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Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity

Although red betalain pigments (betacyanins) have been associated with salinity tolerance in some halophytes like Disphyma australe, efforts to determine whether they have a causal role and the underlying mechanisms have been hampered by a lack of a model system. To address this, we engineered betal...

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Autores principales: Zhou, Yanfei, Karl, Tanja, Lewis, David H., McGhie, Tony K., Arathoon, Steve, Davies, Kevin M., Ryan, Ken G., Gould, Kevin S., Schwinn, Kathy E.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8121086/
https://www.ncbi.nlm.nih.gov/pubmed/33995448
http://dx.doi.org/10.3389/fpls.2021.653147
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author Zhou, Yanfei
Karl, Tanja
Lewis, David H.
McGhie, Tony K.
Arathoon, Steve
Davies, Kevin M.
Ryan, Ken G.
Gould, Kevin S.
Schwinn, Kathy E.
author_facet Zhou, Yanfei
Karl, Tanja
Lewis, David H.
McGhie, Tony K.
Arathoon, Steve
Davies, Kevin M.
Ryan, Ken G.
Gould, Kevin S.
Schwinn, Kathy E.
author_sort Zhou, Yanfei
collection PubMed
description Although red betalain pigments (betacyanins) have been associated with salinity tolerance in some halophytes like Disphyma australe, efforts to determine whether they have a causal role and the underlying mechanisms have been hampered by a lack of a model system. To address this, we engineered betalain-producing Nicotiana tabacum, by the introduction of three betalain biosynthetic genes. The plants were violet-red due to the accumulation of three betacyanins: betanin, isobetanin, and betanidin. Under salt stress, betacyanic seedlings had increased survivability and leaves of mature plants had higher photochemical quantum yields of photosystem II (F(v)/F(m)) and faster photosynthetic recovery after saturating light treatment. Under salt stress, compared to controls betacyanic leaf disks had no loss of carotenoids, a slower rate of chlorophyll degradation, and higher F(v)/F(m) values. Furthermore, simulation of betacyanin pigmentation by using a red filter cover improved F(v)/F(m) value of green tissue under salt stress. Our results confirm a direct causal role of betacyanins in plant salinity tolerance and indicate a key mechanism is photoprotection. A role in delaying leaf senescence was also indicated, and the enhanced antioxidant capability of the betacyanic leaves suggested a potential contribution to scavenging reactive oxygen species. The study can inform the development of novel biotechnological approaches to improving agricultural productivity in saline-affected areas.
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spelling pubmed-81210862021-05-15 Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity Zhou, Yanfei Karl, Tanja Lewis, David H. McGhie, Tony K. Arathoon, Steve Davies, Kevin M. Ryan, Ken G. Gould, Kevin S. Schwinn, Kathy E. Front Plant Sci Plant Science Although red betalain pigments (betacyanins) have been associated with salinity tolerance in some halophytes like Disphyma australe, efforts to determine whether they have a causal role and the underlying mechanisms have been hampered by a lack of a model system. To address this, we engineered betalain-producing Nicotiana tabacum, by the introduction of three betalain biosynthetic genes. The plants were violet-red due to the accumulation of three betacyanins: betanin, isobetanin, and betanidin. Under salt stress, betacyanic seedlings had increased survivability and leaves of mature plants had higher photochemical quantum yields of photosystem II (F(v)/F(m)) and faster photosynthetic recovery after saturating light treatment. Under salt stress, compared to controls betacyanic leaf disks had no loss of carotenoids, a slower rate of chlorophyll degradation, and higher F(v)/F(m) values. Furthermore, simulation of betacyanin pigmentation by using a red filter cover improved F(v)/F(m) value of green tissue under salt stress. Our results confirm a direct causal role of betacyanins in plant salinity tolerance and indicate a key mechanism is photoprotection. A role in delaying leaf senescence was also indicated, and the enhanced antioxidant capability of the betacyanic leaves suggested a potential contribution to scavenging reactive oxygen species. The study can inform the development of novel biotechnological approaches to improving agricultural productivity in saline-affected areas. Frontiers Media S.A. 2021-04-30 /pmc/articles/PMC8121086/ /pubmed/33995448 http://dx.doi.org/10.3389/fpls.2021.653147 Text en Copyright © 2021 Zhou, Karl, Lewis, McGhie, Arathoon, Davies, Ryan, Gould and Schwinn. 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
Zhou, Yanfei
Karl, Tanja
Lewis, David H.
McGhie, Tony K.
Arathoon, Steve
Davies, Kevin M.
Ryan, Ken G.
Gould, Kevin S.
Schwinn, Kathy E.
Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity
title Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity
title_full Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity
title_fullStr Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity
title_full_unstemmed Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity
title_short Production of Betacyanins in Transgenic Nicotiana tabacum Increases Tolerance to Salinity
title_sort production of betacyanins in transgenic nicotiana tabacum increases tolerance to salinity
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8121086/
https://www.ncbi.nlm.nih.gov/pubmed/33995448
http://dx.doi.org/10.3389/fpls.2021.653147
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