Reversible down-regulation of photosystems I and II leads to fast photosynthesis recovery after long-term drought in Jatropha curcas

Abstract

Jatropha curcas is a drought-tolerant plant that maintains the photosynthetic pigments under prolonged drought, and quickly regains its photosynthetic capacity when water is available. It has been reported that drought stress leads to increased thermal dissipation in photosystem (PS) II, but that of PSI has been barely investigated, one reason which could be a technical limitation in measuring the PSI absolute quantum yield. In this study, we combined biochemical analysis and spectroscopic measurements using an integrating sphere and verified that the quantum yields of both photosystems are temporarily down-regulated under drought. We found that the decrease in the quantum yield of PSII was accompanied by a decrease in the core complexes of PSII while light-harvesting complexes are maintained under drought. In addition, in drought-treated plants, we observed a decrease in the absolute quantum yield of PSI as compared to the well-watered control, while the amount of PSI did not change, indicating that non-photochemical quenching occurs in PSI. The down-regulation of both photosystems was quickly lifted in a few days upon re-watering. Our results indicate, that in Jatropha curcas under drought, the down-regulation of both PSII and PSI quantum yield protects the photosynthetic machinery from uncontrolled photodamage.

Non-photochemical quenching of photosystem I as an adaptive response to prolonged drought

“…Compelling evidence for NPQ in PSI-LHCI of J. curcas was obtained after monitoring the difference in fluorescence intensity at low temperature between purified PSI-LHCI complexes of control and drought-stressed plants using an integrating sphere with which the numbers of photons absorbed by both complexes were normalized. Another important finding was that zeaxanthin remained high during darkness in J. curcas ( Sapeta et al , 2023 ), suggesting that, together with flexible NPQ in PSII-LHCII, sustained, ΔpH-independent thermal dissipation also occurred in J. curcas during drought stress as observed in evergreen species adapted to endure unfavorable conditions over their seasonal life cycle ( Demmig-Adams and Adams, 2006 ). Intriguingly, the kinetic analysis of the low temperature decay-associated spectra showed a significant decrease in the overall fluorescence lifetime of PSII-LHCII after prolonged drought stress, while the overall lifetime of PSI-LHCI showed insignificant variation, a result that Sapeta et al .…”

“…Excess excitation energy (EEE) dissipation in photosystem II (PSII) is well established, while it is less studied and documented for PSI. Using Jatropha curcas , a semi-evergreen, tropical, non-edible oil-seed-bearing shrub, Sapeta et al (2023) provide evidence for the significance of energy quenching in PSI under prolonged drought. Jatropha curcas receives considerable attention for sustainable (green) manufacturing of biodiesel and is recognized for its high tolerance to drought, capable of arresting growth while maintaining steady shoot water content and green leaves after several weeks of water withdrawal.…”

“…singlet oxygen) should be less efficient in PSI-LHCI than in PSII-LHCII. In this context, elucidating whether or not PSI-LHCI can realize NPQ is the challenge faced by Sapeta et al . (2023) and other plant spectroscopists.…”

“…In the npq2 mutant of A. thaliana , zeaxanthin was claimed to induce NPQ in LHCI when connected to PSI ( Ballottari et al , 2014 ), but no evidence was found for NPQ in PSI-LHCI of wild-type plants even when PSI-LHCI accumulated zeaxanthin molecules after the plants were exposed to a short high light stress (Tian et al ., 2017). Because of the divergent conclusions on the biological significance of the potential role of zeaxanthin in NPQ in PSI-LHCI, Sapeta et al . (2023) endeavored to use an alternative spectroscopic approach with PSI-LHCI of J. curcas .…”

“…This shrub can stand prolonged periods of drought by up-regulating abscisic acid (ABA) synthesis, chlorophyll metabolism, and ROS-detoxifying enzymes ( Sapeta et al , 2016 ). An important finding of particular interest for the spectroscopic analysis of NPQ in PSI-LHCI was that this photosynthetic complex in J. curcas could accumulate large amounts of zeaxanthin by efficient conversion of violaxanthin to zeaxanthin and de novo synthesis of zeaxanthin during exposure to water deficit for weeks ( Sapeta et al , 2023 ). This represents a notable advantage compared with the former two studies performed on A. thaliana , in which either zeaxanthin was constitutively present in npq2 at high levels independent of the light treatment, or zeaxanthin accumulation in PSI-LHCI of wild-type A. thaliana plants briefly exposed to high light stress was lower than that found in PSI-LHCI of J. curcas after prolonged water withdrawal (~2–2.4 zeaxanthin molecules per 100 chlorophyll molecules).…”