Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development

Background Heat shock factors (HSFs) play important roles during normal plant growth and development and when plants respond to diverse stressors. Although most studies have focused on the involvement of HSFs in the response to abiotic stresses, especially in model plants, there is little research o...

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Main Authors: Bin Tan, Liu Yan, Huannan Li, Xiaodong Lian, Jun Cheng, Wei Wang, Xianbo Zheng, Xiaobei Wang, Jidong Li, Xia Ye, Langlang Zhang, Zhiqian Li, Jiancan Feng
Format: Article
Language:English
Published: PeerJ Inc. 2021-03-01
Series:PeerJ
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Online Access:https://peerj.com/articles/10961.pdf
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author Bin Tan
Liu Yan
Huannan Li
Xiaodong Lian
Jun Cheng
Wei Wang
Xianbo Zheng
Xiaobei Wang
Jidong Li
Xia Ye
Langlang Zhang
Zhiqian Li
Jiancan Feng
author_facet Bin Tan
Liu Yan
Huannan Li
Xiaodong Lian
Jun Cheng
Wei Wang
Xianbo Zheng
Xiaobei Wang
Jidong Li
Xia Ye
Langlang Zhang
Zhiqian Li
Jiancan Feng
author_sort Bin Tan
collection DOAJ
description Background Heat shock factors (HSFs) play important roles during normal plant growth and development and when plants respond to diverse stressors. Although most studies have focused on the involvement of HSFs in the response to abiotic stresses, especially in model plants, there is little research on their participation in plant growth and development or on the HSF (PpHSF) gene family in peach (Prunus persica). Methods DBD (PF00447), the HSF characteristic domain, was used to search the peach genome and identify PpHSFs. Phylogenetic, multiple alignment and motif analyses were conducted using MEGA 6.0, ClustalW and MEME, respectively. The function of PpHSF5 was confirmed by overexpression of PpHSF5 into Arabidopsis. Results Eighteen PpHSF genes were identified within the peach genome. The PpHSF genes were nonuniformly distributed on the peach chromosomes. Seventeen of the PpHSFs (94.4%) contained one or two introns, except PpHSF18, which contained three introns. The in silico-translated PpHSFs were classified into three classes (PpHSFA, PpHSFB and PpHSFC) based on multiple alignment, motif analysis and phylogenetic comparison with HSFs from Arabidopsis thaliana and Oryza sativa. Dispersed gene duplication (DSD at 67%) mainly contributed to HSF gene family expansion in peach. Promoter analysis showed that the most common cis-elements were the MYB (abiotic stress response), ABRE (ABA-responsive) and MYC (dehydration-responsive) elements. Transcript profiling of 18 PpHSFs showed that the expression trend of PpHSF5 was consistent with shoot length changes in the cultivar ‘Zhongyoutao 14’. Further analysis of the PpHSF5 was conducted in 5-year-old peach trees, Nicotiana benthamiana and Arabidopsis thaliana, respectively. Tissue-specific expression analysis showed that PpHSF5 was expressed predominantly in young vegetative organs (leaf and apex). Subcellular localization revealed that PpHSF5 was located in the nucleus in N. benthamiana cells. Two transgenic Arabidopsis lines were obtained that overexpressed PpHSF5. The root length and the number of lateral roots in the transgenic seedlings were significantly less than in WT seedlings and after cultivation for three weeks. The transgenic rosettes were smaller than those of the WT at 2–3 weeks. The two transgenic lines exhibited a dwarf phenotype three weeks after transplanting, although there was no significant difference in the number of internodes. Moreover, the PpHSF5-OE lines exhibited enhanced thermotolerance. These results indicated that PpHSF5 might be act as a suppresser of growth and development of root and aerial organs.
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spelling doaj.art-a0e51e0d157347a3b3e9113b03a0a5dc2023-12-03T13:35:45ZengPeerJ Inc.PeerJ2167-83592021-03-019e1096110.7717/peerj.10961Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ developmentBin Tan0Liu Yan1Huannan Li2Xiaodong Lian3Jun Cheng4Wei Wang5Xianbo Zheng6Xiaobei Wang7Jidong Li8Xia Ye9Langlang Zhang10Zhiqian Li11Jiancan Feng12College of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaCollege of Horticulture, Henan Agricultural University, Zhengzhou, ChinaBackground Heat shock factors (HSFs) play important roles during normal plant growth and development and when plants respond to diverse stressors. Although most studies have focused on the involvement of HSFs in the response to abiotic stresses, especially in model plants, there is little research on their participation in plant growth and development or on the HSF (PpHSF) gene family in peach (Prunus persica). Methods DBD (PF00447), the HSF characteristic domain, was used to search the peach genome and identify PpHSFs. Phylogenetic, multiple alignment and motif analyses were conducted using MEGA 6.0, ClustalW and MEME, respectively. The function of PpHSF5 was confirmed by overexpression of PpHSF5 into Arabidopsis. Results Eighteen PpHSF genes were identified within the peach genome. The PpHSF genes were nonuniformly distributed on the peach chromosomes. Seventeen of the PpHSFs (94.4%) contained one or two introns, except PpHSF18, which contained three introns. The in silico-translated PpHSFs were classified into three classes (PpHSFA, PpHSFB and PpHSFC) based on multiple alignment, motif analysis and phylogenetic comparison with HSFs from Arabidopsis thaliana and Oryza sativa. Dispersed gene duplication (DSD at 67%) mainly contributed to HSF gene family expansion in peach. Promoter analysis showed that the most common cis-elements were the MYB (abiotic stress response), ABRE (ABA-responsive) and MYC (dehydration-responsive) elements. Transcript profiling of 18 PpHSFs showed that the expression trend of PpHSF5 was consistent with shoot length changes in the cultivar ‘Zhongyoutao 14’. Further analysis of the PpHSF5 was conducted in 5-year-old peach trees, Nicotiana benthamiana and Arabidopsis thaliana, respectively. Tissue-specific expression analysis showed that PpHSF5 was expressed predominantly in young vegetative organs (leaf and apex). Subcellular localization revealed that PpHSF5 was located in the nucleus in N. benthamiana cells. Two transgenic Arabidopsis lines were obtained that overexpressed PpHSF5. The root length and the number of lateral roots in the transgenic seedlings were significantly less than in WT seedlings and after cultivation for three weeks. The transgenic rosettes were smaller than those of the WT at 2–3 weeks. The two transgenic lines exhibited a dwarf phenotype three weeks after transplanting, although there was no significant difference in the number of internodes. Moreover, the PpHSF5-OE lines exhibited enhanced thermotolerance. These results indicated that PpHSF5 might be act as a suppresser of growth and development of root and aerial organs.https://peerj.com/articles/10961.pdfHeat shock factors familyRoot developmentPeach (Prunus persica)Functional identificationPpHSF5Aerial organ
spellingShingle Bin Tan
Liu Yan
Huannan Li
Xiaodong Lian
Jun Cheng
Wei Wang
Xianbo Zheng
Xiaobei Wang
Jidong Li
Xia Ye
Langlang Zhang
Zhiqian Li
Jiancan Feng
Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development
PeerJ
Heat shock factors family
Root development
Peach (Prunus persica)
Functional identification
PpHSF5
Aerial organ
title Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development
title_full Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development
title_fullStr Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development
title_full_unstemmed Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development
title_short Genome-wide identification of HSF family in peach and functional analysis of PpHSF5 involvement in root and aerial organ development
title_sort genome wide identification of hsf family in peach and functional analysis of pphsf5 involvement in root and aerial organ development
topic Heat shock factors family
Root development
Peach (Prunus persica)
Functional identification
PpHSF5
Aerial organ
url https://peerj.com/articles/10961.pdf
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