Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages

Detalhes bibliográficos
Autor(a) principal: Messerschmid, Thibaud F.E.
Data de Publicação: 2021
Outros Autores: Wehling, Judith, Bobon, Nadine, Kahmen, Ansgar, Klak, Cornelia, Los, Jessica A., Nelson, Daniel B., Dos Santos, Patrícia, de Vos, Jurriaan M., Kadereit, Gudrun
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10451/49415
Resumo: The stable carbon isotope composition of plant tissues, commonly expressed as δ13C, holds a wealth of information about photosynthetic pathway, water relations and stress physiology. Crassulacean acid metabolism (CAM) is a derived form of photosynthesis that allows plants to fix carbon at a higher water-use efficiency compared to the ancestral C3 photosynthesis. While the central carbon-fixing enzyme of C3 plants, Rubisco, strongly discriminates against the heavy 13C isotope, CAM is characterized by a dual use of Rubisco and the much less discriminating PEP carboxylase as carbon-fixing enzymes, causing the δ13C values of CAM plant tissues to be generally less negative than those found in C3 plants. Past studies of δ13C variation in CAM plant lineages have repeatedly found a bimodal distribution with very few samples representative of the range around -20‰ that is intermediate between C3- and CAM-like values. Although δ13C values of facultative CAM plants have long been known to extend well into the range below -20‰, this value is often tentatively used as threshold for character coding to distinguish C3 from CAM species in studies of CAM evolution. Compiling 6623 δ13C values reported in the literature for CAM/C3 vascular plant lineages and presenting new data for 581 accessions mainly of the succulent Mesembryanthemoideae (Aizoaceae) and Aeonieae (Crassulaceae), we here investigate the diverse patterns of δ13C distribution in different plant families and sub-familial taxa and demonstrate that a bimodal distribution is not universally present in all lineages. Moreover, we show by means of mixture modelling that the bimodal distribution of δ13C values in the full dataset as well as in the very well-sampled Bromeliaceae is best described by a combination of three rather than two Gaussian distributions with one intermediary cluster between the more evident clusters of C3- and CAM-like values. In view of these results and the furthermore emerging unimodal distribution of δ13C values in Mesembryanthemoideae with mean close to -20‰, we conclude that the evident continuum between CAM and C3 photosynthesis cautions against the usage of a δ13C threshold in macroevolutionary studies. Finally, the observed diversity of δ13C distribution patterns between monophyletic lineages urges for lineage-specific reconstructions rather than a unifying model of CAM evolution.
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spelling Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineagesδ13CAeonieaeAizoaceaeCrassulaceaeCrassulacean Acid MetabolismMesembryanthemumThe stable carbon isotope composition of plant tissues, commonly expressed as δ13C, holds a wealth of information about photosynthetic pathway, water relations and stress physiology. Crassulacean acid metabolism (CAM) is a derived form of photosynthesis that allows plants to fix carbon at a higher water-use efficiency compared to the ancestral C3 photosynthesis. While the central carbon-fixing enzyme of C3 plants, Rubisco, strongly discriminates against the heavy 13C isotope, CAM is characterized by a dual use of Rubisco and the much less discriminating PEP carboxylase as carbon-fixing enzymes, causing the δ13C values of CAM plant tissues to be generally less negative than those found in C3 plants. Past studies of δ13C variation in CAM plant lineages have repeatedly found a bimodal distribution with very few samples representative of the range around -20‰ that is intermediate between C3- and CAM-like values. Although δ13C values of facultative CAM plants have long been known to extend well into the range below -20‰, this value is often tentatively used as threshold for character coding to distinguish C3 from CAM species in studies of CAM evolution. Compiling 6623 δ13C values reported in the literature for CAM/C3 vascular plant lineages and presenting new data for 581 accessions mainly of the succulent Mesembryanthemoideae (Aizoaceae) and Aeonieae (Crassulaceae), we here investigate the diverse patterns of δ13C distribution in different plant families and sub-familial taxa and demonstrate that a bimodal distribution is not universally present in all lineages. Moreover, we show by means of mixture modelling that the bimodal distribution of δ13C values in the full dataset as well as in the very well-sampled Bromeliaceae is best described by a combination of three rather than two Gaussian distributions with one intermediary cluster between the more evident clusters of C3- and CAM-like values. In view of these results and the furthermore emerging unimodal distribution of δ13C values in Mesembryanthemoideae with mean close to -20‰, we conclude that the evident continuum between CAM and C3 photosynthesis cautions against the usage of a δ13C threshold in macroevolutionary studies. Finally, the observed diversity of δ13C distribution patterns between monophyletic lineages urges for lineage-specific reconstructions rather than a unifying model of CAM evolution.ElsevierRepositório da Universidade de LisboaMesserschmid, Thibaud F.E.Wehling, JudithBobon, NadineKahmen, AnsgarKlak, CorneliaLos, Jessica A.Nelson, Daniel B.Dos Santos, Patríciade Vos, Jurriaan M.Kadereit, Gudrun2021-09-06T08:30:52Z2021-062021-06-01T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10451/49415engMesserschmid, T. F. E., Wehling, J., Bobon, N., Kahmen, A., Klak, C., Los, J. A., … Kadereit, G. (2021). Perspectives in Plant Ecology , Evolution and Systematics Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism ( CAM ) continuum in the majority of CAM lineages. Perspectives in Plant Ecology, Evolution and Systematics, 51(May), 125619. https://doi.org/10.1016/j.ppees.2021.1256191433-831910.1016/j.ppees.2021.125619info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-11-08T16:52:59Zoai:repositorio.ul.pt:10451/49415Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T22:00:57.805535Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
title Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
spellingShingle Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
Messerschmid, Thibaud F.E.
δ13C
Aeonieae
Aizoaceae
Crassulaceae
Crassulacean Acid Metabolism
Mesembryanthemum
title_short Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
title_full Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
title_fullStr Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
title_full_unstemmed Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
title_sort Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism (CAM) continuum in the majority of CAM lineages
author Messerschmid, Thibaud F.E.
author_facet Messerschmid, Thibaud F.E.
Wehling, Judith
Bobon, Nadine
Kahmen, Ansgar
Klak, Cornelia
Los, Jessica A.
Nelson, Daniel B.
Dos Santos, Patrícia
de Vos, Jurriaan M.
Kadereit, Gudrun
author_role author
author2 Wehling, Judith
Bobon, Nadine
Kahmen, Ansgar
Klak, Cornelia
Los, Jessica A.
Nelson, Daniel B.
Dos Santos, Patrícia
de Vos, Jurriaan M.
Kadereit, Gudrun
author2_role author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Repositório da Universidade de Lisboa
dc.contributor.author.fl_str_mv Messerschmid, Thibaud F.E.
Wehling, Judith
Bobon, Nadine
Kahmen, Ansgar
Klak, Cornelia
Los, Jessica A.
Nelson, Daniel B.
Dos Santos, Patrícia
de Vos, Jurriaan M.
Kadereit, Gudrun
dc.subject.por.fl_str_mv δ13C
Aeonieae
Aizoaceae
Crassulaceae
Crassulacean Acid Metabolism
Mesembryanthemum
topic δ13C
Aeonieae
Aizoaceae
Crassulaceae
Crassulacean Acid Metabolism
Mesembryanthemum
description The stable carbon isotope composition of plant tissues, commonly expressed as δ13C, holds a wealth of information about photosynthetic pathway, water relations and stress physiology. Crassulacean acid metabolism (CAM) is a derived form of photosynthesis that allows plants to fix carbon at a higher water-use efficiency compared to the ancestral C3 photosynthesis. While the central carbon-fixing enzyme of C3 plants, Rubisco, strongly discriminates against the heavy 13C isotope, CAM is characterized by a dual use of Rubisco and the much less discriminating PEP carboxylase as carbon-fixing enzymes, causing the δ13C values of CAM plant tissues to be generally less negative than those found in C3 plants. Past studies of δ13C variation in CAM plant lineages have repeatedly found a bimodal distribution with very few samples representative of the range around -20‰ that is intermediate between C3- and CAM-like values. Although δ13C values of facultative CAM plants have long been known to extend well into the range below -20‰, this value is often tentatively used as threshold for character coding to distinguish C3 from CAM species in studies of CAM evolution. Compiling 6623 δ13C values reported in the literature for CAM/C3 vascular plant lineages and presenting new data for 581 accessions mainly of the succulent Mesembryanthemoideae (Aizoaceae) and Aeonieae (Crassulaceae), we here investigate the diverse patterns of δ13C distribution in different plant families and sub-familial taxa and demonstrate that a bimodal distribution is not universally present in all lineages. Moreover, we show by means of mixture modelling that the bimodal distribution of δ13C values in the full dataset as well as in the very well-sampled Bromeliaceae is best described by a combination of three rather than two Gaussian distributions with one intermediary cluster between the more evident clusters of C3- and CAM-like values. In view of these results and the furthermore emerging unimodal distribution of δ13C values in Mesembryanthemoideae with mean close to -20‰, we conclude that the evident continuum between CAM and C3 photosynthesis cautions against the usage of a δ13C threshold in macroevolutionary studies. Finally, the observed diversity of δ13C distribution patterns between monophyletic lineages urges for lineage-specific reconstructions rather than a unifying model of CAM evolution.
publishDate 2021
dc.date.none.fl_str_mv 2021-09-06T08:30:52Z
2021-06
2021-06-01T00:00:00Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10451/49415
url http://hdl.handle.net/10451/49415
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Messerschmid, T. F. E., Wehling, J., Bobon, N., Kahmen, A., Klak, C., Los, J. A., … Kadereit, G. (2021). Perspectives in Plant Ecology , Evolution and Systematics Carbon isotope composition of plant photosynthetic tissues reflects a Crassulacean Acid Metabolism ( CAM ) continuum in the majority of CAM lineages. Perspectives in Plant Ecology, Evolution and Systematics, 51(May), 125619. https://doi.org/10.1016/j.ppees.2021.125619
1433-8319
10.1016/j.ppees.2021.125619
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
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dc.publisher.none.fl_str_mv Elsevier
publisher.none.fl_str_mv Elsevier
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
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