Skip to main content
Log in

Development of molecular markers based on retrotransposons for the analysis of genetic variability in Moniliophthora perniciosa

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Moniliophthora perniciosa is a fungus that causes witches’ broom disease (WBD) in the cacao tree (Theobroma cacao). The M. perniciosa genome contains different transposable elements; this prompted an evaluation of the use of its retrotransposons as molecular markers for population studies. The inter-retrotransposon amplified polymorphism (IRAP) and retrotransposon-microsatellite amplified polymorphism (REMAP) techniques were used to study the variability of 70 M. perniciosa isolates from different geographic origins and biotypes. A total of 43 loci was amplified. Cluster analysis of different geographical regions of C biotype revealed two large groups in the state of Bahia, Brazil. Techniques using retrotransposon-based molecular markers showed advantages over previously used molecular techniques for the study of genetic variability in M. perniciosa.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Agapow, P.-M., & Burt, A. (2001). Indices of multilocus linkage disequilibrium. Molecular Ecology Notes, 1, 101–102.

    Article  CAS  Google Scholar 

  • Aime, M. C., & Phillips-Mora, W. (2005). The causal agents of witches’ broom and frosty pod rot of cacao (chocolate, Theobroma cacao) form a new lineage of Marasmiaceae. Mycology, 97, 1012–1022.

    Article  CAS  Google Scholar 

  • Andebrhan, T., Figueira, A., Yamada, M. M., Cascardo, J., & Furtek, D. B. (1999). Molecular fingerprinting suggests two primary outbreaks of Witches’ broom disease (Crinipellis perniciosa) of Theobroma cacao in Bahia, Brazil. European Journal of Plant Pathology, 105, 167–175.

    Article  CAS  Google Scholar 

  • Anderbrhan, T., & Furtek, D. B. (1994). Random amplified polymorphism DNA (RAPD) analysis of Crinipellis perniciosa isolates from different hosts. Plant Pathology, 43, 1020–1027.

    Article  Google Scholar 

  • Bastos, C. N., & Anderbrahn, T. (1986). Urucum (Bixa orellana): nova espécie da Vassoura-de-Bruxa (Crinipellis perniciosa) do cacaueiro. Fitopatologia Brasileira, 13, 963–965.

    Google Scholar 

  • Bouvet, G. F., Jacobi, V., Plourde, K. V., & Bernier, L. (2008). Stress-induced mobility of OPHO1 and OPHO2, DNA transposons of the Dutch elm disease fungi. Fungal Genetics and Biology, 45, 565–578.

    Article  PubMed  CAS  Google Scholar 

  • Chadha, S., & Gopalakrishna, T. (2005). Retrotransposon-microsatellite amplified polymorphism (REMAP) markers for genetic diversity assessment of the rice blast pathogen (Magnaporthe grisea). Genome, 48, 943–945.

    Article  PubMed  CAS  Google Scholar 

  • Chang, R.-Y., O’donoughue, L. S., & Bureau, T. E. (2001). Inter-MITE polymorphisms (IMP): a high throughput transposon-based genome mapping and fingerprinting approach. Theoretical and Applied Genetics, 102, 773–781.

    Article  CAS  Google Scholar 

  • Crouch, J. A., Glasheen, B. M., Giunta, M. A., Clarke, B. B., & Hillman, B. I. (2008). The evolution of transposon repeat-induced point mutation in the genome of Colletotrichum cereale: reconciling sex, recombination and homoplasy in an “asexual” pathogen. Fungal Genetics and Biology, 45, 190–206.

    Article  PubMed  CAS  Google Scholar 

  • Daboussi, M. J., & Capy, P. (2003). Transposable elements in filamentous fungi. Annual Review of Microbiology, 57, 275–299.

    Article  PubMed  CAS  Google Scholar 

  • De Arruda, M. C. C., Miller, R. N. G., Ferreira, M. A. S. V., & Felipe, M. S. S. (2003). Comparison of Crinipellis perniciosa isolates from Brazil by ERIC repetitive element sequence-based PCR genome fingerprinting. Plant Pathology, 52, 236–244.

    Article  Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2006). Arlequin ver 3.01. An integrated software package for population genetics data analysis. Computational and molecular population genetics Lab (CMPG). Institute of Zoology. University of Berne.

  • Flavell, A. J., Knox, M. R., Pearce, S. R., & Ellis, T. H. N. (1998). Retrotransposon-based insertion polymorphism (RBIP) for high throughput marker analysis. The Plant Journal, 16, 643–650.

    Article  PubMed  CAS  Google Scholar 

  • Gramacho, K. P., Risterucci, A. M., Lanaud, C., Lima, L. S., & Lopes, U. V. (2007). Characterization of microsatellites in the fungal plant pathogen Crinipellis perniciosa. Molecular Ecology Notes, 7, 153–155.

    Article  CAS  Google Scholar 

  • Griffith, G. W., & Hedger, J. N. (1994a). The breeding biology of biotypes of the witches’ broom pathogen of cocoa, Crinipellis perniciosa. Heredity, 71, 278–289.

    Article  Google Scholar 

  • Griffith, G. W., & Hedger, J. N. (1994b). Spatial distribution of mycelia of the liana (L-) biotype of the agaric Crinipellis perniciosa (Stahel) Singer in tropical forest. New Phytolologist, 127, 243–259.

    Article  Google Scholar 

  • Griffith, G. M., Nicholson, J. N., Nenninger, A., Birch, R. N., & Hedger, J. N. (2003). Witches’ brooms and frosty pods: Two major pathogens of cacao. New Zealand Journal of Botany, 41, 423–435.

    Article  Google Scholar 

  • Grzebeleus, D. (2006). Transposon insertion polymorphism as a new source of molecular markers. Journal of Fruit and Ornamental Plant Research, 14, 21–29.

    Google Scholar 

  • Hansen, C. N., & Heslop-Harrison, J. S. (2004). Sequences and phylogenies of plant pararetroviruses, viruses and transposable elements. Advances in Botanical Research, 41, 165–193.

    Article  CAS  Google Scholar 

  • Hill, M. O. (1973). Diversity and evenness: A unifying notation and its consequences. Ecology, 54, 427–432.

    Article  Google Scholar 

  • Huan-Van, A., Ruzic, L., Maisonhaute, C., & Capy, P. (2005). Abundance, distribution and dynamics of retrotransposable elements and transposons: similarities and differences. Cytogenetic and Genome Research, 110, 426–440.

    Article  Google Scholar 

  • Ikeda, K., Nakayashiki, H., Takagi, M., Tosa, Y., & Mayama, S. (2001). Heat shock, cooper sulfate and oxidative stress active the retrotransposon MAGGY resident in the plant pathogenic fungus Magnaporthe grisea. Molecular Genetics and Genomics, 266, 318–325.

    Article  PubMed  CAS  Google Scholar 

  • Kalendar, R., & Schulman, A. H. (2006). IRAP and REMAP for retrotransposon-based genotyping and fingerprint. Nature Protocols, 1, 24782484.

    Article  Google Scholar 

  • Kalendar, R., Grob, T., Regina, M., Suoniemi, A., & Schulman, A. H. (1999). IRAP and REMAP: Two new retrotransposon-based DNA fingerprinting techniques. Theoretical and Applied Genetics, 98, 704–711.

    Article  CAS  Google Scholar 

  • Kalendar, R., Flavell, A. J., Ellis, T. H. N., Stakste, T., Moisy, C., & Schulman, A. H. (2011). Analysis of plant diversity with retrotransposon-based molecular markers. Heredity, 106, 520–530.

    Article  PubMed  CAS  Google Scholar 

  • Kumar, P., Gupta, V. K., Misra, A. K., Modi, D. R., & Pandey, B. K. (2009). Potential of molecular markers in plant biotechnology. Plant Omics Journal, 2, 141–162.

    CAS  Google Scholar 

  • Maynard-Smith, L., Smith, N. H., O’rourke, M., & Spratt, B. G. (1993). How clonal are bacteria? Proceedings of the National Academy of Sciences, 90, 4384–4388.

    Article  Google Scholar 

  • Mondego, J. M. C., Carazzolle, M. F., Costa, G. G. L., Formighieri, E. F., Parizzi, L. P., Rincones, J., et al. (2008). A genome survey of Moniliophthora perniciosa gives new insights into witches’ broom disease of cacao. BMC Genomics, 9, 548.

    Article  PubMed  Google Scholar 

  • Murata, H., Babasaki, K., Saegusa, T., Takemoto, K., Yamada, A., & Ohta, A. (2008). Traceability of Asian Matsutake, specialty mushrooms produced by the ectomycorrhizal basideomycetes Tricholoma matsutake, on the basis of retroelement-based DNA markers. Applied and Environmental Microbiology, 74, 2023–2031.

    Article  PubMed  CAS  Google Scholar 

  • Nei, M. (1973). Analysis of gene diversity in subdivided populations. Proceedings of the National Academy of Sciences USA, 70, 3321–3323.

    Article  CAS  Google Scholar 

  • Neto, A. D., Corrêa, R. X., Monteiro, W. R., Luz, E. D. M. N., Gramacho, K. P., & Lopes, U. V. (2005). Characterization of a cocoa population for mapping of genes of resistance to Witches’ Broom and Phytophthora pod rot. Fitopatolologia Brasileira, 30, 380–386.

    Article  Google Scholar 

  • Novikova, O. S., Fet, V., & Blinov, A. G. (2007). Homology-dependent inactivation of LTR retrotransposons in Aspergillus fumigatus and A. nidulans genome. Molecular Biology, 41, 886–893.

    Article  CAS  Google Scholar 

  • Oliveira, M. L., & Luz, E. D. M. N. (2005). Identificação e manejo das principais doenças do cacaueiro no Brasil. Ilhéus: CEPLAC/CEPEC/SEFIT. 132p.

    Google Scholar 

  • Pasquali, M., Dematheis, F., Gullino, M. L., & Garibaldi, A. (2007). Identification of race 1 of Fusarium oxysporum f. sp. lactucae on lettuce by inter-retrotransposon sequence-characterized amplified region technique. Phytopathology, 97, 987–996.

    Article  PubMed  CAS  Google Scholar 

  • Pereira, J. F. (2005). Caracterização, distribuição e estudo da atividade de elementos transponíveis em Crinipellis perniciosa, agente causal da vassoura-de-bruxa no cacaueiro (Theobroma cacao). Dissertation, Universidade Federal de Viçosa, Brazil

  • Pereira, J. L., Ram, A., Figueiredo, J. M., & Almeida, L. C. C. (1989). Primeira ocorrência de vassoura-de-bruxa na principal região produtora de cacau do Brasil. Agrotópica, 1, 79–81.

    Google Scholar 

  • Pereira, J. F., Ignacchiti, M. D. C., Araújo, E. F., Brommonshenkel, S. H., Cascardo, J. C. M., Pereira, G. A. G., et al. (2007). PCR amplification and sequence analyses of reverse transcriptase-like genes in Crinipellis perniciosa isolates. Fitopatologia Brasileira, 32, 373–381.

    Article  Google Scholar 

  • Ploetz, R. C., Schnell, R. J., Ting, Z., Zheng, Q., Olano, C. T., Motamayor, J. C., et al. (2005). Analysis of molecular diversity in Crinipellis perniciosa with AFLP markers. European Journal of Plant Pathology, 111, 317–326.

    Article  CAS  Google Scholar 

  • R Development Core Team. (2007). R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Rincones, J., Meinhardt, L. W., Vidal, B. C., & Pereira, G. A. G. (2003). Electrophoretic karyotype analysis of Crinipellis perniciosa, the causal agent of witches’ broom disease of Theobroma cacao. Mycological Research, 107, 452–458.

    Article  PubMed  CAS  Google Scholar 

  • Rozen, S. & Skaletsky, H. J. (2000). Primer3 on the WWW for general users and for biologist programmers. In: Krawetz S, Misener S (eds) Bioinformatics methods and protocols: Methods in molecular biology, 132, 365–386.

  • Silva, J. R. Q., Figueira, A., Pereira, G. A. G., & Albuquerque, P. (2008). Development of novel microsatellites from Moniliophthora perniciosa, causal agent of the witches’ broom disease of Theobroma caçao. Molecular Ecology Resources, 8, 783–785.

    Article  PubMed  CAS  Google Scholar 

  • SUFRAMA—Superintendência da Zona Franca de Manaus, (2003). Potencialidades regionais – Estudo da viabilidade econômica – Cacau- p 34.

  • Waugh, R., Mclean, K., Flavell, A. J., Pearce, S. R., Kumar, A., Thomas, B. B., et al. (1997). Genetic distribution of BARE-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Molecular Genetics and Genomics, 253, 687–694.

    CAS  Google Scholar 

  • Yeh, F. C., Yang, R., & Boyle, T. (1999). POPGENE. Microsoft window-based freeware for population genetic analysis. Release 1.31. Edmonton: University of Alberta, Canada.

    Google Scholar 

Download references

Acknowledgments

We are grateful to Brazilian agencies CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico), and CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Marisa Vieira de Queiroz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Santana, M.F., de Araújo, E.F., de Souza, J.T. et al. Development of molecular markers based on retrotransposons for the analysis of genetic variability in Moniliophthora perniciosa . Eur J Plant Pathol 134, 497–507 (2012). https://doi.org/10.1007/s10658-012-0031-4

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-012-0031-4

Keywords

Navigation