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Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita

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Abstract

In eukaryotes, repeat proteins (i.e. proteins that contain a tandem arrangement of repeated structural elements) are often considered as an extra source of variability, and gains and losses of repeats may be an important force driving the evolution and diversification of such proteins, that could allow fast adaptation to new environments. Here, we report genomic sequences of the MAP-1 protein family from of the asexual, plant-parasitic nematode Meloidogyne incognita. The encoded proteins exhibited highly conserved repeats of 13 and 58 aa, and variation in the number and arrangement of these repeats in the MAP-1 proteins was correlated with nematode (a)virulence, suggesting a possible role in the specificity of the plant–nematode interaction. Search in the complete genome sequence of M. incognita confirmed that a small gene family encoding proteins harboring conserved 58 and 13 aa-repeats is present in this nematode, and that the repetitive region of these proteins is modular. Both gene duplication and intragenic gain and loss of repeats have contributed to the complex evolutionary history of the map-1 gene family, and active selection pressure of the plant host probably induced recent additional gene loss, finally resulting in the present-day gene and repeat diversity observed among nematode lines. The genomic differences characterized here between avirulent and virulent individuals are assumed to reflect, at the DNA level, the adaptive capacity of these asexual root-knot nematodes.

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References

  • Abad P, Gouzy J, Aury JM, Castagnone-Sereno P, Danchin EGJ, Deleury E, Perfus-Barbeoch L, Anthouard V, Artiguenave F, Blok VC, Caillaud MC, Coutinho PM, Dasilva C, De Luca F, Deau F, Esquibet M, Flutre T, Goldstone JV, Hamamouch N, Hewezi T, Jaillon O, Jubin C, Leonetti P, Magliano M, Maier TR, Markov GV, McVeigh P, Pesole G, Poulain J, Robinson-Rechavi M, Sallet E, Ségurens B, Steinbach D, Tytgat T, Ugarte E, van Ghelder C, Veronico P, Baum TJ, Blaxter M, Bleve-Zacheo T, Davis EL, Ewbank JJ, Favery B, Grenier E, Henrissat B, Jones JT, Laudet V, Maule AG, Quesneville H, Rosso MN, Schiex T, Smant G, Weissenbach J, Wincker P (2008) Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nat Biotechnol 26:906–915

    Article  Google Scholar 

  • Apic G, Gough J, Teichmann SA (2001) Domain combination in archeal, eubacterial, and eukaryotic proteomes. J Mol Biol 310:311–325

    Article  CAS  PubMed  Google Scholar 

  • Björklund AK, Ekman D, Elofsson A (2006) Expansion of protein domain repeats. PLoS Comput Biol 2:114

    Article  Google Scholar 

  • Butlin R (2002) The costs and benefits of sex: new insights from old asexual lineages. Nat Rev Genet 3:311–317

    Article  CAS  PubMed  Google Scholar 

  • Castagnone-Sereno P (2006) Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96:282–289

    Article  CAS  PubMed  Google Scholar 

  • Castagnone-Sereno P, Wajnberg E, Bongiovanni M, Leroy F, Dalmasso A (1994) Genetic variation in Meloidogyne incognita virulence against the tomato Mi resistance gene: evidence from isofemale line selection studies. Theor Appl Genet 88:749–753

    Article  CAS  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Wajnberg E (2007) Selection and parasite evolution: a reproductive fitness cost associated with virulence in the parthenogenetic nematode Meloidogyne incognita. Evol Ecol 21:259–270

    Article  Google Scholar 

  • Demuth JP, Hahn MW (2009) The life and death of gene families. BioEssays 31:29–39

    Article  PubMed  Google Scholar 

  • Depledge DP, Lower RPJ, Smith DF (2007) RepSeq—a database of amino acid repeats present in lower eukaryotic pathogens. BMC Bioinformatics 8:122

    Article  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797

    Article  CAS  PubMed  Google Scholar 

  • Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284

    Article  CAS  PubMed  Google Scholar 

  • Fankhauser N, Nguyen-Ha TM, Adler J, Mäser P (2007) Surface antigens and potential virulence factors from parasites detected by comparative genomics of perfect amino acid repeats. Proteome Sci 5:20

    Article  PubMed  Google Scholar 

  • Fong JH, Geer LW, Panchenko AR, Bryant SH (2007) Modeling the evolution of protein domain architectures using maximum parsimony. J Mol Biol 366:307–315

    Article  CAS  PubMed  Google Scholar 

  • Garb JE, Hayashi CY (2005) Modular evolution of egg case silk genes across orb-weaving spider superfamilies. Proc Natl Acad Sci USA 102:11379–11384

    Article  CAS  PubMed  Google Scholar 

  • Gasteiger E, Hoogland C, Gattiker A, Duvaud S, Wilkins MR, Appel RD, Bairoch A (2005) Protein identification and analysis tools on the ExPASy server. In: Walker JM (ed) The proteomics protocols handbook. Humana Press, Totowa, pp 571–607

  • Gibbs HL, Rossiter W (2008) Rapid evolution by positive selection and gene gain and loss: PLA(2) venom genes in closely related Sistrurus rattlesnakes with divergent diets. J Mol Evol 66:151–166

    Article  CAS  PubMed  Google Scholar 

  • Hahn MW, Demuth JP, Han SG (2007) Accelerated rate of gene gain and loss in primates. Genetics 177:1941–1949

    Article  PubMed  Google Scholar 

  • Hayashi CY, Lewis RV (2000) Molecular architecture and evolution of a modular spider silk protein gene. Science 287:1477–1479

    Article  CAS  PubMed  Google Scholar 

  • Herbers K, Conrads-Strauch J, Bonas U (1992) Race-specificity of plant resistance to bacterial spot disease determined by repetitive motifs in a bacterial avirulence protein. Nature 356:172–174

    Article  CAS  Google Scholar 

  • Jarquin-Barberena H, Dalmasso A, De Guiran G, Cardin MC (1991) Acquired virulence in the plant parasitic nematode Meloidogyne incognita 1. Biol Anal Phenom Rev Nématol 14:299–303

    Google Scholar 

  • Laterrot H (1975) Séries de lignées isogéniques de tomate ne différant que par certains gènes de résistance aux maladies. Phytopathol Med 14:129–130

    Google Scholar 

  • Lushai G, Loxdale HD, Allen JA (2003) The dynamic clonal genome and its adaptative potential. Biol J Linn Soc 79:193–208

    Article  Google Scholar 

  • Marcotte EM, Pellegrini M, Yeates TO, Eisenberg D (1999) A census of protein repeats. J Mol Biol 293:151–160

    Article  CAS  PubMed  Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379

    Article  CAS  PubMed  Google Scholar 

  • Parfrey LW, Lahr DJG, Katz LA (2008) The dynamic nature of eukaryotic genomes. Mol Biol Evol 25:787–794

    Article  CAS  PubMed  Google Scholar 

  • Pevzner PA, Tang H, Tesler G (2004) De novo repeat classification and fragment assembly. Genome Res 14:1786–1796

    Article  CAS  PubMed  Google Scholar 

  • Powell AJ, Conant GC, Brown DE, Carbone I, Dean RA (2008) Altered patterns of gene duplication and differential gene gain and loss in fungal pathogens. BMC Genom 9:147

    Article  Google Scholar 

  • Rasteiro R, Pereira-Leal JB (2007) Multiple domain insertions and losses in the evolution of the Rab prenylation complex. BMC Evol Biol 7:140

    Article  PubMed  Google Scholar 

  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor

    Google Scholar 

  • Semblat JP, Rosso MN, Hussey RS, Abad P, Castagnone-Sereno P (2001) Molecular cloning of a cDNA encoding an amphid-secreted putative avirulence protein from the root-knot nematode Meloidogyne incognita. Mol Plant Microbe Interact 14:72–79

    Article  CAS  PubMed  Google Scholar 

  • Swofford DL (1998) PAUP*: (phylogenetic analysis using parsimony*) and other methods Version 4. Sinauer Associates, Sunderland

    Google Scholar 

  • Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77

    Article  CAS  PubMed  Google Scholar 

  • Victoir K, Dujardin JC (2002) How to succeed in parasitic life without sex? Asking Leishmania. Trends Parasitol 18:81–85

    Article  CAS  PubMed  Google Scholar 

  • Yang B, White FF (2004) Diverse members of the AvrBs3/PthA family of type III effectors are major virulence determinants in bacterial blight disease of rice. Mol Plant Microbe Interact 17:1192–1200

    Article  CAS  PubMed  Google Scholar 

  • Zhu W, Yang B, Chittoor JM, Johnson LB, White FF (1998) AvrXA10 contains an acidic transcriptional activation domain in the functionally conserved C terminus. Mol Plant Microbe Interact 11:824–832

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by the European Community (grant FAIR1-PL95-0896). We thank M. Bongiovanni for the maintenance of nematode cultures, E. Danchin for helpful discussion, and an anonymous reviewer for constructive comments on a previous version of the manuscript.

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Correspondence to Philippe Castagnone-Sereno.

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Communicated by S. Hohmann.

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Castagnone-Sereno, P., Semblat, JP. & Castagnone, C. Modular architecture and evolution of the map-1 gene family in the root-knot nematode Meloidogyne incognita . Mol Genet Genomics 282, 547–554 (2009). https://doi.org/10.1007/s00438-009-0487-x

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