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Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato

BACKGROUND: Low temperature (LT) is one of the main limiting factors that affect growth and development in grape. Increasing soluble sugar and scavenging reactive oxygen species (ROS) play critical roles in grapevine resistance to cold stress. However, the mechanism of β-amylase (BAM) involved in th...

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Autores principales: Liang, Guoping, He, Honghong, Nai, Guojie, Feng, Lidan, Li, Yanmei, Zhou, Qi, Ma, Zonghuan, Yue, Yuan, Chen, Baihong, Mao, Juan
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8004407/
https://www.ncbi.nlm.nih.gov/pubmed/33771117
http://dx.doi.org/10.1186/s12870-021-02916-8
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author Liang, Guoping
He, Honghong
Nai, Guojie
Feng, Lidan
Li, Yanmei
Zhou, Qi
Ma, Zonghuan
Yue, Yuan
Chen, Baihong
Mao, Juan
author_facet Liang, Guoping
He, Honghong
Nai, Guojie
Feng, Lidan
Li, Yanmei
Zhou, Qi
Ma, Zonghuan
Yue, Yuan
Chen, Baihong
Mao, Juan
author_sort Liang, Guoping
collection PubMed
description BACKGROUND: Low temperature (LT) is one of the main limiting factors that affect growth and development in grape. Increasing soluble sugar and scavenging reactive oxygen species (ROS) play critical roles in grapevine resistance to cold stress. However, the mechanism of β-amylase (BAM) involved in the regulation of sugar levels and antioxidant enzyme activities in response to cold stress is unclear. RESULTS: In this study, six BAM genes were identified and clustered into four groups. Multiple sequence alignment and gene structure analysis showed that VvBAM6 lacked the Glu380 residue and contained only an exon. The transcript abundance of VvBAM1 and VvBAM3 significantly increased as temperature decreased. After LT stress, VvBAM1 was highly expressed in the leaves, petioles, stems, and roots of overexpressing tomato lines. The total amylase and BAM activities increased by 6.5- and 6.01-fold in transgenic plants compared with those in wild-type tomato plants (WT) subjected to LT, respectively. The glucose and sucrose contents in transgenic plants were significantly higher than those in WT plants, whereas the starch contents in the former decreased by 1.5-fold compared with those in the latter under LT stress. The analysis of transcriptome sequencing data revealed that 541 genes were upregulated, and 663 genes were downregulated in transgenic plants. One sugar transporter protein gene (SlSTP10), two peroxidase (POD)-related genes (SlPER7 and SlPER5), and one catalase (CAT)-related gene (SlCAT1) were upregulated by 8.6-, 3.6-, 3.0-, and 2.3-fold in transgenic plants after LT stress, respectively. CONCLUSIONS: Our results suggest that VvBAM1 overexpression promotes ROS scavenging and improves cold tolerance ability by modulating starch hydrolysis to affect soluble sugar levels in tomato plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02916-8.
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spelling pubmed-80044072021-03-30 Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato Liang, Guoping He, Honghong Nai, Guojie Feng, Lidan Li, Yanmei Zhou, Qi Ma, Zonghuan Yue, Yuan Chen, Baihong Mao, Juan BMC Plant Biol Research Article BACKGROUND: Low temperature (LT) is one of the main limiting factors that affect growth and development in grape. Increasing soluble sugar and scavenging reactive oxygen species (ROS) play critical roles in grapevine resistance to cold stress. However, the mechanism of β-amylase (BAM) involved in the regulation of sugar levels and antioxidant enzyme activities in response to cold stress is unclear. RESULTS: In this study, six BAM genes were identified and clustered into four groups. Multiple sequence alignment and gene structure analysis showed that VvBAM6 lacked the Glu380 residue and contained only an exon. The transcript abundance of VvBAM1 and VvBAM3 significantly increased as temperature decreased. After LT stress, VvBAM1 was highly expressed in the leaves, petioles, stems, and roots of overexpressing tomato lines. The total amylase and BAM activities increased by 6.5- and 6.01-fold in transgenic plants compared with those in wild-type tomato plants (WT) subjected to LT, respectively. The glucose and sucrose contents in transgenic plants were significantly higher than those in WT plants, whereas the starch contents in the former decreased by 1.5-fold compared with those in the latter under LT stress. The analysis of transcriptome sequencing data revealed that 541 genes were upregulated, and 663 genes were downregulated in transgenic plants. One sugar transporter protein gene (SlSTP10), two peroxidase (POD)-related genes (SlPER7 and SlPER5), and one catalase (CAT)-related gene (SlCAT1) were upregulated by 8.6-, 3.6-, 3.0-, and 2.3-fold in transgenic plants after LT stress, respectively. CONCLUSIONS: Our results suggest that VvBAM1 overexpression promotes ROS scavenging and improves cold tolerance ability by modulating starch hydrolysis to affect soluble sugar levels in tomato plants. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-021-02916-8. BioMed Central 2021-03-26 /pmc/articles/PMC8004407/ /pubmed/33771117 http://dx.doi.org/10.1186/s12870-021-02916-8 Text en © The Author(s) 2021 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/. 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 in a credit line to the data.
spellingShingle Research Article
Liang, Guoping
He, Honghong
Nai, Guojie
Feng, Lidan
Li, Yanmei
Zhou, Qi
Ma, Zonghuan
Yue, Yuan
Chen, Baihong
Mao, Juan
Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
title Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
title_full Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
title_fullStr Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
title_full_unstemmed Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
title_short Genome-wide identification of BAM genes in grapevine (Vitis vinifera L.) and ectopic expression of VvBAM1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
title_sort genome-wide identification of bam genes in grapevine (vitis vinifera l.) and ectopic expression of vvbam1 modulating soluble sugar levels to improve low-temperature tolerance in tomato
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8004407/
https://www.ncbi.nlm.nih.gov/pubmed/33771117
http://dx.doi.org/10.1186/s12870-021-02916-8
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