Photosystem II Function and Dynamics in Three Widely Used Arabidopsis thaliana Accessions

Lan Yin,Fikret Mamedov,Mats X Andersson,Benoît Schoefs,Alexander V Vener,Rikard Fristedt,Martine Bertrand,Andrei Herdean,Cornelia Spetea,Katalin Solymosi

doi:10.1371/journal.pone.0046206

Abstract

Columbia-0 (Col-0), Wassilewskija-4 (Ws-4), and Landsberg erecta-0 (Ler-0) are used as background lines for many public Arabidopsis mutant collections, and for investigation in laboratory conditions of plant processes, including photosynthesis and response to high-intensity light (HL). The photosystem II (PSII) complex is sensitive to HL and requires repair to sustain its function. PSII repair is a multistep process controlled by numerous factors, including protein phosphorylation and thylakoid membrane stacking. Here we have characterized the function and dynamics of PSII complex under growth-light and HL conditions. Ws-4 displayed 30% more thylakoid lipids per chlorophyll and 40% less chlorophyll per carotenoid than Col-0 and Ler-0. There were no large differences in thylakoid stacking, photoprotection and relative levels of photosynthetic complexes among the three accessions. An increased efficiency of PSII closure was found in Ws-4 following illumination with saturation flashes or continuous light. Phosphorylation of the PSII D1/D2 proteins was reduced by 50% in Ws-4 as compared to Col-0 and Ler-0. An increase in abundance of the responsible STN8 kinase in response to HL treatment was found in all three accessions, but Ws-4 displayed 50% lower levels than Col-0 and Ler-0. Despite this, the HL treatment caused in Ws-4 the lagest extent of PSII inactivation, disassembly, D1 protein degradation, and the largest decrease in the size of stacked thylakoids. The dilution of chlorophyll-protein complexes with additional lipids and carotenoids in Ws-4 may represent a mechanism to facilitate lateral protein traffic in the membrane, thus compensating for the lack of a full complement of STN8 kinase. Nevertheless, additional PSII damage occurs in Ws-4, which exceeds the D1 protein synthesis capacity, thus leading to enhanced photoinhibition. Our findings are valuable for selection of appropriate background line for PSII characterization in Arabidopsis mutants, and also provide the first insights into natural variation of PSII protein phosphorylation.

Highlights

Chloroplasts are plant organelles performing a unique and complex process named oxygenic photosynthesis, on which aerobic life depends
photosystem II (PSII) is the main target for inactivation by high-intensity light (HL) alone or in combination with other stress factors, a process known as photoinhibition
In this study we report that Ws-4 is the most susceptible to HL, and explain this based on a lipid-Chl-carotenoid stoichiometry in the thylakoid membrane, which is significantly distinct from the one in the other two accessions

Summary

Introduction

Chloroplasts are plant organelles performing a unique and complex process named oxygenic photosynthesis, on which aerobic life depends. The water-oxidizing PSII complex in plants is a supercomplex located exclusively in the grana stacks of the thylakoid membrane. This complex consists of a dimeric core with over 25 subunits per monomer and of a trimeric outer light-harvesting antenna (LHCII), connected to the core via a monomeric inner antenna. To replace the damaged subunit, PSII undergoes a multistep repair cycle This involves reversible phosphorylation of PSII core proteins (D1, D2, CP43 and PsbH) in the grana stacks, PSII monomerization, migration to the nonappressed (stroma) thylakoid regions and partial disassembly, to allow degradation of the damaged D1 and insertion of a new copy Stacking of thylakoids is important for several other processes, including biogenesis of photosynthetic complexes, regulation of light harvesting and thermal dissipation of excess light energy [6]

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