Light and High Temperature Dependent Decline in Photosystem II Efficiency in Holcus Is Associated with Photoprotective Roles of Volatile Signals Methyl Salicylate and cis-β-Ocimene

Leaves must sustain high rates of photosynthesis to support growth while avoiding over-reduction of the chloroplast electron transport chain and the formation of damaging reactive oxygen species during daily exposure to high light and temperature. This challenge is particularly acute for C₃ species such as Holcus lanatus, which experience high rates of photorespiration under the warm, high-light conditions typical of grassland ecosystems.In leaves of H. lanatus at the Point Reyes Field Station (California, USA), we observed a pronounced midday decline (approximately ten-fold) in the quantum efficiency of photosystem II (ΦPSII) despite elevated electron transport rates (ETR), temperature, and incident light, followed by full recovery in the evening. Controlled light- and temperature-response experiments revealed that net CO₂ assimilation, ETR, and volatile organic compound (VOC) emissions remained tightly coupled during periods of ΦPSII suppression, indicating sustained biosynthetic activity even as photochemical efficiency declined.Among emitted VOCs, methyl salicylate (MeSA) and cis-β-ocimene—derived from the shikimate and isoprenoid pathways and linked to the Calvin–Benson cycle through carbon skeleton supply—showed strong light and temperature responsiveness. In contrast, α-pinene and sabinene emissions were largely light-independent and negatively temperature-sensitive. Given their established roles as potent phytohormones, these observations raise the possibility that photosynthesis-derived compounds such as MeSA and cis-β-ocimene act as internal feedback signals regulating the photosynthetic light reactions.Although trans-β-ocimene is widely regarded as the dominant isomer in plant emissions, particularly under biotic stress, our sequence analysis predicts that approximately 18% of β-ocimene-producing species possess a cis-β-ocimene synthase, including a validated plastid-localized example in Cannabis sativa. By comparison, UniProt currently annotates cis-β-ocimene synthases in only ~7% of species. Together, these findings suggest three paradigm shifts: (i) photosynthetic products such as MeSA may directly regulate light reactions; (ii) MeSA may stimulate β-ocimene production, enhancing thermoprotection of photosynthesis; and (iii) cis-β-ocimene is likely far more abundant in nature than previously assumed. This dynamic decoupling of ΦPSII from electron transport, CO₂ assimilation, and biosynthesis under thermal and light stress has important implications for photosynthesis modeling and the interpretation of solar-induced fluorescence.