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.
Similar content being viewed by others
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
Apic G, Gough J, Teichmann SA (2001) Domain combination in archeal, eubacterial, and eukaryotic proteomes. J Mol Biol 310:311–325
Björklund AK, Ekman D, Elofsson A (2006) Expansion of protein domain repeats. PLoS Comput Biol 2:114
Butlin R (2002) The costs and benefits of sex: new insights from old asexual lineages. Nat Rev Genet 3:311–317
Castagnone-Sereno P (2006) Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96:282–289
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
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
Demuth JP, Hahn MW (2009) The life and death of gene families. BioEssays 31:29–39
Depledge DP, Lower RPJ, Smith DF (2007) RepSeq—a database of amino acid repeats present in lower eukaryotic pathogens. BMC Bioinformatics 8:122
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797
Ellis J, Dodds P, Pryor T (2000) Structure, function and evolution of plant disease resistance genes. Curr Opin Plant Biol 3:278–284
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
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
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
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
Hahn MW, Demuth JP, Han SG (2007) Accelerated rate of gene gain and loss in primates. Genetics 177:1941–1949
Hayashi CY, Lewis RV (2000) Molecular architecture and evolution of a modular spider silk protein gene. Science 287:1477–1479
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
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
Laterrot H (1975) Séries de lignées isogéniques de tomate ne différant que par certains gènes de résistance aux maladies. Phytopathol Med 14:129–130
Lushai G, Loxdale HD, Allen JA (2003) The dynamic clonal genome and its adaptative potential. Biol J Linn Soc 79:193–208
Marcotte EM, Pellegrini M, Yeates TO, Eisenberg D (1999) A census of protein repeats. J Mol Biol 293:151–160
McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379
Parfrey LW, Lahr DJG, Katz LA (2008) The dynamic nature of eukaryotic genomes. Mol Biol Evol 25:787–794
Pevzner PA, Tang H, Tesler G (2004) De novo repeat classification and fragment assembly. Genome Res 14:1786–1796
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
Rasteiro R, Pereira-Leal JB (2007) Multiple domain insertions and losses in the evolution of the Rab prenylation complex. BMC Evol Biol 7:140
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
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
Swofford DL (1998) PAUP*: (phylogenetic analysis using parsimony*) and other methods Version 4. Sinauer Associates, Sunderland
Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77
Victoir K, Dujardin JC (2002) How to succeed in parasitic life without sex? Asking Leishmania. Trends Parasitol 18:81–85
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by S. Hohmann.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-009-0487-x