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Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)

BACKGROUND: MicroRNA319 (miR319) acts as an essential regulator of gene expression during plant development and under stress conditions. Although the role of miR319a in regulating leaf development has been well studied in tomato (Solanum lycopersicum), the function of the recently discovered wild to...

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Autores principales: Shi, Xiaopu, Jiang, Fangling, Wen, Junqin, Wu, Zhen
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6533698/
https://www.ncbi.nlm.nih.gov/pubmed/31122194
http://dx.doi.org/10.1186/s12870-019-1823-x
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author Shi, Xiaopu
Jiang, Fangling
Wen, Junqin
Wu, Zhen
author_facet Shi, Xiaopu
Jiang, Fangling
Wen, Junqin
Wu, Zhen
author_sort Shi, Xiaopu
collection PubMed
description BACKGROUND: MicroRNA319 (miR319) acts as an essential regulator of gene expression during plant development and under stress conditions. Although the role of miR319a in regulating leaf development has been well studied in tomato (Solanum lycopersicum), the function of the recently discovered wild tomato Solanum habrochaites miRNA319d (sha-miR319d) remains poorly understood. In this study, we overexpressed sha-miR319d in cultivated tomato ‘Micro-Tom’ to further investigate its role in tomato temperature stress responses. RESULTS: Under chilling or heat stress, sha-miR319d-overexpressing plants showed enhanced stress tolerance, including lower relative electrolyte leakage (REL), malondialdehyde (MDA) concentration, O(2)(−) generation and H(2)O(2) concentration and higher chlorophyll contents and Fv/Fm values than wild-type (WT) plants. Overexpression of sha-miR319d enhanced the activities of superoxide dismutase (SOD) and catalase (CAT), with possible correlation with elevated expression levels of the genes FeSOD, CuZnSOD and CAT. Moreover, different expression levels of key genes involved in chilling (MYB83 and CBF1), heat (HsfA1a, HsfA1b and Hsp90), and reactive oxygen species (ROS) (ZAT12 and ZAT10) signaling in transgenic plants and WT were determined, suggesting a role for sha-miR319d in regulating tomato temperature stress via chilling, heat and ROS signaling. Silencing GAMYB-like1 increased tomato chilling tolerance as well as the expression levels of CBF1, CuZnSOD, CAT, APX1, APX2, ZAT12 and ZAT10. Additionally, overexpression of sha-miR319d in tomato caused plant leaf crinkling and reduced height. CONCLUSIONS: Overexpression of sha-miR319d confers chilling and heat stress tolerance in tomato. Sha-miR319d regulates tomato chilling tolerance, possibly by inhibiting expression of GAMYB-like1 and further alters chilling, heat and ROS signal transduction. Our research provides insight for further study of the role of sha-miR319d in tomato growth and stress regulation and lays a foundation for the genetic improvement of tomato. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1823-x) contains supplementary material, which is available to authorized users.
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spelling pubmed-65336982019-05-29 Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum) Shi, Xiaopu Jiang, Fangling Wen, Junqin Wu, Zhen BMC Plant Biol Research Article BACKGROUND: MicroRNA319 (miR319) acts as an essential regulator of gene expression during plant development and under stress conditions. Although the role of miR319a in regulating leaf development has been well studied in tomato (Solanum lycopersicum), the function of the recently discovered wild tomato Solanum habrochaites miRNA319d (sha-miR319d) remains poorly understood. In this study, we overexpressed sha-miR319d in cultivated tomato ‘Micro-Tom’ to further investigate its role in tomato temperature stress responses. RESULTS: Under chilling or heat stress, sha-miR319d-overexpressing plants showed enhanced stress tolerance, including lower relative electrolyte leakage (REL), malondialdehyde (MDA) concentration, O(2)(−) generation and H(2)O(2) concentration and higher chlorophyll contents and Fv/Fm values than wild-type (WT) plants. Overexpression of sha-miR319d enhanced the activities of superoxide dismutase (SOD) and catalase (CAT), with possible correlation with elevated expression levels of the genes FeSOD, CuZnSOD and CAT. Moreover, different expression levels of key genes involved in chilling (MYB83 and CBF1), heat (HsfA1a, HsfA1b and Hsp90), and reactive oxygen species (ROS) (ZAT12 and ZAT10) signaling in transgenic plants and WT were determined, suggesting a role for sha-miR319d in regulating tomato temperature stress via chilling, heat and ROS signaling. Silencing GAMYB-like1 increased tomato chilling tolerance as well as the expression levels of CBF1, CuZnSOD, CAT, APX1, APX2, ZAT12 and ZAT10. Additionally, overexpression of sha-miR319d in tomato caused plant leaf crinkling and reduced height. CONCLUSIONS: Overexpression of sha-miR319d confers chilling and heat stress tolerance in tomato. Sha-miR319d regulates tomato chilling tolerance, possibly by inhibiting expression of GAMYB-like1 and further alters chilling, heat and ROS signal transduction. Our research provides insight for further study of the role of sha-miR319d in tomato growth and stress regulation and lays a foundation for the genetic improvement of tomato. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-019-1823-x) contains supplementary material, which is available to authorized users. BioMed Central 2019-05-23 /pmc/articles/PMC6533698/ /pubmed/31122194 http://dx.doi.org/10.1186/s12870-019-1823-x Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Shi, Xiaopu
Jiang, Fangling
Wen, Junqin
Wu, Zhen
Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)
title Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)
title_full Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)
title_fullStr Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)
title_full_unstemmed Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)
title_short Overexpression of Solanum habrochaites microRNA319d (sha-miR319d) confers chilling and heat stress tolerance in tomato (S. lycopersicum)
title_sort overexpression of solanum habrochaites microrna319d (sha-mir319d) confers chilling and heat stress tolerance in tomato (s. lycopersicum)
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6533698/
https://www.ncbi.nlm.nih.gov/pubmed/31122194
http://dx.doi.org/10.1186/s12870-019-1823-x
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