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Evolution of the Aspergilli : stuff for genomicists to think about

This article explores the evolution of the Aspergilli genus, discussing its major players, comparative questions, and the use of genomics in studying its evolution. It also provides insights into the different sexual stages and ascomatal types in the Eurotiomycetes group.

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Evolution of the Aspergilli : stuff for genomicists to think about

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  1. Evolution of the Aspergilli:stuff for genomicists to think about David M. Geiser Penn State University, USA dgeiser@psu.edu

  2. Aspergillus evolution • What is Aspergillus? • The major players in the genus and how are they related • Interesting comparative questions about Aspergillus • Studying evolution using genomics and studying genomics using evolution

  3. What is Aspergillus? • Aspergillus is a Eurotiomycete (or “Plectomycete”) • Aspergillus species appear to have a common evolutionary origin • this is a weak inference • Aspergillus species are diverse in their life histories • Homothallic • Heterothallic • Not seen to undergo sex • Nine different described sexual stages (Emericella, Eurotium, Neosartorya, Petromyces, Fennellia, Sclerocleista, Warcupiella, Hemicarpenteles, Chaetosartorya)

  4. Aspergillus is a Eurotiomycete 18S rDNA Geiser and Lo Buglio 2001

  5. Eurotiomycetes • Thallic (Ascosphaerales, Onygenales) and Phialidic (Eurotiales) anamorphs • Asci produced naked, in wefts of hyphae (gymnothecia) or in a solid enclosed fruiting body (cleistothecia) • Cleistothecia may be borne in a stroma • Many human and animal pathogens • Onygenales: Cocci, Histo, Blasto, dermatophytes • Eurotiales: Aspergillus, P. marneffei • Very chemically creative • An ectomycorrhizal fungus! (Elaphomyces) • NO LICHENIZED FUNGI • Osmophiles, thermophiles • Industrial fungi

  6. Conidiation in the Plectomycetes • thallic (T): Onygenales, Ascosphaerales • blastic (B): Eurotiales T biseriate B T B T B B uniseriate Geiser and LoBuglio 2001

  7. Ascomatal types in the Eurotiomycetes • cleistothecia borne in a stroma (C/S) • cleistothecia not borne in a stroma (C) • stroma, with no cleistothecia (S) • no cleistothecia and no stroma (N) Trichocoma Eupenicillium Emericella Petromyces C/S C/S C/S Gymnoascus Onygena S S Monascus Byssochlamys Ascosphaera Eurotium C nutriocyte C C N Geiser and LoBuglio 2001

  8. Sexual stages associated phylogenetically with important Aspergillus spp. • Emericella and Aspergillus nidulans • True cleistothecium surrounded by a stroma of hülle cells • Petromyces and A. flavus/oryzae/parasiticus/niger (?) • Cleistothecia embedded in a stroma (sclerotia) • Neosartorya and A. fumigatus • Cleistothecia/gymnothecia with wall composed of cottony hyphae.

  9. Aspergillus phylogenetics • Not a lot of data useful for inferring large-scale relationships • Take many of the trees I show with a grain of salt…

  10. 18S rDNA Aspergillus -- monophyletic? Tamura, M. Kawahara, K. Sugiyama, J. 2000.

  11. Aspergillus 25S rDNA tree • Based on a single locus, ~600 bp • Backbone of tree gets poor support • Major traditional species groups are supported • The morphologists did/are doing a pretty good job

  12. Petromyces sexual stage multiloculate stroma Emericella sexual stage cleistothecium surrounded by hülle cells (stroma) Eurotium sexual stage cleistothecium, no stroma Sclerocleista Warcupiella Neosartorya sexual stage cleistothecium composed of cottony hyphae Fennellia sexual stage Chaetosartorya sexual stage

  13. Subgenus Circumdati: Association with plants,seeds psychrotolerance Xerophilicty/tolerance heat-resistant ascospores Thermotolerance heat-resistant ascospores

  14. The players in Aspergillus genomics • Aspergillus nidulans • “Emericella clade” • Aspergillus nidulans group • Aspergillus section Nidulantes • Aspergillus fumigatus • Aspergillus oryzae

  15. Emericella clade NJ analysis of Steve Peterson’s 25S data • A. nidulans • A. sydowii - coral pathogen • Hülle cells • Homothallics • Putative asexuals • Heterothallic

  16. Aspergillosis of sea fan corals Aspergillus sydowii in culture: a relative of A. nidulans! Geiser, D.M. Ritchie, K. Smith, G. Taylor, J.W. Nature, 1998 Kiho Kim Aspergillosis of sea fan coral

  17. Sexual versus asexual strategies • Aspergillus heterothallicus - described by June Kwon-Chung (Raper and Fennell 1965) • One of three known heterothallic species (other two are Neosartoryas, clademates with A. fumigatus) • Known asexuals should be predicted to be recombining: • Population genetic evidence: a rich literature • Taylor et al. 2000, Annu. Rev. Phytopath. • MAT locus molecular genetics/phylogenetics • Turgeon, Berbee and others • Homothallics do not necessarily outcross less than heterothallics!

  18. Known heterothallics

  19. Early eventsin ascus developmentin theEurotiales:designed forhomothallism? Benjamin, 1955

  20. The players in Aspergillus genomics • Aspergillus nidulans • Aspergillus fumigatus • Neosartorya clade • Aspergillus fumigatus group • Aspergillus section Fumigati • Aspergillus oryzae

  21. Geiser, D.M. Frisvad, J. Taylor, J.W. Mycologia,1998 Beta-tubulin + rodA hydrophobin heterothallic heterothallic

  22. Geiser, D.M. Frisvad, J. Taylor, J.W. Mycologia 1998 Beta-tubulin + rodA hydrophobin

  23. Geiser, D.M. Frisvad, J. Taylor, J.W. Mycologia 1998 Beta-tubulin + rodA hydrophobin

  24. Evolution in Aspergillus fumigatus group • Monophyletic • A. fumigatus and N. fischeri are close relatives • Heterothallism derived? • Secondary metabolite data contrasts with benA/rodA phylogeny • Pringle, Taylor and others: asking the question whether it’s asexual

  25. The players in Aspergillus genomics • Aspergillus nidulans • Aspergillus fumigatus • Aspergillus oryzae • Petromyces clade • Aspergillus flavus group • Aspergillus Section Circumdati

  26. A.flavus, A. oryzae, A. niger and relatives (Petromyces) NJ analysis of Steve Peterson’s 25S data

  27. Geiser, DM Pitt, JI Taylor JW PNAS 1998

  28. Geiser, DM Horn, BW Dorner, JW Taylor JW FG&B 2001

  29. Using evolution to do good genomics • Comparative genomics IS evolutionary biology • Conservation of function is an adaptive process • Clark et al. 2003. Inferring non-neutral evolution from human-chimp-mouse orthologous gene trios. Science 302; 1960-62.

  30. The future • Genomics helps traditional evolutionary biologists to do their jobs because it provides tools • Understanding how genes evolve provides a framework for thinking about how they might function

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