Abstract
Energy-dependent (qE) non-photochemical quenching (NPQ) thermally dissipates excess absorbed light energy as a protective mechanism to prevent the over reduction of photosystem II and the generation of reactive oxygen species (ROS). The xanthophyll cycle, induced when the level of absorbed light energy exceeds the capacity of photochemistry, contributes to qE. In this work, we show that ethylene regulates the xanthophyll cycle in Arabidopsis. Analysis of eto1-1, exhibiting increased ethylene production, and ctr1-3, exhibiting constitutive ethylene response, revealed defects in NPQ resulting from impaired de-epoxidation of violaxanthin by violaxanthin de-epoxidase (VDE) encoded by NPQ1. Elevated ethylene signaling reduced the level of active VDE through decreased NPQ1 promoter activity and impaired VDE activation resulting from a lower transthylakoid membrane pH gradient. Increasing the concentration of CO2 partially corrected the ethylene-mediated defects in NPQ and photosynthesis, indicating that changes in ethylene signaling affect stromal CO2 solubility. Increasing VDE expression in eto1-1 and ctr1-3 restored light-activated de-epoxidation and qE, reduced superoxide production and reduced photoinhibition. Restoring VDE activity significantly reversed the small growth phenotype of eto1-1 and ctr1-3 without altering ethylene production or ethylene responses. Our results demonstrate that ethylene increases ROS production and photosensitivity in response to high light and the associated reduced plant stature is partially reversed by increasing VDE activity.
Highlights
Ethylene is involved in regulating multiple aspects of plant development, most notably, fruit ripening, cell expansion, programmed cell death, and organ senescence and is involved in several biotic and abiotic stress responses [1, 2, 3, 4, 5, 6, 7]
Following exposure of dark-adapted plants to 336 μmol photons m-2 s-1 (PFD), an aberrant non-photochemical quenching (NPQ) induction profile was observed in leaves of eto1-1, in which ethylene production is elevated, and in ctr1-3, in which the ethylene response is constitutive (Fig 1)
We show that eto1-1, in which ethylene production is increased moderately, and ctr1-3, in which ethylene responses are constitutive exhibit an impaired quenching singlet-excited chlorophyll (qE) that is due, in part, to a reduction in violaxanthin de-epoxidase (VDE) activity
Summary
Ethylene is involved in regulating multiple aspects of plant development, most notably, fruit ripening, cell expansion, programmed cell death, and organ senescence and is involved in several biotic and abiotic stress responses [1, 2, 3, 4, 5, 6, 7]. Ethylene is produced from methionine by its conversion to S-adenosylmethionine (AdoMet) by S-adenosylmethionine synthase which 1-aminocyclopropane-1-carboxylate synthase (ACS) converts to methylthioadenosine (MTA) and 1-aminocyclopropane-1-carboxylate (ACC) [8]. ACC oxidase (ACO) oxidizes ACC to produce ethylene. Ethylene Regulates the Xanthophyll Cycle publish, or preparation of the manuscript. This does not alter our adherence to PLOS ONE policies on sharing data and materials. No patent applications pertaining to the findings in this study have been filed
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