Abstract
Hypocrealean arthropod pathogenic fungi have profound impact on the regulation of agricultural and medical pests. However, until now the genetic and phylogenetic relationships among species have not been clarified, such studies could clarify host specificity relationships and define species boundaries. Our purpose was to compare the sequences of the mitochondrial SSU rDNA fragments from several mitosporic entomopathogenic Hypocreales to infer relationships among them and to evaluate the possibility to use these sequences as species diagnostic tool in addition to the more commonly studied sequences of nuclear SSU rDNA. The SSU mt-rDNA proved to be useful to help in differentiation of species inside several genera. Clusters obtained with Parsimony, Bayesian, and Maximum Likelihood analyses were congruent with a new classification of the Clavicipitaceae (Sung et al. Stud Mycol. 2007;57:5–59) in which the anamorphic genera Nomuraea and Metarhizium species remain in the Clavicipitaceae and Isaria species sequenced here are assigned to the family Cordycipitaceae. Mitochondrial genomic information indicates the same general pattern of relationships demonstrated by nuclear gene sequences.
Similar content being viewed by others
References
Kish LP, Allen GE. The Biology and Ecology of Nomuraea rileyi and a program for predicting its incidence on Anticarsia gemmatalis in soybean. Tech Bull. 1978;795:1–48.
Lacey LA, Goettel MS. Current developments in microbial control of insect pests and prospects for the early 21st century. Entomophaga. 1995;40(1):3–27. doi:10.1007/BF02372677.
Alves SB, editor. Controle microbiano de insetos. 2nd ed. Piracicaba: FEALQ; 1998.
Van Der Geest LPS, Elliot SL, Breeuwer JAJ, Beerling EAM. Diseases of mites. Exp Appl Acarol. 2000;24:497–560. doi:10.1023/A:1026518418163.
Luangsa-ard JJ, Hywel-Jones NL, Manoch L, Samson RA. On the relationships of Paecilomyces sect. Isarioidea species. Mycol Res. 2005;109:581–9. doi:10.1017/S0953756205002741.
Kalkar O, Carner GR, Scharf D, Boucias DG. Characterization of an Indonesian isolate of Paecilomyces reniformis. Mycopathologia. 2006;161:109–18. doi:10.1007/s11046-005-0133-z.
Nikoh N, Fukatsu T. Interkingdom hosts jumping underground: phylogenetic analysis of entomoparasitic fungi of the genus Cordyceps. Mol Biol Evol. 2000;17:629–38.
Artjariyasripong S, Mitchell J, Hywel-Jones NL, Jones EBG. Relationship of the genus Cordyceps and related genera, based on parsimony and spectral analysis of partial 18S and 28S ribosomal gene sequences. Mycoscience. 2001;42:503–17. doi:10.1007/BF02460949.
Pantou M, Mavridou A, Typas M. IGS sequences variation, group-I introns and the complete nuclear ribosomal DNA of the entomopathogenic fungus Metarhizium: excellent tool for isolate detection and phylogenetic analysis. Fungal Genet Biol. 2003;38:159–74. doi:10.1016/S1087-1845(02)00536-4.
Stensrud O, Hywel-Jones NL, Schumacher T. Towards a phylogenetic classification of Cordyceps: ITS nrDNAsequence data confirm divergent lineages and paraphyly. Mycol Res. 2005;109:41–56. doi:10.1017/S095375620400139X.
Inglis PW, Tigano MS. Identification and taxonomy of some entomopathogenic Paecilomyces spp. (Ascomycota) isolates using rDNA-ITS sequences. Genet Mol Biol. 2006;29:132–6. doi:10.1590/S1415-47572006000100025.
Driver F, Milner RJ, Trueman WH. A taxonomic revision of Metarhizium based on a phylogenetic analysis of rDNA sequence data. Mycol Res. 2000;104:134–50. doi:10.1017/S0953756299001756.
Nikoh N, Fukatsu T. Evolutionary dynamics of multiple group-I introns in nuclear ribosomal RNA genes of endoparasitic fungi of the Genus Cordyceps. Mol Biol Evol. 2001;18:1631–42.
Moncalvo JM, Drehmel D, Vilgalys R. Variation in modes and rates of evolution in nuclear and mitochondrial ribosomal DNA in the mushroom genus Amanita (Agaricales, Basidiomycota): phylogenetic implications. Mol Phylogenet Evol. 2000;16:48–63. doi:10.1006/mpev.2000.0782.
Skovgaard K, Rosendahl S, O’Donnell K, Nirenberg HI. Fusarium commune is a new species identified by morphological and molecular phylogenetic data. Mycologia. 2003;95:630–6. doi:10.2307/3761939.
Sosa-Gómez DR. Fungos Entomopatogênicos: Catálogo de Isolados. Série Documentos. Embrapa Soja. 2002;188:1–32.
Humber RA, Hansen K. Collection of entomopathogenic fungal cultures. Catalog of isolates, USDA-ARS, Ithaca, NY: 2005. http://arsef.fpsnl.cornell.edu/. Accessed 28 Mar 2008.
Rogers SO, Bendich AJ. Extraction of DNA from plant tissues. In: Gelvin SB, Schilperoort RA, Verma DPS, editors. Plant Molecular Biology Manual, vol. A6. Dordrecht: Kluwer Academic Publishers; 1988. p. 1–10.
White TJ, Bruns TD, Lee SB, Taylor JW. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ, editors. PCR protocols: a guide to methods and applications––a laboratory manual. New York: Academic Press; 1990. p. 315–22.
Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–80. doi:10.1093/nar/22.22.4673.
Tamura K, Dudley J, Nei M, Kumar S. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol. 2007;24:1596–9. doi:10.1093/molbev/msm092.
Kumar S, Filipski A. Multiple sequence alignment: in pursuit of homologous DNA positions. Genome Res. 2007;17:127–35. doi:10.1101/gr.5232407.
Hall BG. Phylogenetic trees made easy: a how-to manual, vol. 3. Sunderland, MA: Sinauer Associates; 2008.
Swofford DL. PAUP*: phylogenetic analysis using parsimony (* and other methods). Sunderland, MA: Sinauer Associates; 2002.
Huelsenbeck JP, Ronquist F. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics. 2001;17:754–5. doi:10.1093/bioinformatics/17.8.754.
Guindon S, Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by Maximum Likelihood. Syst Biol. 2003;52:696–704. doi:10.1080/10635150390235520.
Felsenstein J. Confidence-limits on phylogenies: an approach using the bootstrap. Evolution. 1985;39:783–91. doi:10.2307/2408678.
Posada D, Crandall KA. MODELTEST: testing the model of DNA substitution. Bioinformatics. 1998;14:817–8. doi:10.1093/bioinformatics/14.9.817.
Rodríguez F, Oliver JL, Marín A, Medina JR. The general stochastic model of nucleotide substitution. J Theor Biol. 1990;142:485–501. doi:10.1016/S0022-5193(05)80104-3.
Kouvelis VN, Ghikas DV, Typas MA. The analysis of the complete mitochondrial genome of Lecanicillium muscarium (synonym Verticillium lecanii) suggests a minimum common gene organization in mt-DNAs of Sordariomycetes: phylogenetic implications. Fungal Genet Biol. 2004;41:930–40. doi:10.1016/j.fgb.2004.07.003.
Boucias DG, Tigano MS, Sosa-Gómez DR, Glare TR, Inglis PW. Genotypic and phenotypic properties of the invertebrate mycopathogen Nomuraea rileyi. Biol Control. 2000;19:124–38. doi:10.1006/bcon.2000.0857.
Han Q, Inglis GD, Hausner G. Phylogenetic relationships among strains of the entomopathogenic fungus Nomuraea rileyi, as revealed by partial β-tubulin sequences and inter-simple sequence repeat (ISSR) analysis. Lett Appl Microbiol. 2002;34:376–83. doi:10.1046/j.1472-765X.2002.01103.x.
Suwannakut S, Boucias DG, Wiwat C. Genotypic analysis of Nomuraea rileyi collected from various noctuid hosts. J Invertebr Pathol. 2005;90:169–76. doi:10.1016/j.jip.2005.08.010.
Sung GH, Hywel-Jones NL, Sung JM, Luangsa-ard JJ, Shrestha B, Spatafora JW. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Stud Mycol. 2007;57:5–59.
Rakotonirainy MS, Dutertre M, Brygoo Y, Riba G. rRNA sequence comparison of Beauveria bassiana, Tolypocladium cylindrosporum, and Tolypocladium extinguens. J Invertebr Pathol. 1991;57:17–22. doi:10.1016/0022-2011(91)90036-P.
Huang B, Li SG, Li Cr, Fan MZ, Li ZZ. Studies on the taxonomy status of Metarhizium cylindrospora and Nomuraea viridula. Mycosystema. 2004;23:33–7.
Ghikas DV, Kouvelis VN, Typas MA. The complete mitochondrial genome of the entomopathogenic fungus Metarhizium anisopliae var. anisopliae: gene order and trn gene clusters reveal a common evolutionary course for all Sordariomycetes, while intergenic regions show variation. Arch Microbiol. 2006;185:393–401. doi:10.1007/s00203-006-0104-x.
Kouvelis VN, Sialakouma A, Typas MA. Mitochondrial gene sequences alone or combined with ITS region sequences provide firm molecular criteria for the classification of Lecanicillium species. Mycol Res. 2008;112:829–44. doi:10.1016/j.mycres.2008.01.016.
Acknowledgments
The study was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) from Brazil and USDA Agricultural Research Service (Ithaca, New York). We wish to acknowledge John Vandenberg for allowing to use his facilities, Drion G. Boucias for the critical review of the manuscript and providing some N. rileyi isolates, Karen Hansen and Louela Castrillo for helping with laboratory work. DRSG thanks CNPq (Project 490348/2004-1 and fellowship 303997/2004–4) and KLSB thanks CNPq (fellowship 151004/2005–6) and Fundação de Amparo à Pesquisa––FAPESP (grants #06/60127–0 and #07/53919–0).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sosa-Gómez, D.R., Humber, R.A., Hodge, K.T. et al. Variability of the Mitochondrial SSU rDNA of Nomuraea Species and Other Entomopathogenic Fungi from Hypocreales. Mycopathologia 167, 145–154 (2009). https://doi.org/10.1007/s11046-008-9157-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11046-008-9157-5