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Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato

Glycine betaine (GB), as a putative compatible substance, protects plants against the damaging effects of abiotic stresses. Phosphorus deficiency is one type of abiotic stress that is detrimental to plant growth. Maintenance of phosphate (Pi) homeostasis is crucial. This study demonstrates GB-regula...

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Autores principales: Li, Daxing, Zhang, Tianpeng, Wang, Mengwei, Liu, Yang, Brestic, Marian, Chen, Tony H. H., Yang, Xinghong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6335352/
https://www.ncbi.nlm.nih.gov/pubmed/30687378
http://dx.doi.org/10.3389/fpls.2018.01995
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author Li, Daxing
Zhang, Tianpeng
Wang, Mengwei
Liu, Yang
Brestic, Marian
Chen, Tony H. H.
Yang, Xinghong
author_facet Li, Daxing
Zhang, Tianpeng
Wang, Mengwei
Liu, Yang
Brestic, Marian
Chen, Tony H. H.
Yang, Xinghong
author_sort Li, Daxing
collection PubMed
description Glycine betaine (GB), as a putative compatible substance, protects plants against the damaging effects of abiotic stresses. Phosphorus deficiency is one type of abiotic stress that is detrimental to plant growth. Maintenance of phosphate (Pi) homeostasis is crucial. This study demonstrates GB-regulated phosphate homeostasis in the tomato (Solanum lycopersicum cv. ‘Moneymaker’) transformed with the choline oxidase gene codA from Arthrobacter globiformis. The codA-transgenic lines displayed more resistance to low-phosphate stress. The data revealed that the wild-type plants were stunted and consistently retained less Pi than transgenic lines, especially when grown under low-phosphate conditions. This difference in Pi retention was attributable to the enhanced Pi uptake ability in the transgenic lines. The transgenic plants translocated more Pi into the plant cell due to the enhanced enzymatic activity of plasma membrane H(+)-ATPase and increased Pi/H(+) co-transport, which improved Pi uptake. The differential expression of ‘PHO regulon’ genes further maintained intracellular Pi homeostasis. Furthermore, GB maintained a higher photosynthesis rate, thus increasing the production and translocation of sucrose via phloem loading to enhance plant response to low-phosphate stress. We conclude that GB mediates Pi uptake and translocation by regulating physiological and biochemical processes that promote adaptation to environmental changes in Pi availability. These processes eventually lead to better growth and development of the codA-transgenic lines. This finding will help to further elucidate the signaling mechanism of how GB perceives and transmits low-phosphate signals to alleviate Pi nutritional stress.
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spelling pubmed-63353522019-01-25 Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato Li, Daxing Zhang, Tianpeng Wang, Mengwei Liu, Yang Brestic, Marian Chen, Tony H. H. Yang, Xinghong Front Plant Sci Plant Science Glycine betaine (GB), as a putative compatible substance, protects plants against the damaging effects of abiotic stresses. Phosphorus deficiency is one type of abiotic stress that is detrimental to plant growth. Maintenance of phosphate (Pi) homeostasis is crucial. This study demonstrates GB-regulated phosphate homeostasis in the tomato (Solanum lycopersicum cv. ‘Moneymaker’) transformed with the choline oxidase gene codA from Arthrobacter globiformis. The codA-transgenic lines displayed more resistance to low-phosphate stress. The data revealed that the wild-type plants were stunted and consistently retained less Pi than transgenic lines, especially when grown under low-phosphate conditions. This difference in Pi retention was attributable to the enhanced Pi uptake ability in the transgenic lines. The transgenic plants translocated more Pi into the plant cell due to the enhanced enzymatic activity of plasma membrane H(+)-ATPase and increased Pi/H(+) co-transport, which improved Pi uptake. The differential expression of ‘PHO regulon’ genes further maintained intracellular Pi homeostasis. Furthermore, GB maintained a higher photosynthesis rate, thus increasing the production and translocation of sucrose via phloem loading to enhance plant response to low-phosphate stress. We conclude that GB mediates Pi uptake and translocation by regulating physiological and biochemical processes that promote adaptation to environmental changes in Pi availability. These processes eventually lead to better growth and development of the codA-transgenic lines. This finding will help to further elucidate the signaling mechanism of how GB perceives and transmits low-phosphate signals to alleviate Pi nutritional stress. Frontiers Media S.A. 2019-01-10 /pmc/articles/PMC6335352/ /pubmed/30687378 http://dx.doi.org/10.3389/fpls.2018.01995 Text en Copyright © 2019 Li, Zhang, Wang, Liu, Brestic, Chen and Yang. http://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
Li, Daxing
Zhang, Tianpeng
Wang, Mengwei
Liu, Yang
Brestic, Marian
Chen, Tony H. H.
Yang, Xinghong
Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato
title Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato
title_full Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato
title_fullStr Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato
title_full_unstemmed Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato
title_short Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato
title_sort genetic engineering of the biosynthesis of glycine betaine modulates phosphate homeostasis by regulating phosphate acquisition in tomato
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6335352/
https://www.ncbi.nlm.nih.gov/pubmed/30687378
http://dx.doi.org/10.3389/fpls.2018.01995
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