Models and mechanisms of the rapidly reversible regulation of photosynthetic light harvesting

The rapid response of photosynthetic organisms to fluctuations in ambient light intensity is incompletely understood at both the molecular and membrane levels. In this review, we describe research from our group over a 10-year period aimed at identifying the photophysical mechanisms used by plants, algae and mosses to control the efficiency of light harvesting by photosystem II on the seconds-to-minutes time scale. To complement the spectroscopic data, we describe three models capable of describing the measured response at a quantitative level. The review attempts to provide an integrated view that has emerged from our work, and briefly looks forward to future experimental and modelling efforts that will refine and expand our understanding of a process that significantly influences crop yields.

Conceptual comments First paragraph of Introduction: -The authors should consider replacing "can cause irreversible damage to photosynthetic proteins" with a statement like "can cause inactivation of photosynthetic proteins" because it has been shown that inactivation of D1, for example, is part of a genetic program to limit production of reactive oxygen species under highly excessive light (see Wagner et al. 2004Science 306, 1183-1185 and probably should not be considered damage (Foyer et al. 2017 Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochemical Journal 474, 877-883;Adams et al. 2013 Photosynth Res 117, 31-44).
-NPQ is not a regulatory mechanism in the sense that it is a consequence of thermal de-excitation rather than its mechanism. Perhaps rephrase to something like "a suite of regulatory mechanisms that are often quantified from their effect on chlorophyll fluorescence as 'nonphotochemical quenching' (NPQ)." -the statement "(qE), turns on in seconds to minutes but turns off rather slowly over a timescale of tens of minutes" is not correct as written. Under field conditions as well as under many experimental conditions, the majority of the actual qE turns off within seconds (Demmig-Adams et al. 2012 Photosynth Res 113, 75-88;Adams et al. 1999 Plant, Cell & Env 22, 125-136), and what takes longer is reconversion of zeaxanthin to violaxanthin. In addition, zeaxanthin-free leaves take longer to induce qE than zeaxanthin-containing leaves (Fig. 5 in Demmig-Adams et al. 1989 Plant Phys 90, 887-893).
Minor comments -use single quotations marks (for British punctuation conventions) throughout -give "A. thaliana" in italics Introduction -replace "qE is often measures" with ""qE is often measured" -replace "plucked" with "excised" (How was the leaf maintained? With the petiole in water?) Spectroscopic probes… -replace "And, What…" with "And what…" -add the reference number after "the model developed by Zaks et al."

25-Feb-2019
Dear Professor Fleming We are pleased to inform you that your manuscript RSOB-19-0043 entitled "Models and Mechanisms of the Rapidly Reversible Regulation of Photosynthetic Light Harvesting" has been accepted by the Editor for publication in Open Biology. The reviewer(s) have recommended publication, but also suggest some minor revisions to your manuscript. Therefore, we invite you to respond to the reviewer(s)' comments and revise your manuscript.
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The paper presents a very clear and logical flow of the argument and will be a very useful guide for future studies.

Referee: 2
Comments to the Author(s) This review summarizes the ground-breaking contributions made by this group to the understanding of photosynthetic light harvesting and outlines remaining questions.
Conceptual comments First paragraph of Introduction: -The authors should consider replacing "can cause irreversible damage to photosynthetic proteins" with a statement like "can cause inactivation of photosynthetic proteins" because it has been shown that inactivation of D1, for example, is part of a genetic program to limit production of reactive oxygen species under highly excessive light (see Wagner et al. 2004Science 306, 1183-1185 and probably should not be considered damage (Foyer et al. 2017 Viewing oxidative stress through the lens of oxidative signalling rather than damage. Biochemical Journal 474, 877-883;Adams et al. 2013 Photosynth Res 117, 31-44).
-NPQ is not a regulatory mechanism in the sense that it is a consequence of thermal de-excitation rather than its mechanism. Perhaps rephrase to something like "a suite of regulatory mechanisms that are often quantified from their effect on chlorophyll fluorescence as 'nonphotochemical quenching' (NPQ)." -the statement "(qE), turns on in seconds to minutes but turns off rather slowly over a timescale of tens of minutes" is not correct as written. Under field conditions as well as under many experimental conditions, the majority of the actual qE turns off within seconds (Demmig-Adams et al. 2012 Photosynth Res 113, 75-88;Adams et al. 1999 Plant, Cell &amp;Env 22, 125-136), and what takes longer is reconversion of zeaxanthin to violaxanthin. In addition, zeaxanthin-free leaves take longer to induce qE than zeaxanthin-containing leaves (Fig. 5 in Demmig-Adams et al. 1989 Plant Phys 90, 887-893).
Minor comments -use single quotations marks (for British punctuation conventions) throughout -give "A. thaliana" in italics Introduction -replace "qE is often measures" with ""qE is often measured" -replace "plucked" with "excised" (How was the leaf maintained? With the petiole in water?) Spectroscopic probes… -replace "And, What…" with "And what…" -add the reference number after "the model developed by Zaks et al." Decision letter (RSOB-19-0043.R1)

07-Mar-2019
Dear Professor Fleming We are pleased to inform you that your manuscript entitled "Models and Mechanisms of the Rapidly Reversible Regulation of Photosynthetic Light Harvesting" has been accepted by the Editor for publication in Open Biology.
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Thank you for your fine contribution. On behalf of the Editors of Open Biology, we look forward to your continued contributions to the journal. Response: We thank the reviewer for suggesting this clarification. We have reworded the first paragraph along the lines suggested. We have also added a reference to Wagner et al 2004.
Comment 2: NPQ is not a regulatory mechanism in the sense that it is a consequence of thermal de-excitation rather than its mechanism. Perhaps rephrase to something like "a suite of regulatory mechanisms that are often quantified from their effect on chlorophyll fluorescence as 'nonphotochemical quenching' (NPQ)." Response: Again we agree that the reviewer's wording is more precise than our original text. We have used the suggested rephrasing. Response: Thank you for pointing this out. We have corrected our statement about the timescales as suggested by the reviewer and have refocused the sentence on the significance of qE in the presence of fluctuating light.

Comment 4:
Minor comments: -use single quotations marks (for British punctuation conventions) throughout -give "A. thaliana" in italics Introduction -replace "qE is often measures" with ""qE is often measured" -replace "plucked" with "excised" (How was the leaf maintained? With the petiole in water?) Spectroscopic probes… -replace "And, What…" with "And what…" -add the reference number after "the model developed by Zaks et al."