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A primary precursor of jasmonates, 12-oxo-phytodienoic acid (OPDA), is an autonomous hormone signal that activates and fine-tunes plant defense responses, as well as growth and development. However, the architecture of its signaling circuits remains largely elusive. Here we describe that OPDA signaling drives photosynthetic reductant powers toward sulfur assimilation in the chloroplasts, incorporating sulfide into cysteine. Under stressed states, OPDA-accumulated in the chloroplasts-binds and promotes cyclophilin 20-3, an OPDA receptor, to transfer electrons from thioredoxin F2, an electron carrier in the photosynthesis reaction, to serine acetyltransferase 1 (SAT1). The charge carrier (H+, e-) then splits dimeric SAT1 trimers in half to signal the recruitment of dimeric O-acetylserine(thiol)lyase B, forming a hetero-oligomeric cysteine synthase complex (CSC). CSC formation and its metabolic products (especially glutathione) then coordinate redox-resolved retrograde signaling from the chloroplasts to the nucleus in adjusting expression of OPDA-responsive genes such as GLUTAREDOXIN 480 and CYTOCHROME P450, and triggering defense responses against various ecological constraints such as salinity and excess oxidants, as well as mechanical wounding. We thus conclude that OPDA signaling regulates a unique metabolic switch in channeling light input into outputs that fuel/shape a multitude of physiological processes, optimizing plant growth fitness and survival capacity under a range of environmental stress cues., (© The Author(s) 2024. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For commercial re-use, please contact reprints@oup.com for reprints and translation rights for reprints. All other permissions can be obtained through our RightsLink service via the Permissions link on the article page on our site—for further information please contact journals.permissions@oup.com.)