Review
The Unprecedented Versatility of the Plant‎ Thioredoxin System

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A complex cellular network of thioredoxin (Trx) isoforms and reduction pathways, in various organelles, enables plants to cope with fluctuating environments by integrating energy transduction, metabolism, gene expression, and growth.

The chloroplast contains two different thiol-redox systems, and a joint operation seems indispensable for light acclimation and photoautotrophic growth of plants.

The extraplastidial Trxs have been shown to be important in the regulation of different processes such as seed germination, seedling establishment, C, N, and mitochondrial metabolism as well as for plant stress tolerance.

Recent evidence suggests that the mitochondrial Trx system regulates the metabolic flux through the tricarboxylic acid cycle in vivo, being of similar importance as the corresponding system in the plastid.

The map of possible Trx-targets from each subcellular compartment is rapidly increasing.

Thioredoxins are ubiquitous enzymes catalyzing reversible disulfide-bond formation to regulate structure and function of many proteins in diverse organisms. In recent years, reverse genetics and biochemical approaches were used to resolve the functions, specificities, and interactions of the different thioredoxin isoforms and reduction systems in planta and revealed the most versatile thioredoxin system of all organisms. Here we review the emerging roles of the thioredoxin system, namely the integration of thylakoid energy transduction, metabolism, gene expression, growth, and development under fluctuating environmental conditions. We argue that these new developments help us to understand why plants organize such a divergent composition of thiol redox networks and provide insights into the regulatory hierarchy that operates between them.

Section snippets

Plants Contain the Most Versatile Thioredoxin System

Thioredoxins (Trx) are ancient proteins serving as redox regulators in prokaryotic and eukaryotic organisms as different as bacteria, fungi, animals, and plants [1]. Containing a redox-active dithiol in their active site, these small proteins are able to catalyze the reduction of disulfide bonds in many target proteins to regulate their structure and function [1]. For a new catalytic cycle, Trxs are reduced by Trx reductases using NADPH or reduced ferredoxin (Fdx) as electron donors. Unlike

The Role of Chloroplast Thioredoxins in Fluctuating Light Environments

Chloroplast Trxs are important to acclimate photosynthesis and stroma metabolism in fluctuating light intensities. In the 1970s, chloroplast Trxs f and m were discovered as the first Trxs in plants 5, 6. They were found to be reduced via FTR using photosynthetic electrons provided by Fdx, providing a mechanism to regulate the Calvin–Benson cycle, ATP synthesis and the export of reducing equivalents in response to light 7, 8 (Figure 2). These pioneering biochemical experiments and subsequent

The Role of NTRC in Low Light and Fluctuating Light

NTRC is important for chloroplast development and to optimize photosynthesis and growth in low light and fluctuating light. In addition to the light-dependent Fdx/Trx system, chloroplasts contain an NADPH-dependent NTRC consisting of an NTR and a Trx domain on a single polypeptide [4]. NTRC has been found to act independently of light since it can use NADPH produced by the oxidative pentose phosphate pathway in the dark. As indicated in Figure 2 and Table 1, biochemical and genetic studies with

Cooperative Control of Chloroplast Functions via Light and NADPH-dependent Thiol Redox Systems

Cooperative control of chloroplast functions via light- and NADPH-dependent thiol redox systems is essential for plant viability, growth and development. Recent studies provided genetic evidence that Fdx–Trx and NADPH–NTRC redox systems coordinately participate to regulate chloroplast functions and plant growth (Figure 2 and Table 1). An arabidopsis double mutant with combined deficiency of Trx f1 and NTRC revealed a severe growth retardation phenotype and was not viable under low light

The Role of Extraplastidial Thioredoxins

Although the Trx system was discovered in the chloroplast and the majority of work on Trxs has centered on their operation in this organelle, work in the last two decades has broadened the Trx horizon to include operation in the mitochondria, cytosol, and nucleus 16, 45. In the current review we limit ourselves to general mechanisms operating at the cellular level, documenting current knowledge concerning the impact of the Trx system on regulation of mitochondrial and cytosolic function as well

The Role of Mitochondrial Thioredoxin for Metabolic Flux

Mitochondrial Trx regulates the metabolic flux through the tricarboxylic acid cycle. Evidence that plant mitochondria, like their animal counterparts, contain Trx was first reported in a seminal paper in 1989 [46] and the protein was purified from spinach mitochondria shortly thereafter [47]. Characteristic mitochondrial Trx o and a mitochondrial NTR were subsequently identified [48]. The completion of the arabidopsis genome revealed two Trx o genes alongside NTRA and demonstrated that AtTrx o1

Cytosolic, ER, and Nuclear Trxs Are Involved in Biotic and Abiotic Stress Responses

Besides the plastid and mitochondria, Trxs can also be found in the cytosol, ER and nucleus of plant cells. Although relatively little is known concerning the function of nucleoredoxins (Nrx) and ER-Trxs, the function of cytosolic Trx h has been well documented (reviewed in [60]). Although the majority of h-type Trxs are found in the cytosol, representatives have also been reported to reside in the plasma membrane [61] and mitochondria [62], the apoplastic space [63], the nucleus [64], and the

Interorganellar Crosstalk between Thioredoxins

In the preceding sections we have presented overviews of the molecular characterization and function of the various Trxs on a subcellular compartment basis. Whilst being a practical way to cover the subject, it is clear, and we have indeed already alluded to the fact, that in reality all of these organellar systems are operating in tandem. The complexity of the interorganellar redox-communication is evidenced by the number of targets that have been already identified to be Trx-regulated in each

Concluding Remarks and Future Outlook

While past research into Trxs mainly focused on biochemical studies on their specificities for different target enzymes, recent studies elucidated the organization and biological significance of this complex thiol redox network in planta. The chloroplast is unique in harboring light and NADPH-dependent Trx systems operating cooperatively to allow dynamic acclimation of photosynthesis in fluctuating light. Joint operation of these two different chloroplast thiol redox systems is indispensable

Acknowledgments

The authors thank the Deutsche Forschungsgemeinschaft for funding (grants SFB-TR 175 B02 to P.G. and B04 to A.R.F.).

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