Thioredoxins m are major players in the multifaceted light‐adaptive response in Arabidopsis thaliana

Abstract

SUMMARY Thioredoxins (TRXs) are well‐known redox signalling players, which carry out post‐translational modifications in target proteins. Chloroplast TRXs are divided into different types and have central roles in light energy uptake and the regulation of primary metabolism. The isoforms TRX m1, m2, and m4 from Arabidopsis thaliana are considered functionally related. Knowing their key position in the hub of plant metabolism, we hypothesized that the impairment of the TRX m signalling would not only have harmful consequences on chloroplast metabolism but also at different levels of plant development. To uncover the physiological and developmental processes that depend on TRX m signalling, we carried out a comprehensive study of Arabidopsis single, double, and triple mutants defective in the TRX m1, m2, and m4 proteins. As light and redox signalling are closely linked, we investigated the response to high light (HL) of the plants that are gradually compromised in TRX m signalling. We provide experimental evidence relating the lack of TRX m and the appearance of novel phenotypic features concerning mesophyll structure, stomata biogenesis, and stomatal conductance. We also report new data indicating that the isoforms of TRX m fine‐tune the response to HL, including the accumulation of the protective pigment anthocyanin. These results reveal novel signalling functions for the TRX m and underline their importance for plant growth and fulfilment of the acclimation/response to HL conditions.

Light Intensity- and Spectrum-Dependent Redox Regulation of Plant Metabolism

“…Anthocyanins are pigmented flavonoids, with sugars at position three or sometimes in another position [ 122 ]. Their HL-induced accumulation was demonstrated in Arabidopsis , and this change was redox-associated based on its fine-tuning by isoforms of TRX [ 232 ]. A further relationship of anthocyanins with the redox system is indicated by their antioxidative properties and role in the tolerance to abiotic stress-induced oxidative stress [ 233 ].…”

Comprehensive Expression Analyses of Plastidial Thioredoxins of Arabidopsis thaliana Indicate a Main Role of Thioredoxin m2 in Roots

“…Wild type lines (ecotypes Columbia-0 (Col0) and Landsberg erecta (Ler)) and TRX-defective mutants trxf1 , trxf2 , trxm1 , trxm2 , trxm4 (genetic background Col0) and trxm3 (genetic background Ler) [ 12 , 21 ] of A. thaliana were grown in 0.5× MS medium supplemented with 0.5% sucrose containing 0.8% agarose for root analyses (for confocal and light microscopy analyses and Western blotting assays). In vitro plants were cultured in a growth chamber at 22 °C/21 °C (light/dark) under long-day conditions (16-h-light/8-h-dark) and with a photosynthetically active radiation of 100 µmol photons m −2 s −1 .…”

“…TRX f proteins are of eukaryotic origin, whereas m -type TRXs are of prokaryotic origin [ 7 ]. Several studies have indicated a wide range of different functions in plant processes [ 8 , 9 , 10 , 11 , 12 ], and it is not evident whether TRX diversity suggests functional redundancy or specificity for target proteins in plants. It has been known for several years that chloroplast TRXs regulate processes such as starch metabolism, oxidative stress response, lipid biosynthesis, nitrogen metabolism, protein folding, and translation [ 13 , 14 , 15 ].…”

Current Knowledge on Mechanisms Preventing Photosynthesis Redox Imbalance in Plants

“…NPQ has different components: qE (energy-dependent quenching), qZ (zeaxanthin-dependent quenching), qT (state-transition quenching), qI (photo-inhibitory quenching) and qH (sustained and slowly reversible quenching) [ 80 , 81 , 82 ]. Behind all these photoprotective mechanisms, there is a dynamic redox network in which TRXs play active roles [ 28 ]. It follows now a discussion of the relevance of TRXs in the regulation of the different NPQ components ( Figure 2 ).…”

“…Usually, this PTM has important effects on protein conformation, activity and even stability, hence becoming a dynamic regulatory mechanism in some proteins that can switch between two redox states (thiol/disulphide) or form multiprotein complexes [ 22 , 23 , 24 ]. Some members of the chloroplast thioredoxin (TRX) family were reported to be key players in the redox regulation of light-dependent processes [ 25 , 26 , 27 , 28 ]. TRXs are redox signalling proteins with an active site containing two Cys separated by two amino acid residues (CXXC).…”