Skip to main content

Advertisement

SpringerLink
Log in

Contrasting phylogenetic patterns of anther smuts (Pucciniomycotina: Microbotryum) reflect phylogenetic patterns of their caryophyllaceous hosts

  • Original Article
  • Published:
Organisms Diversity & Evolution Aims and scope Submit manuscript

Abstract

Anther smuts in the genus Microbotryum often show very high host specificity toward their caryophyllaceous hosts, but some of the larger host groups such as Dianthus are crucially undersampled for these parasites so that the question of host specificity cannot be answered conclusively. In this study we sequenced the internal transcribed spacer (ITS) region of members of the Microbotryum dianthorum species complex as well as their Dianthus hosts. We compared phylogenetic trees of these parasites including sequences of anther smuts from other Caryophyllaceae, mainly Silene, with phylogenies of Caryophyllaceae that are known to harbor anther smuts. Additionally we tested whether observed patterns in parasites are due to shared ancestry or if geographic separation is a factor that should be taken into consideration in delimitating species. Parasites on Dianthus showed mainly an arbitrary distribution on Dianthus hosts, whereas parasites on other Caryophyllaceae formed well-supported monophyletic clades that corresponded to restricted host groups. The same pattern was observed in the Caryophyllaceae studied: morphologically described Dianthus species did not correspond well with monophyletic clades based on molecular data, whereas other Caryophyllaceae mainly did. We suggest that these different patterns primarily result from different breeding systems and speciation times between different host groups as well as difficulties in species delimitations in the genus Dianthus.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Anderson, E., & Hubricht, L. (1938). Hybridization in Tradescantia. III. The evidence for introgressive hybridization. American Journal of Botany, 25(6), 396–402.

    Article  Google Scholar 

  • Barrett, L. G., Thrall, P. H., Burdon, J. J., & Linde, C. C. (2008). Life history determines genetic structure and evolutionary potential of host-parasite interactions. Trends in Ecology & Evolution, 23(12), 678–685.

    Article  Google Scholar 

  • Bernal, M., Laínz, M., & Muñoz Garmendia, F. (1990). Dianthus L. In S. Castroviejo, M. Laínz, G. López González, P. Montserrat, F. Muñoz Garmendia, J. Paiva, & L. Vilar (Eds.), Flora Iberica: Vol. II. Plantanaceae-Plumbaginaceae (partim) (pp. 426–464). Madrid, Spain: Real Jardín Botánico. CSIC.

    Google Scholar 

  • Carolin, R. C. (1957). Cytological and hybridization studies in the genus Dianthus. New Phytologist, 56(1), 81–97.

    Article  Google Scholar 

  • Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution, 17(4), 540–552.

    Article  PubMed  CAS  Google Scholar 

  • Crespi, A. L., Fernandes, C. P., Castro, A., Bernardos, S., & Amich, F. (2007). Morpho-environmental characterization of the genus Dianthus (Caryophyllaceae) in the Iberian Peninsula: D. pungens group. Annales Botanici Fennici, 44, 241–255.

    Google Scholar 

  • De Wet, J., Slippers, B., Preisig, O., Wingfield, B. D., & Wingfield, M. J. (2008). Phylogeny of the Botryosphaeriaceae reveals patterns of host association. Molecular Phylogenetics and Evolution, 46(1), 116–126.

    Article  PubMed  Google Scholar 

  • Denchev, C. M. (2007). Microbotryum lagerheimii sp nov (Microbotryaceae). Mycologia Balcanica, 4(1–2), 61–67.

    Google Scholar 

  • Denchev, C. M., Giraud, T., & Hood, M. E. (2009). Three new species of anthericolous smut fungi on Caryophyllaceae. Mycologia Balcanica, 6, 79–84.

    Google Scholar 

  • Duminil, J., Fineschi, S., Hampe, A., Jordano, P., Salvini, D., Vendramin, G. G., et al. (2007). Can population genetic structure be predicted from life-history traits? The American Naturalist, 169(5), 662–672.

    Article  PubMed  Google Scholar 

  • Ersts, P. J. Geographic distance matrix generator (version 1.2.3). American Museum of Natural History, Center for Biodiversity and Conservation. http://biodiversityinformatics.amnh.org/open_source/gdmg/.

  • Felsenstein, J. (1981). Evolutionary trees from DNA sequences: a maximum likelihood approach. Journal of Molecular Evolution, 17(6), 368–376.

    Article  PubMed  CAS  Google Scholar 

  • Fior, S., Karis, P. O., Casazza, G., Minuto, L., & Sala, F. (2006). Molecular phylogeny of the Caryophyllaceae (Caryophyllales) inferred from chloroplast matK and nuclear rDNA ITS sequences. American Journal of Botany, 93(3), 399–411.

    Article  PubMed  CAS  Google Scholar 

  • Fitch, W. M. (1971). Toward defining the course of evolution: minimum change for a specific tree topology. Systematic Zoolology, 20(4), 406–416.

    Article  Google Scholar 

  • Frajman, B., & Oxelman, B. (2007). Reticulate phylogenetics and phytogeographical structure of Heliosperma (Sileneae, Caryophyllaceae) inferred from chloroplast and nuclear DNA sequences. Molecular Phylogenetics and Evolution, 43, 140–155.

    Article  PubMed  CAS  Google Scholar 

  • Frajman, B., Heidari, N., & Oxelman, B. (2009). Phylogenetic relationships of Atocion and Viscaria (Sileneae, Caryophyllaceae) inferred from chloroplast, nuclear ribosomal, and low-copy gene DNA sequences. Taxon, 58, 811–824.

    Google Scholar 

  • Frajman, B., Eggens, F., & Oxelman, B. (2009). Hybrid origins and homoploid reticulate evolution within Heliosperma (Sileneae, Caryophyllaceae) - a multigene phylogenetic approach with relative dating. Systematic Biology, 58(3), 328–345.

    Article  PubMed  CAS  Google Scholar 

  • Gardes, M., & Bruns, T. D. (1993). ITS primers with enhanced specificity for basidiomycetes - application to the identification of mycorrhizae and rusts. Molecular Ecology, 2(2), 113–118.

    Article  PubMed  CAS  Google Scholar 

  • Gatesy, J., DeSalle, R., & Wheeler, W. (1993). Alignment-ambiguous nucleotide sites and the exclusion of systematic data. Molecular Phylogenetics and Evolution, 2(2), 152–157.

    Article  PubMed  CAS  Google Scholar 

  • Giraud, T., Gladieux, P., & Gavrilets, S. (2010). Linking the emergence of fungal plant diseases with ecological speciation. Trends in Ecology & Evolution, 25, 387–395.

    Article  Google Scholar 

  • Giribet, G., & Wheeler, W. C. (1999). On gaps. Molecular Phylogenetics and Evolution, 13(1), 132–143.

    Article  PubMed  CAS  Google Scholar 

  • Hall, R. (1974). Pathogenism and parasitism as concepts of symbiotic relationships. Phytopathology, 64, 576–577.

    Article  Google Scholar 

  • Hamrick, J. L., & Godt, M. J. W. (1996). Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 351(1345), 1291–1298.

    Article  Google Scholar 

  • Hawksworth, D. L. (2001). The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological Research, 105(12), 1422–1432.

    Article  Google Scholar 

  • Hillis, D. M. (1996). Inferring complex phylogenies. Nature, 383(6596), 130–131.

    Article  PubMed  CAS  Google Scholar 

  • Hillis, D. M. (1998). Taxonomic sampling, phylogenetic accuracy, and investigator bias. Systematic Biology, 47(1), 3–8.

    Article  PubMed  CAS  Google Scholar 

  • Janz, N., & Nylin, S. (2008). The oscillation hypothesis of host-plant range and speciation. In K. J. Tilmon (Ed.), Specialization, speciation, and radiation: The evolutionary biology of herbivorous insects (pp. 203–215). Berkeley, California: University of California Press.

    Google Scholar 

  • Karrenberg, S., & Favre, A. (2008). Genetic and ecological differentiation in the hybridizing campions Silene dioica and S. latifolia. Evolution, 62(4), 763–773.

    Article  PubMed  Google Scholar 

  • Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research, 30(14), 3059–3066.

    Article  PubMed  CAS  Google Scholar 

  • Katoh, K., Kuma, K., Toh, H., & Miyata, T. (2005). MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Research, 33(2), 511–518.

    Article  PubMed  CAS  Google Scholar 

  • Kemler, M., Göker, M., Oberwinkler, F., & Begerow, D. (2006). Implications of molecular characters for the phylogeny of the Microbotryaceae (Basidiomycota: Urediniomycetes). BMC Evolutionary Biology, 6(1), 35.

    Article  PubMed  Google Scholar 

  • Kemler, M., Lutz, M., Göker, M., Oberwinkler, F., & Begerow, D. (2009). Hidden diversity in the non-caryophyllaceous plant-parasitic members of Microbotryum (Pucciniomycotina: Microbotryales). Systematics and Biodiversity, 7(3), 297–306.

    Article  Google Scholar 

  • Kruckeberg, A. R. (1955). Interspecific hybridization in Silene. American Journal of Botany, 42, 373–378.

    Article  Google Scholar 

  • Lajeunesse, M. J., & Forbes, M. R. (2002). Host range and local parasite adaptation. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 269(1492), 703–710.

    Google Scholar 

  • Le Gac, M., Hood, M. E., Fournier, E., & Giraud, T. (2007). Phylogenetic evidence of host-specific cryptic species in the anther smut fungus. Evolution, 61(1), 15–26.

    Article  PubMed  Google Scholar 

  • Lindeberg, B. O. (1959). Ustilaginales of Sweden. Symbolae Botanicae Upsaliensis, 16, 1–175.

  • Liro, J. I. (1924). Die Ustilagineen Finnlands I. Annales Academiae Scientiarum Fennicae, Series A, 17, 1–636.

    Google Scholar 

  • Loveless, M. D., & Hamrick, J. L. (1984). Ecological determinants of genetic structure in plant populations. Annual Review of Ecology and Systematics, 15, 65–95.

    Article  Google Scholar 

  • Lutz, M., Göker, M., Piątek, M., Kemler, M., Begerow, D., & Oberwinkler, F. (2005). Anther smuts of Caryophyllaceae: molecular characters indicate host-dependent species delimitation. Mycological Progress, 4(3), 225–238.

    Article  Google Scholar 

  • Lutz, M., Piątek, M., Kemler, M., Chlebicki, A., & Oberwinkler, F. (2008). Anther smuts of Caryophyllaceae: molecular analyses reveal further new species. Mycological Research, 112, 1280–1296.

    Article  PubMed  Google Scholar 

  • Minder, A. M., & Widmer, A. (2008). A population genomic analysis of species boundaries: neutral processes, adaptive divergence and introgression between two hybridizing plant species. Molecular Ecology, 17(6), 1552–1563.

    Article  PubMed  CAS  Google Scholar 

  • Minder, A. M., Rothenbuehler, C., & Widmer, A. (2007). Genetic structure of hybrid zones between Silene latifolia and Silene dioica (Caryophyllaceae): evidence for introgressive hybridization. Molecular Ecology, 16(12), 2504–2516.

    Article  PubMed  CAS  Google Scholar 

  • Nannfeldt, J. A. (1966). Fungi as plant taxonomists. Acta Universitatis Upsaliensis, 17, 85–95.

    Google Scholar 

  • Nylander, J. A., Ronquist, F., Huelsenbeck, J. P., & Nieves-Aldrey, J. L. (2004). Bayesian phylogenetic analysis of combined data. Systematic Biology, 53(1), 47–67.

    Article  PubMed  Google Scholar 

  • Oxelman, B., Liden, M., Rabeler, R. K., & Popp, M. (2001). A revised generic classification of the tribe Sileneae (Caryophyllaceae). Nordic Journal of Botany, 20(6), 743–748.

    Article  Google Scholar 

  • Parker, J., Rambaut, A., & Pybus, O. G. (2008). Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infection, Genetics and Evolution, 8(3), 239–246.

    Article  PubMed  CAS  Google Scholar 

  • Piątek, M., Lutz, M., Ronikier, A., Kemler, M., & Swiderska-Burek, U. (2012). Microbotryum heliospermae, a new anther smut fungus parasitic on Heliosperma pusillum in the mountains of the European Alpine System. Fungal Biology, 116(2), 185–195.

    Article  PubMed  Google Scholar 

  • Popp, M., Erixon, P., Eggens, F., & Oxelman, B. (2005). Origin and evolution of a circumpolar polyploid species complex in Silene (Caryophyllaceae) inferred from low copy nuclear RNA polymerase introns, rDNA, and chloroplast DNA. Systematic Botany, 30, 302–313.

    Article  Google Scholar 

  • Poulin, R., & Keeney, D. B. (2008). Host specificity under molecular and experimental scrutiny. Trends in Parasitology, 24(1), 24–28.

    Article  PubMed  CAS  Google Scholar 

  • Poulin, R., & Morand, S. (2000). The diversity of parasites. The Quarterly Review of Biology, 75(3), 277–293.

    Article  PubMed  CAS  Google Scholar 

  • Poulin, R., Krasnov, B. R., Mouillot, D., & Thieltges, D. W. (2011). The comparative ecology and biogeography of parasites. Philosophical Transactions of the Royal Society B: Biological Sciences, 366(1576), 2379–2390.

    Article  Google Scholar 

  • Price, P. W. (1980). Evolutionary Biology of Parasites (MPB-15). Princeton, USA: Princeton University Press.

    Google Scholar 

  • Refregier, G., Le Gac, M., Jabbour, F., Widmer, A., Shykoff, J. A., Yockteng, R., et al. (2008). Cophylogeny of the anther smut fungi and their caryophyllaceous hosts: prevalence of host shifts and importance of delimiting parasite species for inferring cospeciation. BMC Evolutionary Biology, 8, 100.

    Article  PubMed  Google Scholar 

  • Rohrbach, P. (1868). Monographie der Gattung Silene. Leipzig: Engelmann.

    Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12), 1572–1574.

    Article  PubMed  CAS  Google Scholar 

  • Roux, C., Almaraz, T., & Durrieu, G. (1998). Phylogeny of fungi responsible for smut of plants based on ITS sequence analysis. Comptes Rendus de l'Academie des Sciences. Serie III, Sciences de la Vie, 321(7), 603–609.

    Article  PubMed  CAS  Google Scholar 

  • Slatkin, M., & Maddison, W. P. (1989). A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics, 123(3), 603–613.

    PubMed  CAS  Google Scholar 

  • Sloan, D. B., Giraud, T., & Hood, M. E. (2008). Maximized virulence in a sterilizing pathogen: the anther-smut fungus and its co-evolved hosts. Journal of Evolutionary Biology, 21(6), 1544–1554.

    Google Scholar 

  • Stamatakis, A. (2006a). Phylogenetic models of rate heterogeneity: a high performance computing perspective. Proceedings of the IPDPS, Rhodos, Greece.

  • Stamatakis, A. (2006b). RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22(21), 2688–2690.

    Article  PubMed  CAS  Google Scholar 

  • Swofford, D. L. (1998). PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sunderland, Massachusetts: Sinauer Associates.

  • Thompson, J. N. (2005). The Geographic Mosaic of Coevolution. Chicago, USA: The University of Chicago Press.

    Google Scholar 

  • Tutin, T. G., & Walters, S. M. (1993). Dianthus L. In T. G. Tutin, N. A. Burges, A. D. Chater, J. R. Edmondson, V. H. Heywood, D. M. Moore, D. H. Valentine, S. M. Walters, & D. A. Webb (Eds.), Flora Europaea Volume 1, (pp. 227–246). Cambrige, UK: Cambridge University Press.

    Google Scholar 

  • Valente, L. M., Savolainen, V., & Vargas, P. (2010). Unparalleled rates of species diversification in Europe. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 277(1687), 1489–1496.

    Google Scholar 

  • Vánky, K. (1994). European Smut Fungi. Stuttgart, Germany: Gustav Fischer Verlag.

    Google Scholar 

  • Vánky, K. (1998). The genus Microbotryum (smut fungi). Mycotaxon, 67, 33–60.

    Google Scholar 

  • Wang, T. H., Donaldson, Y. K., Brettle, R. P., Bell, J. E., & Simmonds, P. (2001). Identification of shared populations of human immunodeficiency virus type 1 infecting microglia and tissue macrophages outside the central nervous system. Journal of Virology, 75(23), 11686–11699.

    Article  PubMed  CAS  Google Scholar 

  • White, T. J., Bruns, T., Lee, S., & Taylor, J. (1990). Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In M. Innis, D. Gelfand, J. Shinsky, & T. White (Eds.), PCR Protocols: A guide to methods and applications (pp. 322–315). San Diego, USA: Academic Press.

    Google Scholar 

  • Zietara, M. S., & Lumme, J. (2002). Speciation by host switch and adaptive radiation in a fish parasite genus Gyrodactylus (Monogenea, Gyrodactylidae). Evolution, 56(12), 2445–2458.

    PubMed  Google Scholar 

Download references

Acknowledgments

This work was funded by various phases of the project Flora Mycologica Iberica (DGES, PB98-0538-C04-01; REN2002-04068-CO2-01GLO), coevolution project (CGL2004-00322/BOS), DFG Be 2201/4-2 and SYNTHESYS & European Commission of Transnational Access to major Research Infrastructures (EC-funded IHP Program) ES-TAF-1431 to MK. Thanks to Teresa Almaraz for some of the collections used in this study conserved in silica gel and SEM photographs obtained during her PhD thesis supported by the Flora Mycologica Iberica project. We would like to thank Félix Muñoz-Garmendia for helping with the taxonomy of the Spanish Dianthus specimens. Thanks to all staff from the herbaria where the collections are allocated (MA and MA-Fungi in Madrid; Herbarium Berolinense; Botanische Staatssammlung München; Tübinger Atlas des Vorderen Orients (TAVO); Herbarium Tubingense) as well as M. Koltzenburg, V. Kummer, M. Lutz and M. Piątek for providing specimens and Birgit Lemke for help with DNA sequencing of Dianthus. We would also like to thank Nicky Creux who helped us to improve the manuscript.

We thank the two anonymous reviewers for helpful comments.

Author information

Author notes

  1. Martin Kemler

    Present address: Centre of Excellence in Tree Health Biotechnology; Forestry and Agricultural Biotechnology Institute (FABI), University of Pretoria, Pretoria, 0002, South Africa

  2. Andrey Yurkov

    Present address: Leibniz Institute DSMZ – German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany

Authors and Affiliations

  1. Lehrstuhl für Evolution und Biodiversität der Pflanzen, AG Geobotanik, Ruhr-Universität Bochum, Bochum, Germany

    Martin Kemler, Angela M. Schäfer, Andrey Yurkov & Dominik Begerow

  2. Departamento de Micología, Real Jardín Botánico-CSIC, Plaza de Murillo 2, 28014, Madrid, Spain

    María P. Martín & M. Teresa Telleria

Authors
  1. Martin Kemler
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. María P. Martín
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. M. Teresa Telleria
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Angela M. Schäfer
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrey Yurkov
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Dominik Begerow
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Kemler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

S1

Genetic and geographic distances and coding for ANOVA of Microbotryum on Dianthus species (PDF 127 kb)

S2

Genetic and geographic distances and coding for ANOVA of Microbotryum on Silene species (PDF 71 kb)

S3

Results for the ANOVA using the reduced data set for the genetic and geographic distances. (PDF 273 kb)

S4

Results of the tip-association study using BaTS (PDF 30 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kemler, M., Martín, M.P., Telleria, M.T. et al. Contrasting phylogenetic patterns of anther smuts (Pucciniomycotina: Microbotryum) reflect phylogenetic patterns of their caryophyllaceous hosts. Org Divers Evol 13, 111–126 (2013). https://doi.org/10.1007/s13127-012-0115-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13127-012-0115-1

Keywords

Search

Navigation