Advances in Genomics of Entomopathogenic Fungi

Advances in Genetics

Volumn 94, Issue , 2016, Pages 67-105

  Wang, J B ^a   St Leger, R J ^a   Wang, C ^b  

^a UNIVERSITY OF MARYLAND   (United States)

^b INSTITUTE OF GEOLOGY AND GEOPHYSICS   (China)

Author keywords

Beauveria; Comparative genomics; Cordyceps; Entomopathogenic fungi; Evolution; Fungus insect interaction; Host range; Metarhizium; Ophiocordyceps; Speciation

Indexed keywords

FUNGAL PROTEIN;

ANIMAL; BEAUVERIA; CORDYCEPS; EVOLUTION; FUNGUS; GENETICS; GENOMICS; HORIZONTAL GENE TRANSFER; HOST PATHOGEN INTERACTION; HOST RANGE; INSECT; METABOLISM; METARHIZIUM; MICROBIOLOGY; PATHOGENICITY; PROCEDURES;

ANIMALS; BEAUVERIA; BIOLOGICAL EVOLUTION; CORDYCEPS; FUNGAL PROTEINS; FUNGI; GENE TRANSFER, HORIZONTAL; GENOMICS; HOST SPECIFICITY; HOST-PATHOGEN INTERACTIONS; INSECTS; METARHIZIUM;

EID: 84960539685     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.adgen.2016.01.002     Document Type: Article

References (153)

1. Agrawal Y., Khatri I., Subramanian S., Shenoy B.D. Genome sequence, comparative analysis, and evolutionary insights into chitinases of entomopathogenic fungus Hirsutella thompsonii. Genome Biology and Evolution 2015, 7:916-930.
2. Alby K., Schaefer D., Bennett R.J. Homothallic and heterothallic mating in the opportunistic pathogen Candida albicans. Nature 2009, 480:890-893.
3. van Asbeck E.C., Clemons K.V., Stevens D.A. Candida parapsilosis: a review of its epidemiology, pathogenesis, clinical aspects, typing and antimicrobial susceptibility. Critical Reviews in Microbiology 2009, 35:283-309.
4. de Bekker C., Ohm R.A., Loreto R.G., Sebastian A., Albert I., Merrow M., Hughes D.P. Gene expression during zombie ant biting behavior reflects the complexity underlying fungal parasitic behavioral manipulation. BMC Genomics 2015, 16:620.
5. Bidochka M.J., Clark D.C., Lewis M.W., Keyhani N.O. Could insect phagocytic avoidance by entomogenous fungi have evolved via selection against soil amoeboid predators?. Microbiology 2010, 156:2164-2171.
6. Bidochka M.J., Kamp A.M., Lavender T.M., Dekoning J., Amritha De Croos J.N. Habitat association in two genetic groups of the insect-pathogenic fungus Metarhizium anisopliae: uncovering cryptic species?. Applied and Environmental Microbiology 2001, 67:1335-1342.
7. Bidochka M.J., St.Leger R.J., Roberts D.W. The rodlet layer from aerial and submerged conidia of the entomopathogenic fungus Beauveria bassiana contains hydrophobin. Mycological Research 1995, 99:403-406.
8. Bischoff J.F., Rehner S.A., Humber R.A. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 2009, 101:512-530.
9. Biswas C., Dey P., Satpathy S., Satya P. Establishment of the fungal entomopathogen Beauveria bassiana as a season long endophyte in jute (Corchorus olitorius) and its rapid detection using SCAR marker. BioControl 2012, 57:565-571.
10. Blair J.E., Coffey M.D., Park S.Y., Geiser D.M., Kang S. A multi-locus phylogeny for Phytophthora utilizing markers derived from complete genome sequences. Fungal Genetics and Biology 2008, 45:266-277.
11. Brownbridge M., Reay S.D., Nelson T.L., Glare T.R. Persistence of Beauveria bassiana (Ascomycota: Hypocreales) as an endophyte following inoculation of radiata pine seed and seedlings. Biological Control 2012, 61:194-200.
12. Bushley K.E., Raja R., Jaiswal P., Cumbie J.S., Nonogaki M., Boyd A.E., Spatafora J.W. The genome of Tolypocladium inflatum: evolution, organization, and expression of the cyclosporin biosynthetic gene cluster. PLoS Genetics 2013, 9:e1003496.
13. Cannon P.F., Hywel-Jones N.L., Maczey N., Norbu L., Samdup T.T., Lhendup P. Steps towards sustainable harvest of Ophiocordyceps sinensis in Bhutan. Biodiversity and Conservation 2009, 18:2263-2281.
14. Chang Y., Wang S., Sekimoto S., Aerts A.L., Choi C., Clum A., Berbee M.L. Phylogenomic analyses indicate that early fungi evolved digesting cell walls of algal ancestors of land plants. Genome Biology and Evolution 2015, 7:1590-1601.
15. Chen Y.X., Feng P., Shang Y.F., Xu Y.-J., Wang C.S. Biosynthesis of non-melanin pigment by a divergent polyketide synthase in Metarhizium robertsii. Fungal Genetics and Biology 2015, 81:142-149.
16. Cheng Q., Wang H., Xu B., Zhu S., Hu L., Huang M. Discovery of a novel small secreted protein family with conserved N-terminal IGY motif in Dikarya fungi. BMC Genomics 2014, 15:1151.
17. Cordaux R., Batzer M.A. The impact of retrotransposons on human genome evolution. Nature Reviews Genetics 2009, 10:691-703.
18. Crešnar B., Petrič S. Cytochrome P450 enzymes in the fungal kingdom. Biochimica et Biophysica Acta 2011, 1814:29-35.
19. Crisp A., Boschetti C., Perry M., Tunnacliffe A., Micklem G. Expression of multiple horizontally acquired genes is a hallmark of both vertebrate and invertebrate genomes. Genome Biology 2015, 16:50.
20. Cuomo C.A., Güldener U., Xu J.R., Trail F., Turgeon B.G., Di Pietro A., Kistler H.C. The Fusarium graminearum genome reveals a link between localized polymorphism and pathogen specialization. Science 2007, 317:1400-1402.
21. Daboussi M.J., Capy P. Transposable elements in filamentous fungi. Annual Review of Microbiology 2003, 57:275-299.
22. De Fine Licht H.H., Hajek A.E., Eilenberg J., Jensen A.B. Utilizing Genomics to Study Entomopathogenicity in the Fungal Phylum Entomophthoromycota: A Review of Current Genetic Resources. Advances in Genetics 2016, 94:41-65.
23. Donzelli B.G.G., Krasnoff S.B., Sun-Moon Y., Churchill A.C.L., Gibson D.M. Genetic basis of destruxin production in the entomopathogen Metarhizium robertsii. Current Genetics 2012, 58:105-116.
24. Donzelli B.G.G., Krasnoff S.B. Molecular Genetics of Secondary Chemistry in Metarhizium Fungi. Advances in Genetics 2016, 94:365-436.
25. Duan Z.B., Chen Y.X., Huang W., Shang Y.F., Chen P.L., Wang C.S. Linkage of autophagy to fungal development, lipid storage and virulence in Metarhizium robertsii. Autophagy 2013, 9:538-549.
26. Duan Z.B., Shang Y.F., Gao Q., Zheng P., Wang C.S. A phosphoketolase Mpk1 of bacterial origin is adaptively required for full virulence in the insect-pathogenic fungus Metarhizium anisopliae. Environmental Microbiology 2009, 11:2351-2360.
27. Dyer P.S., O'Gorman C.M. Sexual development and cryptic sexuality in fungi: insights from Aspergillus species. FEMS Microbiology Review 2012, 36:165-192.
28. Eadie M.J. Convulsive ergotism: epidemics of the serotonin syndrome?. Lancet Neruology 2003, 2:429-434.
29. Fang W.G., Pava-Ripoll M., Wang S.B., St.Leger R.J. Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fungal Genetic and Biology 2009, 46:277-285.
30. Fang W.G., St.Leger R.J. Mrt, a gene unique to fungi, encodes an oligosaccharide transporter and facilitates rhizosphere competency in Metarhizium robertsii. Plant Physiology 2010, 154:1549-1557.
31. Fang W.G., St.Leger R.J. RNA binding proteins mediate the ability of a fungus to adapt to the cold. Environmental Microbiology 2010, 12:810-820.
32. Feng P., Shang Y.F., Cen K., Wang C.S. Fungal biosynthesis of the bibenzoquinone oosporein to evade insect immunity. Proceedings of the National Academy of Sciences of the United States of America 2015, 112:11365-11370.
33. Fitzpatrick D.A. Horizontal gene transfer in fungi. FEMS Microbiology Letters 2012, 329:1-8.
34. Fraser J.A., Diezmann S., Subaran R.L., Allen A., Lengeler K.B., Dietrich F.S., Heitman J. Convergent evolution of chromosomal sex-determining regions in the animal and fungal kingdoms. PLoS Biology 2004, 2:e384.
35. Freimoser F.M., Hu G., St.Leger R.J. Variation in gene expression patterns as the insect pathogen Metarhizium anisopliae adapts to different host cuticles or nutrient deprivation in vitro. Microbiology 2005, 151:361-371.
36. Galagan J.E., Calvo S.E., Borkovich K.A., Selker E.U., Read N.D., Jaffe D., Birren B. The genome sequence of the filamentous fungus Neurospora crassa. Nature 2003, 422:859-868.
37. Galagan J.E., Calvo S.E., Cuomo C., Ma L.J., Wortman J.R., Batzoglou S., Birren B.W. Sequencing of Aspergillus nidulans and comparative analysis with A. fumigatus and A. oryzae. Nature 2005, 438:1105-1115.
38. Gao Q., Jin K., Ying S.H., Zhang Y., Xiao G., Shang Y., Wang C. Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genetics 2011, 7:e1001264.
39. Gao Q., Shang Y.F., Huang W., Wang C.S. Glycerol-3-phosphate acyltransferase contributes to triacylglycerol biosynthesis, lipid droplet formation and host invasion in Metarhizium robertsii. Applied and Environmental Microbiology 2013, 79:7646-7653.
40. Geiser D.M., Timberlake W.E., Arnold M.L. Loss of meiosis in Aspergillus. Molecular Biology and Evolution 1996, 13:809-817.
41. Gladieux P., Ropars J., Badouin H., Branca A., Aguileta G., de Vienne D.M., Giraud T. Fungal evolutionary genomics provides insight into the mechanisms of adaptive divergence in eukaryotes. Molecular Ecology 2014, 23:753-773.
42. Hajek A.E., McManus M.L., Delalibera I. A review of introductions of pathogens and nematodes for classical biological control of insects and mites. Biological Control 2007, 41:1-13.
43. Hajek A.E., Tobin P.C. Introduced pathogens follow the invasion front of a spreading alien host. Journal of Animal Ecology 2011, 80:1217-1226.
44. Hay W.W., Soeding E., DeConto R.M., Wold C.N. The late cenozoic uplift-climate change paradox. International Journal of Earth Science 2002, 91:746-774.
45. Hu G., St.Leger R.J. Field studies using a recombinant mycoinsecticide (Metarhizium anisopliae) reveal that it is rhizosphere competent. Applied and Environmental Microbiology 2002, 68:6383-6387.
46. Hu G., St.Leger R.J. A phylogenomic approach to reconstructing the diversification of serine proteases in fungi. Journal of Evolutionary Biology 2004, 17:1204-1214.
47. Hu X., Xiao G., Zheng P., Shang Y., Su Y., Zhang X., Wang C.S. Trajectory and genomic determinants of fungal-pathogen speciation and host adaptation. Proceedings of the National Academy of Sciences of the United States of America 2014, 111:16796-16801.
48. Hu X., Zhang Y.J., Xiao G.H., Zheng P., Xia Y.L., Zhang X.Y., Wang C.S. Genome survey uncovers the secrets of sex and lifestyle in caterpillar fungus. Chinese Science Bulletin 2013, 58:2846-2854.
49. Huang W., Shang Y.F., Chen P.L., Cen K., Wang C.S. Basic leucine zipper (bZIP) domain transcription factor MBZ1 regulates cell wall integrity, spore adherence, and virulence in Metarhizium robertsii. Journal of Biological Chemistry 2015, 290:8218-8231.
50. Huang W., Shang Y.F., Chen P.L., Gao Q., Wang C.S. MrpacC regulates sporulation, insect cuticle penetration and immune evasion in Metarhizium robertsii. Environmental Microbiology 2015, 17:994-1008.
51. Hughes D.P., Araujo J.P.M., Loreto R.G., Quevillon L., de Bekker C., Evans H.C. From So Simple a Beginning: The Evolution of Behavioral Manipulation by Fungi. Advances in Genetics 2016, 94:437-469.
52. Hugouvieux-Cotte-Pattat N., Condemine G., Nasser W., Reverchon S. Regulation of pectinolysis in Erwinia chrysanthemi. Annunal Review and Microbiology 1996, 50:213-257.
53. Idnurm A. Sex and speciation: the paradox that non-recombining DNA promotes recombination. Fungal Biology Reviews 2011, 25:121-127.
54. Isaka M., Kittakoop P., Kirtikara K., Hywel-Jones N.L., Thebtaranonth Y. Bioactive substances from insect pathogenic fungi. Accounts of Chemical Research 2005, 38:813-823.
55. Jackson A.P. A reconciliation analysis of host switching in plant-fungal symbioses. Evolution 2004, 58:1909-1923.
56. Juenger T., Bergelson J. Pairwise versus diffuse natural selection and the multiple herbivores of scarlet gilia, Ipomopsis aggregata. Evolution 1998, 52:1583-1592.
57. Kang C.S., Goo B.Y., Gyu L.D., Heon Y. Antifungal activities of Metarhizium anisopliae against Fusarium oxysporum, Botrytis cinerea and Alternaria solani. Korean Journal of Mycology 1996, 24:49-55.
58. Kepler R.M., Sung G.H., Ban S., Nakagiri A., Chen M.J., Huang B., Spatafora J.W. New teleomorph combinations in the entomopathogenic genus Metacordyceps. Mycologia 2012, 104:182-197.
59. Kershaw M.J., Moorhouse E.R., Bateman R., Reynolds S.E., Charnley A.K. The role of destruxins in the pathogenicity of Metarhizium anisopliae for three species of insects. Journal of Invertebrate Pathology 1999, 74:213-223.
60. Kim H.G., Song H., Yoon D.H., Song B.W., Park S.M., Sung G.H., Kim T.W. Cordyceps pruinosa extracts induce apoptosis of HeLa cells by a caspase dependent pathway. Journal of Ethnopharmacology 2010, 128:342-351.
61. Koo B.S., An H.G., Moon S.K., Lee Y.C., Kim H.M., Ko J.H., Kim C.H. Bombycis corpus extract (BCE) protects hippocampal neurons against excitatory amino acid-induced neurotoxicity. Immunopharmacology and Immunotoxicology 2003, 25:191-201.
62. Krasnoff S.B., Gupta S., St.Leger R.J., Renwick J.A.A., Roberts D.W. Antifungal and insecticidal properties of the efrapeptins: metabolites of the fungus Tolypocladium niveum. Journal of Invertebrate Pathology 1991, 58:180-188.
63. Kronstad J.W., Staben C. Mating type in filamentous fungi. Annual Review of Genetics 1997, 31:245-276.
64. Kubicek C.P., Herrera-Estrella A., Seidl-Seiboth V., Martinez D.A., Druzhinina I.S., Thon M., Grigoriev I.V. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biology 2011, 12:R40.
65. Kulkarni R.D., Thon M.R., Pan H., Dean R.A. Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea. Genome Biology 2005, 6:R24.
66. Li Z., Li C., Huang B., Fan M. Discovery and demonstration of the teleomorph of Beauveria bassiana (Bals.) Vuill., an important entomogenous fungus. Chinese Science Bulletin 2001, 46:751-753.
67. Liao X., Fang W., Lin L., Lu H.L., St.Leger R.J. Metarhizium robertsii produces an extracellular invertase (MrINV) that plays a pivotal role in rhizospheric interactions and root colonization. PLoS One 2013, 8:e78118.
68. Liao Y., Ling J., Zhang G., Liu F., Tao S., Han Z., Le H. Cordycepin induces cell cycle arrest and apoptosis by inducing DNA damage and up-regulation of p53 in Leukemia cells. Cell Cycle 2015, 14:761-771.
69. Lin L.C., Fang W.G., Liao X.G., Wang F.Q., Wei D.Z., St.Leger R.J. The MrCYP52 cytochrome P450 monoxygenase gene of Metarhizium robertsii is important for utilizing insect epicuticular hydrocarbons. PLoS One 2011, 6:e28984.
70. Liu L.S., Zhang J., Chen C., Teng J.T., Wang C.S., Luo D.Q. Structure and biosynthesis of fumosorinone, a new protein phosphatase 1B inhibitor firstly isolated from the entomogenous fungus Isaria fumosorosea. Fungal Genetics and Biology 2015, 81:191-200.
71. Liu Z.Y., Liang Z.Q., Whalley A.J., Yao Y.J., Liu A.Y. Cordyceps brittlebankisoides, a new pathogen of grubs and its anamorph, Metarhizium anisopliae var. majus. Journal of Invertebrate Pathology 2001, 78:178-182.
72. Lovett B., St.Leger R.J. Stress is the rule rather than the exception for Metarhizium. Current Genetics 2015, 61:253-261.
73. Luo X., Keyhani N.O., Yu X., He Z., Luo Z., Pei T., Zhang Y. The MAP kinase Bbslt2 controls growth, conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genetics and Biology 2012, 49:544-545.
74. Ma L.J., van der Does H.C., Borkovich K.A., Coleman J.J., Daboussi M.-J., Pietro A.D. Comparative genomics reveals mobile pathogenicity chromosomes in Fusarium. Nature 2010, 464:367-373.
75. Martin F., Aerts A., Ahren D., Brun A., Danchin E.G.J., Duchaussoy F., Grigoriev I.V. The genome of Laccaria bicolor provides insights into mycorrhizal symbiosis. Nature 2008, 452:88-92.
76. Martinez D., Berka R.M., Henrissat B., Saloheimo M., Arvas M., Baker S.E., Brettin T.S. Genome sequencing and analysis of the biomass-degrading fungus Trichoderma reesei (syn. Hypocrea jecorina). Nature Biotechnology 2008, 26:553-560.
77. Meyling N.V., Lübeck M., Buckley E.P., Eilenberg J., Rehner S.A. Community composition, host range and genetic structure of the fungal entomopathogen Beauveria in adjoining agricultural and seminatural habitats. Molecular Ecology 2009, 18:1282-1293.
78. Moonjely S., Barrelli R., Bidochka M.J. Insect Pathogenic Fungi as Endophytes. Advances in Genetics 2016, 94:107-136.
79. Molnár I., Gibson D.M., Krasnoff S.B. Secondary metabolites from entomopathogenic Hypocrealean fungi. Natural Product Reports 2010, 27:1241-1275.
80. Morschhauser J. Regulation of multidrug resistance in pathogenic fungi. Fungal Genetics and Biology 2010, 47:94-106.
81. Ni M., Feretzaki M., Sun S., Wang X., Heitman J. Sex in fungi. Annual Review of Genetics 2011, 45:405-430.
82. Noda J., Brito N., González C. The Botrytis cinerea xylanase Xyn11A contributes to virulence with its necrotizing activity, not with its catalytic activity. BMC Plant Biology 2010, 10:38.
83. Nygren K., Strandberg R., Wallberg A., Nabholz B., Gustafsson T., García D., Johannesson H. A comprehensive phylogeny of Neurospora reveals a link between reproductive mode and molecular evolution in fungi. Molecular Phylogenetics and Evolution 2011, 59:649-663.
84. Ohm R., Feau N., Henrissat B., Schoch C.L., Horwitz B.A., Barry K.W., Grigoriev I. Diverse lifestyles and strategies of plant pathogenesis encoded in the genomes of eighteen Dothideomycetes fungi. PLoS Pathogens 2012, 8:e1003037.
85. Ortiz-Urquiza A., Keyhani N.O. Action on the surface: entomopathogenic fungi versus the insect cuticle. Insects 2013, 4:357-374.
86. Ortiz-Urquiza A., Keyhani N.O. Stress response signaling and virulence: insights from entomopathogenic fungi. Current Genetics 2015, 61:239-249.
87. Ortiz-Urquiza A., Keyhani N.O. Molecular Genetics of Beauveria bassiana Infection of Insects. Advances in Genetics 2016, 94:165-250.
88. Ownley B.H., Gwinn K.D., Vega F.E. Endophytic fungal entomopathogens with activity against plant pathogens: ecology and evolution. BioControl 2010, 55:113-128.
89. Pal S., St.Leger R.J., Wu L.P. Fungal peptide Destruxin A plays a specific role in suppressing the innate immune response in Drosophila Melanogaster. Journal of Biological Chemistry 2007, 292:8969-8977.
90. Paterson R.R. Cordyceps: a traditional Chinese medicine and another fungal therapeutic biofactory?. Phytochemistry 2008, 69:1469-1495.
91. Pattemore J.A., Hane J.K., Williams A.H., Wilson B.A., Stodart B.J., Ash G.J. The genome sequence of the biocontrol fungus Metarhizium anisopliae and comparative genomics of Metarhizium species. BMC Genomics 2014, 15:660.
92. Pava-Ripoll M., Angelini C., Fang W.G., Wang S., Posada F.J., St.Leger R.J. The rhizosphere-competent entomopathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudate. Microbiology 2011, 157:47-55.
93. Pereira J.L., Noronha E.F., Miller R.N., Franco O.L. Novel insights in the use of hydrolytic enzymes secreted by fungi with biotechnological potential. Letters in Applied Microbiology 2007, 44:573-581.
94. Peterson S.W. Phylogenetic analysis of Aspergillus species using DNA sequences from four loci. Mycologia 2008, 100:205-226.
95. Raffaele S., Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews Microbiology 2012, 10:417-430.
96. Rangel D.E., Alston D.G., Roberts D.W. Effects of physical and nutritional stress conditions during mycelial growth on conidial germination speed, adhesion to host cuticle, and virulence of Metarhizium anisopliae, an entomopathogenic fungus. Mycological Research 2008, 112:1355-1361.
97. Rhee Y.J., Hillier S., Gadd G.M. Lead transformation to pyromorphite by fungi. Current Biology 2012, 22:237-241.
98. Richards T.A., Leonard G., Soanes M., Talbot N.J. Gene transfer into the fungi. Fungal Biology Reviews 2011, 25:98-110.
99. Roberts D.W., St.Leger R.J. Metarhizium spp., cosmopolitan insect-pathogenic fungi: mycological aspects. Advances in Applied Microbiology 2004, 54:1-70.
100. Scazzocchio C. The fungal GATA factors. Current Opinion in Microbiology 2000, 3:126-131.
101. Schaible U.E., Kaufmann S.H.E. A nutritive view on the host-pathogen interplay. Trends in Microbiology 2005, 13:373-380.
102. Schulze-Lefert P., Panstruga R. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends in Plant Science 2011, 16:117-125.
103. Screen S.E., St.Leger R.J. Cloning, expression and substrate specificity of a fungal chymotrypsin. Journal of Biological Chemistry 2000, 275:6689-6694.
104. Seidl V. Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biology Reviews 2008, 22:36-42.
105. Shang Y., Feng P., Wang C. Fungi that infect insects: altering host behavior and beyond. PLoS Pathogens 2015, 11:e1005037.
106. Sharpton T.J., Stajich J.E., Rounsley S.D., Gardner M.J., Wortman J.R., Jordar V.S., Taylor J.W. Comparative genomic analyses of the human fungal pathogens Coccidioides and their relatives. Genome Research 2009, 19:1722-1731.
107. Silva W.O.B., Santi L., Berger M., Pinto A.F.M., Guimaraes J.A., Schrank A., Vainstein M.H. Characterization of a spore surface lipase from the biocontrol agent Metarhizium anisopliae. Processing Biochemistry 2009, 44:829-834.
108. St.Leger R.J. Studies on adaptations of Metarhizium anisopliae to life in the soil. Journal of Invertebrate Pathology 2008, 98:271-276.
109. St.Leger R.J., Bidochka M.J., Roberts D.W. Germination triggers of Metarhizium anisopliae conidia are related to host species. Microbiology 1994, 140:1651-1660.
110. St.Leger R.J., Cooper R.M., Charnley A.K. Cuticle-degrading enzymes of entomopathogenic fungi: regulation of production of chitinolytic enzymes. Journal of General Microbiology 1986, 132:1509-1517.
111. St.Leger R.J., Cooper R.M., Charnley A.K. Cuticle-degrading enzymes of entomopathogenic fungi: cuticle degradation in vitro by enzymes from entomopathogens. Journal of Invertebrate Pathology 1986, 47:167-177.
112. St.Leger R.J., Joshi L., Bidochka M.J., Roberts D.W. Construction of an improved mycoinsecticide overexpressing a toxic protease. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:6349-6354.
113. St.Leger R.J., May B., Allee L.L., Frank D.C., Staples R.C., Roberts D.W. Genetic differences in allozymes and in formation of infection structures among isolates of the entomopathogenic fungus Metarhizium anisopliae. Journal of Invertebrate Pathology 1992, 60:89-101.
114. St.Leger R.J., Nelson J.O., Screen S.E. The entomopathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology 1999, 145:2691-2699.
115. St.Leger R.J., Wang C.S., Fang W.G. New perspectives on insect pathogens. Fungal Biology Reviews 2011, 25:84-88.
116. Staats C.C., Junges A., Guedes R.L., Thompson C.E., de Morais G.L., Boldo J.T., Schrank A. Comparative genome analysis of entomopathogenic fungi reveals a complex set of secreted proteins. BMC Genomics 2014, 15:822.
117. Steinwender B.M., Enkerli J., Widmer F., Eilenberg J., Kristensen H.L., Bidochka M.J., Meyling N.V. Root isolations of Metarhizium spp. from crops reflect diversity in the soil and indicate no plant specificity. Journal of Invertebrate Pathology 2015, 132:142-148.
118. Stidham T.A., Stidham J.A. A new Miocene band-winged grasshopper (Orthoptera: Acrididae) from Nevada. Annals of the Entomological Society of America 2000, 93:405-407.
119. Stukenbrock E.H., Bataillon T., Dutheil J.Y., Hansen T.T., Li R., Zala M. The making of a new pathogen: insights from comparative population genomics of the domesticated wheat pathogen Mycosphaerella graminicola and its wild sister species. Genome Research 2011, 21:2157-2166.
120. Suh S.O., Noda H., Blackwell M. Insect symbiosis: derivation of yeast-like endosymbionts within an entomopathogenic filamentous lineage. Molecular Biology and Evolution 2001, 18:995-1000.
121. Sun S., Heitman J. Is sex necessary?. BMC Biology 2011, 9:56-59.
122. Sung G.H., Hywel-Jones N.L., Sung J.M., Jennifer Luangsa-ard J., Shrestha N., Spatafora J.W. Phylogenetic classification of Cordyceps and the clavicipitaceous fungi. Studies in Mycology 2007, 57:5-59.
123. Thomas M.B., Read A.F. Can fungal biopesticides control malaria?. Nature Reviews Microbiology 2007, 5:377-383.
124. Torres M.S., Singh A.P., Vorsa N., White J.F. An analysis of ergot alkaloids in the Clavicipitaceae (Hypocreales, Ascomycota) and ecological implications. Symbiosis 2008, 46:11-19.
125. Vega F.E., Posada F., Aime M.C., Pava-Ripoll M., Infante F., Rehner S.A. Entomopathogenic fungal endophytes. Biological Control 2008, 46:72-82.
126. Wagner B.L., Lewis L.C. Colonization of corn, Zea mays, by the entomopathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology 2000, 66:3468-3473.
127. Wang B., Kang Q.J., Lu Y.Z., Bai L., Wang C. Unveiling the biosynthetic puzzle of destruxins in Metarhizium species. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:1287-1292.
128. Wang C., Butt T.M., St.Leger R.J. Colony sectorization of Metarhizium anisopliae is a sign of ageing. Microbiology 2005, 151:3223-3236.
129. Wang C., Fan M.Z., Li Z.Z., Butt T.M. Molecular monitoring and evaluation of the application of the insect-pathogenic fungus Beauveria bassiana in southeast China. Journal of Applied Microbiology 2004, 96:861-870.
130. Wang C., Feng M.-G. Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biological Control 2014, 68:129-135.
131. Wang C., St.Leger R.J. A collagenous protective coat enables Metarhizium anisopliae to evade insect immune responses. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:6647-6652.
132. Wang C., St.Leger R.J. The Metarhizium anisopliae perilipin homolog MPL1 regulates lipid metabolism, appressorial turgor pressure, and virulence. Journal of Biological Chemistry 2007, 282:21110-21115.
133. Wang C., Zhang S., Hou R., Zheng Q., Xu Q., Zheng D., Xu J. Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathogens 2011, 12:e1002460.
134. Wang C.S., Duan Z.B., St.Leger R.J. MOS1 osmosensor of Metarhizium anisopliae is required for adaptation to insect host hemolymph. Eukaryotic Cell 2008, 7:302-309.
135. Wang C.S., Hu G., St.Leger R.J. Differential gene expression by Metarhizium anisopliae growing in root exudate and host (Manduca sexta) cuticle or hemolymph reveals mechanisms of physiological adaptation. Fungal Genetics and Biology 2005, 42:704-718.
136. Wang C.S., St.Leger R.J. Developmental and transcriptional responses to host and non-host cuticles by the specific locust pathogen Metarhizium anisopliae sf. acridum. Eukaryotic Cell 2005, 4:937-947.
137. Wang C.S., St.Leger R.J. The MAD1 adhesin of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryotic Cell 2007, 6:808-816.
138. Wang C.S., St.Leger R.J. Genomics of entomopathogenic fungi. The ecological genomics of fungi 2014, 243-260. John Wiley & Sons, Inc. F. Martin (Ed.).
139. Wang S.B., Fang W.G., Wang C.S., St.Leger R.J. Insertion of an esterase gene into a specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars. PLoS Pathogens 2011, 7:e1002097.
140. Wang S., O'Brien T.R., Pava-Ripoll M., St.Leger R.J. Local adaptation of an introduced transgenic insect fungal pathogen due to new beneficial mutations. Proceedings of the National Academy of Sciences 2011, 108:20449-20454.
141. Whittle C.A., Nygren K., Johannesson H. Consequences of reproductive mode on genome evolution in fungi. Fungal Genetics and Biology 2011, 48:661-667.
142. Xiao G.H., Ying S.-H., Zheng Z., Wang Z.L., Zhang S., Xie X.Q., Feng M.G. Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Scientific Reports 2012, 2:483.
143. Xu J.R., Peng Y.L., Dickman M.B., Sharon A. The dawn of fungal pathogen genomics. Annual Reviews of Phytopathology 2006, 44:337-366.
144. Xu Y.J., Luo F.F., Gao Q., Shang Y.F., Wang C.S. Metabolomics reveals insect metabolic responses associated with fungal infection. Analytical and Bioanalytical Chemistry 2015, 407:4815-4821.
145. Xue C., Hsueh Y.P., Heitman J. Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi. FEMS Microbiology Review 2008, 32:1010-1032.
146. Xue Y., Batlle M., Hirsch J.P. GPR1 encodes a putative G protein-coupled receptor that associates with the Gpa2p G-alpha subunit and functions in a Ras-independent pathway. EMBO Journal 1998, 17:1996-2007.
147. Yokoyama E., Arakawa M., Yamagishi K., Hara A. Phylogenetic and structural analyses of the mating-type loci in Clavicipitaceae. FEMS Microbiology Letter 2006, 264:182-191.
148. Zhang S., Widemann E., Bernard G., Lesot A., Pinot F., Pedrini N., Keyhani N.O. CYP52X1, representing new cytochrome P450 subfamily, displays fatty acid hydroxylase activity and contributes to virulence and growth on insect cuticular substrates in entomopathogenic fungus Beauveria bassiana. Journal of Biological Chemistry 2012, 287:13477-13486.
149. Zhang S.Z., Xia Y.X., Keyhani N.O. Contribution of the gas1 gene of the entomopathogenic fungus Beauveria bassiana, encoding a putative glycosylphosphatidylinositol-anchored beta-1,3-glucanosyltransferase, to conidial thermotolerance and virulence. Applied and Environmental Microbiology 2011, 77:2676-2684.
150. Zhang Y., Zhao J., Fang W., Zhang J., Luo Z., Zhang M., Pei Y. Mitogen-activated protein kinase hog1 in the entomopathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Applied and Environmental Microbiology 2009, 75:3787-3795.
151. Zhao H., Xu C., Lu H.L., Chen X., St.Leger R.J., Fang W. Host-to-pathogen gene transfer facilitated infection of insects by a pathogenic fungus. PLoS Pathogens 2014, 10:e10040.
152. Zheng P., Xia Y., Xiao G., Xiong C., Hu X., Zhang S., Wang C.S. Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biology 2011, 12:R116.
153. Zheng P., Xia Y., Zhang S., Wang C. Genetics of Cordyceps and related fungi. Applied Microbiology and Biotechnology 2013, 97:2797-2804.