Fast structural remodeling of Jatropha curcas thylakoids upon recovery underpins chloroplast resilience to drought

Abstract Jatropha curcas is a moderate stem-succulent oil crop renowned for its drought tolerance. While the photosynthetic activity of drought-stressed and rewatered Jatropha curcas has been investigated, little is known about the effects of drought and rewatering on chloroplast integrity and thylakoid architecture, critical determinants of photosynthetic performance under stress. Here, we exposed J. curcas seedlings to 19 days of water withdrawal followed by rewatering. Leaf relative water content remained unchanged throughout, indicating efficient water retention. Leaf anatomy was largely preserved, but chloroplasts became slightly smaller. Small-angle neutron scattering and transmission electron microscopy revealed a 2–4 nm decrease in granum repeat distance under drought. Electron microscopy further showed that this decrease was stronger in palisade than in spongy parenchyma chloroplasts. In thylakoids, the photosynthetic complexes were adjusted differently under drought: photosystem (PS) I and light harvesting complex (LHC) II remained unchanged, whereas PSII complexes decreased, increasing the PSI/PSII and LHCII/PSII ratios. Among the remaining PSII, larger supercomplexes were proportionally enriched, suggesting their higher drought stability. These changes coincided with a moderate decrease in PSII activity ( F v /F m ) and increased non-photochemical quenching. After rewatering, granum repeat distances recovered within hours (0.5–1 h in spongy and 5 h in palisade chloroplasts), revealing the involvement of rapidly reversible membrane remodeling under drought, while full recovery of photosynthetic performance and thylakoid protein composition was slower, requiring days. The high plasticity and rapid recovery of the thylakoid architecture is proposed to enable Jatropha curcas to restore its drought-affected photosynthetic apparatus and resume photosynthesis once water becomes available.