Cyclophilin 20–3 is positioned as a regulatory hub between light-dependent redox and 12-oxo-phytodienoic acid signaling

Abstract

The jasmonate family of phytohormones plays central roles in plant development and stress acclimation. However, the regulatory modes of their signaling circuitry remain largely unknown. Here we describe that cyclophilin 20–3 (CYP20–3), a binding protein of (+)-12-oxo-phytodienoic acid (OPDA), crisscrosses stress responses with light-dependent redox reactions, which fine-tunes the activity of key enzymes in the plastid photosynthetic carbon assimilation and sulfur assimilation pathways. Under stressed states, OPDA – accumulated in the chloroplasts – binds and promotes CYP20–3 to transfer electron (e−) from thioredoxins (i.e., type-f2 and -x) to 2-Cys peroxiredoxin B (2-CysPrxB) or serine acetyltransferase 1 (SAT1). Reduction (activation) of 2-CysPrxB then optimizes peroxide detoxification and carbon metabolisms in the photosynthesis, whereas the activation of SAT1 stimulates sulfur assimilation which in turn coordinates redox-resolved nucleus gene expressions in defense responses against biotic and abiotic stresses. Thus, we conclude that CYP20–3 is positioned as a unique metabolic hub in the interface between photosynthesis (light) and OPDA signaling, where controls resource (e−) allocations between plant growth and defense responses.

CYP20-3 deglutathionylates 2-CysPRX A and suppresses peroxide detoxification during heat stress

“…A series of protein–protein interaction and DNA protection analyses have inferred that CYP20-3 is another electron donor of 2CPs ( Laxa et al, 2007 ; Muthuramalingam et al, 2009 ; Cheong et al, 2017 ), but our redox-shifting assays did not detect any reductase activity of CYP20-3 towards 2CPs GS ( Fig S7 ). We therefore speculated whether CYP20-3 confers rather PPIase activity and protects 2CPs GS from thermal aggregations (at 45°C, Bhuwan et al, 2017 ).…”

“…Under stressed conditions, OPDA, accumulates in the chloroplasts, binds and promotes CYP20-3 to transfer electrons from the photosystem I (PSI) via TRXs (type-f2 and -x) towards 2CPs (Motohashi et al, 2001;Laxa et al, 2007;Dominguez-Soils et al, 2008;Cheong et al, 2017) or a serine acetyltransferase 1 (SAT1, Dominguez-Soils et al, 2008;Park et al, 2013). Reduction of 2CPs then controls peroxide (photo-oxidant) detoxifications and photosynthetic carbon metabolisms (Dietz et al, 2006;Caporaletti et al, 2007), whereas the activation of SAT1 stimulates the plastid sulfur assimilation, which leads to the production of Cys and thiol metabolites (e.g., glutathione; GSH), and the buildup of cellular reduction potential (Park et al, 2013).…”

“…Among several plastid enzymes of which transcripts are coregulated with 2CPs, stromal CYP20-3 is one that appeared to directly interact with them ( Muthuramalingam et al, 2009 ; Cheong et al, 2017 ). CYP20-3 is a dual enzyme, exerting chaperon (i.e., peptidyl-prolyl cis – trans isomerase and PPIase) and reductase activities ( Laxa et al, 2007 ; Park et al, 2013 ), positioned as a regulatory hub between the light-dependent reaction in photosynthesis and 12- oxo -phytodienoic acid (OPDA) signaling ( Cheong et al, 2017 ).…”

“…Among several plastid enzymes of which transcripts are coregulated with 2CPs, stromal CYP20-3 is one that appeared to directly interact with them ( Muthuramalingam et al, 2009 ; Cheong et al, 2017 ). CYP20-3 is a dual enzyme, exerting chaperon (i.e., peptidyl-prolyl cis – trans isomerase and PPIase) and reductase activities ( Laxa et al, 2007 ; Park et al, 2013 ), positioned as a regulatory hub between the light-dependent reaction in photosynthesis and 12- oxo -phytodienoic acid (OPDA) signaling ( Cheong et al, 2017 ). OPDA is a primary precursor of (-)-jasmonic acid (JA), able to trigger an autonomous signaling pathway that regulates unique subsets of jasmonate-responsive genes, activating and fine-tuning plant defense responses, as well as growth processes ( Bӧttcher & Pollmann, 2009 ; Dave & Graham, 2012 ).…”

“…Gels were stained with Coomassie Brilliant Blue, and standard molecular weight sizes were indicated in the left of gels. Source data are available for this figure. electron transfers from TRX-f2 to both SAT1 and 2CPA GS (Cheong et al, 2017). Reduction (deglutathionylation) of 2CPA GS then inactivates photooxidant detoxification and energy biogenesis (Figs 4 and 5), whereas the activation of SAT1 stimulates CSC formation and builds up reduction capacity, which in turn triggers the retrograde regulation of defense gene expression (Park et al, 2013;Cheong et al, 2017).…”