Skip to main content
Log in

Evolutionary history and genetic diversity study of heat-shock protein 60 of Rhizophagus irregularis

  • Research Article
  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

Despite the ubiquitous occurrence of heat-shock protein 60 (Hsp60) and their role in maintenance of cell activity and integrity, this protein remains poorly characterized in many of the symbiotic soil mycorrhizal fungi such as Rhizophagus irregularis. Thus, in the current study, an attempt has been made to elucidate the evolutionary history, time of divergence followed by estimation of population genetic parameters of hsp60 using R. irregularis as a model organism. Sequence alignment reported here identified several close homologues for hsp60 (gene) and Hsp60 (protein) from diverse taxa, while the output from protein-based phylogenetic tree indicates that mitochondrial Hsp60 of R. irregularis shares close evolutionary relationship with classical \(\alpha \)-proteobacteria. This is perhaps the first line of evidence elucidating the likelihood of hsp60 from fungal taxa sharing a close evolutionary relationship with classical \(\alpha \)-proteobacteria as a common ancestor. Comprehensive analysis of mitochondrial hsp60 from selected fungal taxa from the evolutionary point of view explains the possibility of gene duplication and or horizontal gene transfer of this gene across various fungal species. Synteny relationships and population genetics credibly explain high genetic variability associated with fungal hsp60 presumably brought by random genetic recombination events. The results presented here also confirm a high level of genetic differentiation of hsp60 among all the three fungal populations analysed. In this context, the outcome of the current study, based on computational approach, stands as a testimony for explaining the possibility of increased genetic differentiation experienced by hsp60 of R. irregularis.

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

Access this article

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

Instant access to the full article PDF.

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

Similar content being viewed by others

References

  • Aguileta G., Refregier G., Yockteng R., Fournier E. and Giraud T. 2009 Rapidly evolving genes in pathogens: methods for detecting positive selection and examples among fungi, bacteria, viruses and protists. Infect. Genet. Evol. 9, 656–670.

    Article  CAS  PubMed  Google Scholar 

  • Alba-Fierro C. A., Pérez-Torres A., Toriello C., Pulido-Camarillo E., López-Romero E., Romo-Lozano Y. et al. 2016 Immune response induced by an immunodominant 60 kDa glycoprotein of the cell wall of Sporothrix schenckii in two mice strains with experimental sporotrichosis. J. Immunol. Res. 2016, article ID 6525831.

  • Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W. et al. 1997 Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389–3402.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Anderson J. B., Kohn L. M. and Leslie J. F. 1992 Genetic mechanisms in fungal adaptation. The fungal community: Its organization and role in the ecosystem, 2nd edition, pp. 73–98. Marcel Dekker, New York.

  • Beaudet D., de la Providencia I. E., Labridy M., Roy-Bolduc A., Daubois L. and Hijri M 2014 Intraisolate mitochondrial genetic polymorphism and gene variants coexpression in arbuscular mycorrhizal fungi. Genome Biol. Evol. 7, 218–227.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bernt M., Donath A., Jühling F., Externbrink F., Florentz C., Fritzsch G. et al. 2013 MITOS: improved de novo metazoan mitochondrial genome annotation. Mol. Phylogenet. Evol. 69, 313–319.

    Article  PubMed  Google Scholar 

  • Blaiotta G., Fusco V., Ercolini D., Aponte M., Pepe O. and Villani F. 2008 Lactobacillus strain diversity based on partial hsp60 gene sequences and design of PCR-restriction fragment length polymorphism assays for species identification and differentiation. Appl. Environ. Microbiol. 74, 208–215.

    Article  CAS  PubMed  Google Scholar 

  • Boisvert D. C., Wang J., Otwinowski Z., Norwich A. L. and Sigler P. B. 1996 The 2.4 Ã… crystal structure of the bacterial chaperonin GroEL complexed with ATP\(\gamma \)S. Nat. Struct. Mol. Biol. 3, 170.

  • Boon E., Zimmerman E., St-Arnaud M. and Hijri M. 2013 Allelic differences within and among sister spores of the arbuscular mycorrhizal fungus Glomus etunicatum suggest segregation at sporulation. PLoS One 8, 8330.

    Google Scholar 

  • Borchiellini C., Boury-Esnault N., Vacelet J. and Le Parco Y. 1998 Phylogenetic analysis of the Hsp70 sequences reveals the monophyly of Metazoa and specific phylogenetic relationships between animals and fungi. Mol. Biol. Evol. 15, 647–655.

    Article  CAS  PubMed  Google Scholar 

  • Borneman A. R., Forgan A. H., Kolouchova R., Fraser J. A. and Schmidt S. A. 2016 Whole genome comparison reveals high levels of inbreeding and strain redundancy across the spectrum of commercial wine strains of Saccharomyces cerevisiae. G3: Genes, Genomes, Genetics (Bethesda) 6, 957–971.

    Article  CAS  PubMed Central  Google Scholar 

  • Börstler B., Raab P. A., Thiéry O., Morton J. and Redecker D. 2008 Genetic diversity of the arbuscular mycorrhizal fungus Glomus intraradices as determined by mitochondrial large subunit rRNA gene sequences is considerably higher than previously expected. New Phytol. 180, 452–465.

    Article  CAS  PubMed  Google Scholar 

  • Brennwald A. and Redecker D. 2005 Mitochondrial large ribosomal subunit sequences are homogeneous within isolates of Glomus (arbuscular mycorrhizal fungi, Glomeromycota). Mycol. Res. 109, 1315–1322.

    Article  CAS  PubMed  Google Scholar 

  • Brinig M. M., Cummings C. A., Sanden G. N., Stefanelli P., Lawrence A. and Relman D. A. 2006 Significant gene order and expression differences in Bordetella pertussis despite limited gene content variation. J. Bacteriol. 188, 2375–2382.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brocchieri L. and Karlin S. 2000 Conservation among HSP60 sequences in relation to structure, function, and evolution. Protein Sci. 9, 476–486.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bukau B. and Horwich A. L. 1998 The Hsp70 and Hsp60 chaperone machines. Cell 92, 351–366.

    Article  CAS  PubMed  Google Scholar 

  • Campbell A. M. 2000 Lateral gene transfer in prokaryotes. Theor. Popul. Biol. 57, 71–77.

    Article  CAS  PubMed  Google Scholar 

  • Cappello F., Conway de Macario E., Marasà L., Zummo G. and Macario A. J. 2008 Hsp60 expression, new locations, functions, and perspectives for cancer diagnosis and therapy. Cancer Biol. Ther. 7, 801–809.

    Article  CAS  PubMed  Google Scholar 

  • Chakraborty U., Chakraborty B., Dey P. and Chakraborty A. P. 2015 Role of microorganisms in alleviation of abiotic stresses for sustainable agriculture. Abiotic stresses in crop plants, pp. 232–253. CABI, Wallingford.

  • Cheng M. Y., Hartl F. U., Martin J., Pollock R. A., Kalousek F., Neuper W. et al. 1989 Mitochondrial heat-shock protein hsp60 is essential for assembly of proteins imported into yeast mitochondria. Nature 337, 620.

    Article  CAS  PubMed  Google Scholar 

  • Cohen S. B. and Dor R. 2018 Phenotypic divergence despite low genetic differentiation in house sparrow populations. Sci. Rep. 8, 394.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Croll D., Wille L., Gamper H. A., Mathimaran N., Lammers P. J., Corradi N. et al. 2008 Genetic diversity and host plant preferences revealed by simple sequence repeat and mitochondrial markers in a population of the arbuscular mycorrhizal fungus Glomus intraradices. New Phytol. 178, 672–687.

    Article  CAS  PubMed  Google Scholar 

  • De la Cruz F. and Davies J. 2000 Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol. 8, 128–133.

    Article  PubMed  Google Scholar 

  • Drummond A. J., Rambaut A., Shapiro B. and Pybus O. G. 2005 Bayesian coalescent inference of past population dynamics from molecular sequences. Mol. Biol. Evol. 22, 1185–1192.

    Article  CAS  PubMed  Google Scholar 

  • Drummond A. J., Suchard M. A., Xie D. and Rambaut A. 2012 Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 29, 1969–1973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Durbin R., Eddy S. R., Krogh A. and Mitchison G. 1998 Biological sequence analysis: Probabilistic models of proteins and nucleic acids. Cambridge University Press, Cambridge UK.

    Book  Google Scholar 

  • Duret L. and Arndt P. F. 2008 The impact of recombination on nucleotide substitutions in the human genome. PLoS Genet. 4, e1000071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ehinger M. O., Croll D., Koch A. M. and Sanders I. R. 2012 Significant genetic and phenotypic changes arising from clonal growth of a single spore of an arbuscular mycorrhizal fungus over multiple generations. New Phytol. 196, 853–861.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier L. and Lischer H. E. 2010 Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol. Ecol. Resour. 10, 564–567.

    Article  PubMed  Google Scholar 

  • Felsenstein J. 1981 Evolutionary trees from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17, 368–376.

    Article  CAS  PubMed  Google Scholar 

  • Fitzpatrick D. A., Logue M. E., Stajich J. E. and Butler G. 2006 A fungal phylogeny based on 42 complete genomes derived from supertree and combined gene analysis. BMC Evol. Biol. 6, 99.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Formey D., Molès M., Haouy A., Savelli B., Bouchez O., Bécard G. et al. 2012 Comparative analysis of mitochondrial genomes of Rhizophagus irregularis—syn. Glomus irregulare – reveals a polymorphism induced by variability generating elements. New Phytol. 196, 1217–1227.

    Article  CAS  PubMed  Google Scholar 

  • Fu Y. X. 1997 Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147, 915–925.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Gadkar V. and Rillig M. C. 2006 The arbuscular mycorrhizal fungal protein glomalin is a putative homolog of heat shock protein 60. FEMS Microbiol. Lett. 263, 93–101.

    Article  CAS  PubMed  Google Scholar 

  • Galagan J. E., Henn M. R., Ma L. J., Cuomo C. A. and Birren B. 2005 Genomics of the fungal kingdom: insights into eukaryotic biology. Genome Res. 15, 1620–1631.

    Article  CAS  PubMed  Google Scholar 

  • Galtier N., Nabholz B., Glémin S. and Hurst G. D. D. 2009 Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol. Ecol. 18, 4541–4550.

    Article  CAS  PubMed  Google Scholar 

  • Gupta R. S. 1995a Evolution of the chaperonin families (HSP60, HSP 10 and TCP-1) of proteins and the origin of eukaryotic cells. Mol. Microbiol. 15, 1–11.

    Article  CAS  PubMed  Google Scholar 

  • Gupta R. S. 1995b Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. Mol. Biol. Evol. 12, 1063–1073.

    CAS  PubMed  Google Scholar 

  • Gupta R. S. and Golding G. B. 1993 Evolution of HSP70 gene and its implications regarding relationships between archaebacteria, eubacteria, and eukaryotes. J. Mol. Evol. 37, 573–582.

    Article  CAS  PubMed  Google Scholar 

  • Gupta S. and Knowlton A. A. 2007 HSP60 trafficking in adult cardiac myocytes: role of the exosomal pathway. Am. J. Physiol.-Heart Circ. Physiol. 292, H3052–H3056.

    Article  CAS  PubMed  Google Scholar 

  • Hall T. A. 1999 Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41, 95–98.

    CAS  Google Scholar 

  • Hamrick J. L. and Godt M. W. 1990 Allozyme diversity in plant species. Plant population genetics, breeding, and genetic resources, pp. 43–63. CABI, USA.

  • Hartl D. L. and Clark A. G. 1997 Principles of population genetics, 4th edition, pp. 318–372. Sinauer Associates, Sunderland.

  • Hartl F. U. and Hayer-Hartl M. 2002 Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852–1858.

    Article  CAS  PubMed  Google Scholar 

  • Heckman D. S., Geiser D. M., Eidell B. R., Stauffer R. L., Kardos N. L. and Hedges S. B. 2001 Molecular evidence for the early colonization of land by fungi and plants. Science 293, 1129–113.3.

    Google Scholar 

  • Hedges S. B. and Kumar S. 2009 Discovering the timetree of life. The timetree of life, 3rd edition. Oxford, New York, pp. 3–18.

  • Heitman J. 2015 Evolution of sexual reproduction: a view from the fungal kingdom supports an evolutionary epoch with sex before sexes. Fungal. Biol. Rev. 29, 108–117.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ho S. Y. 2007 Calibrating molecular estimates of substitution rates and divergence times in birds. J. Avian Biol. 38, 409–414.

    Article  Google Scholar 

  • Holbrook E. D. and Rappleye C. A. 2008 Histoplasma capsulatum pathogenesis: making a lifestyle switch. Curr. Opin. Microbiol. 11, 318–324.

    Article  CAS  PubMed  Google Scholar 

  • Judson O. P. and Normark B. B. 1996 Ancient asexual scandals. Trends Ecol. Evol. 11, 41–46.

    Article  CAS  PubMed  Google Scholar 

  • Karlin S. and Brocchieri L. 2000 Heat shock protein 60 sequence comparisons: duplications, lateral transfer, and mitochondrial evolution. Proc. Natl. Acad. Sci. USA 97, 11348–11353.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaufman B. A., Kolesar J. E., Perlman P. S. and Butow R. A. 2003 A function for the mitochondrial chaperonin Hsp60 in the structure and transmission of mitochondrial DNA nucleoids in Saccharomyces cerevisiae. J. Cell Biol. 163, 457–461.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn G., Hijri M. and Sanders I. R. 2001 Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414, 745.

    Article  CAS  PubMed  Google Scholar 

  • Kumar S., Stecher G. and Tamura K. 2016 MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 33, 1870–1874.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamoth, F., Juvvadi, P. R., Soderblom, E. J., Moseley, M. A., Asfaw, Y. G. and Steinbach W. J. 2014 Identification of a key lysine residue in heat shock protein 90 required for azole and echinocandin resistance in Aspergillus fumigatus. Antimicrob. Agents Chemother. 58, 1889–1896.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lane N. and Martin W. 2010 The energetics of genome complexity. Nature 467, 929.

    Article  CAS  PubMed  Google Scholar 

  • Lang B. F., Gray M. W. and Burger G. 1999 Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33, 351–397.

    Article  CAS  PubMed  Google Scholar 

  • Latef A. A. H. A., Hashem A., Rasool S., Abd\_Allah E. F., Alqarawi A. A., Egamberdieva D. et al. 2016 Arbuscular mycorrhizal symbiosis and abiotic stress in plants: a review. J. Plant Biol. 59, 407–426.

  • Lee J. and Young J. P. W. 2009 The mitochondrial genome sequence of the arbuscular mycorrhizal fungus Glomus intraradices isolate 494 and implications for the phylogenetic placement of Glomus. New Phytol. 183, 200–211.

    Article  CAS  PubMed  Google Scholar 

  • Leonhardt S. A., Fearson K., Danese P. N. and Mason T. L. 1993 HSP78 encodes a yeast mitochondrial heat shock protein in the Clp family of ATP-dependent proteases. Mol. Cell. Biol. 13, 6304–6313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lindquist S. and Craig E. A. 1988 The heat-shock proteins. Annu. Rev. Genet. 22, 631–677.

    Article  CAS  PubMed  Google Scholar 

  • Liu W., Zhang Y., Jiang S., Deng Y., Christie P., Murray P. J. et al. 2016 Arbuscular mycorrhizal fungi in soil and roots respond differently to phosphorus inputs in an intensively managed calcareous agricultural soil. Sci. Rep. 6, 24902.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • López-García P. and Moreira D. 1999 Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88–93.

    Article  PubMed  Google Scholar 

  • Lorch M., Mason J. M., Sessions R. B. and Clarke A. R. 2000 Effects of mutations on the thermodynamics of a protein folding reaction: implications for the mechanism of formation of the intermediate and transition states. Biochemistry 39, 3480–3485.

    Article  CAS  PubMed  Google Scholar 

  • Lucking R., Huhndorf S., Pfister D. H., Plata E. R. and Lumbsch H. T. 2009 Fungi evolved right on track. Mycologia 101, 810–822.

    Article  PubMed  Google Scholar 

  • Marleau J., Dalpé Y., St-Arnaud M. and Hijri M. 2011 Spore development and nuclear inheritance in arbuscular mycorrhizal fungi. BMC Evol. Biol. 11, 51.

    Article  PubMed  PubMed Central  Google Scholar 

  • McDonald B. A. 1997 The population genetics of fungi: tools and techniques. Phytopathology 87, 448–453.

    Article  CAS  PubMed  Google Scholar 

  • Meng Q., Li B. X. and Xiao X. 2018 Toward developing chemical modulators of Hsp60 as potential therapeutics. Front. Mol. Biosci. 5, 35.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muse S. V. and Gaut B. S. 1994 A likelihood approach for comparing synonymous and nonsynonymous nucleotide substitution rates, with application to the chloroplast genome. Mol. Biol. Evol. 11, 715–724.

    CAS  PubMed  Google Scholar 

  • Naylor D. J. and Hartl F. U 2001 Contribution of molecular chaperones to protein folding in the cytoplasm of prokaryotic and eukaryotic cells. Biochem. Soc. Symp. 68, 45–68.

    Article  CAS  Google Scholar 

  • Nei M. and Kumar S. 2000 Molecular evolution and phylogenetics. Oxford, New York.

  • Nybom H. and Bartish I. V. 2000 Effects of life history traits and sampling strategies on genetic diversity estimates obtained with RAPD markers in plants. Perspect. Plant. Ecol. Evol. Syst. 3, 93–114.

    Article  Google Scholar 

  • Ostermann J., Horwich A. L., Neupert W. and Hartl F. U. 1989 Protein folding in mitochondria requires complex formation with hsp60 and ATP hydrolysis. Nature 341, 125.

    Article  CAS  PubMed  Google Scholar 

  • Pond S. L. K. and Muse S. V. 2005 Hyphy: Hypothesis testing using phylogenies. Statistical methods in molecular evolution, pp. 125–181. Springer, New York.

  • Porcel R., Aroca R., Cano C., Bago A. and Ruiz-Lozano J. M. 2006 Identification of a gene from the arbuscular mycorrhizal fungus Glomus intraradices encoding for a 14-3-3 protein that is up-regulated by drought stress during the AM symbiosis. Microb. Ecol. 52, 575.

    Article  PubMed  Google Scholar 

  • Priya S., Sharma S. K. and Goloubinoff P. 2013 Molecular chaperones as enzymes that catalytically unfold misfolded polypeptides. FEBS Lett. 587, 1981–1987.

    Article  CAS  PubMed  Google Scholar 

  • Raggam R. B., Salzer H. J., Marth E., Heiling B. and Paulitsch A. H. and Buzina W. 2011 Molecular detection and characterisation of fungal heat shock protein 60. Mycoses 54, e394–e399.

    Article  PubMed  Google Scholar 

  • Rambaut A. and Drummond A. J. 2010 Treeannotator version 1.6. 1. University of Edinburgh, Edinburgh, UK.

  • Redecker D., Morton J. B. and Bruns T. D. 2000 Ancestral lineages of arbuscular mycorrhizal fungi (Glomales). Mol. Phylogenet. Evol. 14, 276–284.

    Article  CAS  PubMed  Google Scholar 

  • Richards T. A., Soanes D. M., Foster P. G., Leonard G., Thornton C. R. and Talbot N. J. 2009 Phylogenomic analysis demonstrates a pattern of rare and ancient horizontal gene transfer between plants and fungi. Plant Cell. 21, 1897–1911.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rozas J., Ferrer-Mata A., Sánchez-DelBarrio J. C., Guirao-Rico S., Librado P., Ramos-Onsins S. E. et al. 2017 DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299–3302.

    Article  CAS  PubMed  Google Scholar 

  • Schüßler A., Schwarzott D and Walker C. 2001 A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol. Res. 105, 1413–1421.

    Article  Google Scholar 

  • Sharma M., Fomda B. A., Mazta S., Sehgal R., Singh B. B. and Malla N. 2013 Genetic diversity and population genetic structure analysis of Echinococcus granulosus sensu stricto complex based on mitochondrial DNA signature. PLoS One 8, e82904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith S. E. and Read D. J. 2010 Mycorrhizal symbiosis. Academic Press, New York.

    Google Scholar 

  • Soltys B. J. and Gupta R. S. 1997 Cell surface localization of the 60 kDa heat shock chaperonin protein (hsp60) in mammalian cells. Cell Biol. Int. 21, 315–320.

    Article  CAS  PubMed  Google Scholar 

  • Somel M., Wilson Sayres M. A., Jordan G., Huerta-Sanchez E., Fumagalli M., Ferrer-Admetlla A. et al. 2013 A scan for human-specific relaxation of negative selection reveals unexpected polymorphism in proteasome genes. Mol. Biol. Evol. 30, 1808–1815.

  • Suzuki Y. and Gojobori T. 1999 A method for detecting positive selection at single amino acid sites. Mol. Biol. Evol. 16, 1315–1328.

    Article  CAS  PubMed  Google Scholar 

  • Tajima F. 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tajima F. 1993 Simple methods for testing the molecular evolutionary clock hypothesis. Genetics 135, 599–607.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tamura K. and Nei M. 1993 Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol. Biol. Evol. 10, 512–526.

    CAS  PubMed  Google Scholar 

  • Thompson J. D., Higgins D. G. and Gibson T. J. 1994 CLUSTAL w: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673–4680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tisserant E., Malbreil M., Kuo A., Kohler A., Symeonidi A., Balestrini R. et al. 2013 Genome of an arbuscular mycorrhizal fungus provides insight into the oldest plant symbiosis. Proc. Natl. Acad. Sci. USA 110, 20117–20122.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tiwari S., Thakur R. and Shankar J. 2015 Role of heat-shock proteins in cellular function and in the biology of fungi. Biotechnol. Res. Int. (https://doi.org/10.1155/2015/132635).

  • Trent J. D. 1996 A review of acquired thermotolerance, heat-shock proteins, and molecular chaperones in archaea. FEMS Microbiol. Rev. 18, 249–258.

    Article  CAS  Google Scholar 

  • Xiong J., Rayner S., Luo K., Li Y. and Chen S. 2006 Genome wide prediction of protein function via a generic knowledge discovery approach based on evidence integration. BMC Bioinf. 7, 268.

    Article  CAS  Google Scholar 

  • Xu Z., Horwich A. L. and Sigler P. B. 1997 The crystal structure of the asymmetric GroEL–GroES–(ADP) 7 chaperonin complex. Nature 388, 741.

    Article  CAS  PubMed  Google Scholar 

  • Yang Z. and Yoder A. D. 1999 Estimation of the transition/transversion rate bias and species sampling. J. Mol. Evol. 48, 274–283.

    Article  CAS  PubMed  Google Scholar 

  • Yang Z. and Nielsen R. 2000 Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32–43.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

We acknowledge Jain University for providing the facilities necessary to carry out our work and for providing the University PhD research scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K. V. Ramesh.

Additional information

Corresponding Editor: Manoj Prasad

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (docx 8656 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mothay, D., Ramesh, K.V. Evolutionary history and genetic diversity study of heat-shock protein 60 of Rhizophagus irregularis. J Genet 98, 48 (2019). https://doi.org/10.1007/s12041-019-1096-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s12041-019-1096-z

Keywords

Navigation