A circadian clock RD29A is an esterase, relaying PGPR stimuli via RD29B and OPDA signaling in priming plant drought...

Drought is a critical limiting factor to crop production. Efforts to combat this problem through genetic engineering have been difficult to implement without growth tradeoffs. Hence, we recently identified two drought-responsive genes, Response to Desiccation (RD)29A and RD29B, which convey plant growth-promoting rhizobacteria-mediated induced systemic tolerance (IST). IST primes enhanced drought tolerance in plants and, concomitantly, promote their growth and productivity. However, the role and activity of RD29s are largely unknown. In this study, we unravel the autonomous, yet intertwined functions and modes of RD29s. RD29A is a circadian clock esterase and RD29B is a constitutive transcriptional regulator, controlling the oscillatory cycle and induction of RD29A expressions in response to IST-inducing PGPR, Paenibacillus polymyxa CR1. A diurnal peak of RD29A activity then facilitates cellular multitasking, allowing plants to concomitantly run "growth and defense" machineries via perhaps time-sharing of limited energy resources to each operation one by one. In line with these findings, the transient overexpression of Arabidopsis RD29s led to the reconstitution of IST in Solanum lycopersicum and Nicotiana benthamiana. On the contrary, RD29A can relay two different hormone, abscisic acid (ABA) and 12-oxo-phytodienoic acid (OPDA), signaling through distinct cis-regulatory, DRE/ABRE, and TGA elements, respectively. Together, RD29s coordinates general and/or systemic defense processes against various environmental constraints including drought and wounding. We hence conclude that RD29s are unique contenders that uncouple critical aspects of plant defenses; OPDA and ABA crosstalk, IST development, and growth and defense coordination, in shaping the optimal phenomes of plant varieties under different ecological conditions.