General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature

Heat shock factors (<i>HSF</i>s) are the key regulators of heat stress responses and play pivotal roles in tissue development and the temperature-induced regulation of secondary metabolites. In order to elucidate the roles of <i>HSF</i>s in <i>Cymbidium ensifolium</i...

Full description

Bibliographic Details
Main Authors: Ruiyue Zheng, Jiemin Chen, Yukun Peng, Xuanyi Zhu, Muqi Niu, Xiuming Chen, Kai Xie, Ruiliu Huang, Suying Zhan, Qiuli Su, Mingli Shen, Donghui Peng, Sagheer Ahmad, Kai Zhao, Zhong-Jian Liu, Yuzhen Zhou
Format: Article
Language:English
Published: MDPI AG 2024-01-01
Series:International Journal of Molecular Sciences
Subjects:
Online Access:https://www.mdpi.com/1422-0067/25/2/1002
_version_ 1797339836308258816
author Ruiyue Zheng
Jiemin Chen
Yukun Peng
Xuanyi Zhu
Muqi Niu
Xiuming Chen
Kai Xie
Ruiliu Huang
Suying Zhan
Qiuli Su
Mingli Shen
Donghui Peng
Sagheer Ahmad
Kai Zhao
Zhong-Jian Liu
Yuzhen Zhou
author_facet Ruiyue Zheng
Jiemin Chen
Yukun Peng
Xuanyi Zhu
Muqi Niu
Xiuming Chen
Kai Xie
Ruiliu Huang
Suying Zhan
Qiuli Su
Mingli Shen
Donghui Peng
Sagheer Ahmad
Kai Zhao
Zhong-Jian Liu
Yuzhen Zhou
author_sort Ruiyue Zheng
collection DOAJ
description Heat shock factors (<i>HSF</i>s) are the key regulators of heat stress responses and play pivotal roles in tissue development and the temperature-induced regulation of secondary metabolites. In order to elucidate the roles of <i>HSF</i>s in <i>Cymbidium ensifolium</i>, we conducted a genome-wide identification of <i>CeHSF</i> genes and predicted their functions based on their structural features and splicing patterns. Our results revealed 22 <i>HSF</i> family members, with each gene containing more than one intron. According to phylogenetic analysis, 59.1% of HSFs were grouped into the A subfamily, while subfamily HSFC contained only two HSFs. And the <i>HSF</i> gene families were differentiated evolutionarily between plant species. Two tandem repeats were found on Chr02, and two segmental duplication pairs were observed on Chr12, Chr17, and Chr19; this provided evidence for whole-genome duplication (WGD) events in <i>C. ensifolium</i>. The core region of the promoter in most <i>CeHSF</i> genes contained cis-acting elements such as AP2/ERF and bHLH, which were associated with plant growth, development, and stress responses. Except for <i>CeHSF11</i>, <i>14</i>, and <i>19</i>, each of the remaining <i>CeHSF</i>s contained at least one miRNA binding site. This included binding sites for miR156, miR393, and miR319, which were responsive to temperature and other stresses. The <i>HSF</i> gene family exhibited significant tissue specificity in both vegetative and floral organs of <i>C. ensifolium</i>. <i>CeHSF13</i> and <i>CeHSF15</i> showed relatively significant expression in flowers compared to other genes. During flower development, CeHSF15 exhibited markedly elevated expression in the early stages of flower opening, implicating critical regulatory functions in organ development and floral scent-related regulations. During the poikilothermic treatment, <i>CeHSF14</i> was upregulated over 200-fold after 6 h of heat treatment. <i>CeHSF13</i> and <i>CeHSF14</i> showed the highest expression at 6 h of low temperature, while the expression of <i>CeHSF15</i> and <i>CeHSF21</i> continuously decreased at a low temperature. The expression patterns of <i>CeHSFs</i> further confirmed their role in responding to temperature stress. Our study may help reveal the important roles of <i>HSFs</i> in plant development and metabolic regulation and show insight for the further molecular design breeding of <i>C. ensifolium</i>.
first_indexed 2024-03-08T09:54:10Z
format Article
id doaj.art-c21e22aca442471db261188e1794d150
institution Directory Open Access Journal
issn 1661-6596
1422-0067
language English
last_indexed 2024-03-08T09:54:10Z
publishDate 2024-01-01
publisher MDPI AG
record_format Article
series International Journal of Molecular Sciences
spelling doaj.art-c21e22aca442471db261188e1794d1502024-01-29T13:56:13ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672024-01-01252100210.3390/ijms25021002General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to TemperatureRuiyue Zheng0Jiemin Chen1Yukun Peng2Xuanyi Zhu3Muqi Niu4Xiuming Chen5Kai Xie6Ruiliu Huang7Suying Zhan8Qiuli Su9Mingli Shen10Donghui Peng11Sagheer Ahmad12Kai Zhao13Zhong-Jian Liu14Yuzhen Zhou15Ornamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Life Sciences, Fujian Normal University, Fuzhou 350117, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaCollege of Life Sciences, Fujian Normal University, Fuzhou 350117, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaOrnamental Plant Germplasm Resources Innovation & Engineering Application Research Center, Key Laboratory of National Forestry and Grassland Administration for Orchid Conservation and Utilization, College of Landscape Architecture and Art, Fujian Agriculture and Forestry University, Fuzhou 350002, ChinaHeat shock factors (<i>HSF</i>s) are the key regulators of heat stress responses and play pivotal roles in tissue development and the temperature-induced regulation of secondary metabolites. In order to elucidate the roles of <i>HSF</i>s in <i>Cymbidium ensifolium</i>, we conducted a genome-wide identification of <i>CeHSF</i> genes and predicted their functions based on their structural features and splicing patterns. Our results revealed 22 <i>HSF</i> family members, with each gene containing more than one intron. According to phylogenetic analysis, 59.1% of HSFs were grouped into the A subfamily, while subfamily HSFC contained only two HSFs. And the <i>HSF</i> gene families were differentiated evolutionarily between plant species. Two tandem repeats were found on Chr02, and two segmental duplication pairs were observed on Chr12, Chr17, and Chr19; this provided evidence for whole-genome duplication (WGD) events in <i>C. ensifolium</i>. The core region of the promoter in most <i>CeHSF</i> genes contained cis-acting elements such as AP2/ERF and bHLH, which were associated with plant growth, development, and stress responses. Except for <i>CeHSF11</i>, <i>14</i>, and <i>19</i>, each of the remaining <i>CeHSF</i>s contained at least one miRNA binding site. This included binding sites for miR156, miR393, and miR319, which were responsive to temperature and other stresses. The <i>HSF</i> gene family exhibited significant tissue specificity in both vegetative and floral organs of <i>C. ensifolium</i>. <i>CeHSF13</i> and <i>CeHSF15</i> showed relatively significant expression in flowers compared to other genes. During flower development, CeHSF15 exhibited markedly elevated expression in the early stages of flower opening, implicating critical regulatory functions in organ development and floral scent-related regulations. During the poikilothermic treatment, <i>CeHSF14</i> was upregulated over 200-fold after 6 h of heat treatment. <i>CeHSF13</i> and <i>CeHSF14</i> showed the highest expression at 6 h of low temperature, while the expression of <i>CeHSF15</i> and <i>CeHSF21</i> continuously decreased at a low temperature. The expression patterns of <i>CeHSFs</i> further confirmed their role in responding to temperature stress. Our study may help reveal the important roles of <i>HSFs</i> in plant development and metabolic regulation and show insight for the further molecular design breeding of <i>C. ensifolium</i>.https://www.mdpi.com/1422-0067/25/2/1002orchidcis-elementsgene expressionabiotic stressfloral scent regulation
spellingShingle Ruiyue Zheng
Jiemin Chen
Yukun Peng
Xuanyi Zhu
Muqi Niu
Xiuming Chen
Kai Xie
Ruiliu Huang
Suying Zhan
Qiuli Su
Mingli Shen
Donghui Peng
Sagheer Ahmad
Kai Zhao
Zhong-Jian Liu
Yuzhen Zhou
General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature
International Journal of Molecular Sciences
orchid
cis-elements
gene expression
abiotic stress
floral scent regulation
title General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature
title_full General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature
title_fullStr General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature
title_full_unstemmed General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature
title_short General Analysis of Heat Shock Factors in the <i>Cymbidium ensifolium</i> Genome Provided Insights into Their Evolution and Special Roles with Response to Temperature
title_sort general analysis of heat shock factors in the i cymbidium ensifolium i genome provided insights into their evolution and special roles with response to temperature
topic orchid
cis-elements
gene expression
abiotic stress
floral scent regulation
url https://www.mdpi.com/1422-0067/25/2/1002
work_keys_str_mv AT ruiyuezheng generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT jieminchen generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT yukunpeng generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT xuanyizhu generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT muqiniu generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT xiumingchen generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT kaixie generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT ruiliuhuang generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT suyingzhan generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT qiulisu generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT minglishen generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT donghuipeng generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT sagheerahmad generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT kaizhao generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT zhongjianliu generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature
AT yuzhenzhou generalanalysisofheatshockfactorsintheicymbidiumensifoliumigenomeprovidedinsightsintotheirevolutionandspecialroleswithresponsetotemperature