Exploring the Functional Relationship between y-Type Thioredoxins and 2-Cys Peroxiredoxins in Arabidopsis Chloroplasts.

Ana Jurado-Flores,Víctor Delgado-Requerey,Juan Manuel Pérez-Ruiz,Alicia Gálvez-Ramírez,Francisco Javier Cejudo,Leonor Puerto-Galán

doi:10.3390/antiox9111072

Abstract

Thioredoxins (Trxs) are small, ubiquitous enzymes that catalyze disulphide–dithiol interchange in target enzymes. The large set of chloroplast Trxs, including f, m, x and y subtypes, use reducing equivalents fueled by photoreduced ferredoxin (Fdx) for fine-tuning photosynthetic performance and metabolism through the control of the activity of redox-sensitive proteins. Although biochemical analyses suggested functional diversity of chloroplast Trxs, genetic studies have established that deficiency in a particular Trx subtype has subtle phenotypic effects, leading to the proposal that the Trx isoforms are functionally redundant. In addition, chloroplasts contain an NADPH-dependent Trx reductase with a joint Trx domain, termed NTRC. Interestingly, Arabidopsis mutants combining the deficiencies of x- or f-type Trxs and NTRC display very severe growth inhibition phenotypes, which are partially rescued by decreased levels of 2-Cys peroxiredoxins (Prxs). These findings indicate that the reducing capacity of Trxs f and x is modulated by the redox balance of 2-Cys Prxs, which is controlled by NTRC. In this study, we explored whether NTRC acts as a master regulator of the pool of chloroplast Trxs by analyzing its functional relationship with Trxs y. While Trx y interacts with 2-Cys Prxs in vitro and in planta, the analysis of Arabidopsis mutants devoid of NTRC and Trxs y suggests that Trxs y have only a minor effect, if any, on the redox state of 2-Cys Prxs.

Highlights

Plant chloroplasts have the primary function of synthesizing metabolic intermediates that confer photoautotrophy to these organisms, but these organelles have developed the ability to sense and respond to the environment, which is a crucial function given the sessile lifestyle of plants
The combined deficiency of NTRC and Trxs y led to a slight, but statistically significant, decrease in growth rate compared to ntrc plants, which was more remarkable under short-day (Figure 1C) than in long-day (Figure S2B) conditions
Previous analyses of the genetic interaction of NTRC and chloroplast Trxs have shown that simultaneous deficiencies of these enzymes result in a dramatic inhibition of growth [29,30,40], which correlates with the disruption of the redox homeostasis in the organelle [31,37]

Summary

Introduction

Plant chloroplasts have the primary function of synthesizing metabolic intermediates that confer photoautotrophy to these organisms, but these organelles have developed the ability to sense and respond to the environment, which is a crucial function given the sessile lifestyle of plants. The function of Trx target enzymes, normally active during the day and inactive in the night, is reversibly controlled in response to light and darkness Based on their selectivity for reducing target enzymes in vitro, different functions have been assigned to these Trxs. Trx subtypes are differently abundant within the organelle [9,10] and appear to have functional specificity, genetic studies have shown that plants devoid of individual Trxs, with the exception of Trx z [11], display subtle mutant phenotypes [12,13,14,15] These observations suggest that remaining redox systems may compensate for the function of a specific Trx, highlighting the partial redundancy among chloroplast Trx subtypes

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Conclusion