Trends in Plant Science
ReviewThe Unprecedented Versatility of the Plant Thioredoxin System
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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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