1887

Abstract

Here we tested the hypothesis that species of the soil-inhabiting insect-pathogenic fungus are not randomly distributed in soils but show plant-rhizosphere-specific associations. We isolated from plant roots at two sites in Ontario, Canada, sequenced the 5′ EF-1α gene to discern species, and developed an RFLP test for rapid species identification. Results indicated a non-random association of three species (, and ) with the rhizosphere of certain types of plant species (identified to species and categorized as grasses, wildflowers, shrubs and trees). was the only species that was found associated with grass roots, suggesting a possible exclusion of and . Supporting this, experiments showed that conidia germinated significantly better in (switchgrass) root exudate than did or . and only associated with wildflower rhizosphere when co-occurring with . With the exception of these co-occurrences, was found to associate exclusively with the rhizosphere of tree species, predominantly (sugar maple), while was found to associate exclusively with the rhizosphere of shrubs and trees. These associations demonstrate that different species of associate with specific plant types.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.051102-0
2011-10-01
2019-10-23
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/10/2904.html?itemId=/content/journal/micro/10.1099/mic.0.051102-0&mimeType=html&fmt=ahah

References

  1. Bainard L. D. , Brown P. D. , Upadhyaya M. K. . ( 2009; ). Inhibitory effect of tall hedge mustard (Sisymbrium loeselii) allelochemicals on rangeland plants and arbuscular mycorrhizal fungi. . Weed Sci 57:, 386–393. [CrossRef]
    [Google Scholar]
  2. Baldi A. , Farkya S. , Jain A. , Gupta N. , Mehra R. , Datta V. , Srivastava A. K. , Bisaria V. S. . ( 2010; ). Enhanced production of podophyllotoxins by co-culture of transformed Linum album cells with plant growth-promoting fungi. . Pure Appl Chem 82:, 227–241. [CrossRef]
    [Google Scholar]
  3. Bidochka M. J. , Kamp A. M. , Lavender T. M. , Dekoning J. , De Croos J. N. A. . ( 2001; ). Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species?. Appl Environ Microbiol 67:, 1335–1342. [CrossRef] [PubMed]
    [Google Scholar]
  4. Bidochka M. J. , Small C. L. , Spironello M. . ( 2005; ). Recombination within sympatric cryptic species of the insect pathogenic fungus Metarhizium anisopliae . . Environ Microbiol 7:, 1361–1368. [CrossRef] [PubMed]
    [Google Scholar]
  5. Bischoff J. F. , Rehner S. A. , Humber R. A. . ( 2006; ). Metarhizium frigidum sp. nov.: a cryptic species of M. anisopliae and a member of the M. flavoviride complex. . Mycologia 98:, 737–745. [CrossRef] [PubMed]
    [Google Scholar]
  6. Bischoff J. F. , Rehner S. A. , Humber R. A. . ( 2009; ). A multilocus phylogeny of the Metarhizium anisopliae lineage. . Mycologia 101:, 512–530. [CrossRef] [PubMed]
    [Google Scholar]
  7. Bridge P. D. , Williams M. A. J. , Prior C. , Paterson R. R. M. . ( 1993; ). Morphological, biochemical and molecular characteristics of Metarhizium anisopliae and M. flavoviride . . J Gen Microbiol 139:, 1163–1169.[CrossRef]
    [Google Scholar]
  8. Bridge P. D. , Prior C. , Sagbohan J. , Lomer C. J. , Carey M. , Buddie A. . ( 1997; ). Molecular characterization of isolates of Metarhizium from locusts and grasshoppers. . Biodivers Conserv 6:, 177–189. [CrossRef]
    [Google Scholar]
  9. Bruck D. J. . ( 2005; ). Ecology of Metarhizium anisopliae in soilless potting media and the rhizosphere: implications for pest management. . Biol Control 32:, 155–163. [CrossRef]
    [Google Scholar]
  10. Bruck D. J. . ( 2010; ). Fungal entomopathogens in the rhizosphere. . BioControl 55:, 103–112. [CrossRef]
    [Google Scholar]
  11. Courty P. E. , Poletto M. , Duchaussoy F. , Buée M. , Garbaye J. , Martin F. . ( 2008; ). Gene transcription in Lactarius quietusQuercus petraea ectomycorrhizas from a forest soil. . Appl Environ Microbiol 74:, 6598–6605. [CrossRef] [PubMed]
    [Google Scholar]
  12. Estrada-Luna A. A. , Davies F. T. Jr , Egilla J. N. . ( 2000; ). Mycorrhizal fungi enhancement of growth and gas exchange of micropropagated guava plantlets (Psidium guajava L.) during ex vitro acclimatization and plant establishment. . Mycorrhiza 10:, 1–8. [CrossRef]
    [Google Scholar]
  13. Fang W. , Pei Y. , Bidochka M. J. . ( 2006; ). Transformation of Metarhizium anisopliae mediated by Agrobacterium tumefaciens . . Can J Microbiol 52:, 623–626. [CrossRef] [PubMed]
    [Google Scholar]
  14. Fegan M. , Manners J. M. , Maclean D. J. , Irwin J. A. G. , Samuels K. D. Z. , Holdom D. G. , Li D. P. . ( 1993; ). Random amplified polymorphic DNA markers reveal a high degree of genetic diversity in the entomopathogenic fungus Metarhizium anisopliae var. anisopliae . . J Gen Microbiol 139:, 2075–2081.[PubMed] [CrossRef]
    [Google Scholar]
  15. Felsenstein J. . ( 2009; ). phylip (phylogeny inference package) version 3.69. Distributed by the author. . Department of Genome Sciences, University of Washington;, Seattle, USA:.
  16. Felten J. , Kohler A. , Morin E. , Bhalerao R. P. , Palme K. , Martin F. , Ditengou F. A. , Legué V. . ( 2009; ). The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling. . Plant Physiol 151:, 1991–2005. [CrossRef] [PubMed]
    [Google Scholar]
  17. Hu G. , St Leger R. J. . ( 2002; ). Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. . Appl Environ Microbiol 68:, 6383–6387. [CrossRef] [PubMed]
    [Google Scholar]
  18. Hunter D. M. , Milner R. J. , Spurgin P. A. . ( 2001; ). Aerial treatment of the Australian plague locust, Chortoicetes terminifera (Orthoptera: Acrididae) with Metarhizium anisopliae (Deuteromycotina: Hyphomycetes). . Bull Entomol Res 91:, 93–99.[PubMed]
    [Google Scholar]
  19. Kennedy P. G. , Peay K. G. , Bruns T. D. . ( 2009; ). Root tip competition among ectomycorrhizal fungi: are priority effects a rule or an exception?. Ecology 90:, 2098–2107. [CrossRef] [PubMed]
    [Google Scholar]
  20. Kernaghan G. , Widden P. , Bergeron Y. , Legare S. , Pare D. . ( 2003; ). Biotic and abiotic factors affecting ectomycorrhizal diversity in boreal mixed-woods. . Oikos 102:, 497–504. [CrossRef]
    [Google Scholar]
  21. Klironomos J. N. . ( 2000; ). Host-specificity and functional diversity among arbuscular mycorrhizal fungi. . In Microbial Biosystems: New Frontiers. Proceedings of the 8th International Symposium on Microbial Ecology , pp. 845–851. Edited by Bell C. R. , Brylinsky M. , Johnson-Green P. . . Halifax, Canada:: Atlantic Canada Society for Microbial Ecology;.
    [Google Scholar]
  22. Larkin M. A. , Blackshields G. , Brown N. P. , Chenna R. , McGettigan P. A. , McWilliam H. , Valentin F. , Wallace I. M. , Wilm A. et al. & other authors ( 2007; ). clustal w and clustal_x version 2.0. . Bioinformatics 23:, 2947–2948. [CrossRef] [PubMed]
    [Google Scholar]
  23. Leal S. C. M. , Bertioli D. J. , Butt T. M. , Peberdy J. F. . ( 1994; ). Characterization of isolates of the entomopathogenic fungus Metarhizium anisopliae by RAPD-PCR. . Mycol Res 98:, 1077–1081. [CrossRef]
    [Google Scholar]
  24. Leal S. C. M. , Bertioli D. J. , Butt T. M. , Carder J. H. , Burrows P. R. , Peberdy J. F. . ( 1997; ). Amplification and restriction endonuclease digestion of the Pr1 gene for the detection and characterization of Metarhizium strains. . Mycol Res 101:, 257–265. [CrossRef]
    [Google Scholar]
  25. Lee J. , Chang I. Y. , Kim H. , Yun S. H. , Leslie J. F. , Lee Y. W. . ( 2009; ). Genetic diversity and fitness of Fusarium graminearum populations from rice in Korea. . Appl Environ Microbiol 75:, 3289–3295. [CrossRef] [PubMed]
    [Google Scholar]
  26. Lomer C. J. , Prior C. , Kooyman C. . ( 1997; ). Development of Metarhizium spp. for control of grasshoppers and locusts. . Mem Entomol Soc Can 129:, 265–286. [CrossRef]
    [Google Scholar]
  27. Lomer C. J. , Bateman R. P. , Johnson D. L. , Langewald J. , Thomas M. . ( 2001; ). Biological control of locusts and grasshoppers. . Annu Rev Entomol 46:, 667–702. [CrossRef] [PubMed]
    [Google Scholar]
  28. Maniania N. K. , Sithanantham S. , Ekesi S. , Ampong-Nyarko K. , Baumgartner J. , Lohr B. , Matoka C. M. . ( 2003; ). A field trial of the entomogenous fungus Metarhizium anisopliae for control of onion thrips, Thrips tabaci . . Crop Prot 22:, 553–559. [CrossRef]
    [Google Scholar]
  29. Martin F. , Nehls U. . ( 2009; ). Harnessing ectomycorrhizal genomics for ecological insights. . Curr Opin Plant Biol 12:, 508–515. [CrossRef] [PubMed]
    [Google Scholar]
  30. Miché L. , Balandreau J. . ( 2001; ). Effects of rice seed surface sterilization with hypochlorite on inoculated Burkholderia vietnamiensis . . Appl Environ Microbiol 67:, 3046–3052. [CrossRef] [PubMed]
    [Google Scholar]
  31. Milner R. J. , Pereira R. M. . ( 2000; ). Microbial control of urban pest-cockroaches, ants and termites. . In Field Manual of Techniques in Invertebrate Pathology, , 1st edn.. pp. 721–740. Edited by Lacey L. A. , Kaya H. K. . . Boston, USA:: Kluwer Academic Publishers;. [CrossRef]
    [Google Scholar]
  32. Molina R. , Massicotte H. , Trappe J. M. . ( 1992; ). Specificity phenomena in mycorrhizal symbioses: community-ecological consequences and practical implications. . In Mycorrhizal Functioning, pp. 357–423. Edited by Allen M. F. . . London, UK:: Chapman & Hall;.
    [Google Scholar]
  33. Pinior A. , Wyss U. , Piche Y. , Vierheilig H. . ( 1999; ). Plants colonized by AM fungi regulate further root colonization by AM fungi through altered root exudation. . Can J Bot 77:, 891–897.
    [Google Scholar]
  34. Piotrowski J. S. , Morford S. L. , Rillig M. C. . ( 2008; ). Inhibition of colonization by a native arbuscular mycorrhizal fungal community via Populus trichocarpa litter, litter extract, and soluble phenolic compounds. . Soil Biol Biochem 40:, 709–717. [CrossRef]
    [Google Scholar]
  35. Rai M. , Acharya D. , Singh A. , Varma A. . ( 2001; ). Positive growth responses of the medicinal plants Spilanthes calva and Withania somnifera to inoculation by Piriformospora indica in a field trial. . Mycorrhiza 11:, 123–128. [CrossRef]
    [Google Scholar]
  36. Rehner S. A. , Buckley E. . ( 2005; ). A Beauveria phylogeny inferred from nuclear ITS and EF1-α sequences: evidence for cryptic diversification and links to Cordyceps teleomorphs. . Mycologia 97:, 84–98. [CrossRef] [PubMed]
    [Google Scholar]
  37. Riba G. , Bouvier-Fourcade I. , Caudal A. . ( 1986; ). Isoenzymes polymorphism in Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) entomogenous fungi. . Mycopathology 96:, 161–169. [CrossRef]
    [Google Scholar]
  38. Shah P. A. , Pell J. K. . ( 2003; ). Entomopathogenic fungi as biological control agents. . Appl Microbiol Biotechnol 61:, 413–423.[PubMed] [CrossRef]
    [Google Scholar]
  39. Sirrenberg A. , Göbel C. , Grond S. , Czempinski N. , Ratzinger A. , Karlovsky P. , Santos P. , Feussner I. , Pawlowski K. . ( 2007; ). Piriformospora indica affects plant growth by auxin production. . Physiol Plant 131:, 581–589. [CrossRef] [PubMed]
    [Google Scholar]
  40. Small C. L. , Donaldson N. , Bidochka M. J. . ( 2004; ). Nucleotide sequence variation does not relate to differences in kinetic properties of neutral trehalase from the insect pathogenic fungus Metarhizium anisopliae . . Curr Microbiol 48:, 428–434. [CrossRef] [PubMed]
    [Google Scholar]
  41. Spatafora J. W. , Sung G. H. , Sung J. M. , Hywel-Jones N. L. , White J. F. Jr . ( 2007; ). Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. . Mol Ecol 16:, 1701–1711. [CrossRef] [PubMed]
    [Google Scholar]
  42. St Leger R. J. , May B. , Allee L. L. , Frank D. C. , Staples R. C. , Roberts D. W. . ( 1992; ). Genetic differences in allozymes and in formation of infection structures among isolates of the entomopathogenic fungus Metarhizium anisopliae . . J Invertebr Pathol 60:, 89–101. [CrossRef]
    [Google Scholar]
  43. Tigano-Milani M. S. , Gomes A. C. M. M. , Sobral B. W. S. . ( 1995; ). Genetic variability among Brazilian isolates of the entomopathogenic fungus Metarhizium anisopliae . . J Invertebr Pathol 65:, 206–210. [CrossRef]
    [Google Scholar]
  44. van Tuinen D. , Jacquot E. , Zhao B. , Gollotte A. , Gianinazzi-Pearson V. . ( 1998; ). Characterization of root colonization profiles by a microcosm community of arbuscular mycorrhizal fungi using 25S rDNA-targeted nested PCR. . Mol Ecol 7:, 879–887. [CrossRef] [PubMed]
    [Google Scholar]
  45. Vega F. E. , Goettel M. S. , Blackwell M. , Chandler D. , Jackson M. A. , Keller S. , Koike M. , Maniania N. K. , Monzon A. , Ownley B. H. . ( 2009; ). Fungal entomopathogens: new insights on their ecology. . Fungal Ecol 2:, 149–159. [CrossRef]
    [Google Scholar]
  46. Vierheilig H. , Lerat S. , Piché Y. . ( 2003; ). Systemic inhibition of arbuscular mycorrhiza development by root exudates of cucumber plants colonized by Glomus mosseae . . Mycorrhiza 13:, 167–170. [CrossRef] [PubMed]
    [Google Scholar]
  47. Wang C. , St Leger R. J. . ( 2007; ). The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. . Eukaryot Cell 6:, 808–816. [CrossRef] [PubMed]
    [Google Scholar]
  48. Wolfe B. E. , Rodgers V. L. , Stinson K. A. , Pringle A. . ( 2008; ). The invasive plant Alliaria petiolata (garlic mustard) inhibits ectomycorrhizal fungi in its introduced range. . J Ecol 96:, 777–783. [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.051102-0
Loading
/content/journal/micro/10.1099/mic.0.051102-0
Loading

Data & Media loading...

Supplements

vol. , part 10, pp. 2904 - 2911

RFLP analysis of (A) and (B) using I for isolates of . Representative isolates HKB1-1b (OG1), 43a-2i (OG2) and ARSEF 2575 (A2575; OG1). Arrows indicate distinctive bands used for identification. and RFLP products were separated on a 1.5% gel at 60 V for 80 min and 2% gel at 100 V for 45 min, respectively. [PDF](530 kb)



PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error