Chloroplastic thioredoxin-f and thioredoxin-m1/4 play important roles in brassinosteroids-induced changes in CO2 assimilation and cellular redox homeostasis in tomato.

Fei Cheng,Jie Zhou,Yan-Hong Zhou,Kai Shi,Jing-Quan Yu,Xiao-Jian Xia

doi:10.1093/jxb/eru207

Abstract

Chloroplast thioredoxins (TRXs) and glutathione function as redox messengers in the regulation of photosynthesis. In this work, the roles of chloroplast TRXs in brassinosteroids (BRs)-induced changes in cellular redox homeostasis and CO2 assimilation were studied in the leaves of tomato plants. BRs-deficient d (^im) plants showed decreased transcripts of TRX-f, TRX-m2, TRX-m1/4, and TRX-x, while exogenous BRs significantly induced CO2 assimilation and the expression of TRX-f, TRX-m2, TRX-m1/4, and TRX-x. Virus-induced gene silencing (VIGS) of the chloroplast TRX-f, TRX-m2, TRX-m1/4, and TRX-y genes individually increased membrane lipid peroxidation and accumulation of 2-Cys peroxiredoxin dimers, and decreased the activities of the ascorbate-glutathione cycle enzymes and the ratio of reduced glutathione to oxidized glutathione (GSH/GSSG) in the leaves. Furthermore, partial silencing of TRX-f, TRX-m2, TRX-m1/4, and TRX-y resulted in decreased expression of genes involved in the Benson-Calvin cycle and decreased activity of the associated enzymes. Importantly, the BRs-induced increase in CO2 assimilation and the increased expression and activities of antioxidant- and photosynthesis-related genes and enzymes were compromised in the partially TRX-f- and TRX-m1/4-silenced plants. All of these results suggest that TRX-f and TRX-m1/4 are involved in the BRs-induced changes in CO2 assimilation and cellular redox homeostasis in tomato.

Highlights

Accumulating evidence supports the hypothesis that the cellular redox signalling and hormone signalling pathways form an integrated redox–hormone network that regulates many plant growth- and defence-related pathways (Bartoli et al, 2013)
Exogenous application of EBR increased Vc,max and Jmax only in the pTRV, pTRV-TRXm2, and pTRV-TRX-y plants and not in the pTRV-TRX-f, pTRV-TRX-m1/4, and pTRV-TRX-x plants. All of these results indicated that chloroplastic TRX-f, TRX-m2, TRXm1/4, and TRX-y are involved in the regulation of CO2 assimilation, whereas only TRX-f and TRX-m1/4 play a role in the EBR-induced increase in CO2 assimilation
Histochemical staining demonstrated that more O2·− and H2O2 accumulates in the leaves of the Virus-induced gene silencing (VIGS)-TRX-f/TRX-m pea plants compared with control plants, confirming that TRX-f and TRX-m are important for the metabolic balance of reactive oxygen species (ROS) in plant cells (Luo et al, 2012)

Summary

Introduction

Accumulating evidence supports the hypothesis that the cellular redox signalling and hormone signalling pathways form an integrated redox–hormone network that regulates many plant growth- and defence-related pathways (Bartoli et al, 2013). Redox regulation is often mediated by thioredoxins (TRXs), which are able to (de-)activate enzymes through the reversible reduction of disulphide bonds (Buchanan and Balmer, 2005; Montrichard et al, 2009). The short peptide motif WC(G/P)PC, with two conserved cysteine residues, has been characterized as the conserved active redox site of TRXs (Jacquot et al, 1997; Buchanan and Balmer, 2005; Meyer et al, 2008). Plant cells contain numerous TRXs in the cytosol, nucleus, mitochondria, endoplasmic reticulum, and chloroplasts, which continue to be identified (Marcus et al, 1991; Baumann and Juttner, 2002; Meyer et al, 2005). Recent proteomic studies using TRX-trapping chromatography or labelled gel electrophoresis in combination with protein identification via mass spectrometry have identified >180 potential in vitro

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