The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation

Abstract Background Alcohol dehydrogenases (ADHs) in plants are encoded by a multigene family. ADHs participate in growth, development, and adaptation in many plant species, but the evolution and function of the ADH gene family in sugarcane is still unclear. Results In the present study, 151 ADH gen...

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Main Authors: Weihua Su, Yongjuan Ren, Dongjiao Wang, Yachun Su, Jingfang Feng, Chang Zhang, Hanchen Tang, Liping Xu, Khushi Muhammad, Youxiong Que
Format: Article
Language:English
Published: BMC 2020-07-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-06929-9
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author Weihua Su
Yongjuan Ren
Dongjiao Wang
Yachun Su
Jingfang Feng
Chang Zhang
Hanchen Tang
Liping Xu
Khushi Muhammad
Youxiong Que
author_facet Weihua Su
Yongjuan Ren
Dongjiao Wang
Yachun Su
Jingfang Feng
Chang Zhang
Hanchen Tang
Liping Xu
Khushi Muhammad
Youxiong Que
author_sort Weihua Su
collection DOAJ
description Abstract Background Alcohol dehydrogenases (ADHs) in plants are encoded by a multigene family. ADHs participate in growth, development, and adaptation in many plant species, but the evolution and function of the ADH gene family in sugarcane is still unclear. Results In the present study, 151 ADH genes from 17 species including 32 ADH genes in Saccharum spontaneum and 6 ADH genes in modern sugarcane cultivar R570 were identified. Phylogenetic analysis demonstrated two groups of ADH genes and suggested that these genes underwent duplication during angiosperm evolution. Whole-genome duplication (WGD)/segmental and dispersed duplications played critical roles in the expansion of ADH family in S. spontaneum and R570, respectively. ScADH3 was cloned and preferentially expressed in response to cold stress. ScADH3 conferred improved cold tolerance in E. coli cells. Ectopic expression showed that ScADH3 can also enhance cold tolerance in transgenic tobacco. The accumulation of reactive oxygen species (ROS) in leaves of transgenic tobacco was significantly lower than in wild-type tobacco. The transcript levels of ROS-related genes in transgenic tobacco increased significantly. ScADH3 seems to affect cold tolerance by regulating the ROS-related genes to maintain the ROS homeostasis. Conclusions This study depicted the size and composition of the ADH gene family in 17 species, and investigated their evolution pattern. Comparative genomics analysis among the ADH gene families of S. bicolor, R570 and S. spontaneum revealed their close evolutionary relationship. Functional analysis suggested that ScADH3, which maintained the steady state of ROS by regulating ROS-related genes, was related to cold tolerance. These findings will facilitate research on evolutionary and functional aspects of the ADH genes in sugarcane, especially for the understanding of ScADH3 under cold stress.
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spelling doaj.art-ed367cdb67994a90be1e4b3abac63aa52022-12-22T03:05:05ZengBMCBMC Genomics1471-21642020-07-0121111710.1186/s12864-020-06929-9The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulationWeihua Su0Yongjuan Ren1Dongjiao Wang2Yachun Su3Jingfang Feng4Chang Zhang5Hanchen Tang6Liping Xu7Khushi Muhammad8Youxiong Que9Key Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityDepartment of Genetics, Hazara UniversityKey Laboratory of Sugarcane Biology and Genetic Breeding, Ministry of Agriculture, Fujian Agriculture and Forestry UniversityAbstract Background Alcohol dehydrogenases (ADHs) in plants are encoded by a multigene family. ADHs participate in growth, development, and adaptation in many plant species, but the evolution and function of the ADH gene family in sugarcane is still unclear. Results In the present study, 151 ADH genes from 17 species including 32 ADH genes in Saccharum spontaneum and 6 ADH genes in modern sugarcane cultivar R570 were identified. Phylogenetic analysis demonstrated two groups of ADH genes and suggested that these genes underwent duplication during angiosperm evolution. Whole-genome duplication (WGD)/segmental and dispersed duplications played critical roles in the expansion of ADH family in S. spontaneum and R570, respectively. ScADH3 was cloned and preferentially expressed in response to cold stress. ScADH3 conferred improved cold tolerance in E. coli cells. Ectopic expression showed that ScADH3 can also enhance cold tolerance in transgenic tobacco. The accumulation of reactive oxygen species (ROS) in leaves of transgenic tobacco was significantly lower than in wild-type tobacco. The transcript levels of ROS-related genes in transgenic tobacco increased significantly. ScADH3 seems to affect cold tolerance by regulating the ROS-related genes to maintain the ROS homeostasis. Conclusions This study depicted the size and composition of the ADH gene family in 17 species, and investigated their evolution pattern. Comparative genomics analysis among the ADH gene families of S. bicolor, R570 and S. spontaneum revealed their close evolutionary relationship. Functional analysis suggested that ScADH3, which maintained the steady state of ROS by regulating ROS-related genes, was related to cold tolerance. These findings will facilitate research on evolutionary and functional aspects of the ADH genes in sugarcane, especially for the understanding of ScADH3 under cold stress.http://link.springer.com/article/10.1186/s12864-020-06929-9SugarcaneAlcohol dehydrogenases (ADH)Cold toleranceROS homeostasisEvolutionGenome-wide analysis
spellingShingle Weihua Su
Yongjuan Ren
Dongjiao Wang
Yachun Su
Jingfang Feng
Chang Zhang
Hanchen Tang
Liping Xu
Khushi Muhammad
Youxiong Que
The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
BMC Genomics
Sugarcane
Alcohol dehydrogenases (ADH)
Cold tolerance
ROS homeostasis
Evolution
Genome-wide analysis
title The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
title_full The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
title_fullStr The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
title_full_unstemmed The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
title_short The alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
title_sort alcohol dehydrogenase gene family in sugarcane and its involvement in cold stress regulation
topic Sugarcane
Alcohol dehydrogenases (ADH)
Cold tolerance
ROS homeostasis
Evolution
Genome-wide analysis
url http://link.springer.com/article/10.1186/s12864-020-06929-9
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