The Role of OPDA Signaling in Induced Systemic Defenses Against Biotic and Abiotic Stresses

Abstract

Plants are vulnerable to a range of biotic and abiotic stressors, which hinder their growth and reduce agricultural yield. Existing management strategies fall short, lacking durable resistant/tolerant cultivars and nontoxic, low-cost pesticides, necessitating an urgent breakthrough, which is not necessarily forthcoming due to an incomplete understanding of plant defense mechanisms and plant growth and defense tradeoffs, a major problem in genetic engineering for plant stress resilience. To understand if and how plants co-ordinate growth and defense responses, we exploited the role and mode of plant growth-promoting rhizobacteria (PGPR)-mediated ‘induced systemic resistance (ISR) and tolerance (IST),’ phenomena capable of priming broad-spectrum durable resistances without the usually accompanied growth penalty to biotic and abiotic stresses, respectively. This study describes that 12-oxophytodienoic acid (OPDA) acts as i) local defense and ii) long-distance phloem-mobile systemic defense signals in ISR, stimulating the cyclophilin 20-3 (CYP20-3)-mediated activation of two-component system, consisting of glutaredoxin transcriptional regulators (e.g., GRX480) and TGA transcription factors (e.g., TGA2, TGA5, TGA6). The GRX/TGA pathway then recruits the nonexpresser of PR1 (NPR1) and conveys both OPDA and salicylic acid (SA) signaling, which prime disease resistance in local and systemic tissues against a broad range of pathogens, including bacterial and fungal microbes and plant parasitic nematodes. Besides biotic stresses, the crosstalk between OPDA and SA signaling simultaneously runs ‘growth and defense machinery’ against abiotic stresses, especially drought. Recently, we have identified two drought-responsive genes, RESPONSIVE TO DESICCATION 29 (RD29)A and RD29B, which are located downstream of the GRX/TGA system, playing an important role in IST development. In the present study, we also found −for the first time− that plants can coordinate cellular multitasking by the circadian rhythmic expression of RD29A, which acts as a noncanonical esterase/hydrolase, and relay CYP20-3/OPDA signaling in priming IST against drought. Although RD29B is also induced by PGPR, we found it to be physiologically distinct from RD29A, acting as a constitutive gene positioned upstream and controlling RD29A-dependent/independent defense responses. Together, we hypothesize CYP20-3-dependent OPDA signaling as a key node helping balance growth and defense against various stresses, synergistically optimizing plant fitness.