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Variation in host specificity and gene content in strains from genetically isolated lineages of the ectomycorrhizal fungus Paxillus involutus s. lat.

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Abstract

Ectomycorrhizal fungi are known to vary in host range. Some fungi can enter into symbiosis with multiple plant species, while others have restricted host ranges. The aim of this study was to examine variation in host specificity among strains from the basidiomycete Paxillus involutus s. lat. Recent studies have shown that this fungus consists of at least four genetically isolated lineages, phylogenetic species (PS) I (which corresponds to the morphological species Paxillus obscurosporus), PS II (P. involutus s. str.), PS III (Paxillus validus), and PS IV (not yet supported by any reference material). Thirty-five Paxillus strains of PS I to IV were examined in microcosms for their capacity to infect birch (Betula pendula) and spruce (Picea abies). Seventeen strains were compatible and formed mycorrhizae with both tree species. Seven strains were incompatible with both birch and spruce. The gene content in three pairs of incompatible and compatible strains PS I, II, and III were compared using microarray-based comparative genomic hybridizations. Of 4,113 P. involutus gene representatives analyzed, 390 varied in copy numbers in at least one of the three pairwise comparisons. Only three reporters showed significant changes in all three pairwise comparisons, and none of these were changed in a similar way in three comparisons. Our data indicate that changes in host range have occurred frequently and independently among strains in P. obscurosporus, P. involutus s. str., and P. validus. No evidence was obtained demonstrating that these changes have been associated with the gain or loss of similar genes in these three species.

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References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    PubMed  CAS  Google Scholar 

  • Apweiler R, Bairoch A, Wu CH, Barker WC, Boeckmann B, Ferro S, Gasteiger E, Huang H, Lopez R, Magrane M, Martin MJ, Natale DA, O'Donovan C, Redaschi N, Yeh LS (2004) UniProt: the Universal Protein knowledgebase. Nucl Acids Res 32:D115–D119

    Article  PubMed  CAS  Google Scholar 

  • Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29

    CAS  Google Scholar 

  • Brun A, Chalot M, Finlay RD, Söderström B (1995) Structure and function of the ectomycorrhizal association between Paxillus involutus (Batsch) Fr. and Betula pendula (Roth.). I. Dynamics of mycorrhiza formation. New Phytol 129:487–493

    Article  Google Scholar 

  • Burgess T, Dell B, Malajczuk N (1994) Variation in mycorrhizal development and growth stimulation by 20 Pisolithus isolates inoculated on to Eucalyptus grandis W. Hill ex Maiden. New Phytol 127:731–739

    Article  Google Scholar 

  • Cairney JWG (1999) Intraspecific physiological variation: implications for understanding functional diversity in ectomycorrhizal fungi. Mycorrhiza 9:125–135

    Article  Google Scholar 

  • Carreto L, Eiriz MF, Gomes AC, Pereira PM, Schuller D, Santos MA (2008) Comparative genomics of wild type yeast strains unveils important genome diversity. BMC Genomics 9:524

    Article  PubMed  Google Scholar 

  • Duddridge JA (1986) The development and ultrastructure of ectomycorrhizas III. Compatible and incompatible interactions between Suillus grevillei (Klotzch) Sing., and 11 species of ectomycorrhizal host in vitro in the absence of exogenous carbohydrate. New Phytol 103:457–464

    Article  CAS  Google Scholar 

  • Dunn B, Levine RP, Sherlock G (2005) Microarray karyotyping of commercial wine yeast strains reveals shared, as well as unique, genomic signatures. BMC Genomics 6:53

    Article  PubMed  Google Scholar 

  • Eisen MB, Spellman PT, Brown PO, Botstein D (1998) Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95:14863–14868

    Article  PubMed  CAS  Google Scholar 

  • Ek H, Andersson S, Arnebrant K, Söderström B (1994) Growth and assimilation of NH4+ and NO3- by Paxillus involutus in association with Betula pendula and Picea abies as affected by substrate pH. New Phytol 128:629–637

    Article  CAS  Google Scholar 

  • Finlay RD, Ek H, Odham G, Söderström B (1988) Mycelial uptake, translocation and assimilation of nitrogen from 15N-labelled ammonium by Pinus sylvestris plants infected with four different ectomycorrhizal fungi. New Phytol 110:59–66

    Article  Google Scholar 

  • Finn RD, Mistry J, Schuster-Bockler B, Griffiths-Jones S, Hollich V, Lassmann T, Moxon S, Marshall M, Khanna A, Durbin R, Eddy SR, Sonnhammer EL, Bateman A (2006) Pfam: clans, web tools and services. Nucl Acids Res 34:D247–D251

    Article  PubMed  CAS  Google Scholar 

  • Fries N (1985) Intersterility groups in Paxillus involutus. Mycotaxon 24:403–410

    Google Scholar 

  • Gafur A, Schützendübel A, Langenfeld-Heyser R, Fritz E, Polle A (2004) Compatible and incompetent Paxillus involutus isolates for ectomycorrhiza formation in vitro with poplar (Populus x canescens) differ in H2O2 production. Plant Biol 6:91–99

    Article  PubMed  CAS  Google Scholar 

  • Goffeau A, Park J, Paulsen IT, Jonniaux JL, Dinh T, Mordant P, Saier MH Jr (1997) Multidrug-resistant transport proteins in yeast: complete inventory and phylogenetic characterization of yeast open reading frames with the major facilitator superfamily. Yeast 13:43–54

    Article  PubMed  CAS  Google Scholar 

  • Gresham D, Dunham MJ, Botstein D (2008) Comparing whole genomes using DNA microarrays. Nat Rev Genet 9:291–302

    Article  PubMed  CAS  Google Scholar 

  • Hahn C, Agerer R (1999) Studies on the Paxillus involutus-complex. Nova Hedwigia 69:241–310

    Google Scholar 

  • Hedh J, Samson P, Erland S, Tunlid A (2008) Multiple gene genealogies and species recognition in the ectomycorrhizal fungus Paxillus involutus. Mycol Res 112:965–975

    Article  PubMed  CAS  Google Scholar 

  • Hu G, Liu I, Sham A, Stajich JE, Dietrich FS, Kronstad JW (2008) Comparative hybridization reveals extensive genome variation in the AIDS-associated pathogen Cryptococcus neoformans. Genome Biol 9:R41

    Article  PubMed  Google Scholar 

  • Johansson T, Le Quéré A, Ahrén D, Söderström B, Erlandsson R, Lundeberg J, Uhlén M, Tunlid A (2004) Transcriptional responses of Paxillus involutus and Betula pendula during formation of ectomycorrhizal root tissue. Mol Plant Microbe Interact 17:202–215

    Article  PubMed  Google Scholar 

  • Laiho O (1970) Paxillus involutus as a mycorrhizal symbiont of forest trees. Acta Forest Fenn 106:1–73

    Google Scholar 

  • Lamhamedi MS, Fortini JA, Kope HH, Kropp BR (1990) Genetic varaition in ectomycorrhiza formation by Pisolithus arhizus on Pinus pinaster and Pinus banksiana. New Phytol 115:689–697

    Article  Google Scholar 

  • Le Quéré A, Johansson T, Tunlid A (2002) Size and complexity of the nuclear genome of the ectomycorrhizal fungus Paxillus involutus. Fung Genet Biol 36:234–241

    Article  Google Scholar 

  • Le Quéré A, Schützendübel A, Rajashekar B, Canbäck B, Hedh J, Erland S, Johansson T, Tunlid A (2004) Divergence in gene expression related to variation in host specificity of an ectomycorrhizal fungus. Mol Ecol 13:3809–3819

    Article  PubMed  Google Scholar 

  • Le Quéré A, Astrup-Eriksen K, Rajashekar B, Schützendübel A, Canbäck B, Johansson T, Tunlid A (2006) Screening for rapidly evolving genes in the ectomycorrhizal fungus Paxillus involutus using cDNA microarrays. Mol Ecol 15:535–550

    Article  PubMed  Google Scholar 

  • Lynch M (2007) The frailty of adaptive hypotheses for the origins of organismal complexity. Proc Natl Acad Sci U S A 104:8597–8604

    Article  PubMed  CAS  Google Scholar 

  • Manning G, Plowman GD, Hunter T, Sudarsanam S (2002) Evolution of protein kinase signaling from yeast to man. Trends Biochem Sci 27:514–520

    Article  PubMed  CAS  Google Scholar 

  • Martin F, Aerts A, Ahren D, Brun A, Danchin EG, Duchaussoy F, Gibon J, Kohler A, Lindquist E, Pereda V, Salamov A, Shapiro HJ, Wuyts J, Blaudez D, Buee M, Brokstein P, Canback B, Cohen D, Courty PE, Coutinho PM, Delaruelle C, Detter JC, Deveau A, DiFazio S, Duplessis S, Fraissinet-Tachet L, Lucic E, Frey-Klett P, Fourrey C, Feussner I, Gay G, Grimwood J, Hoegger PJ, Jain P, Kilaru S, Labbe J, Lin YC, Legue V, Le TF, Marmeisse R, Melayah D, Montanini B, Muratet M, Nehls U, Niculita-Hirzel H, Oudot-Le Secq MP, Peter M, Quesneville H, Rajashekar B, Reich M, Rouhier N, Schmutz J, Yin T, Chalot M, Henrissat B, Kues U, Lucas S, Van de PY, Podila GK, Polle A, Pukkila PJ, Richardson PM, Rouze P, Sanders IR, Stajich JE, Tunlid A, Tuskan G, Grigoriev IV (2008) The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 452:88–92

    Article  PubMed  CAS  Google Scholar 

  • Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:695–700

    Article  PubMed  CAS  Google Scholar 

  • Molina R, Trappe JM (1982) Patterns of ectomycorrhizal host specificity and potential among pacific northwest conifers and fungi. Forest Sci 28:423–458

    Google Scholar 

  • Molina R, Massicotte H, Trappe JM (1992) Specificity phenomena in mycorrhizal symbiosis: community-ecological consequences and practical implications. In: Allen MF (ed) Mycorrhizal functioning, an interactive plant-fungal process. Chapmann and Hall, New York, pp 357–423

    Google Scholar 

  • Moran G, Stokes C, Thewes S, Hube B, Coleman DC, Sullivan D (2004) Comparative genomics using Candida albicans DNA microarrays reveals absence and divergence of virulence-associated genes in Candida dubliniensis. Microbiology 150:3363–3382

    Article  PubMed  CAS  Google Scholar 

  • Nelson DR (1999) Cytochrome P450 and the individuality of species. Arch Biochem Biophys 369:1–10

    Article  PubMed  CAS  Google Scholar 

  • Rajashekar B, Samson P, Johansson T, Tunlid A (2007) Evolution of nucleotide sequences and expression patterns of hydrophobin genes in the ectomycorrhizal fungus Paxillus involutus. New Phytol 174:399–411

    Article  PubMed  CAS  Google Scholar 

  • Ridley AJ (2001) Rho family proteins: coordinating cell responses. Trends Cell Biol 11:471–477

    Article  PubMed  CAS  Google Scholar 

  • Smith SE, Read DJ (eds) (1997) Mycorrhizal symbiosis, 2nd edn. Academic, San Diego

    Google Scholar 

  • Taylor AF, Alexander I (2005) The ectomycorrhizal symbiosis: life in the real world. Mycologist 19:102–112

    Article  Google Scholar 

  • Trappe JM (1962) Fungus associates of ectotrophic mycorrhizae. Bot Rev 28:538–606

    Article  Google Scholar 

  • Tunlid A, Talbot NJ (2002) Genomics of parasitic and symbiotic fungi. Curr Opin Microbiol 5:513–519

    Article  PubMed  CAS  Google Scholar 

  • Westfall PJ, Ballon DR, Thorner J (2004) When the stress of your environment makes you go HOG wild. Science 306:1511–1512

    Article  PubMed  CAS  Google Scholar 

  • Winzeler EA, Castillo-Davis CI, Oshiro G, Liang D, Richards DR, Zhou Y, Hartl DL (2003) Genetic diversity in yeast assessed with whole-genome oligonucleotide arrays. Genetics 163:79–89

    PubMed  CAS  Google Scholar 

  • Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules RS (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comp Biol 8:625–637

    Article  CAS  Google Scholar 

  • Wong KKY, Montpetit D, Piche Y, Lei J (1990) Root colonization by four closely related genotypes of the ectomycorrhizal basidiomycete Laccaria bicolor (Maire) Orton - comparative studies using electron microscopy. New Phytol 116:669–680

    Article  Google Scholar 

  • Wösten HA (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646

    Article  PubMed  Google Scholar 

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Acknowledgements

This study was supported by grants from the Swedish Research Council (VR) and the Swedish Research Council for Environment, Agricultural Sciences and Spatial Planning (FORMAS). Custom microarrays were produced at the DNA Microarray Resource Center at the BioMedical Center B10 in Lund, and DNA sequencing was performed at the Center of Genomic Ecology at the Ecology Building in Lund. We acknowledge Dr. Björn Canbäck and Balaji Rajashekar for help with bioinformatics. We thank Dr. Susanne Erland for valuable discussion on this work.

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  1. Department of Microbial Ecology, Lund University, Ecology Building, 223 62, Lund, Sweden

    Jenny Hedh, Tomas Johansson & Anders Tunlid

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  1. Jenny Hedh
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Correspondence to Anders Tunlid.

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Hedh, J., Johansson, T. & Tunlid, A. Variation in host specificity and gene content in strains from genetically isolated lineages of the ectomycorrhizal fungus Paxillus involutus s. lat.. Mycorrhiza 19, 549–558 (2009). https://doi.org/10.1007/s00572-009-0252-3

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