Mycological Progress

, Volume 9, Issue 2, pp 181–194 | Cite as

Genetic variability and molecular phylogeny of Pleurotus eryngii species-complex isolates from Iran, and notes on the systematics of Asiatic populations

  • Rudabe Ravash
  • Behrouz Shiran
  • Aziz-Allah Alavi
  • Fereshteh Bayat
  • Saeideh Rajaee
  • Georgios I. Zervakis
Original Article

Abstract

The Pleurotus eryngii species-complex includes taxa of the northern hemisphere growing in association with plants of the family Apiaceae (umbellifers). In this study, 45 Pleurotus strains were isolated from five different host-plants: Ferula ovina, F. assa-foetida, Smyrniopsis aucheri, Kellusia odoratissima, and Cachrys ferulacea; all plant species, with the exception of C. ferulacea, are reported for the first time as hosts for this fungal group. Random amplified polymorphic DNA-PCR (RAPD) analysis and nucleotide sequence data from the internal transcribed spacer of the nuclear rRNA genes (ITS1, 5.8S and ITS2) were used for assessing genetic diversity and for determining phylogenetic relationships among the populations studied. Results permitted the grouping of the strains studied into three major clusters corresponding mainly to the nature of the host-plant: the first included isolates collected from Ferula spp. only, the second included isolates originating from C. ferulacea only but from various sampling locations, and the third included all K. odoratissima and S. aucheri associated strains plus a few isolates collected from F. ovina and C. ferulacea. The grouping of the Iranian material, in conjunction with the position in the resulting phylograms of other previously obtained P. eryngii complex sequences, revealed that the first cluster is related to the asiatic ‘P. nebrodensis’ (or to the asiatic Ferula spp. associated Pleuroti), the second forms a rather distinct lineage which is linked with reference strains originally classified as P. fossulatus, whereas the third cluster falls within the main part (or the “core”) of this complex, i.e., P. eryngii. Pleurotus populations growing on umbellifers in Iran seem either to have recently diverged through a sympatric speciation process based mainly on ecological factors (e.g., P. fossulatus), or they form part of a rather wide agglomerate associated with various host-plants where exchange of genetic material is still in progress (i.e., P. eryngii).

Keywords

Pleurotus nebrodensis Pleurotus fossulatus Apiaceae Host specificity Edible mushroom Speciation 

References

  1. Abdollahzadeh J, Asef MR, Mirmahmoodi T (2007) The Pleurotus eryngii species-complex in Kurdistan region of Iran. Pak J Biol Sci 10:3006–3009CrossRefPubMedGoogle Scholar
  2. Ajani Y, Ajani A, Cordes JM, Watson MF, Downie SR (2008) Phylogenetic analysis of nrDNA ITS sequences reveals relationships within five groups of Iranian Apiaceae subfamily Apioideae. Taxon 57:383–401CrossRefGoogle Scholar
  3. Amiri H (2007) Chemical composition and antibacterial activity of essential oil of Prangos ferulacea (L.) Lindl. J Medicinal Plants 6:36–41Google Scholar
  4. Babbel GR, Selander RK (1974) Genetic variability in edaphically restricted and widespread plant species. Evolution 28:619–630CrossRefGoogle Scholar
  5. Chiu H-H (2007) Phylogenetic analysis of Antrodia species and Antrodia camphorata inferred from internal transcribed spacer region. Antonie Van Leeuwenhoek 91:267–276CrossRefPubMedGoogle Scholar
  6. De Gioia T, Sisto D, Rana GL, Figliulo G (2005) Genetic structure of the Pleurotus eryngii species complex. Mycol Res 109:71–80CrossRefPubMedGoogle Scholar
  7. Doherty KR, Zweifel EW, Elde NC, McKone MJ, Zweifel SG (2003) Random amplified polymorphic DNA markers reveal genetic variation in the symbiotic fungus of leaf-cutting ants. Mycologia 95:19–23CrossRefGoogle Scholar
  8. Esfandiari E (1948) Troisième liste des fungi ramassé en Iran. Entomol Phytopathol Appl 8:1–15Google Scholar
  9. Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491PubMedGoogle Scholar
  10. Faridi P, Ghasemi Y, Gholami A, Mehregan I, Mohagheghzadeh A (2008) Antimicrobial essential oil from Smyrniopsis aucheri. Chem Nat Compd 44:116–118CrossRefGoogle Scholar
  11. Farris JS, Albert VA, Källersjö M, Lipscomb D, Kluge AG (1996) Parsimony jackknifing out-performs neighbor-joining. Cladistics 12:99–124CrossRefGoogle Scholar
  12. Felsenstein J (1978) Number of evolutionary trees. Syst Zool 27:27–33CrossRefGoogle Scholar
  13. Frøslev TG, Jeppesen TS, Læssøe T, Kjøller R (2007) Molecular phylogenetics and delimitation of species in Cortinarius section Calochroi (Basidiomycota, Agaricales) in Europe. Mol Phylogenet Evol 44:217–227CrossRefPubMedGoogle Scholar
  14. Ge ZW, Yang ZL, Zhang P, Matheny PB, Hibbett DS (2008) Flammulina species from China inferred by morphological and molecular data. Fungal Divers 32:59–68Google Scholar
  15. Ghorbani A (2005) Studies on pharmaceutical ethnobotany in the region of Turkmen Sahra, north of Iran (Part 1): general results. J Ethnopharmacol 102:58–68CrossRefPubMedGoogle Scholar
  16. Gouveia MMC, Ribeiro A, Várzea VMP, Rodrigues CJ Jr (2005) Genetic diversity in Hemileia vastatrix based on RAPD markers. Mycologia 97:396–404CrossRefPubMedGoogle Scholar
  17. Gryta H, Carriconde F, Charcosset J-Y, Jargeat P, Gardes M (2006) Population dynamics of the ectomycorrhizal fungal species Tricholoma populinum and Tricholoma scalpturatum associated with black poplar under differing environmental conditions. Environ Microbiol 8:773–786CrossRefPubMedGoogle Scholar
  18. Hamrick JL, Godt MJ (1990) Allozyme diversity in plant species. In: Brown AHD, Clegg MT, Kahler AL, Weir BS (eds) Plant Population Genetics - Breeding and Genetic Resources. Sinauer, Sunderland, MA, pp 43–63Google Scholar
  19. Healy M, Reece K, Walton D, Huong J, Shah K, Kontoyiannis DP (2004) Identification to the species level and differentiation between strains of Aspergillus clinical isolates by automated repetitive-sequence based. PCR. Clin Microbiol 42:4016–4024CrossRefGoogle Scholar
  20. Heim R (1960) Le Pleurote des Ombellifères en Iran. Rev Mycol 25:242–247Google Scholar
  21. Hilber O (1982) Die Gattung Pleurotus (Fr.) Kummer unter besonderer Berücksichtigung des Pleurotus eryngii-Formenkomplexes. Bibliotheca Mycologica 87. Cramer J, VaduzGoogle Scholar
  22. Hughes KW, Petersen RH, Johnson JE, Moncalvo J-M, Vilgalys R, Redhead SA, Thomas TA, McGhee LL (2001) Infragenic phylogeny of Collybia s. str. based on sequences of ribosomal ITS and LSU regions. Mycol Res 105:164–172CrossRefGoogle Scholar
  23. James TY, Porter D, Hamrick JL, Vilgalys R (1999) Evidence for limited intercontinental gene flow in the cosmopolitan mushroom. Schizophyllum commune. Evolution 53:1665–1667CrossRefGoogle Scholar
  24. Joly P, Cailleux R, Cerceau MT (1990) La sterilité male pathologique, élément de la co-adaptation entre populations de champignons et de plantes-hôtes: modèle des Pleurotus des Ombellifères. Bull Soc Bot Fr 137:71–85Google Scholar
  25. Jungehülsing U, Tudzynski P (1997) Analysis of genetic diversity in Claviceps purpurea by RAPD markers. Mycol Res 101:1–6CrossRefGoogle Scholar
  26. Kawai G, Babasaki K, Neda H (2008) Taxonomic position of a Chinese Pleurotus “Bai-Ling-Gu”: it belongs to Pleurotus eryngii (DC.: Fr.) Quél. and evolved independently in China. Mycoscience 49:5–87CrossRefGoogle Scholar
  27. Khajeh M, Yamini Y, Bahramifar N, Sefidkon F, Reza Pirmoradei M (2005) Comparison of essential oils compositions of Ferula assa-foetida obtained by supercritical carbon dioxide extraction and hydrodistillation methods. Food Chem 91:639–644CrossRefGoogle Scholar
  28. Kretzer A, Li Y, Szaro T, Bruns TD (1996) Internal transcribed spacer sequences from 38 recognized species of Suillus sensu lato: phylogenetic and taxonomic implications. Mycologia 88:776–785CrossRefGoogle Scholar
  29. Krüger D, Petersen RH, Hughes KW (2006) Molecular phylogenies and mating study data in Polyporus with special emphasis on group “Melanopus” (Basidiomycota). Mycol Progress 5:185–206CrossRefGoogle Scholar
  30. Lappalainen JH, Yli-Mattila T (1999) Genetic diversity in Finland of the birch endophyte Gnomonia setacea as determined by RAPD-PCR markers. Mycol Res 103:28–332CrossRefGoogle Scholar
  31. Lewinsohn D, Nevo E, Wasser SP, Hadar Y, Beharav A (2001) Genetic diversity in populations of the Pleurotus eryngii complex in Israel. Mycol Res 105:941–951CrossRefGoogle Scholar
  32. Moncalvo J-M, Buchanan PK (2008) Molecular evidence for long distance dispersal across the Southern Hemisphere in the Ganoderma applanatum-australe species complex (Basidiomycota). Mycol Res 112:425–436CrossRefPubMedGoogle Scholar
  33. Moreno G, Platas P, Peláez F, Bernedo M, Vargas A, Daza A, Santamaría C, Camacho M, Romero de la Osa L, Manjón JL (2008) Molecular phylogenetic analysis shows that Amanita ponderosa and A. curtipes are distinct species. Mycol Progress 7:41–47CrossRefGoogle Scholar
  34. Nuytinck J, Verbeken A (2007) Species delimitation and phylogenetic relationships in Lactarius section Deliciosi in Europe. Mycol Res 111:1285–1297CrossRefPubMedGoogle Scholar
  35. Pegler DN (1977) Pleurotus (Agaricales) in India, Nepal and Pakistan. Kew Bull 31:501–510CrossRefGoogle Scholar
  36. Petrak F (1939) Fungi. In: Rechinger KH (ed), Ergebnisse einer Botanische Reise nach dem Iran, 1937. Annalen Naturhistorischen Mus Wien 40:414–521Google Scholar
  37. Pimenov MG, Leonov MV (2004) The Asian Umbelliferae Biodiversity Database (ASIUM) with particular references to southwest Asian taxa. Turk J Bot 28:139–145Google Scholar
  38. Ro H-S, Kim SS, Rye JS, Jeon C-O, Lee TS, Lee H-S (2007) Comparative studies on the diversity of the edible mushroom Pleurotus eryngii: ITS sequence analysis, RAPD fingerprinting, and physiological characteristics. Mycol Res 111:710–715CrossRefPubMedGoogle Scholar
  39. Rogers SO, Bendich AJ (1988) Extraction of DNA from plant tissues. In: Gevin SB, Schilperoort RA, Verma DP (eds) Plant Molecular Biology Manual. Kluwer Academic Publishers, New York, pp 1–11Google Scholar
  40. Rohlf FJ (1998) NTSYS-PC. Numerical taxonomy and multivariate analysis system, Version 2.00. Exeter Software, Setauket, NYGoogle Scholar
  41. Saar I, Põldmaa K, Kõljalg U (2009) The phylogeny and taxonomy of genera Cystoderma and Cystodermella (Agaricales) based on nuclear ITS and LSU sequences. Mycol Progress 8:59–73CrossRefGoogle Scholar
  42. Saber M (1990) Contribution to the knowledge of Agaricales, pleurotoid in habit in Iran. Iran J Plant Pathol 26:29–40Google Scholar
  43. Saber M (1997) New records of Agaricales (pleurotoid in habit) for Iran. Iran J Plant Pathol 33:51–56Google Scholar
  44. Schneider S, Roessli D, Excoffier L (2001) Arlequin: a software for population genetics data analysis, version 2.00. Genetics and Biometry Lab, Department of Anthropology, University of Geneva, GenevaGoogle Scholar
  45. Singh BK, Munro S, Reid E, Ord B, Potts JM, Paterson E, Millard P (2006) Investigating microbial community structure in soils by physiological, biochemical and molecular fingerprinting methods. Eur J Soil Sci 57:72–82CrossRefGoogle Scholar
  46. Stott K, Desmerger C, Holford P (2005) Relationship among Lepista species determined by CAPS and RAPD. Mycol Res 109:205–211CrossRefPubMedGoogle Scholar
  47. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), Version 4.0b10. Sinauer Associates, Sunderland, MAGoogle Scholar
  48. Taylor JW, Jacobson DJ, Kroken S, Kasuga T, Geiser DM, Hibbett DS, Fisher MC (2000) Phylogenetic species recognition and species concepts in fungi. Fungal Genet Biol 31:21–32CrossRefPubMedGoogle Scholar
  49. Urbanelli S, Della Rosa V, Punelli F, Porretta D, Reverberi M, Fabbri AA, Fanelli C (2007) DNA-fingerprinting (AFLP and RFLP) for genotypic identification in species of the Pleurotus eryngii complex. Appl Microbiol Biotechnol 74:592–600CrossRefPubMedGoogle Scholar
  50. Venturella G, Zervakis G, La Rocca S (2000) Pleurotus eryngii var. elaeoselini var. nov. from Sicily. Mycotaxon 76:419–427Google Scholar
  51. Venturella G, Zervakis G, Saitta A (2002) Pleurotus eryngii var. thapsiae var. nov. from Sicily. Mycotaxon 81:69–74Google Scholar
  52. Vilgalys R, Sun BL (1994) Ancient and recent patterns of geographic speciation in the oyster mushroom Pleurotus revealed by phylogenetic analysis of ribosomal DNA sequences. Proc Natl Acad Sci USA 91:4599–4603CrossRefPubMedGoogle Scholar
  53. White TJ, Bruns T, Lee S, Taylor JW (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sininsky JJ, White TJ (eds) PCR Protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322Google Scholar
  54. Williams JG, Kubelik AR, Livak KJ, Rafalski JA, Tinger SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535CrossRefPubMedGoogle Scholar
  55. Zervakis G, Balis C (1996) A pluralistic approach on the study of Pleurotus species, with emphasis on compatibility and physiology of the European morphotaxa. Mycol Res 100:717–731CrossRefGoogle Scholar
  56. Zervakis G, Sourdis J, Balis C (1994) Genetic variability and systematics of eleven Pleurotus species based on isozyme analysis. Mycol Res 98:329–341CrossRefGoogle Scholar
  57. Zervakis GI, Venturella G, Papadopoulou K (2001) Genetic polymorphism and taxonomic infrastructure of the Pleurotus eryngii species-complex as determind by RAPD analysis, isozyme profiles and ecomorphological characters. Microbiology UK 147:3183–3194Google Scholar
  58. Zervakis GI, Moncalvo J-M, Vilgalys R (2004) Molecular phylogeny, biogeography and speciation of the mushroom species Pleurotus cystidiosus and allied taxa. Microbiology UK 150:715–726CrossRefGoogle Scholar
  59. Zhang JX, Huang CY, Ng TB, Wang HX (2006) Genetic polymorphism of ferula mushroom grown on Ferula sinkiangensis. Appl Microbiol Biotechnol 71:304–309CrossRefPubMedGoogle Scholar
  60. Zhang LF, Yang JB, Yang ZL (2004) Molecular phylogeny of eastern Asian species of Amanita (Agaricales, Basidiomycota): taxonomic and biogeographic implications. Fungal Divers 17:219–238Google Scholar

Copyright information

© German Mycological Society and Springer 2009

Authors and Affiliations

  • Rudabe Ravash
    • 1
  • Behrouz Shiran
    • 1
  • Aziz-Allah Alavi
    • 2
  • Fereshteh Bayat
    • 1
  • Saeideh Rajaee
    • 3
  • Georgios I. Zervakis
    • 4
    • 5
  1. 1.Department of Agronomy and Plant Breeding, Faculty of AgricultureShahrekord UniversityShahrekordIran
  2. 2.Department of Horticulture, Faculty of AgricultureShahrekord UniversityShahrekordIran
  3. 3.Department of Soil Science, Faculty of AgricultureShahrekord UniversityShahrekordIran
  4. 4.National Agricultural Research FoundationInstitute of KalamataKalamataGreece
  5. 5.Laboratory of General and Agricultural Microbiology, Department of Agricultural BiotechnologyAgricultural University of AthensAthensGreece

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