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

Abstract

In plants, growth-defense trade-offs occur because of limited resources, which demand prioritization towards either of them depending on various external and internal factors. However, very little is known about molecular mechanisms underlying their occurrence. Here, we describe that cyclophilin 20-3 (CYP20-3), a 12-oxo-phytodienoic acid (OPDA)–binding protein, crisscrosses stress responses with light-dependent electron reactions, which fine-tunes activities of key enzymes in plastid sulfur assimilations and photosynthesis. Under stressed states, OPDA, accumulates in the chloroplasts, binds and stimulates CYP20-3 to convey electrons towards serine acetyltransferase 1 (SAT1) and 2-Cys peroxiredoxin A (2CPA). The latter is a thiol-based peroxidase, protecting and optimizing photosynthesis by reducing its toxic byproducts (e.g., H2O2). Reduction of 2CPA then inactivates its peroxidase activity, suppressing the peroxide detoxification machinery, whereas the activation of SAT1 promotes thiol synthesis and builds up reduction capacity, which in turn triggers the retrograde regulation of defense gene expressions against abiotic stress. Thus, we conclude that CYP20-3 is a unique metabolic hub conveying resource allocations between plant growth and defense responses (trade-offs), ultimately balancing optimal growth phonotype.

12-oxo-Phytodienoic Acid: A Fuse and/or Switch of Plant Growth and Defense Responses?

“…It is, however, still unclear how these signaling mechanisms ultimately stimulate global, spatiotemporal gene expression dynamics with both distinctive and redundant transcriptional outputs. Our study suggests though that OPDA can target and fine-tune an interface between photosynthesis-derived ETC and sulfur assimilation processes in the chloroplasts (Cheong et al, 2017;Liu et al, 2020). This interplay enables plants to make an adaptive decision in allocating resources (e − ) between growth and defense responses (e.g., fitness trade-offs or balances) toward different ecological challenges such as pathogens, pests, tissue injury as well as light and oxidative stresses, in the end, ensuring optimal growth, reproduction, and survival of plants.…”

“…As described in this review, the emerging evidence has espied that OPDA is a versatile signal molecule involved in a variety of metabolic pathways, coordinating plant growth and survival in optimal condition as well as under various forms of environmental stresses (Table 1). In the recent decade, a large number of efforts have been devoted and begun to delineate the mechanistical modus operandi of OPDA signaling; thus far, three working Regulation of seed dormancy and germination Inhibition of primary root growth Stintzi et al, 2001;Buseman et al, 2006;Mueller et al, 2008;Park et al, 2013;Dave et al, 2016;Gleason et al, 2016;Balfagón et al, 2019;Liu et al, 2020.…”

“…Plastid 2CPA is a thiol-based peroxidase involved in protecting and optimizing photosynthesis. When arrived at the chloroplasts, 2CPA is activated by either different e − donors such as NADPH-dependent TRX reductase C (NTRC), TRXs, and CYP20-3, or—as recently proposed—oxidation folding with GSH (also called S-glutathionylation), which in turn reduces toxic by-products (e.g., H 2 O 2 ) in photosynthesis or activates Calvin cycle enzymes such as a fructose 1,6-bisphosphatase (Konig et al, 2002 ; Peltier et al, 2006 ; Caporaletti et al, 2007 ; Laxa et al, 2007 ; Muthuramalingam et al, 2009 ; Liebthal et al, 2016 ; Pérez-Ruiz et al, 2017 ; Liu et al, 2020 ).…”

“…In this context, OPDA binding promotes the interaction of CYP20-3 with TRXs (e.g., type-f2 and x; Cheong et al, 2017 ), illuminating a mode of OPDA/CYP20-3 signaling in transferring e − from TRXs to 2CPA and/or SAT1 ( Figure 3 , orange arrow). The latter then stimulates plastid sulfur assimilations (e.g., GSH and thiol accumulations), which coordinate redox-resolved nucleus gene expressions in defense responses against biotic and abiotic stresses (Park et al, 2013 ), while accelerating the S-glutathionylation (activation) of 2CPA that promotes photosynthetic energy productions (Liu et al, 2020 ), postulating that OPDA/CYP20-3 signaling optimizes the growth, reproduction, and survival of plants under constant environmental stresses. Traditionally, the cost of resistance (often referred to as growth and defense tradeoff) has been typically described as a teeter-totter model where for defense to increase, growth must decrease and vice versa (Huot et al, 2014 ).…”

The In Vitro Interaction of 12-Oxophytodienoic Acid and Related Conjugated Carbonyl Compounds with Thiol Antioxidants

“…2-CysPRX and TRX-m1 physically interact with Cyp20-3 and regulate Cyp20-3 activity in response to redox alterations [ 32 , 33 , 45 , 46 ]. This type of reversible activity regulation involves Cys sidechains of Cyp20-3.…”