Characterization of 12-Oxo-phytodienoic Acid Signaling in Broad-spectrum Plant Defense Responses and Its Coordination with Growth Fitness

Abstract

The jasmonate family of phytohormones plays central roles in plant development and stress acclimation. However, the architecture of their signaling circuits remains largely unknown. Here, we describe the versatile activity of jasmonate family binding protein, cyclophilin 20-3 (CYP20- 3), positioned as a key regulator in controlling the interface between 12-oxo-phytodienoic acid (OPDA, defense) and light-dependent redox (growth) signaling. The latter, also known as the electron (e¯) transport chain (ETC) photosystem I (PSI), is a primary metabolism converting solar energy into biologically useful chemical energies, necessary for the production of overall biomass of plants and living organisms. When the PSI captures solar energy, it excites e¯ that reduce thioredoxins (TRXs) via a ferredoxin (Fd) and a Fd-TRX reductase (FTR). TRXs, small oxidoreductases, then deliver e¯ and activate target enzymes in the Calvin cycle that balances consumption in photosynthesis. The present study validated that TRXs can also reduce other Calvin cycle-unrelated proteins including CYP20-3 and photosynthetic ETC as an e¯ donor of 2- cysteine (Cys) peroxiredoxin A (2CPA). Plastid 2CPA is a thiol-based peroxidase involved in protecting and optimizing photosynthesis. When arrived at the chloroplasts, 2CPA is activated by oxidation folding with GSH (also called, S-glutathionylation), which in turn reduces toxic byproducts (e.g., H2O2) in photosynthesis or activates Calvin cycle enzymes such as a fructose 1,6-bisphosphatase. In line with this scenario, OPDA-binding promotes the interaction of CYP20- 3 with TRXs (esp., type-f2), illuminating the mode of OPDA/CYP20-3 signaling in transferring e¯ from TRX-f2 to SAT1. This then stimulates plastid sulfur assimilations and subsequently GSH accumulations, which coordinates redox-resolved nucleus gene expressions in defense responses against biotic and abiotic stresses, while accelerating the S-glutathionylation (activation) of 2CPA that promotes photosynthetic energy productions, postulating that OPDA/CYP20-3 signaling optimizes 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 3 and vice versa. This model well circumstantiates the responses of plants to the persistent and excess surge of environmental stresses. However, in nature, plants are more often situated to encounter a consistent array of temporal and modest levels of environmental changes, while concurrently trying to ensure normal growth and developmental processes, in order to maximize their yields and production. Hence, recent studies have begun to elaborate an alternative model, “growth and defense coordination”, wherein a balancing act between growth and defense can synergistically optimize plant fitness. In agreement, plant acclimations towards environmental changes and pressures causing oxidative stresses (e.g., tissue injury, excess light and temperature, and drought and salinity) accompany the accumulation of OPDA on a time sale of hours with concomitant accumulation of reduced, nonprotein thiols.