M-type thioredoxins are involved in the xanthophyll cycle and proton motive force to alter NPQ under low-light conditions in Arabidopsis

Abstract

M-type thioredoxins are required to regulate zeaxanthin epoxidase activity and to maintain the steady-state level of the proton motive force, thereby influencing NPQ properties under low-light conditions in Arabidopsis. Non-photochemical quenching (NPQ) helps protect photosynthetic organisms from photooxidative damage via the non-radiative dissipation of energy as heat. Energy-dependent quenching (qE) is a major constituent of NPQ. However, the mechanism underlying the regulation of qE is not well understood. In this study, we demonstrate that the m-type thioredoxins TRX-m1, TRX-m2, and TRX-m4 (TRX-ms) interact with the xanthophyll cycle enzyme zeaxanthin epoxidase (ZE) and are required for maintaining the redox-dependent stabilization of ZE by regulating its intermolecular disulfide bridges. Reduced ZE activity and accumulated zeaxanthin levels were observed under TRX-ms deficiency. Furthermore, concurrent deficiency of TRX-ms resulted in a significant increase in proton motive force (pmf) and acidification of the thylakoid lumen under low irradiance, perhaps due to the significantly reduced ATP synthase activity under TRX-ms deficiency. The increased pmf, combined with acidification of the thylakoid lumen and the accumulation of zeaxanthin, ultimately contribute to the elevated stable qE in VIGS-TRX-m2m4/m1 plants under low-light conditions. Taken together, these results indicate that TRX-ms are involved in regulating NPQ-dependent photoprotection in Arabidopsis.

The zeaxanthin epoxidase is degraded along with the D1 protein during photoinhibition of photosystem II

“…Like ntrc mutants, also trxm mutants accumulate higher levels of Zx than wild-type plants upon illumination at non-saturating light intensities. Moreover, this work provided evidence for a redox modification of ZEP and a direct interaction of Trx m and ZEP (Da et al, 2017). These data underline, that the ZEP protein becomes (at least partially) inactive in darkness along with the oxidation of Trx, and requires light activation through the Trx system for full activity.…”

“…Although no redox modification of the ZEP was detectable in that work, reduction of sulfhydryl group of the ZEP protein by either NTRC or via thioredoxins (Trx) may be involved in the regulation of ZEP activity. The latter idea was strongly supported by recent analyses of Arabidopsis plants with silenced Trx m proteins (Da et al, 2017). Like ntrc mutants, also trxm mutants accumulate higher levels of Zx than wild-type plants upon illumination at non-saturating light intensities.…”

“…However, the molecular basis of ZEP regulation is not fully understood. Recent work showed that ZEP activity is regulated in the short‐term by Trx (Da et al, ) and NTRC (Naranjo et al, ), implying an essential function of redox‐sensitive sulfhydryl groups of ZEP protein in regulation. On basis of the proposed redox regulation, it can be assumed that ZEP has low or no activity in the dark, and is fully activated under illumination through Trx mediated reduction of specific sulfhydryl groups.…”

Regulation of cyclic electron flow by chloroplast NADPH‐dependent thioredoxin system

“…Light-dependent reductive activation of the ATP synthase, the CBC, and the NADP-malate dehydrogenase (NADP-MDH) by TRXs has been well established for several decades (reviewed in Buchanan, 2016). More recently, knowledge of TRX-mediated control has been extended to various regulatory and photoprotective mechanisms of photosynthesis, including regulation of state transitions (Rintamäki, Martinsuo, Pursiheimo, & Aro, 2000;Shapiguzov et al, 2016), NPQ (Brooks, Sylak-Glassman, Fleming, & Niyogi, 2013;Da et al, 2017;Hall et al, 2010;Naranjo et al, 2016) and CEF (Courteille et al, 2013;Hertle et al, 2013;Strand, Fisher, Davis, et al, 2016). We propose here a model, comprising a cooperative function of the two chloroplast TRX systems with distinct reductants and redox potentials that allows the maintenance of redox balance between the two photosystems and stromal metabolism during fluctuations in light conditions.…”

Multilevel regulation of non‐photochemical quenching and state transitions by chloroplast NADPH‐dependent thioredoxin reductase

“…Based on our results from OE-NTRC and ntrc together with other recent reports on ntrc mutant, we suggest that stromal thiol redox state regulates the induction of NPQ via multiple mechanisms. Firstly by affecting pmf generation through control of the ATP synthase and CEF pathways (Carrillo et al 2016, Naranjo et al 2016, Nikkanen et al 2016, Nikkanen et al 2018, secondly through regulation of the xanthophyll cycle (Da et al 2018), and thirdly, through a new type of ΔpH-independent PSII antenna quenching mechanism involving lumenal lipocalin and named qH (Malnoë et al 2017). Suppression of qH occurs via a thioredoxin-like protein SOQ1 in thylakoid membranes (Brooks et al 2013).…”