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.