Skip to main content
SpringerLink
Log in

A comparative genomic analysis of the small heat shock proteins in Caenorhabditis elegans and briggsae

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The small heat shock proteins (sHSPs) are a ubiquitous family of molecular chaperones. We have identified 18 sHSPs in the Caenorhabditis elegans genome and 20 sHSPs in the Caenorhabditis briggsae genome. Analysis of phylogenetic relationships and evolutionary dynamics of the sHSPs in these two genomes reveals a very complex pattern of evolution. The sHSPs in C. elegans and C. briggsae do not display clear orthologous relationships with other invertebrate sHSPs. But many sHSPs in C. elegans have orthologs in C. briggsae. One group of sHSPs, the HSP16s, has a very unusual evolutionary history. Although there are a number of HSP16s in both the C. elegans and C. briggsae genomes, none of the HSP16s display orthologous relationships across these two species. The HSP16s have an unusual gene pair structure and a complex evolutionary history shaped by gene duplication, gene conversion, and purifying selection. We found no evidence of recent positive selection acting on any of the sHSPs in C. elegans or in C. briggsae. There is also no evidence of functional divergence within the pairs of orthologous C. elegans and C. briggsae sHSPs. However, the evolutionary patterns do suggest that functional divergence has occurred between the sHSPs in C. elegans and C. briggsae and the sHSPs in more distantly related invertebrates.

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

Similar content being viewed by others

Abbreviations

HSP:

Heat shock protein

sHSP:

Small heat shock proteins

bp:

Base pair

kDa:

Kilodaltons

HSEs:

Heat shock response elements

ESRE:

Ethanol stress response element

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Boorstein WR, Ziegelhoffer T, Craig EA (1994) Molecular evolution of the HSP70 multigene family. J Mol Evo 38:1–17

    CAS  Google Scholar 

  • Caspers GJ, Leunissen JA, de Jong WW (1995) The expanding small heat-shock protein family, and structure predictions of the conserved “alpha-crystallin domain”. J Mol Evol 40:238–248

    Article  PubMed  CAS  Google Scholar 

  • de Jong WW, Caspers GJ, Leunissen JA (1998) Genealogy of the alpha-crystallin-small heat-shock protein superfamily. Int J Biol Macromol 22:151–162

    Article  PubMed  Google Scholar 

  • Drouin G (2002) Characterization of the gene conversion between the multigene family members of the yeast genome. J Mol Evol 55:14–23

    Google Scholar 

  • Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531–1545

    Google Scholar 

  • Franck E, Madsen O, van Rheede T, Ricard G, Huynen MA, de Jong WW (2004) Evolutionary diversity of vertebrate small heat shock proteins. J Mol Evol 59:792–805

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Jiao W, Chang Z (2006) Phylogenetic and biochemical studies reveal a potential evolutionary origin of small heat shock proteins of animals from bacterial class A. J Mol Evol 62:257–266

    Article  PubMed  CAS  Google Scholar 

  • Hall T (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows. Nucleic Acids Symp Ser 41:95–98

    CAS  Google Scholar 

  • Haslbeck M, Franzmann T, Weinfurtner D, Buchner J (2005) Some like it hot: the structure and function of small heat-shock proteins. Nat Struct Mol Biol 12:842–846

    Article  PubMed  CAS  Google Scholar 

  • Higgins DG, Thompson JD, Gibson TJ (1996) Using CLUSTAL for multiple sequence alignments. Methods Enzymol 226:383–402

    Google Scholar 

  • Hong M, Kwon JY, Shim J, Lee J (2004) Differential hypoxia response of hsp-16 genes in the nematode. J Mol Biol 344:369–381

    Article  PubMed  CAS  Google Scholar 

  • Jones D, Russnak RH, Kay RJ, Candido EP (1986) Structure, expression, and evolution of a heat shock gene locus in Caenorhabditis elegans that is flanked by repetitive elements. J Biol Chem 261:12006–12015

    PubMed  CAS  Google Scholar 

  • Jones SJ, Riddle DL, Pouzyrev AT, Velculescu VE, Hillier L, Eddy SR, Stricklin SL, Baillie DL, Waterston R, Marra MA (2001) Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Res 11:1346–1352

    Article  PubMed  CAS  Google Scholar 

  • Kim KK, Kim R, Kim SH (1998) Crystal structure of a small heat-shock protein. Nature 394:595–599

    Article  PubMed  CAS  Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lee GJ, Vierling E (2000) A small heat shock protein cooperates with heat shock protein 70 systems to reactivate a heat-denatured protein. Plant Physiol 122:189–198

    Article  PubMed  CAS  Google Scholar 

  • Leroux MR, Ma BJ, Batelier G, Melki R, Candido EP (1997a) Unique structural features of a novel class of small heat shock proteins. J Biol Chem 272:12847–12853

    Article  PubMed  CAS  Google Scholar 

  • Leroux MR, Melki R, Gordon B, Batelier G, Candido EP (1997b) Structure–function studies on small heat shock protein oligomeric assembly and interaction with unfolded polypeptides. J Biol Chem 272:24646–24656

    Article  PubMed  CAS  Google Scholar 

  • Lynch M, Force A (2000) The probability of duplicate gene preservation by subfunctionalization. Genetics 154:459–473

    PubMed  CAS  Google Scholar 

  • Lynch M, Katju V (2004) The altered evolutionary trajectories of gene duplicates. Trends Genet 20:544–549

    Article  PubMed  CAS  Google Scholar 

  • Mondragon-Palomino M, Gaut BS (2005) Gene conversion and the evolution of three leucine-rich repeat gene families in Arabidopsis thaliana. Mol Biol Evol 22:2444–2456

    Article  PubMed  CAS  Google Scholar 

  • Nakamoto H, Vigh L (2007) The small heat shock proteins and their clients. Cell Mol Life Sci 64:294–306

    Article  PubMed  CAS  Google Scholar 

  • Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39:121–152

    Article  PubMed  CAS  Google Scholar 

  • Nikolaidis N, Nei M (2004) Concerted and nonconcerted evolution of the Hsp70 gene superfamily in two sibling species of nematodes. Mol Biol Evol 21:498–505

    Article  PubMed  CAS  Google Scholar 

  • Ohno S (1970) Evolution by gene duplication. New York, Springer-Verlag

    Google Scholar 

  • Piatigorsky J, Wistow G (1991) The recruitment of crystallins: new functions precede gene duplication. Science 252:1078–1079

    Article  CAS  Google Scholar 

  • Piatigorsky J, Wistow GJ (1989) Enzyme/crystallins: gene sharing as an evolutionary strategy. Cell 57:197–199

    Article  PubMed  CAS  Google Scholar 

  • Plesofsky-Vig N, Vig J, Brambl R (1992) Phylogeny of the alpha-crystallin-related heat shock proteins. J Mol Evol 35:537–545

    Article  PubMed  CAS  Google Scholar 

  • Posada D, Buckley T (2004) Model selection and model averaging in phylogenetics: advantages of akaike information criterion and Bayesian approaches over likelihood ratio tests. Syst Biol 53:793–808

    Article  PubMed  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    Article  PubMed  CAS  Google Scholar 

  • Rost B, Yachdav G, Liu J (2004) The PredictProtein server. Nucleic Acids Res 32:W321–326

    Article  PubMed  CAS  Google Scholar 

  • Russnak RH, Candido EP (1985) Locus encoding a family of small heat shock genes in Caenorhabditis elegans: two genes duplicated to form a 3.8-kilobase inverted repeat. Mol Cell Biol 5:1268–1278

    PubMed  CAS  Google Scholar 

  • Sawyer SA (1999) GENECONV: a computer package for the statistical detection of gene conversion. Distributed by the author, Department of Mathematics, Washington University, St. Louis

  • Sheps JA, Ralph S, Zhao Z, Baillie D, Ling V (2004) The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol 5:R15

    Article  PubMed  Google Scholar 

  • Stein LD, Bao Z, Blasiar D, Blumenthal T, Brent MR, Chen N, Chinwalla A, Clarke L, Clee C, Coghlan A, Coulson A, D’Eustachio P, Fitch DH, Fulton LA, Fulton RE, Griffiths-Jones S, Harris TW, Hillier LW, Kamath R, Kuwabara PE, Mardis ER, Marra MA, Miner TL, Minx P, Mullikin JC, Plumb RW, Rogers J, Schein JE, Sohrmann M, Spieth J, Stajich JE, Wei C, Willey D, Wilson RK, Durbin R, Waterston RH (2003) The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biol 1:E45

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, MacRae TH (2005) Small heat shock proteins: molecular structure and chaperone function. Cell Mol Life Sci 62:2460–2476

    Article  PubMed  CAS  Google Scholar 

  • Thomas JH (2007) Rapid birth-death evolution specific to xenobiotic cytochrome P450 genes in vertebrates. PLoS Genet 3:e67

    Article  PubMed  CAS  Google Scholar 

  • Thomas JH, Kelley JL, Robertson HM, Ly K, Swanson WJ (2005) Adaptive evolution in the SRZ chemoreceptor families of Caenorhabditis elegans and Caenorhabditis briggsae. Proc Natl Acad Sci USA 102:4476–4481

    Article  PubMed  CAS  Google Scholar 

  • van Montfort RL, Basha E, Friedrich KL, Slingsby C, Vierling E (2001) Crystal structure and assembly of a eukaryotic small heat shock protein. Nat Struct Biol 8:1025–1030

    Article  PubMed  CAS  Google Scholar 

  • van Montfort RL, Slingsby C, Vierling E (2002) Structure and function of the small heat shock protein/alpha-crystallin family of molecular chaperones. Adv Protein Chem 59:105–156

    Article  Google Scholar 

  • Waters ER (1995) The molecular evolution of the small heat shock proteins in plants. Genetics 141:785–795

    PubMed  CAS  Google Scholar 

  • Waters ER, Vierling E (1999) Chloroplast small heat shock proteins: evidence for atypical evolution of an organelle-localized protein. Proc Natl Acad Sci USA 96:14394–14399

    Article  PubMed  CAS  Google Scholar 

  • Waters ER, Aevermann BD, Sanders-Reed Z (in press) Comparative analysis of the small heat shock proteins in three angiosperm genomes indentifies new subfamilies and reveals diverse evolutionary patterns. Cell Stress Chaperon

  • Yang Z (1997) PAML: a program package for phylogenic analysis by maximum likelihood. Comput Appl BioSci 13:555–556

    PubMed  CAS  Google Scholar 

  • Zhao Z, Thomas JH, Chen N, Sheps JA, Baillie DL (2007) Comparative genomics and adaptive selection of the ATP-binding-cassette gene family in Caenorhabditis species. Genetics 175:1407–1418

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This manuscript is based on B. D. Aevermann’s Master of Sciences thesis at San Diego State University. Aevermann’s M.S. thesis committee members Drs. R. Zeller and T. Larsen provided useful comments on earlier versions of this manuscript. The Waters lab, and in particular Jim Starrett, provided useful comments and assistance in evaluating the results. We also wish to thank one anonymous reviewer and Dr. R. Krebs for helpful comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

  1. Oregon Health Sciences University, MMI Core Facility, 3181 S.W. Sam Jackson Park Road, Portland, OR, 97239-3098, USA

    Brian D. Aevermann

  2. Department of Biology, San Diego State University, 5500 Campanile Drive, San Diego, CA, 92182, USA

    Elizabeth R. Waters

Authors
  1. Brian D. Aevermann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Elizabeth R. Waters
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elizabeth R. Waters.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Aevermann, B.D., Waters, E.R. A comparative genomic analysis of the small heat shock proteins in Caenorhabditis elegans and briggsae . Genetica 133, 307–319 (2008). https://doi.org/10.1007/s10709-007-9215-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-007-9215-9

Keywords

Search

Navigation