Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance

BackgroundKandelia obovata is an important mangrove species extensively distributed in Eastern Asia that is susceptible to low-temperature stress. NAC (NAM, ATAF1/2 and CUC2) domain proteins are transcription factors (TFs) that play various roles in plant growth and development and in the plant resp...

Full description

Bibliographic Details
Main Authors: Zhaokui Du, Shixian You, Dang Yang, Yutian Tao, Yunxiao Zhu, Wen Sun, Zhengman Chen, Junmin Li
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-11-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2022.1048822/full
_version_ 1811307440042409984
author Zhaokui Du
Shixian You
Dang Yang
Yutian Tao
Yunxiao Zhu
Wen Sun
Zhengman Chen
Junmin Li
author_facet Zhaokui Du
Shixian You
Dang Yang
Yutian Tao
Yunxiao Zhu
Wen Sun
Zhengman Chen
Junmin Li
author_sort Zhaokui Du
collection DOAJ
description BackgroundKandelia obovata is an important mangrove species extensively distributed in Eastern Asia that is susceptible to low-temperature stress. NAC (NAM, ATAF1/2 and CUC2) domain proteins are transcription factors (TFs) that play various roles in plant growth and development and in the plant response to environmental stresses. Nevertheless, genome-wide analyses of K. obovata NAC genes (KoNACs) and their responses to chilling stress have rarely been studied.MethodsThe KoNAC gene family was identified and characterized using bioinformatic analysis, the subcellular location of some NAC proteins was confirmed using confocal microscopy analysis, and the KoNACs that responded to chilling stress were screened using RNA-seq and qRT-PCR analysis.ResultsA total of 79 KoNACs were identified, and they were unequally distributed across all 18 chromosomes of K. obovata. The KoNAC proteins could be divided into 16 subgroups according to the phylogenetic tree based on NAC family members of Arabidopsis thaliana. The KoNACs exhibited greater synteny with A. thaliana sequences than with Oryza sativa sequences, indicating that KoNACs underwent extensive evolution after the divergence of dicotyledons and monocotyledons. Segmental duplication was the main driving force of the expansions of KoNAC genes. Confocal microscopy analysis verified that the four randomly selected KoNACs localized to the nucleus, indicating the accuracy of the bioinformatic predictions. Tissue expression pattern analysis demonstrated that some KoNAC genes showed tissue-specific expression, suggesting that these KoNACs might be important for plant development and growth. Additionally, the expression levels of 19 KoNACs were significantly (15 positively and 4 negatively) induced by cold treatment, demonstrating that these KoNACs might play important roles during cold stress responses and might be candidate genes for the genetic engineering of K. obovata with enhanced chilling stress tolerance. Coexpression network analysis revealed that 381 coexpressed pairs (between 13 KoNACs and 284 other genes) were significantly correlated.ConclusionsSeventy-nine KoNACs were identified in K. obovata, nineteen of which displayed chilling-induced expression patterns. These genes may serve as candidates for functional analyses of KoNACs engaged in chilling stress. Our results lay the foundation for evolutionary analyses of KoNACs and their molecular mechanisms in response to environmental stress.
first_indexed 2024-04-13T09:04:26Z
format Article
id doaj.art-7b4566f9794246d3a503b204b39523e4
institution Directory Open Access Journal
issn 1664-462X
language English
last_indexed 2024-04-13T09:04:26Z
publishDate 2022-11-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Plant Science
spelling doaj.art-7b4566f9794246d3a503b204b39523e42022-12-22T02:53:01ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2022-11-011310.3389/fpls.2022.10488221048822Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling toleranceZhaokui Du0Shixian You1Dang Yang2Yutian Tao3Yunxiao Zhu4Wen Sun5Zhengman Chen6Junmin Li7Zhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, ChinaSection of Maritime Space and Island Management, Yuhuan Municipal Bureau of Natural Resources and Planning, Yuhuan, ChinaZhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, ChinaZhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, ChinaZhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, ChinaZhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, ChinaDepartment of Security Production Management, Taizhou Circular Economy Development Co., Ltd., Taizhou, ChinaZhejiang Provincial Key Laboratory of Plant Evolutionary Ecology and Conservation, Taizhou University, Taizhou, ChinaBackgroundKandelia obovata is an important mangrove species extensively distributed in Eastern Asia that is susceptible to low-temperature stress. NAC (NAM, ATAF1/2 and CUC2) domain proteins are transcription factors (TFs) that play various roles in plant growth and development and in the plant response to environmental stresses. Nevertheless, genome-wide analyses of K. obovata NAC genes (KoNACs) and their responses to chilling stress have rarely been studied.MethodsThe KoNAC gene family was identified and characterized using bioinformatic analysis, the subcellular location of some NAC proteins was confirmed using confocal microscopy analysis, and the KoNACs that responded to chilling stress were screened using RNA-seq and qRT-PCR analysis.ResultsA total of 79 KoNACs were identified, and they were unequally distributed across all 18 chromosomes of K. obovata. The KoNAC proteins could be divided into 16 subgroups according to the phylogenetic tree based on NAC family members of Arabidopsis thaliana. The KoNACs exhibited greater synteny with A. thaliana sequences than with Oryza sativa sequences, indicating that KoNACs underwent extensive evolution after the divergence of dicotyledons and monocotyledons. Segmental duplication was the main driving force of the expansions of KoNAC genes. Confocal microscopy analysis verified that the four randomly selected KoNACs localized to the nucleus, indicating the accuracy of the bioinformatic predictions. Tissue expression pattern analysis demonstrated that some KoNAC genes showed tissue-specific expression, suggesting that these KoNACs might be important for plant development and growth. Additionally, the expression levels of 19 KoNACs were significantly (15 positively and 4 negatively) induced by cold treatment, demonstrating that these KoNACs might play important roles during cold stress responses and might be candidate genes for the genetic engineering of K. obovata with enhanced chilling stress tolerance. Coexpression network analysis revealed that 381 coexpressed pairs (between 13 KoNACs and 284 other genes) were significantly correlated.ConclusionsSeventy-nine KoNACs were identified in K. obovata, nineteen of which displayed chilling-induced expression patterns. These genes may serve as candidates for functional analyses of KoNACs engaged in chilling stress. Our results lay the foundation for evolutionary analyses of KoNACs and their molecular mechanisms in response to environmental stress.https://www.frontiersin.org/articles/10.3389/fpls.2022.1048822/fullchilling stressexpression profilesgene duplicationKandelia obovataNAC gene familyphylogenetic analysis
spellingShingle Zhaokui Du
Shixian You
Dang Yang
Yutian Tao
Yunxiao Zhu
Wen Sun
Zhengman Chen
Junmin Li
Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance
Frontiers in Plant Science
chilling stress
expression profiles
gene duplication
Kandelia obovata
NAC gene family
phylogenetic analysis
title Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance
title_full Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance
title_fullStr Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance
title_full_unstemmed Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance
title_short Comprehensive analysis of the NAC transcription factor gene family in Kandelia obovata reveals potential members related to chilling tolerance
title_sort comprehensive analysis of the nac transcription factor gene family in kandelia obovata reveals potential members related to chilling tolerance
topic chilling stress
expression profiles
gene duplication
Kandelia obovata
NAC gene family
phylogenetic analysis
url https://www.frontiersin.org/articles/10.3389/fpls.2022.1048822/full
work_keys_str_mv AT zhaokuidu comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT shixianyou comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT dangyang comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT yutiantao comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT yunxiaozhu comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT wensun comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT zhengmanchen comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance
AT junminli comprehensiveanalysisofthenactranscriptionfactorgenefamilyinkandeliaobovatarevealspotentialmembersrelatedtochillingtolerance