ mobility, inferred from the kinetics of its oxidation in dark, contributes to the mitigation of the pgr6(abc1k1) photosynthetic defect. Our results also demonstrate that ABC1K3 contributes to the regulation of other mechanisms involved in the adaptation of the photosynthetic apparatus to changes in light quality and intensity such as the induction of thermal dissipation and state transitions. Overall, we suggests that, besides the absolute concentration of PQ, its mobility and exchange between storage and active pools are critical for light acclimation in plants.

Highlights

  • The photosynthetic conversion of light energy into chemical energy occurs via a series of redox reactions resulting in electron transport along the thylakoid membrane

  • Independent studies indicate that abc1k1 is impaired in nonphotochemical quenching (NPQ) as well as electron transport (Shikanai et al, 1999; Martinis et al, 2014; Pralon et al, 2019), while the abc1k3 mutant did not show defects in those parameters even after prolonged high light exposure (Martinis et al, 2013)

  • To further characterize the abc1k1/abc1k3 double mutant, we measured photosynthetic parameters such as photosystem II (PSII) maximum efficiency [φMAX (= FV/FM)], NPQ as well as electron capacity of the electron transport chain (ETC) in 4–5 weeks old plants grown under moderate light (120 μmol m−2 s−1) (ML) and after 3 h of high light (500 μmol m−2 s−1)

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Summary

Introduction

The photosynthetic conversion of light energy into chemical energy occurs via a series of redox reactions resulting in electron transport along the thylakoid membrane. The linear electron transport begins with water splitting at the level of photosystem II (PSII) and ends at photosystem I (PSI) with the reduction of NADP+ by ferredoxin. Both PSII and PSI utilize photonic energy to fuel the redox reactions. Electrons are transferred from PSII to PSI via the cytochrome b6f complex (cyt b6f ). The PQH2 can diffuse within the thylakoid membrane to reach the QO site of cyt b6f. The proportion of PQ that participates in electron transport in the thylakoid membrane is considered as the photoactive PQ pool; whereas the remaining proportion, which is approximately 60–70% of the total PQ, constitutes the non-photoactive pool and is largely stored inside thylakoid-associated lipid droplets known as plastoglobules (PG) (Kruk and Karpinski, 2006; Block et al, 2013; Ksas et al, 2018)

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