Single Cystathionine β-Synthase Domain–Containing Proteins Modulate Development by Regulating the Thioredoxin System in Arabidopsis    

Abstract

Plant thioredoxins (Trxs) participate in two redox systems found in different cellular compartments: the NADP-Trx system (NTS) in the cytosol and mitochondria and the ferredoxin-Trx system (FTS) in the chloroplast, where they function as redox regulators by regulating the activity of various target enzymes. The identities of the master regulators that maintain cellular homeostasis and modulate timed development through redox regulating systems have remained completely unknown. Here, we show that proteins consisting of a single cystathionine b-synthase (CBS) domain pair stabilize cellular redox homeostasis and modulate plant development via regulation of Trx systems by sensing changes in adenosine-containing ligands. We identified two CBS domain-containing proteins in Arabidopsis thaliana, CBSX1 and CBSX2, which are localized to the chloroplast, where they activate all four Trxs in the FTS. CBSX3 was found to regulate mitochondrial Trx members in the NTS. CBSX1 directly regulates Trxs and thereby controls H 2 O 2 levels and regulates lignin polymerization in the anther endothecium. It also affects plant growth by regulating Calvin cycle enzymes, such as malate dehydrogenase, via homeostatic regulation of Trxs. Based on our findings, we suggest that the CBSX proteins (or a CBS pair) are ubiquitous redox regulators that regulate Trxs in the FTS and NTS to modulate development and maintain homeostasis under conditions that are threatening to the cell.

A Medicago truncatula Cystathionine-β-Synthase-like Domain-Containing Protein Is Required for Rhizobial Infection and Symbiotic Nitrogen Fixation

“…Mutations in CBS domains impair the function of the associated enzymes (Kushwaha et al, 2009). Enzyme activation by CBS proteins occurs through binding to S-adenosylMet, AMP, or ATP, which changes the CBS pair domain structure and thereby activates the enzyme (Kushwaha et al, 2009;Yoo et al, 2011).…”

“…Perhaps, as we speculated above, MtCBS1 is involved in formation of the IT wall. Interestingly, in Arabidopsis it has been shown that a single soluble CBS domain-containing protein regulates cellular redox homeostasis by interacting with thioredoxin and thereby controls maturation of the cell wall (Yoo et al, 2011). Currently, it is thought that regulation of reactive oxygen species (ROS) in the IT is important to ensure an appropriate level of cross linking within the plant cell wall to maintain its integrity while allowing IT growth and bacterial infection (Santos et al, 2001;Brewin, 2004;Jamet et al, 2007).…”

Comparative Transcriptomic Approaches Exploring Contamination Stress Tolerance in Salix sp. Reveal the Importance for a Metaorganismal de Novo Assembly Approach for Nonmodel Plants

“…Calvin cycle CP12 (Fig. 3), a small chloroplast protein increasingly recognized as master regulator of the Calvin cycle, complexes to downregulate GAPDH under oxidative conditions to form the binary complex A4-GAPDH/CP12, which strongly suppresses GAPDH activity (see GAPDH expression above; Wedel et al, 1997;Gontero and Maberly, 2012;Michelet et al, 2013;López-Calcagno et al, 2014) and is essential to the leaves' response to abiotic/oxidative stress (Yoo et al, 2011). The consistent up-regulation of universal stress protein and isoprene synthesis also agrees with the high abiotic stress conditions potentially produced by hydrocarbon contamination (Maqbool RNA biding proteins are emerging as regulators of plant responses to environmental stress (Ambrosone et al, 2012).…”

Genome-Wide Association Mapping Combined with Reverse Genetics Identifies New Effectors of Low Water Potential-Induced Proline Accumulation in Arabidopsis

“…Regions 15 and 47 also contain thioredoxin genes, and region 73 contains CYSTATHIONINE b-SYNTHASE DOMAIN-CONTAINING PROTEIN3 (CBSX3). CBSX3 is one of several CBSX proteins that regulate the thioredoxin system (Yoo et al, 2011). Investigation of these genes may reveal additional details of the connection of Pro metabolism to redox status.…”