Description and phylogenetic placement of Beauveria hoplocheli sp. nov. used in the biological control of the sugarcane white grub, Hoplochelus marginalis, on Reunion Island

Literature Cited

• Aquino de MuroMMehtaSMooreD. 2003. The use of amplified fragment length polymorphism for molecular analysis of Beauveria bassiana isolates from Kenya and other countries and their correlation with host and geographical origin. FEMS Microbiol Lett 229:249–257, doi:10.1016/S0378-1097(03)00841-3
   Google Scholar
• BoniMFPosadaDFeldmanMW. 2007. An exact nonparametric method for inferring mosaic structure in sequence triplets. Genetics 176:1035–1047, doi:10.1534/genetics.106.068874
   PubMed Web of Science ®Google Scholar
• BrownJHedtkeSLemmonARLemmonEM. 2010. When trees grow too long: investigating the causes of highly inaccurate bayesian branch-length estimates. Syst Biol 59:145–161, doi:10.1093/sysbio/syp081
   PubMed Web of Science ®Google Scholar
• CallotGVercambreBNeuvégliseCRibaG. 1996. Hyphasmata and conidial pellets: an original morphological aspect of soil colonization by Beauveria brongniartii. J Invertebr Pathol 68:173–176, doi:10.1006/jipa.1996.0077
   Google Scholar
• CravanzolaFPiattiPBridgePDOzinoOI. 1997. Detection of genetic polymorphism by RAPD-PCR in strains of the entomopathogenic fungus Beauveria brongniartii isolated from the European cockchafer (Melolontha spp.). Lett Appl Microbiol 25:289–294, doi:10.1046/j.1472-765X.1997.00226.x
   Web of Science ®Google Scholar
• DarribaDTaboadaGLDoalloRPosadaD. 2012. jModel-Test 2: more models, new heuristics and parallel computing. Nat Methods 9:772, doi:10.1038/nmeth.2109
   PubMed Web of Science ®Google Scholar
• EdgarRC. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797, doi:10.1093/nar/gkh340
   PubMed Web of Science ®Google Scholar
• FernandesÉKKMoraesÁMLPachecoRSRangelDENMillerMPBittencourtVREPRobertsDW. 2009. Genetic diversity among Brazilian isolates of Beauveria bassiana: comparisons with non-Brazilian isolates and other Beauveria species. J Appl Microbiol 107:760–774, doi:10.1111/j.1365-2672.2009.04258.x
   PubMed Web of Science ®Google Scholar
• GhikasDVKouvelisVNTypasMA. 2010. Phylogenetic and biogeographic implications inferred by mitochondrial intergenic region analyses and ITS1-5.8 S-ITS2 of the entomopathogenic fungi Beauveria bassiana and B. brongniartii. BMC Microbiol 10:174, doi:10.1186/1471-2180-10-174
   PubMed Web of Science ®Google Scholar
• GibbsMJArmstrongJSGibbsAJ. 2000. Sister-scanning: a Monte Carlo procedure for assessing signals in recombinant sequences. Bioinformatics 16:573–582, doi:10.1093/bioinformatics/16.7.573
   PubMed Web of Science ®Google Scholar
• GlareTRInwoodAJ. 1998. Morphological and genetic characterization of Beauveria spp. from New Zealand. Mycol Res 102:250–256, doi:10.1017/S0953756297005005
   Web of Science ®Google Scholar
• GuindonSDufayardJFLefortVAnisimovaMHordijkWGascuelO. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59:307–321, doi:10.1093/sysbio/syq010
   PubMed Web of Science ®Google Scholar
• HarrisJL. 2000. Safe, low-distortion tape touch method for fungal slide mounts. J Clin Microbiol 38:4683–4684.
   PubMed Web of Science ®Google Scholar
• HolmesECWorobeyMRambautA. 1999. Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 16:405–409 doi:10.1093/oxfordjournals.molbev.a026121
   PubMed Web of Science ®Google Scholar
• HumberRAHansenKSWheelerMM. 2012. ARSEF ARS Collection of Entomopathogenic Fungal Cultures. Catalog of Species. New York, USDA-ARS Biological Integrated Pest Management Research. 502 p.
   Google Scholar
• JeuffraultERoletAReynaudBManikomRGeorgerSTayeTChiroleuFFouillaudMVercambreB. 2004. Vingt ans de lutte contre le ver blanc de la canne à sucre à la Réunion. Un succès, mais il reste des questionnements scientifiques pour confirmer la durabilité de la lutte biologique. Phytoma, la défense des végétaux 573:16–19.
   Google Scholar
• KellerSZimmermannG. 1989. Mycopathogens of soil insects. In: WildingNCollinsNMHammondPMWebberJF, eds. Insect-fungus interactions. London: Academic Press. p 239–270, doi:10.1016/B978-0-12-751800-8.50016-1
   Google Scholar
• MartinDPLemeyPLottMMoultonVPosadaDLefeuvreP. 2010. RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26:2462–2463, doi:10.1093/bioinformatics/btq467
   PubMed Web of Science ®Google Scholar
• MartinDPPosadaDCrandallKWilliamsonC. 2005. A modified bootscan algorithm for automated identification of recombinant sequences and recombination breakpoints. AIDS Res Hum Retroviruses 21:98–102, doi:10.1089/aid.2005.21.98
   PubMed Web of Science ®Google Scholar
• MartinDPRybickiE. 2000. RDP: detection of recombination amongst aligned sequences. Bioinformatics 16:562–563, doi:10.1093/bioinformatics/16.6.562
   PubMed Web of Science ®Google Scholar
• MaurerPCouteaudierYGirardPBridgePRibaG. 1997. Genetic diversity of Beauveria bassiana and relatedness to host insect range. Mycol Res 101:159–164, doi:10.1017/S0953756296002213
   Web of Science ®Google Scholar
• McGuireMRUlloaMParkY-HHudsonN. 2005. Biological and molecular characteristics of Beauveria bassiana isolates from California Lygus hesperus (Hemiptera: Miridae) populations. Biol Control 33:307–314, doi:10.1016/j.biocontrol.2005.03.009
   Web of Science ®Google Scholar
• NéronBMénagerHMaufraisCJolyNMaupetitJLetortSCarrereSTufferyPLetondalC. 2009. Mobyle: a new full web bioinformatics framework. Bioinformatics 25:3005–3011, doi:10.1093/bioinformatics/btp493
   PubMed Web of Science ®Google Scholar
• NeuvégliseCBrygooY. 1994. Identification of group I introns in the 28s rDNA of the entomopathogenic fungus Beauveria brongniartii. Curr Genet 27:38–45, doi:10.1007/BF00326577
   Google Scholar
• NeuvégliseCBrygooYRibaG. 1997. 28s rDNA group-I introns: a powerful tool for identifying strains of Beauveria brongniartii. Mol Ecol 6:373–381, doi:10.1046/j.1365-294X.1997.00202.x
   PubMed Web of Science ®Google Scholar
• NeuvégliseCBrygooYVercambreBRibaG. 1994. Comparative analysis of molecular and biological characteristics of strains of Beauveria brongniartii isolated from insects. Mycol Res 98:322–328, doi:10.1016/S0953-7562(09)80460-7
   Google Scholar
• ParadisEClaudeJStrimmerK. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290, doi:10.1093/bioinformatics/btg412
   PubMed Web of Science ®Google Scholar
• PosadaDCrandallKA. 2001. Evaluation of methods for detecting recombination from DNA sequences: computer simulations. Proc Natl Acad Sci USA 98:13757–13762, doi:10.1073/pnas.241370698
   PubMed Web of Science ®Google Scholar
• RambautASuchardMAXieDAJD. 2014. TRACER 1.6. Available from http://beast.bio.ed.ac.uk/Tracer
   Google Scholar
• RehnerSAAquino de MuroMBischoffJNIH. 2006a. Description and phylogenetic placement of Beauveria malawiensis sp. nov.(Cordycipitaceae, Hypocreales). Mycotaxon 98:137–145.
   Google Scholar
• RehnerSABuckleyEP. 2003. Isolation and characterization of microsatellite loci from the entomopathogenic fungus Beauveria bassiana (Ascomycota: Hypocreales). Mol Ecol Notes 3:409–411, doi:10.1046/j.1471-8286.2003.00464.x
   Google Scholar
• RehnerSABuckleyEP. 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, doi:10.3852/mycologia.97.1.84
   PubMed Web of Science ®Google Scholar
• RehnerSAMinnisAMSungGHLuangsa-ardJJDevottoLHumberRA. 2011. Phylogeny and systematics of the anamorphic, entomopathogenic genus Beauveria. Mycologia 103:1055–1073, doi:10.3852/10-302
   PubMed Web of Science ®Google Scholar
• RehnerSAPosadaFBuckleyEPInfanteFCastilloAVegaFE. 2006b. Phylogenetic origins of African and Neotropical Beauveria bassiana s.l. pathogens of the coffee berry borer, Hypothenemus hampei. J Invertebr Pathol 93: 11–21, doi:10.1016/j.jip.2006.04.005
   Google Scholar
• RonquistFTeslenkoMvan der MarkPAyresDLDarlingAHöhnaSLargetBLiuLSuchardMAHuelsenbeckJP. 2012. MrBayes 3.2: efficient bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542, doi:10.1093/sysbio/sys029
   PubMed Web of Science ®Google Scholar
• SawyerS. 1999. GENECONV: a computer package for the statistical detection of gene conversion. St Louis, Missouri: Washington University St. Louis. Available from http://www.math.wustl.edu/~sawyer
   Google Scholar
• SchliepKP. 2011. phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593, doi:10.1093/bioinformatics/btq706
   PubMed Web of Science ®Google Scholar
• SchwarzGE. 1978. Estimating the dimension of a model. Ann Stat 6:461–464, doi:10.1214/aos/1176344136
   Web of Science ®Google Scholar
• ShimodairaMHasegawaM. 1999. Multiple comparisons of log-likelihoods with applications to phylogenetic inference. Mol Biol Evol 16:1114–1116, doi:10.1093/oxfordjournals.molbev.a026201
   Web of Science ®Google Scholar
• SmithJM. 1992. Analyzing the mosaic structure of genes. J Mol Evol 34:126–129, doi:10.1007/BF00182389
   PubMed Web of Science ®Google Scholar
• TamuraKStecherGPetersonDFilipskiAKumarS. 2013. MEGA 6: molecular evolutionary genetics analysis. Mol Biol Evol 30:2725–2729, doi:10.1093/molbev/mst197
   PubMed Web of Science ®Google Scholar
• VercambreBGoebelORibaGMarchalMNeuvégliseCFerronP. 1994. Success in biological control of a soil pest, Hoplochelus marginalis, in Reunion Island: choice of a suitable fungus. 6th International Colloquium on Invertebrate Pathology and Microbial Control; 7–9 Dec 1993; Montpellier, France: Society for Invertebrate Pathology. p 283–288.
   Google Scholar
• VercambreBGoebelORibaGMorelGRobertPGuillonM. 1991. Programme de lutte biologique contre Hoplochelus marginalis (Coleoptera: Melolonthinae), nouveau ravageur des cultures à l’île de la Réunion. In: PavisCKermarrecA, eds. Les Colloques n 58. Rencontres Caraïbes en Lutte Biologique; 5–7 Nov 1990. Guadeloupe: INRA. p 371–378.
   Google Scholar
• VercambreBRobertPMarchalM. 1989. Le ver blanc (Hoplochelus marginalis Fairmaire, Coleoptera, Melolonthinae). Quel avenir? Quelle stratégie? 3e Congrès ARTAS; 16–23 Oct 1988; La Réunion: ARTAS. p 445–453.
   Google Scholar
• WangCShahFAPatelNLiZButtTM. 2003. Molecular investigation on strain genetic relatedness and population structure of Beauveria bassiana. Environ Microbiol 5:908–915, doi:10.1046/j.1462-2920.2003.00485.x
   PubMed Web of Science ®Google Scholar
• WeillerGF. 1998. Phylogenetic profiles: a graphical method for detecting genetic recombinations in homologous sequences. Mol Biol Evol 15:326–335, doi:10.1093/oxfordjournals.molbev.a025929
   PubMed Web of Science ®Google Scholar
• WhiteTBrunsTLeeSTaylorJ. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: InnisMGelfandDSninskyJ, eds. PCR protocols: a guide to methods and applications. San Diego, California: Academic Press. p 315–322.
   Google Scholar
• XiaX. 2013. DAMBE5: a comprehensive software package for data analysis in molecular biology and evolution. Mol Biol Evol 30:1720–1728, doi:10.1093/molbev/mst064
   PubMed Web of Science ®Google Scholar
• ZhangSLHeLMChenXHuengB. 2012. Beauveria lii sp. nov. isolated from Henosepilachna vigintioctopunctata. Mycotaxon 121:199–206, doi:10.5248/121.199
   Google Scholar
• ZimmermannG. 2007. Review on safety of the entomopathogenic fungi Beauveria bassiana and Beauveria brongniartii. Biocontrol Sci Technol 17:553–596, doi:10.1080/09583150701309006
   Web of Science ®Google Scholar