Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening

Abstract Background E2 ubiquitin-conjugating (UBC) enzymes are an integral component of the ubiquitin proteasome system that play an important role in plant development, growth, and external stress responses. Several UBC genes have been identified in various plants. However, no studies exploring the...

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Main Authors: Mengyao Li, Liangxin Wang, Yiting Liu, Yuanxiu Lin, Yunting Zhang, Yu Long, Chuanying Luo, Yong Zhang, Qing Chen, Pinwen Chen, Yan Wang, Xiaorong Wang, Haoru Tang, Ya Luo
Format: Article
Language:English
Published: BMC 2022-01-01
Series:BMC Plant Biology
Subjects:
Online Access:https://doi.org/10.1186/s12870-021-03421-8
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author Mengyao Li
Liangxin Wang
Yiting Liu
Yuanxiu Lin
Yunting Zhang
Yu Long
Chuanying Luo
Yong Zhang
Qing Chen
Pinwen Chen
Yan Wang
Xiaorong Wang
Haoru Tang
Ya Luo
author_facet Mengyao Li
Liangxin Wang
Yiting Liu
Yuanxiu Lin
Yunting Zhang
Yu Long
Chuanying Luo
Yong Zhang
Qing Chen
Pinwen Chen
Yan Wang
Xiaorong Wang
Haoru Tang
Ya Luo
author_sort Mengyao Li
collection DOAJ
description Abstract Background E2 ubiquitin-conjugating (UBC) enzymes are an integral component of the ubiquitin proteasome system that play an important role in plant development, growth, and external stress responses. Several UBC genes have been identified in various plants. However, no studies exploring the functions of UBC genes in regulating fruit of strawberry have been reported. In the present study, a systematic analysis of the entire UBC family members were conducted in the genome of strawberry (Fragaria ×ananassa) based on bioinformatics method, and the gene functioning in strawberry ripening was explored. Results A total of 191 UBC genes were identified in the genome of cultivated strawberry. These genes were unevenly distributed across the 28 chromosomes from the 4 subgenomes of cultivated strawberry, ranging from 3 to 11 genes per chromosome. Moreover, the expansion of FaUBC genes in strawberry was mainly driven by WGD. All the FaUBC genes were clarified into 13 groups and most of them were included in the group VI. The gene structure analysis showed that the number of exons varied from 1 to 23, and the structure of genes had few differences within the same groups but a distinction in different groups. Identification of the cis-acting elements of the promoter revealed multiple regulatory elements that responded to plant growth and development, phytohormone responsive, and abiotic and biotic stress. Data from functional annotation indicated that FaUBC genes play a role in a variety of biological processes. The RNA-seq data showed that FaUBC genes displayed different expression pattern during the fruit ripening process and clarified into 6 clusters. In particular, cluster 3 exhibiting a sudden expression increase in the turning red stage were speculated to be involved in fruit ripening. Hence, two FaUBC genes (FaUBC76 and FaUBC78) were selected for gene function analysis by transient over-expression method. The results indicated that FaUBC76 has a positive effect on the fruit development and ripening in strawberry by up-regulating accumulation of anthocyanins. Moreover, expression of some maturity-related genes were also significantly increased, further supporting a role for FaUBC76 in the regulation of fruit ripening or softening. On the contrary, the overexpression of FaUBC78 significantly increased the firmness of strawberry fruit, indicating that FaUBC78 had a positive role in inhibiting the decrease of strawberry fruit firmness. Conclusion Our study not only provide comprehensive information on system evolution and function on UBC genes, but also give a new insight into explore the roles of FaUBC genes in the regulation of strawberry ripening.
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spelling doaj.art-9e92992b3b694b63b491f3b06e3de3d72022-12-21T19:43:47ZengBMCBMC Plant Biology1471-22292022-01-0122111610.1186/s12870-021-03421-8Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripeningMengyao Li0Liangxin Wang1Yiting Liu2Yuanxiu Lin3Yunting Zhang4Yu Long5Chuanying Luo6Yong Zhang7Qing Chen8Pinwen Chen9Yan Wang10Xiaorong Wang11Haoru Tang12Ya Luo13College of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityDepartmental and Municipal Co-construction of Crops Genetic Improvement of Hill Land Key Laboratory of SichuanCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityCollege of Horticulture, Sichuan Agricultural UniversityAbstract Background E2 ubiquitin-conjugating (UBC) enzymes are an integral component of the ubiquitin proteasome system that play an important role in plant development, growth, and external stress responses. Several UBC genes have been identified in various plants. However, no studies exploring the functions of UBC genes in regulating fruit of strawberry have been reported. In the present study, a systematic analysis of the entire UBC family members were conducted in the genome of strawberry (Fragaria ×ananassa) based on bioinformatics method, and the gene functioning in strawberry ripening was explored. Results A total of 191 UBC genes were identified in the genome of cultivated strawberry. These genes were unevenly distributed across the 28 chromosomes from the 4 subgenomes of cultivated strawberry, ranging from 3 to 11 genes per chromosome. Moreover, the expansion of FaUBC genes in strawberry was mainly driven by WGD. All the FaUBC genes were clarified into 13 groups and most of them were included in the group VI. The gene structure analysis showed that the number of exons varied from 1 to 23, and the structure of genes had few differences within the same groups but a distinction in different groups. Identification of the cis-acting elements of the promoter revealed multiple regulatory elements that responded to plant growth and development, phytohormone responsive, and abiotic and biotic stress. Data from functional annotation indicated that FaUBC genes play a role in a variety of biological processes. The RNA-seq data showed that FaUBC genes displayed different expression pattern during the fruit ripening process and clarified into 6 clusters. In particular, cluster 3 exhibiting a sudden expression increase in the turning red stage were speculated to be involved in fruit ripening. Hence, two FaUBC genes (FaUBC76 and FaUBC78) were selected for gene function analysis by transient over-expression method. The results indicated that FaUBC76 has a positive effect on the fruit development and ripening in strawberry by up-regulating accumulation of anthocyanins. Moreover, expression of some maturity-related genes were also significantly increased, further supporting a role for FaUBC76 in the regulation of fruit ripening or softening. On the contrary, the overexpression of FaUBC78 significantly increased the firmness of strawberry fruit, indicating that FaUBC78 had a positive role in inhibiting the decrease of strawberry fruit firmness. Conclusion Our study not only provide comprehensive information on system evolution and function on UBC genes, but also give a new insight into explore the roles of FaUBC genes in the regulation of strawberry ripening.https://doi.org/10.1186/s12870-021-03421-8StrawberryUbiquitin-conjugating enzymesPhylogenetic analysisExpression patterns analysisFruit ripening
spellingShingle Mengyao Li
Liangxin Wang
Yiting Liu
Yuanxiu Lin
Yunting Zhang
Yu Long
Chuanying Luo
Yong Zhang
Qing Chen
Pinwen Chen
Yan Wang
Xiaorong Wang
Haoru Tang
Ya Luo
Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening
BMC Plant Biology
Strawberry
Ubiquitin-conjugating enzymes
Phylogenetic analysis
Expression patterns analysis
Fruit ripening
title Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening
title_full Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening
title_fullStr Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening
title_full_unstemmed Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening
title_short Characterization and regulation mechanism analysis of ubiquitin-conjugating family genes in strawberry reveals a potential role in fruit ripening
title_sort characterization and regulation mechanism analysis of ubiquitin conjugating family genes in strawberry reveals a potential role in fruit ripening
topic Strawberry
Ubiquitin-conjugating enzymes
Phylogenetic analysis
Expression patterns analysis
Fruit ripening
url https://doi.org/10.1186/s12870-021-03421-8
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