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Title: Evolutionary Divergence of Duplicated Hsf Genes in Populus

Abstract

Heat shock transcription factors (Hsfs), which function as the activator of heat shock proteins (Hsps), play multiple roles in response to environmental stress and the development of plants. The Hsf family had experienced gene expansion via whole-genome duplication from a single cell algae to higher plants. Yet, how the Hsf gene family went through evolutionary divergence after genome duplication is unknown. As a model wood species, Populus trichocarpa is widely distributed in North America with various ecological and climatic environments. In this study, we used P. trichocarpa as materials and identified the expression divergence of the PtHsf gene family in developmental processes, such as dormant bud formation and opening, catkins development, and in response to environments. Through the co-expression network, we further discovered the divergent co-expressed genes that related to the functional divergence of PtHsf. Then, we studied the alternative splicing events, single nucleotide polymorphism distribution and tertiary structures of members of the PtHsf gene family. In addition to expression divergence, we uncovered the evolutionary divergence in the protein level which may be important to new function formations and for survival in changing environments. This study comprehensively assessed the evolutionary divergence of a member of the PtHsf gene family aftermore » genome duplication, paving the way for further gene function analysis and genetic engineering.« less

Authors:
ORCiD logo [1];  [2]; ORCiD logo [3]
  1. Fujian Agriculture and Forestry Univ., Fuzhou (China)
  2. Chinese Academy of Forestry, Beijing (China)
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1513366
Grant/Contract Number:  
[AC05-00OR22725]
Resource Type:
Accepted Manuscript
Journal Name:
Cells
Additional Journal Information:
[ Journal Volume: 8; Journal Issue: 5]; Journal ID: ISSN 2073-4409
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Populus; heat shock transcription factors; gene duplication; gene expression; alternative splicing; single nucleotide polymorphism; protein structure; co-expression network

Citation Formats

Liu, Bobin, Hu, Jianjun, and Zhang, Jin. Evolutionary Divergence of Duplicated Hsf Genes in Populus. United States: N. p., 2019. Web. doi:10.3390/cells8050438.
Liu, Bobin, Hu, Jianjun, & Zhang, Jin. Evolutionary Divergence of Duplicated Hsf Genes in Populus. United States. doi:10.3390/cells8050438.
Liu, Bobin, Hu, Jianjun, and Zhang, Jin. Fri . "Evolutionary Divergence of Duplicated Hsf Genes in Populus". United States. doi:10.3390/cells8050438. https://www.osti.gov/servlets/purl/1513366.
@article{osti_1513366,
title = {Evolutionary Divergence of Duplicated Hsf Genes in Populus},
author = {Liu, Bobin and Hu, Jianjun and Zhang, Jin},
abstractNote = {Heat shock transcription factors (Hsfs), which function as the activator of heat shock proteins (Hsps), play multiple roles in response to environmental stress and the development of plants. The Hsf family had experienced gene expansion via whole-genome duplication from a single cell algae to higher plants. Yet, how the Hsf gene family went through evolutionary divergence after genome duplication is unknown. As a model wood species, Populus trichocarpa is widely distributed in North America with various ecological and climatic environments. In this study, we used P. trichocarpa as materials and identified the expression divergence of the PtHsf gene family in developmental processes, such as dormant bud formation and opening, catkins development, and in response to environments. Through the co-expression network, we further discovered the divergent co-expressed genes that related to the functional divergence of PtHsf. Then, we studied the alternative splicing events, single nucleotide polymorphism distribution and tertiary structures of members of the PtHsf gene family. In addition to expression divergence, we uncovered the evolutionary divergence in the protein level which may be important to new function formations and for survival in changing environments. This study comprehensively assessed the evolutionary divergence of a member of the PtHsf gene family after genome duplication, paving the way for further gene function analysis and genetic engineering.},
doi = {10.3390/cells8050438},
journal = {Cells},
number = [5],
volume = [8],
place = {United States},
year = {2019},
month = {5}
}

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Works referenced in this record:

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journal, December 2005


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    Works referencing / citing this record:

    Poplar as a feedstock for biofuels: A review of compositional characteristics
    journal, March 2010

    • Sannigrahi, Poulomi; Ragauskas, Arthur J.; Tuskan, Gerald A.
    • Biofuels, Bioproducts and Biorefining, Vol. 4, Issue 2
    • DOI: 10.1002/bbb.206

    Conversion of a β-strand to anα-helix induced by a single-site mutation observed in the crystal structure of fis mutant pro 26 Ala
    journal, September 1998


    SNP alleles in human disease and evolution
    journal, November 2002


    Regulation of plant biomass production
    journal, June 2010


    Beyond Genomics: Studying Evolution with Gene Coexpression Networks
    journal, April 2017


    Role of PHABULOSA and PHAVOLUTA in determining radial patterning in shoots
    journal, June 2001

    • McConnell, Jane R.; Emery, John; Eshed, Yuval
    • Nature, Vol. 411, Issue 6838
    • DOI: 10.1038/35079635

    Population genomics of Populus trichocarpa identifies signatures of selection and adaptive trait associations
    journal, August 2014

    • Evans, Luke M.; Slavov, Gancho T.; Rodgers-Melnick, Eli
    • Nature Genetics, Vol. 46, Issue 10
    • DOI: 10.1038/ng.3075

    The I-TASSER Suite: protein structure and function prediction
    journal, December 2014

    • Yang, Jianyi; Yan, Renxiang; Roy, Ambrish
    • Nature Methods, Vol. 12, Issue 1
    • DOI: 10.1038/nmeth.3213

    ModelFinder: fast model selection for accurate phylogenetic estimates
    journal, May 2017

    • Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
    • Nature Methods, Vol. 14, Issue 6
    • DOI: 10.1038/nmeth.4285

    Regulation of heat shock transcription factors and their roles in physiology and disease
    journal, August 2017

    • Gomez-Pastor, Rocio; Burchfiel, Eileen T.; Thiele, Dennis J.
    • Nature Reviews Molecular Cell Biology, Vol. 19, Issue 1
    • DOI: 10.1038/nrm.2017.73

    Heat shock factors: integrators of cell stress, development and lifespan
    journal, July 2010

    • Åkerfelt, Malin; Morimoto, Richard I.; Sistonen, Lea
    • Nature Reviews Molecular Cell Biology, Vol. 11, Issue 8
    • DOI: 10.1038/nrm2938

    Structures of HSF2 reveal mechanisms for differential regulation of human heat-shock factors
    journal, January 2016

    • Jaeger, Alex M.; Pemble, Charles W.; Sistonen, Lea
    • Nature Structural & Molecular Biology, Vol. 23, Issue 2
    • DOI: 10.1038/nsmb.3150

    Leaf expansion - an integrating plant behaviour: Leaf expansion
    journal, December 1999


    Functional association between promoter structure and transcript alternative splicing
    journal, October 1997

    • Cramer, P.; Pesce, C. G.; Baralle, F. E.
    • Proceedings of the National Academy of Sciences, Vol. 94, Issue 21
    • DOI: 10.1073/pnas.94.21.11456

    Populus: Arabidopsis for Forestry. Do We Need a Model Tree?
    journal, October 2002


    Cytoscape 2.8: new features for data integration and network visualization
    journal, December 2010


    Multiple functions of Drosophila heat shock transcription factor in vivo
    journal, May 1997


    UFBoot2: Improving the Ultrafast Bootstrap Approximation
    journal, October 2017

    • Hoang, Diep Thi; Chernomor, Olga; von Haeseler, Arndt
    • Molecular Biology and Evolution, Vol. 35, Issue 2
    • DOI: 10.1093/molbev/msx281

    W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis
    journal, April 2016

    • Trifinopoulos, Jana; Nguyen, Lam-Tung; von Haeseler, Arndt
    • Nucleic Acids Research, Vol. 44, Issue W1
    • DOI: 10.1093/nar/gkw256

    Interactive tree of life (iTOL) v3: an online tool for the display and annotation of phylogenetic and other trees
    journal, April 2016

    • Letunic, Ivica; Bork, Peer
    • Nucleic Acids Research, Vol. 44, Issue W1
    • DOI: 10.1093/nar/gkw290

    PlantPAN3.0: a new and updated resource for reconstructing transcriptional regulatory networks from ChIP-seq experiments in plants
    journal, November 2018

    • Chow, Chi-Nga; Lee, Tzong-Yi; Hung, Yu-Cheng
    • Nucleic Acids Research, Vol. 47, Issue D1
    • DOI: 10.1093/nar/gky1081

    Twilight zone of protein sequence alignments
    journal, February 1999


    Evolution of alternative splicing after gene duplication
    journal, December 2005


    The dynamic nature of bud dormancy in trees: environmental control and molecular mechanisms: Bud dormancy in trees
    journal, July 2012


    Geographical and environmental gradients shape phenotypic trait variation and genetic structure in Populus trichocarpa
    journal, November 2013

    • McKown, Athena D.; Guy, Robert D.; Klápště, Jaroslav
    • New Phytologist, Vol. 201, Issue 4
    • DOI: 10.1111/nph.12601

    The heat-shock protein/chaperone network and multiple stress resistance
    journal, February 2017

    • Jacob, Pierre; Hirt, Heribert; Bendahmane, Abdelhafid
    • Plant Biotechnology Journal, Vol. 15, Issue 4
    • DOI: 10.1111/pbi.12659

    The Genome of Black Cottonwood, Populus trichocarpa (Torr. & Gray)
    journal, September 2006


    The Amborella Genome and the Evolution of Flowering Plants
    journal, December 2013


    Regulation of H SF 1 Function in the Heat Stress Response: Implications in Aging and Disease
    journal, July 2011


    Populus : A Model System for Plant Biology
    journal, June 2007


    The Heat-Shock Response
    journal, June 1986


    A SNP associated with alternative splicing of RPT5b causes unequal redundancy between RPT5a and RPT5b among Arabidopsis thaliana natural variation
    journal, January 2010

    • Guyon-Debast, Anouchka; Lécureuil, Alain; Bonhomme, Sandrine
    • BMC Plant Biology, Vol. 10, Issue 1
    • DOI: 10.1186/1471-2229-10-158

    Helical ambivalency induced by point mutations
    journal, January 2013

    • Bhattacharjee, Nicholus; Biswas, Parbati
    • BMC Structural Biology, Vol. 13, Issue 1
    • DOI: 10.1186/1472-6807-13-9

    Identification and distribution of the NBS-LRR gene family in the Cassava genome
    journal, May 2015


    Functional diversification accompanies gene family expansion of MED2 homologs in Candida albicans
    journal, April 2018


    The Evolutionary Relationship between Alternative Splicing and Gene Duplication
    journal, February 2017


    Analysis of the role of Arabidopsis class I TCP genes AtTCP7, AtTCP8, AtTCP22, and AtTCP23 in leaf development
    journal, January 2013


    The Plant Heat Stress Transcription Factors (HSFs): Structure, Regulation, and Function in Response to Abiotic Stresses
    journal, February 2016


    Evolutionary Origin, Gradual Accumulation and Functional Divergence of Heat Shock Factor Gene Family with Plant Evolution
    journal, February 2018


    Poplars: Trees of the people, trees of the future
    journal, April 2001