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Differential sensitivities of photosynthetic component processes govern oxidative stress levels and net assimilation rates in virus-infected cotton

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Abstract

Cotton (Gossypium hirsutum L.) leafroll dwarf virus disease (CLRDD) is a yield-limiting threat to cotton production and can substantially limit net photosynthetic rates (AN). Previous research showed that AN was more sensitive to CLRDD-induced reductions in stomatal conductance than electron transport rate (ETR) through photosystem II (PSII). This observation coupled with leaf reddening symptomology led to the hypothesis that differential sensitivities of photosynthetic component processes to CLRDD would contribute to declines in AN and increases in oxidative stress, stimulating anthocyanin production. Thus, an experiment was conducted to define the relative sensitivity of photosynthetic component processes to CLRDD and to quantify oxidative stress and anthocyanin production in field-grown cotton. Among diffusional limitations to AN, reductions in mesophyll conductance and CO2 concentration in the chloroplast were the greatest constraints to AN under CLRDD. Multiple metabolic processes were also adversely impacted by CLRDD. ETR, RuBP regeneration, and carboxylation were important metabolic (non-diffusional) limitations to AN in symptomatic plants. Photorespiration and dark respiration were less sensitive than photosynthetic processes, contributing to declines in AN in symptomatic plants. Among thylakoid processes, reduction of PSI end electron acceptors was the most sensitive to CLRDD. Oxidative stress indicators (H2O2 production and membrane peroxidation) and anthocyanin contents were substantially higher in symptomatic plants, concomitant with reductions in carotenoid content and no change in energy dissipation by PSII. We conclude that differential sensitivities of photosynthetic processes to CLRDD and limited potential for energy dissipation at PSII increases oxidative stress, stimulating anthocyanin production as an antioxidative mechanism.

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Data availability

The data supporting the findings of this study are available from the corresponding author (Ved Parkash), upon request.

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Acknowledgements

The authors would like to thank Cotton Incorporated, Georgia Cotton Commission, and the University of Georgia for their financial and material support of this research. We would also like to thank Lola Sexton, Will Vance, Devendra Prasad Chalise, Amrit Pokhrel, Joshua Lee, and Navneet Kaur for their support in the field.

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  1. Department of Crop and Soil Sciences, University of Georgia, Tifton, GA, 31794, USA

    Ved Parkash, John L. Snider, Cristiane Pilon & Gurpreet Virk

  2. Department of Plant Pathology, University of Georgia, Tifton, GA, 31794, USA

    Sudeep Bag

  3. Department of Crop and Soil Sciences, University of Georgia, Griffin, GA, 30223, USA

    David Jespersen

  4. Institute of Plant Breeding, Genetics, and Genomics, University of Georgia, Tifton, GA, 31794, USA

    Kamalpreet Kaur Dhillon

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  1. Ved Parkash
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Contributions

Conceptualization: JS and VP; Data curation: JS and VP; Formal analysis: JS, and VP; Funding acquisition: JS; Investigation: JS, VP, GV, SB, CP, and KD; Methodology: JS and VP; Project administration: JS and VP; Resources: JS, CP, SB, and DJ; Writing—Original draft: VP and JS; Writing—review and editing: JS, VP, CP, SB, DJ, GV, and KD.

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Parkash, V., Snider, J.L., Pilon, C. et al. Differential sensitivities of photosynthetic component processes govern oxidative stress levels and net assimilation rates in virus-infected cotton. Photosynth Res 158, 41–56 (2023). https://doi.org/10.1007/s11120-023-01038-6

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