Skip to main content
SpringerLink
Log in

Genome Duplication and Evolution of Heat Shock Transcription Factor (HSF) Gene Family in Four Model Angiosperms

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Whole-genome duplication events played important roles in the evolution of angiosperms. Many modern angiosperms genomes have experienced one or more rounds of paleopolyploidy. Given that an ancient large-scale duplication will result in an excess of relatively old duplicated genes with similar ages, we analyzed the timing of duplication pairs in four model angiosperms (Populus trichocarpa, Arabidopsis thaliana, Oryza sativa, and Vitis vinifera). By searching for intraspecies microsynteny, we identified 18 paralogous gene pairs of duplicated segments resulting from a whole-genome duplication in poplar, Arabidopsis, and rice. Notably no paralogous gene pairs existed in grapevine. However, by comparing interspecies microsynteny, we confirmed that the majority of HSF-containing segments in the Arabidopsis, rice, and grapevine genomes show extensive conservation with duplicated regions in poplar. Microarray and quantitative reverse transcriptase PCR analysis showed that most of the poplar HSF genes are differentially expressed upon exposure to various stresses. In conclusion, this study comprehensively analyzed the evolution and duplication relationship of HSF across four model angiosperms, which demonstrated the rates of gene gain in different species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Adams KL, Wendel JF (2005) Polyploidy and genome evolution in plants. Curr Opin Plant Biol 8:135–141. doi:10.1016/j.pbi.2005.01.001

    Article  CAS  PubMed  Google Scholar 

  • Barrett T, Edgar R (2006) Gene expression omnibus: microarray data storage, submission, retrieval, and analysis. Methods Enzymol 411:352–369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bateman A et al (2004) The Pfam protein families database. Nucleic acids Res 32:D138–D141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanc G, Wolfe KH (2004) Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16:1667–1678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blanc G, Hokamp K, Wolfe KH (2003) A recent polyploidy superimposed on older large-scale duplications in the Arabidopsis genome. Genome Res 13:137–144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bryfczynski SP, Pargas RP (2009) GraphPad: a graph creation tool for CS2/CS7. In: ACM SIGCSE Bulletin. vol 3. ACM, pp 389–389

  • Cannon SB et al (2003) Evolution and microsynteny of the apyrase gene family in three legume genomes. Mol Genet Genomics 270:347–361

    Article  CAS  PubMed  Google Scholar 

  • Chai G et al (2012) Comprehensive analysis of CCCH zinc finger family in poplar (Populus trichocarpa). BMC Genomics 13:253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Chen Z, Zhao H, Zhao Y, Cheng B, Xiang Y (2014) Genome-wide analysis of soybean HD-Zip gene family and expression profiling under salinity and drought treatments. PloS one. doi:10.1371/journal.pone.0087156

    Google Scholar 

  • Chen W-J et al (2015) Significant microsynteny with new evolutionary highlights is detected through comparative genomic sequence analysis of maize CCCH IX gene subfamily. Int J Genomics. doi:10.1155/2015/824287

    Google Scholar 

  • Clos J, Westwood JT, Becker PB, Wilson S, Lambert K, Wu C (1990) Molecular cloning and expression of a hexameric Drosophila heat shock factor subject to negative regulation. Cell 63:1085–1097

    Article  CAS  PubMed  Google Scholar 

  • Durrant-Whyte H, Bailey T (2006) Simultaneous localization and mapping: part I. IEEE Robot Autom Mag 13:99–110

    Article  Google Scholar 

  • Feng L, Chen Z, Ma H, Chen X, Li Y, Wang Y, Xiang Y (2014) The IQD gene family in soybean: structure, phylogeny, evolution and expression. PloS one 9(10):e110896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Finn RD et al (2013) Pfam: the protein families database. Nucleic Acids Res. doi:10.1093/nar/gkv1344

    Google Scholar 

  • Gasteiger E, Gattiker A, Hoogland C, Ivanyi I, Appel RD, Bairoch A (2003) ExPASy: the proteomics server for in-depth protein knowledge and analysis. Nucleic Acids Res 31:3784–3788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giorno F, Guerriero G, Baric S, Mariani C (2012) Heat shock transcriptional factors in Malus domestica: identification, classification and expression analysis. BMC Genom 13:639

    Article  CAS  Google Scholar 

  • Goodstein DM et al (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40:D1178–D1186

    Article  CAS  PubMed  Google Scholar 

  • Guidone A, Zotta T, Matera A, Ricciardi A, De Filippis F, Ercolini D, Parente E (2016) The microbiota of high-moisture mozzarella cheese produced with different acidification methods. Int J Food Microbiol 216:9–17

    Article  CAS  PubMed  Google Scholar 

  • Guo A, Zhu Q, Chen X, Luo J (2007) GSDS: a gene structure display server. Yi chuan = Hereditas/Zhongguo yi chuan xue hui bian ji 29:1023–1026

    Article  CAS  Google Scholar 

  • Guo J et al (2008) Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis. J Genet Genom 35:105–118

    Article  CAS  Google Scholar 

  • Guo L, Chen Y, Ye N, Dai X, Yang W, Yin T (2014) Differential retention and expansion of the ancestral genes associated with the paleopolyploidies in modern rosid plants, as revealed by analysis of the extensins super-gene family. BMC Genom 15:612

    Article  CAS  Google Scholar 

  • Guyot R, Keller B (2004) Ancestral genome duplication in rice. Genome 47:610–614

    Article  CAS  PubMed  Google Scholar 

  • Horiuchi H (2009) Functional diversity of chitin synthases of Aspergillus nidulans in hyphal growth, conidiophore development and septum formation. Med Mycol 47:S47–S52

    Article  CAS  PubMed  Google Scholar 

  • Hu R, Qi G, Kong Y, Kong D, Gao Q, Zhou G (2010) Comprehensive analysis of NAC domain transcription factor gene family in Populus trichocarpa. BMC Plant Biol 10:145

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y et al (2015) Heat shock factors in carrot: genome-wide identification, classification, and expression profiles response to abiotic stress. Mol Biol Rep 42:893–905

    Article  CAS  PubMed  Google Scholar 

  • Jaillon O et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–467

    Article  CAS  PubMed  Google Scholar 

  • Jian B, Liu B, Bi Y, Hou W, Wu C, Han T (2008) Validation of internal control for gene expression study in soybean by quantitative real-time PCR. BMC Mol Biol 9:59

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I et al (2004) SMART 4.0: towards genomic data integration. Nucleic Acids Res 32:D142–D144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:D302–D305

    Article  CAS  PubMed  Google Scholar 

  • Li Z et al (2014) Molecular evolution of the HD-ZIP I gene family in legume genomes. Gene 533:218–228

    Article  CAS  PubMed  Google Scholar 

  • Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452

    Article  CAS  PubMed  Google Scholar 

  • Lin Y-X, Jiang H-Y, Chu Z-X, Tang X-L, Zhu S-W, Cheng B-J (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genom 12:76

    Article  CAS  Google Scholar 

  • Lin Y, Cheng Y, Jin J, Jin X, Jiang H, Yan H, Cheng B (2014a) Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes. PloS one 9:e102825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin Y, Cheng Y, Jin J, Jin X, Jiang H, Yan H, Cheng B (2014b) Genome duplication and gene loss affect the evolution of heat shock transcription factor genes in legumes. PloS one 9(7):e102825

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Ma H, Feng L, Chen Z, Chen X, Zhao H, Xiang Y (2014) Genome-wide identification and expression analysis of the IQD gene family in Populus trichocarpa. Plant Sci 229:96–110

    Article  CAS  PubMed  Google Scholar 

  • Maher C, Stein L, Ware D (2006) Evolution of Arabidopsis microRNA families through duplication events. Genome Res 16:510–519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Messing J et al (2004) Sequence composition and genome organization of maize. Proc the Natl Acad Sci USA 101:14349–14354

    Article  CAS  Google Scholar 

  • Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489

    Article  CAS  PubMed  Google Scholar 

  • Mittal D, Chakrabarti S, Sarkar A, Singh A, Grover A (2009) Heat shock factor gene family in rice: genomic organization and transcript expression profiling in response to high temperature, low temperature and oxidative stresses. Plant Physiol Biochem 47:785–795

    Article  CAS  PubMed  Google Scholar 

  • Moore RC, Purugganan MD (2005) The evolutionary dynamics of plant duplicate genes. Curr Opin Plant Biol 8:122–128

    Article  CAS  PubMed  Google Scholar 

  • Nam J, Kim J, Lee S, An G, Ma H, Nei M (2004) Type I MADS-box genes have experienced faster birth-and-death evolution than type II MADS-box genes in angiosperms. Proc Natl Acad Sci USA 101:1910–1915

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishizawa A, Yabuta Y, Yoshida E, Maruta T, Yoshimura K, Shigeoka S (2006) Arabidopsis heat shock transcription factor A2 as a key regulator in response to several types of environmental stress. Plant J 48:535–547

    Article  CAS  PubMed  Google Scholar 

  • Ogawa D, Yamaguchi K, Nishiuchi T (2007) High-level overexpression of the Arabidopsis HsfA2 gene confers not only increased themotolerance but also salt/osmotic stress tolerance and enhanced callus growth. J Exp Bot 58:3373–3383

    Article  CAS  PubMed  Google Scholar 

  • Otto SP (2007) The evolutionary consequences of polyploidy Cell 131:452–462

    CAS  PubMed  Google Scholar 

  • Paterson AH et al (2000) Comparative genomics of plant chromosomes. Plant Cell 12:1523–1539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng X, Wu Q, Teng L, Tang F, Pi Z, Shen S (2015) Transcriptional regulation of the paper mulberry under cold stress as revealed by a comprehensive analysis of transcription factors. BMC Plant Biol 15:108

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci 103:18822–18827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato S et al (2008) Genome structure of the legume, Lotus japonicus. DNA Res 15:227–239

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Scharf K-D, Berberich T, Ebersberger I, Nover L (2012) The plant heat stress transcription factor (Hsf) family: structure, function and evolution. Biochim et Biophys Acta (BBA) 1819:104–119

    Article  CAS  Google Scholar 

  • Schlueter JA, Scheffler BE, Jackson S, Shoemaker RC (2008) Fractionation of synteny in a genomic region containing tandemly duplicated genes across Glycine max, Medicago truncatula, and Arabidopsis thaliana. J Hered 99:390–395

    Article  CAS  PubMed  Google Scholar 

  • Schramm F, Ganguli A, Kiehlmann E, Englich G, Walch D, von Koskull-Döring P (2006) The heat stress transcription factor HsfA2 serves as a regulatory amplifier of a subset of genes in the heat stress response in Arabidopsis. Plant Mol Biol 60:759–772

    Article  CAS  PubMed  Google Scholar 

  • Song X et al (2014) Genome-wide identification, classification and expression analysis of the heat shock transcription factor family in Chinese cabbage. Mol Genet Genom 289:541–551

    Article  CAS  Google Scholar 

  • Sorger PK, Pelham HR (1988) Yeast heat shock factor is an essential DNA-binding protein that exhibits temperature-dependent phosphorylation. Cell 54:855–864

    Article  CAS  PubMed  Google Scholar 

  • Sturn A, Quackenbush J, Trajanoski Z (2002) Genesis: cluster analysis of microarray data. Bioinformatics 18:207–208

    Article  CAS  PubMed  Google Scholar 

  • Swindell WR, Huebner M, Weber AP (2007) Transcriptional profiling of Arabidopsis heat shock proteins and transcription factors reveals extensive overlap between heat and non-heat stress response pathways. BMC Genom 8:125

    Article  CAS  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang H, Bowers JE, Wang X, Ming R, Alam M, Paterson AH (2008) Synteny and collinearity in plant genomes. Science 320:486–488

    Article  CAS  PubMed  Google Scholar 

  • Tuskan GA et al (2006) The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Science 313:1596–1604

    Article  CAS  PubMed  Google Scholar 

  • Wang L et al (2010) Expression profiling and integrative analysis of the CESA/CSL superfamily in rice. BMC Plant Biol 10:282

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Dong Q, Jiang H, Zhu S, Chen B, Xiang Y (2012) Genome-wide analysis of the heat shock transcription factors in Populus trichocarpa and Medicago truncatula. Mol Biol Rep 39:1877–1886

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Feng L, Zhu Y, Li Y, Yan H, Xiang Y (2015a) Comparative genomic analysis of the WRKY III gene family in populus, grape, arabidopsis and rice. Biol Direct 10:1–27

    Article  CAS  Google Scholar 

  • Wang Y, Wang Q, Zhao Y, Han G, Zhu S (2015b) Systematic analysis of maize class III peroxidase gene family reveals a conserved subfamily involved in abiotic stress response. Gene 566:95–108

    Article  CAS  PubMed  Google Scholar 

  • Wilkins O, Nahal H, Foong J, Provart NJ, Campbell MM (2009) Expansion and diversification of the Populus R2R3-MYB family of transcription factors. Plant Physiol 149:981–993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Li J, Yu J (2006) Computing Ka and Ks with a consideration of unequal transitional substitutions. BMC Evol Biol 6:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang H, Yang J, Chen Y, Mao X, Wang Z, Li C (2013a) Identification and expression analysis of the heat shock transcription factor (HSF) gene family in Populus trichocarpa. Plant Omics 6:415

    CAS  Google Scholar 

  • Zhang J, Li J, Liu B, Zhang L, Chen J, Lu M (2013b) Genome-wide analysis of the Populus Hsp90 gene family reveals differential expression patterns, localization, and heat stress responses. BMC Genom 14:532

    Article  CAS  Google Scholar 

  • Zhang J et al (2015) Hsf and Hsp gene families in Populus: genome-wide identification, organization and correlated expression during development and in stress responses. BMC Genom 16:1–19

    Article  CAS  Google Scholar 

  • Zhou Q, Wang S, Anderson DJ (2000) Identification of a novel family of oligodendrocyte lineage-specific basic helix–loop–helix transcription factors. Neuron 25:331–343

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Grants from the National Natural Science Foundation of China (No. 31370561), Specialized research Fund for the Doctoral Program of Higher Education (No. 20133418110005), Anhui Provincial Natural Science Foundation (No. 1308085MC36), and Anhui Agricultural University disciplinary construction Foundation (No. XKTS2013001).

Author Contributions

Conceived and designed the experiments: YXZ YYW LF. Performed the experiments: YXZ. Analyzed the data: YXZ HWY YYW LF ZC. Wrote the paper: YXZ HWY YYW. Participated in the design of this study and revised manuscript: YXZ HWY YYW.

Author information

Author notes

    Authors and Affiliations

    1. Laboratory of Modern Biotechnology, School of Forestry and Landscape Architecture, Anhui Agricultural University, Hefei, 230036, China

      Yuxin Zhu, Hanwei Yan, Yiyi Wang, Lin Feng, Zhu Chen & Yan Xiang

    2. Key Laboratory of Crop Biology of Anhui Agriculture University, Hefei, 230036, China

      Yan Xiang

    Authors
    1. Yuxin Zhu
      View author publications

      You can also search for this author in PubMed Google Scholar

    2. Hanwei Yan
      View author publications

      You can also search for this author in PubMed Google Scholar

    3. Yiyi Wang
      View author publications

      You can also search for this author in PubMed Google Scholar

    4. Lin Feng
      View author publications

      You can also search for this author in PubMed Google Scholar

    5. Zhu Chen
      View author publications

      You can also search for this author in PubMed Google Scholar

    6. Yan Xiang
      View author publications

      You can also search for this author in PubMed Google Scholar

    Corresponding author

    Correspondence to Yan Xiang.

    Ethics declarations

    Conflict of Interest

    The authors declare that they have no conflict of interest.

    Additional information

    The authors Yuxin Zhu and Hanwei Yan have contributed equally to this work.

    Electronic supplementary material

    Rights and permissions

    Reprints and permissions

    About this article

    Check for updates. Verify currency and authenticity via CrossMark

    Cite this article

    Zhu, Y., Yan, H., Wang, Y. et al. Genome Duplication and Evolution of Heat Shock Transcription Factor (HSF) Gene Family in Four Model Angiosperms. J Plant Growth Regul 35, 903–920 (2016). https://doi.org/10.1007/s00344-016-9590-5

    Download citation

    • Received:

    • Accepted:

    • Published:

    • Issue Date:

    • DOI: https://doi.org/10.1007/s00344-016-9590-5

    Keywords

    Search

    Navigation