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The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress

BACKGROUND: Late embryogenesis abundant (LEA) proteins are widely distributed in higher plants and play crucial roles in regulating plant growth and development processes and resisting abiotic stress. Cultivated tomato (Solanum lycopersicum) is an important vegetable crop worldwide; however, its gro...

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Autores principales: Jia, Chunping, Guo, Bin, Wang, Baike, Li, Xin, Yang, Tao, Li, Ning, Wang, Juan, Yu, Qinghui
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9762057/
https://www.ncbi.nlm.nih.gov/pubmed/36536303
http://dx.doi.org/10.1186/s12870-022-03953-7
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author Jia, Chunping
Guo, Bin
Wang, Baike
Li, Xin
Yang, Tao
Li, Ning
Wang, Juan
Yu, Qinghui
author_facet Jia, Chunping
Guo, Bin
Wang, Baike
Li, Xin
Yang, Tao
Li, Ning
Wang, Juan
Yu, Qinghui
author_sort Jia, Chunping
collection PubMed
description BACKGROUND: Late embryogenesis abundant (LEA) proteins are widely distributed in higher plants and play crucial roles in regulating plant growth and development processes and resisting abiotic stress. Cultivated tomato (Solanum lycopersicum) is an important vegetable crop worldwide; however, its growth, development, yield, and quality are currently severely constrained by abiotic stressors. In contrast, wild tomato species are more tolerant to abiotic stress and can grow normally in extreme environments. The main objective of this study was to identify, characterize, and perform gene expression analysis of LEA protein families from cultivated and wild tomato species to mine candidate genes and determine their potential role in abiotic stress tolerance in tomatoes. RESULTS: Total 60, 69, 65, and 60 LEA genes were identified in S. lycopersicum, Solanum pimpinellifolium, Solanum pennellii, and Solanum lycopersicoides, respectively. Characterization results showed that these genes could be divided into eight clusters, with the LEA_2 cluster having the most members. Most LEA genes had few introns and were non-randomly distributed on chromosomes; the promoter regions contained numerous cis-acting regulatory elements related to abiotic stress tolerance and phytohormone responses. Evolutionary analysis showed that LEA genes were highly conserved and that the segmental duplication event played an important role in evolution of the LEA gene family. Transcription and expression pattern analyses revealed different regulatory patterns of LEA genes between cultivated and wild tomato species under normal conditions. Certain S. lycopersicum LEA (SlLEA) genes showed similar expression patterns and played specific roles under different abiotic stress and phytohormone treatments. Gene ontology and protein interaction analyses showed that most LEA genes acted in response to abiotic stimuli and water deficit. Five SlLEA proteins were found to interact with 11 S. lycopersicum WRKY proteins involved in development or resistance to stress. Virus-induced gene silencing of SlLEA6 affected the antioxidant and reactive oxygen species defense systems, increased the degree of cellular damage, and reduced drought resistance in S. lycopersicum. CONCLUSION: These findings provide comprehensive information on LEA proteins in cultivated and wild tomato species and their possible functions under different abiotic and phytohormone stresses. The study systematically broadens our current understanding of LEA proteins and candidate genes and provides a theoretical basis for future functional studies aimed at improving stress resistance in tomato. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03953-7.
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spelling pubmed-97620572022-12-20 The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress Jia, Chunping Guo, Bin Wang, Baike Li, Xin Yang, Tao Li, Ning Wang, Juan Yu, Qinghui BMC Plant Biol Research BACKGROUND: Late embryogenesis abundant (LEA) proteins are widely distributed in higher plants and play crucial roles in regulating plant growth and development processes and resisting abiotic stress. Cultivated tomato (Solanum lycopersicum) is an important vegetable crop worldwide; however, its growth, development, yield, and quality are currently severely constrained by abiotic stressors. In contrast, wild tomato species are more tolerant to abiotic stress and can grow normally in extreme environments. The main objective of this study was to identify, characterize, and perform gene expression analysis of LEA protein families from cultivated and wild tomato species to mine candidate genes and determine their potential role in abiotic stress tolerance in tomatoes. RESULTS: Total 60, 69, 65, and 60 LEA genes were identified in S. lycopersicum, Solanum pimpinellifolium, Solanum pennellii, and Solanum lycopersicoides, respectively. Characterization results showed that these genes could be divided into eight clusters, with the LEA_2 cluster having the most members. Most LEA genes had few introns and were non-randomly distributed on chromosomes; the promoter regions contained numerous cis-acting regulatory elements related to abiotic stress tolerance and phytohormone responses. Evolutionary analysis showed that LEA genes were highly conserved and that the segmental duplication event played an important role in evolution of the LEA gene family. Transcription and expression pattern analyses revealed different regulatory patterns of LEA genes between cultivated and wild tomato species under normal conditions. Certain S. lycopersicum LEA (SlLEA) genes showed similar expression patterns and played specific roles under different abiotic stress and phytohormone treatments. Gene ontology and protein interaction analyses showed that most LEA genes acted in response to abiotic stimuli and water deficit. Five SlLEA proteins were found to interact with 11 S. lycopersicum WRKY proteins involved in development or resistance to stress. Virus-induced gene silencing of SlLEA6 affected the antioxidant and reactive oxygen species defense systems, increased the degree of cellular damage, and reduced drought resistance in S. lycopersicum. CONCLUSION: These findings provide comprehensive information on LEA proteins in cultivated and wild tomato species and their possible functions under different abiotic and phytohormone stresses. The study systematically broadens our current understanding of LEA proteins and candidate genes and provides a theoretical basis for future functional studies aimed at improving stress resistance in tomato. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-022-03953-7. BioMed Central 2022-12-19 /pmc/articles/PMC9762057/ /pubmed/36536303 http://dx.doi.org/10.1186/s12870-022-03953-7 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Jia, Chunping
Guo, Bin
Wang, Baike
Li, Xin
Yang, Tao
Li, Ning
Wang, Juan
Yu, Qinghui
The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress
title The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress
title_full The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress
title_fullStr The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress
title_full_unstemmed The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress
title_short The LEA gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of SlLEA6 in drought stress
title_sort lea gene family in tomato and its wild relatives: genome-wide identification, structural characterization, expression profiling, and role of sllea6 in drought stress
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9762057/
https://www.ncbi.nlm.nih.gov/pubmed/36536303
http://dx.doi.org/10.1186/s12870-022-03953-7
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