Cargando…

Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world

Photorespiration, commonly viewed as a loss in photosynthetic productivity of C3 plants, is expected to decline with increasing atmospheric CO(2), even though photorespiration plays an important role in the oxidative stress responses. This study aimed to quantify the role of photorespiration and alt...

Descripción completa

Detalles Bibliográficos
Autores principales: Celebi-Ergin, Billur, Zimmerman, Richard C., Hill, Victoria J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9692008/
https://www.ncbi.nlm.nih.gov/pubmed/36438084
http://dx.doi.org/10.3389/fpls.2022.1025416
_version_ 1784837162822270976
author Celebi-Ergin, Billur
Zimmerman, Richard C.
Hill, Victoria J.
author_facet Celebi-Ergin, Billur
Zimmerman, Richard C.
Hill, Victoria J.
author_sort Celebi-Ergin, Billur
collection PubMed
description Photorespiration, commonly viewed as a loss in photosynthetic productivity of C3 plants, is expected to decline with increasing atmospheric CO(2), even though photorespiration plays an important role in the oxidative stress responses. This study aimed to quantify the role of photorespiration and alternative photoprotection mechanisms in Zostera marina L. (eelgrass), a carbon-limited marine C3 plant, in response to ocean acidification. Plants were grown in controlled outdoor aquaria at different [CO(2)](aq) ranging from ~55 (ambient) to ~2121 μM for 13 months and compared for differences in leaf photochemistry by simultaneous measurements of O(2) flux and variable fluorescence. At ambient [CO(2)], photosynthesis was carbon limited and the excess photon absorption was diverted both to photorespiration and non-photochemical quenching (NPQ). The dynamic range of NPQ regulation in ambient grown plants, in response to instantaneous changes in [CO(2)](aq), suggested considerable tolerance for fluctuating environmental conditions. However, 60 to 80% of maximum photosynthetic capacity of ambient plants was diverted to photorespiration resulting in limited carbon fixation. The photosynthesis to respiration ratio (P (E) : R (D)) of ambient grown plants increased 6-fold when measured under high CO(2) because photorespiration was virtually suppressed. Plants acclimated to high CO(2) maintained 4-fold higher P (E) : R (D) than ambient grown plants as a result of a 60% reduction in photorespiration. The O(2) production efficiency per unit chlorophyll was not affected by the CO(2) environment in which the plants were grown. Yet, CO(2) enrichment decreased the light level to initiate NPQ activity and downregulated the biomass specific pigment content by 50% and area specific pigment content by 30%. Thus, phenotypic acclimation to ocean carbonation in eelgrass, indicating the coupling between the regulation of photosynthetic structure and metabolic carbon demands, involved the downregulation of light harvesting by the photosynthetic apparatus, a reduction in the role of photorespiration and an increase in the role of NPQ in photoprotection. The quasi-mechanistic model developed in this study permits integration of photosynthetic and morphological acclimation to ocean carbonation into seagrass productivity models, by adjusting the limits of the photosynthetic parameters based on substrate availability and physiological capacity.
format Online
Article
Text
id pubmed-9692008
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-96920082022-11-26 Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world Celebi-Ergin, Billur Zimmerman, Richard C. Hill, Victoria J. Front Plant Sci Plant Science Photorespiration, commonly viewed as a loss in photosynthetic productivity of C3 plants, is expected to decline with increasing atmospheric CO(2), even though photorespiration plays an important role in the oxidative stress responses. This study aimed to quantify the role of photorespiration and alternative photoprotection mechanisms in Zostera marina L. (eelgrass), a carbon-limited marine C3 plant, in response to ocean acidification. Plants were grown in controlled outdoor aquaria at different [CO(2)](aq) ranging from ~55 (ambient) to ~2121 μM for 13 months and compared for differences in leaf photochemistry by simultaneous measurements of O(2) flux and variable fluorescence. At ambient [CO(2)], photosynthesis was carbon limited and the excess photon absorption was diverted both to photorespiration and non-photochemical quenching (NPQ). The dynamic range of NPQ regulation in ambient grown plants, in response to instantaneous changes in [CO(2)](aq), suggested considerable tolerance for fluctuating environmental conditions. However, 60 to 80% of maximum photosynthetic capacity of ambient plants was diverted to photorespiration resulting in limited carbon fixation. The photosynthesis to respiration ratio (P (E) : R (D)) of ambient grown plants increased 6-fold when measured under high CO(2) because photorespiration was virtually suppressed. Plants acclimated to high CO(2) maintained 4-fold higher P (E) : R (D) than ambient grown plants as a result of a 60% reduction in photorespiration. The O(2) production efficiency per unit chlorophyll was not affected by the CO(2) environment in which the plants were grown. Yet, CO(2) enrichment decreased the light level to initiate NPQ activity and downregulated the biomass specific pigment content by 50% and area specific pigment content by 30%. Thus, phenotypic acclimation to ocean carbonation in eelgrass, indicating the coupling between the regulation of photosynthetic structure and metabolic carbon demands, involved the downregulation of light harvesting by the photosynthetic apparatus, a reduction in the role of photorespiration and an increase in the role of NPQ in photoprotection. The quasi-mechanistic model developed in this study permits integration of photosynthetic and morphological acclimation to ocean carbonation into seagrass productivity models, by adjusting the limits of the photosynthetic parameters based on substrate availability and physiological capacity. Frontiers Media S.A. 2022-11-11 /pmc/articles/PMC9692008/ /pubmed/36438084 http://dx.doi.org/10.3389/fpls.2022.1025416 Text en Copyright © 2022 Celebi-Ergin, Zimmerman and Hill https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Celebi-Ergin, Billur
Zimmerman, Richard C.
Hill, Victoria J.
Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world
title Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world
title_full Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world
title_fullStr Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world
title_full_unstemmed Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world
title_short Photorespiration in eelgrass (Zostera marina L.): A photoprotection mechanism for survival in a CO(2)-limited world
title_sort photorespiration in eelgrass (zostera marina l.): a photoprotection mechanism for survival in a co(2)-limited world
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9692008/
https://www.ncbi.nlm.nih.gov/pubmed/36438084
http://dx.doi.org/10.3389/fpls.2022.1025416
work_keys_str_mv AT celebierginbillur photorespirationineelgrasszosteramarinalaphotoprotectionmechanismforsurvivalinaco2limitedworld
AT zimmermanrichardc photorespirationineelgrasszosteramarinalaphotoprotectionmechanismforsurvivalinaco2limitedworld
AT hillvictoriaj photorespirationineelgrasszosteramarinalaphotoprotectionmechanismforsurvivalinaco2limitedworld