Abstract
The responses of plant photosynthesis to rapid fluctuations in environmental conditions are critical for efficient conversion of light energy. These responses are not well-seen laboratory conditions and are difficult to probe in field environments. We demonstrate an open science approach to this problem that combines multifaceted measurements of photosynthesis and environmental conditions, and an unsupervised statistical clustering approach. In a selected set of data on mint (Mentha sp.), we show that ‘light potentials’ for linear electron flow and non-photochemical quenching (NPQ) upon rapid light increases are strongly suppressed in leaves previously exposed to low ambient photosynthetically active radiation (PAR) or low leaf temperatures, factors that can act both independently and cooperatively. Further analyses allowed us to test specific mechanisms. With decreasing leaf temperature or PAR, limitations to photosynthesis during high light fluctuations shifted from rapidly induced NPQ to photosynthetic control of electron flow at the cytochrome b6f complex. At low temperatures, high light induced lumen acidification, but did not induce NPQ, leading to accumulation of reduced electron transfer intermediates, probably inducing photodamage, revealing a potential target for improving the efficiency and robustness of photosynthesis. We discuss the implications of the approach for open science efforts to understand and improve crop productivity.
Highlights
While oxygenic photosynthesis supplies energy to drive essentially all biology in our ecosystem, it involves highly energetic intermediates that can generate highly toxic reactive oxygen species (ROS) that can damage the organisms it powers [1]
Slower forms of non-photochemical quenching (NPQ) have been demonstrated [12], including qI, which is related to the photodamage and repair of photosystem II (PSII) or qZ, which related to the accumulation of Zx [13], qH, related to cold and high light stress [13], and qT, related to antenna state transitions [14]
We introduce an approach to both measure and analyse these variations in LP, focusing on one species, Mentha sp., under a limited set of conditions, and applied these to testing among a set of mechanisms for modulating that can be distinguished based on a range of optical measurements available using the MultispeQ 2.0 device, including: (i) PSI acceptor-side limitations to electron transfer; (ii) increased NPQ, which limits the input of light energy into photosystem II (PSII); and (iii) photosynthetic control (PCON), in which acidification of the lumen slows electron transfer at the level of plastoquinol (PQH2) oxidation by the cytochrome b6f complex
Summary
While oxygenic photosynthesis supplies energy to drive essentially all biology in our ecosystem, it involves highly energetic intermediates that can generate highly toxic reactive oxygen species (ROS) that can damage the organisms it powers [1]. One class of photoprotective processes, known as non-photochemical quenching (NPQ), dissipates absorbed light energy as heat, diverting energy away from photosystem II (PSII) [2], decreasing the accumulation of reactive intermediates. This photoprotective capacity comes at the cost of decreased photochemical efficiency, and the organisms must regulate NPQ to balance the avoidance of photodamage with efficient energy conversion [3,4]. Slower forms of NPQ have been demonstrated [12], including qI, which is related to the photodamage and repair of photosystem II (PSII) or qZ, which related to the accumulation of Zx (independently from qE) [13], qH, related to cold and high light stress [13], and qT, related to antenna state transitions [14]
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