Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress
BACKGROUND: Elevated temperature and drought stress have substantial impacts on fruit quality, especially in terms of sugar metabolism and content. β-Amylase (BAM) plays a critical role in regulating jujube fruit sugar levels and abiotic stress response. Nevertheless, little is known about the regul...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9195466/ https://www.ncbi.nlm.nih.gov/pubmed/35698031 http://dx.doi.org/10.1186/s12864-022-08630-5 |
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author | Ma, Yaping Han, Yaru Feng, Xuerui Gao, Handong Cao, Bing Song, Lihua |
author_facet | Ma, Yaping Han, Yaru Feng, Xuerui Gao, Handong Cao, Bing Song, Lihua |
author_sort | Ma, Yaping |
collection | PubMed |
description | BACKGROUND: Elevated temperature and drought stress have substantial impacts on fruit quality, especially in terms of sugar metabolism and content. β-Amylase (BAM) plays a critical role in regulating jujube fruit sugar levels and abiotic stress response. Nevertheless, little is known about the regulatory functions of the BAM genes in jujube fruit. RESULTS: Nine jujube BAM genes were identified, clustered into four groups, and characterized to elucidate their structure, function, and distribution. Multiple sequence alignment and gene structure analysis showed that all ZjBAM genes contain Glu-186 and Glu-380 residues and are highly conserved. Phylogenetic and synteny analysis further indicated that the ZjBAM gene family is evolutionarily conserved and formed collinear pairs with the BAM genes of peach, apple, poplar, Arabidopsis thaliana, and cucumber. A single tandem gene pair was found within the ZjBAM gene family and is indicative of putative gene duplication events. We also explored the physicochemical properties, conserved motifs, and chromosomal and subcellular localization of ZjBAM genes as well as the interaction networks and 3D structures of ZjBAM proteins. A promoter cis-acting element analysis suggested that ZjBAM promoters comprise elements related to growth, development, phytohormones, and stress response. Furthermore, a metabolic pathways annotation analysis showed that ZjBAMs are significantly upregulated in the starch and sucrose metabolism, thereby controlling starch-maltose interconversion and hydrolyzing starch to maltose. Transcriptome and qRT-PCR analyses revealed that ZjBAMs respond positively to elevated temperature and drought stress. Specifically, ZjBAM1, ZjBAM2, ZjBAM5, and ZjBAM6 are significantly upregulated in response to severe drought. Bimolecular fluorescence complementation analysis demonstrated ZjBAM1-ZjAMY3, ZjBAM8-ZjDPE1, and ZjBAM7-ZjDPE1 protein interactions that were mainly present in the plasma membrane and nucleus. CONCLUSION: The jujube BAM gene family exhibits high evolutionary conservation. The various expression patterns of ZjBAM gene family members indicate that they play key roles in jujube growth, development, and abiotic stress response. Additionally, ZjBAMs interact with α-amylase and glucanotransferase. Collectively, the present study provides novel insights into the structure, evolution, and functions of the jujube BAM gene family, thus laying a foundation for further exploration of ZjBAM functional mechanisms in response to elevated temperature and drought stress, while opening up avenues for the development of economic forests in arid areas. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08630-5. |
format | Online Article Text |
id | pubmed-9195466 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-91954662022-06-15 Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress Ma, Yaping Han, Yaru Feng, Xuerui Gao, Handong Cao, Bing Song, Lihua BMC Genomics Research BACKGROUND: Elevated temperature and drought stress have substantial impacts on fruit quality, especially in terms of sugar metabolism and content. β-Amylase (BAM) plays a critical role in regulating jujube fruit sugar levels and abiotic stress response. Nevertheless, little is known about the regulatory functions of the BAM genes in jujube fruit. RESULTS: Nine jujube BAM genes were identified, clustered into four groups, and characterized to elucidate their structure, function, and distribution. Multiple sequence alignment and gene structure analysis showed that all ZjBAM genes contain Glu-186 and Glu-380 residues and are highly conserved. Phylogenetic and synteny analysis further indicated that the ZjBAM gene family is evolutionarily conserved and formed collinear pairs with the BAM genes of peach, apple, poplar, Arabidopsis thaliana, and cucumber. A single tandem gene pair was found within the ZjBAM gene family and is indicative of putative gene duplication events. We also explored the physicochemical properties, conserved motifs, and chromosomal and subcellular localization of ZjBAM genes as well as the interaction networks and 3D structures of ZjBAM proteins. A promoter cis-acting element analysis suggested that ZjBAM promoters comprise elements related to growth, development, phytohormones, and stress response. Furthermore, a metabolic pathways annotation analysis showed that ZjBAMs are significantly upregulated in the starch and sucrose metabolism, thereby controlling starch-maltose interconversion and hydrolyzing starch to maltose. Transcriptome and qRT-PCR analyses revealed that ZjBAMs respond positively to elevated temperature and drought stress. Specifically, ZjBAM1, ZjBAM2, ZjBAM5, and ZjBAM6 are significantly upregulated in response to severe drought. Bimolecular fluorescence complementation analysis demonstrated ZjBAM1-ZjAMY3, ZjBAM8-ZjDPE1, and ZjBAM7-ZjDPE1 protein interactions that were mainly present in the plasma membrane and nucleus. CONCLUSION: The jujube BAM gene family exhibits high evolutionary conservation. The various expression patterns of ZjBAM gene family members indicate that they play key roles in jujube growth, development, and abiotic stress response. Additionally, ZjBAMs interact with α-amylase and glucanotransferase. Collectively, the present study provides novel insights into the structure, evolution, and functions of the jujube BAM gene family, thus laying a foundation for further exploration of ZjBAM functional mechanisms in response to elevated temperature and drought stress, while opening up avenues for the development of economic forests in arid areas. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12864-022-08630-5. BioMed Central 2022-06-13 /pmc/articles/PMC9195466/ /pubmed/35698031 http://dx.doi.org/10.1186/s12864-022-08630-5 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 Ma, Yaping Han, Yaru Feng, Xuerui Gao, Handong Cao, Bing Song, Lihua Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress |
title | Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress |
title_full | Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress |
title_fullStr | Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress |
title_full_unstemmed | Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress |
title_short | Genome-wide identification of BAM (β-amylase) gene family in jujube (Ziziphus jujuba Mill.) and expression in response to abiotic stress |
title_sort | genome-wide identification of bam (β-amylase) gene family in jujube (ziziphus jujuba mill.) and expression in response to abiotic stress |
topic | Research |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9195466/ https://www.ncbi.nlm.nih.gov/pubmed/35698031 http://dx.doi.org/10.1186/s12864-022-08630-5 |
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