Utilizing Genomics to Study Entomopathogenicity in the Fungal Phylum Entomophthoromycota. A Review of Current Genetic Resources.

Advances in Genetics

Volumn 94, Issue , 2016, Pages 41-65

  De Fine Licht, H H ^a   Hajek, A E ^b   Eilenberg, J ^a   Jensen, A B ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b Cornell University ^*  (United States)

Author keywords

Basal fungi; Genomics; Host pathogen genetics; Nonmodel organisms; Transcriptomics

Indexed keywords

ANIMAL; EVOLUTION; FUNGAL GENOME; FUNGUS; GENOMICS; HOST PATHOGEN INTERACTION; INSECT; MICROBIOLOGY; PATHOGENICITY; PHYLOGENY; PROCEDURES;

ANIMALS; BIOLOGICAL EVOLUTION; FUNGI; GENOME, FUNGAL; GENOMICS; HOST-PATHOGEN INTERACTIONS; INSECTS; PHYLOGENY;

EID: 84958078725     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.adgen.2016.01.003     Document Type: Article

References (116)

1. Andersson K.-M., Kumar D., Bentzer J., Friman E., Ahren D., Tunlid A. Interspecific and host-related gene expression patterns in nematode-trapping fungi. BMC Genomics 2014, 15:968.
2. Bałazy S. Flora of Poland. Fungi (Mycota), vol XXIV, Entomophthorales 1993, Polish Academy of Sciences, Krakow, Poland.
3. Beauvais A., Latgé J.-P., Vey A., Prevost M.-C. The role of surface components of the entomopathogenic fungus Entomophaga aulicae in the cellular immune response of Galleria mellonella (Lepidoptera). Microbiology 1989, 135:489-498.
4. Becker F., Schnorr K., Wilting R., Tolstrup N., Bendtsen J.D., Olsen P.B. Development of in vitro transposon assisted signal sequence trapping and its use in screening Bacillus halodurans C125 and Sulfolobus solfataricus P2 gene libraries. Journal of Microbiological Methods 2004, 57:123-133.
5. Bidochka M.J., Hajek A.E. Protoplast plasma membrane glycoproteins in two species. Mycological Research 1996, 100:1094-1098.
6. Bidochka M.J., Walsh S.R., Ramos M.E., St.Leger R.J., Silver J.C., Roberts D.W. Pathotypes in the Entomophaga grylli species complex of grasshopper pathogens differentiated with random amplification of polymorphic DNA and cloned-DNA probes. Applied and Environmental Microbiology 1995, 61:556-560.
7. Blackwell M. The fungi: 1, 2, 3. . . 5.1 million species?. American Journal of Botany 2011, 98:426-438.
8. Boomsma J.J., Jensen A.B., Meyling N.V., Eilenberg J. Evolutionary interaction networks of insect pathogenic fungi. Annual Review of Entomology 2014, 59:467-485.
9. Brey P.T., Latgé J.P., Prevost M.C. Integumental penetration of the pea aphid, Acyrthosiphon pisum, by Conidiobolus obscurus (Entomophthoraceae). Journal of Invertebrate Pathology 1986, 48:34-41.
10. Brown G.D., Denning D.W., Gow N.A.R., Levitz S.M., Netea M.G., White T.C. Hidden killers: human fungal infections. Science Translational Medicine 2012, 4:165rv13.
11. Brown S.P., Cornforth D.M., Mideo N. Evolution of virulence in opportunistic pathogens: generalism, plasticity, and control. Trends in Microbiology 2012, 20:336-342.
12. Burmester A., Shelest E., Glöckner G., Heddergott C., Schindler S., Staib P., Brakhage A.A. Comparative and functional genomics provide insights into the pathogenicity of dermatophytic fungi. Genome Biology 2011, 12:R7.
13. Castrillo L.A., Thomsen L., Juneja P., Hajek A.E. Detection and quantification of Entomophaga maimaiga resting spores in forest soil using real-time PCR. Mycological Research 2007, 111:324-331.
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. Charnley A.K. Fungal pathogens of insects: cuticle degrading enzymes and toxins. Advances in Botanical Research 2003, 40:242-321.
16. Chayakulkeeree M., Ghannoum M.A., Perfect J.R. Zygomycosis: the re-emerging fungal infection. European Journal of Clinical Microbiology & Infectious Diseases 2006, 25:215-229.
17. Claydon N. Insecticidal secondary metabolites from entomogenous fungi: Entomophthora virulenta. Journal of Invertebrate Pathology 1978, 32:319-324.
18. Delalibera I., Hajek A.E., Humber R.A. Neozygites tanajoae sp. nov., a pathogen of the cassava green mite. Mycologia 2004, 96:1002-1009.
19. Dunphy G.B., Nolan R.A. Mycotoxin production by the protoplast stage of Entomophthora egressa. Journal of Invertebrate Pathology 1982, 39:261-263.
20. Donzelli B.G.G., Krasnoff S.B. Molecular Genetics of Secondary Chemistry in Metarhizium Fungi. Advances in Genetics 2016, 94:365-436.
21. Eilenberg J., Bresciani J., Latgé J.P. Ultrastructural studies of primary spore formation and discharge in the genus Entomophthora. Journal of Invertebrate Pathology 1986, 48:318-324.
22. Eilenberg J., Bresciani J., Olesen U., Olson L. Ultrastructural studies of secondary spore formation and discharge in the genus Entomophthora. Journal of Invertebrate Pathology 1995, 65:179-185.
23. Eilenberg J., Michelsen V. Natural host range and prevalence of the genus Strongwellsea (Zygomycota: Entomophthorales) in Denmark. Journal of Invertebrate Pathology 1999, 73:189-198.
24. Einax E., Voigt K. Oligonucleotide primers for the universal amplification of beta-tubulin genes facilitate phylogenetic analyses in the regnum fungi. Organisms Diversity & Evolution 2003, 3:185-194.
25. Evans H.C. Mycopathogens of insects of epigeal and aerial habitats. Insect-fungus interactions 1989, 205-238. Academic Press, London. N. Wilding, N.M. Collins, P.M. Hammond, J.F. Weber (Eds.).
26. Fisher M.C., Henk D.A., Briggs C.J., Brownstein J.S., Madoff L.C., McCraw S.L., Gurr S.J. Emerging fungal threats to animal, plant and ecosystem health. Nature 2012, 484:186-194.
27. Fournier A., Enkerli J., Keller S., Widmer F. A PCR-based tool for the cultivation-independent monitoring of Pandora neoaphidis. Journal of Invertebrate Pathology 2008, 99:49-56.
28. Fournier A., Widmer F., Enkerli J. Development of a single-nucleotide polymorphism (SNP) assay for genotyping of Pandora neoaphidis. Fungal Biology 2010, 114:498-506.
29. Freimoser F.M., Jensen A.B., Tuor U., Aebi M., Eilenberg J. Isolation and in vitro cultivation of the aphid pathogenic fungus Entomophthora planchoniana. Canadian Journal of Microbiology 2001, 47:1082-1087.
30. Freimoser F.M., Screen S., Hu G., St.Leger EST analysis of genes expressed by the zygomycete pathogen Conidiobolus coronatus during growth on insect cuticle. Microbiology 2003, 149:1893-1900.
31. 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.
32. 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.
33. Gregory T.R., Nicol J.A., Tamm H., Kullman B., Kullman K., Leitch I.J., Bennett M.D. Eukaryotic genome size databases. Nucleic Acids Research 2007, 35:D332-D338.
34. Grell M.N., Jensen A.B., Olsen P.B., Eilenberg J., Lange L. Secretome of fungus-infected aphids documents high pathogen activity and weak host response. Fungal Genetics and Biology 2011, 48:343-352.
35. Gryganskyi A.P., Humber R.A., Smith M.E., Hodge K., Huang B., Voigt K., Vilgalys R. Phylogenetic lineages in Entomophthoromycota. Persoonia - Molecular Phylogeny and Evolution of Fungi 2013, 30:94-105.
36. Gryganskyi A.P., Humber R.A., Smith M.E., Miadlikovska J., Wu S., Voigt K., Vilgalys R. Molecular phylogeny of the Entomophthoromycota. Molecular Phylogenetics and Evolution 2012, 65:682-694.
37. Gryganskyi A.P., Humber R.A., Stajich J.E., Mullens B., Anishchenko I.M., Vilgalys R. Sequential utilization of hosts from different fly families by genetically distinct, sympatric populations within the Entomophthora muscae species complex. PLoS One 2013, 8:e71168.
38. Gryganskyi A.P., Lee S.C., Litvintseva A.P., Smith M.E., Bonito G., Porter T.M., Vilgalys R. Structure, function, and phylogeny of the mating locus in the Rhizopus oryzae complex. PLoS One 2010, 5:e15273.
39. Gryganskyi A.P., Muszewska A. Whole genome sequencing and the Zygomycota. Fungal Genomics & Biology 2014, 04:e116.
40. Guzmán-Franco A.W., Atkins S.D., Alderson P.G., Pell J.K. Development of species-specific diagnostic primers for Zoophthora radicans and Pandora blunckii; two co-occurring fungal pathogens of the diamondback moth, Plutella xylostella. Mycological Research 2008, 112:1227-1240.
41. Guzmán-Franco A.W., Atkins S.D., Clark S.J., Alderson P.G., Pell J.K. Use of quantitative PCR to understand within-host competition between two entomopathogenic fungi. Journal of Invertebrate Pathology 2011, 107:155-158.
42. Hajek A.E. Introduction of a fungus into North America for control of gypsy moth. Biological control: International case studies 2007, 53-62. CABI Publishing, UK. C. Vincent, M. Goettel, G. Lazarovits (Eds.).
43. Hajek A.E., Butler L., Walsh S., Silver J.C., Hain F.P., Hastings F.L., Hain F.P. Host range of the gypsy moth (Lepidoptera: Lymantriidae) pathogen Entomophaga maimaiga (Zygomycetes: Entomophthorales) in the field versus laboratory. Environmental Entomology 1996, 25:709-721.
44. Hajek A.E., Hodge K.T., Liebherr J.K., Day W.H., Vandenberg J.D. Use of RAPD analysis to trace the origin of the weevil pathogen Zoophthora phytonomi in North America. Mycological Research 1996, 100:349-355.
45. Hajek A.E., Humber R.A., Elkinton J.S., May B., Walsh S., Silver J.C. Allozyme and restriction fragment length polymorphism analyses confirm Entomophaga maimaiga responsible for 1989 epizootics in North American gypsy moth populations. Proceedings of the National Academy of Sciences of the United States of America 1990, 87:6979-6982.
46. Hajek A.E., Humber R.A., Walsh S., Silver J.C. Sympatric occurrence of two Entomophaga aulicae (Zygomycetes: Entomophthorales) complex species attacking forest Lepidoptera. Journal of Invertebrate 1991, 58:373-380.
47. Hajek A.E., Jensen A.B., Thomsen L., Hodge K.T., Eilenberg J. PCR-RFLP is used to investigate relations among species in the entomopathogenic genera Eryniopsis and Entomophaga. Mycologia 2003, 95:262-268.
48. Hajek A.E., Walsh S.R., Strong D.R., Silver J.C. A disjunct Californian strain of Entomophaga aulicae infecting Orgyia vetusta. Journal of Invertebrate Pathology 1996, 68:260-268.
49. Henk D.A., Fisher M.C. The gut fungus Basidiobolus ranarum has a large genome and different copy numbers of putatively functionally redundant elongation factor genes. PLoS One 2012, 7:e31268.
50. Hibbett D.S., Binder M., Bischoff J.F., Blackwell M., Cannon P.F., Eriksson O.E., Zhang N. A higher-level phylogenetic classification of the fungi. Mycological Research 2007, 111:509-547.
51. Hodge K.T., Sawyer A.J., Humber R.A. RAPD-PCR for identification of Zoophthora radicans isolates in biological control of the potato leafhopper. Journal of Invertebrate Pathology 1995, 65:1-9.
52. 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.
53. Hu X., Xiao G., Zheng P., Shang Y., Su Y., Zhang X., Wang C. 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.
54. 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.
55. Humber R.A. Strongwellsea vs. Erynia: the case for a phylogenetic classification of the Entomophthorales (Zygomycetes). Mycotaxon 1982, 15:167-184.
56. Humber R.A. Synopsis of a revised classification for the Entomophthorales (Zygomycotina). Mycotaxon 1989, 34:441-460.
57. Humber R.A. Evolution of entomopathogenicity in fungi. Journal of Invertebrate Pathology 2008, 98:262-266.
58. Humber R.A. Entomophthoromycota: a new phylum and reclassification for entomophthoroid fungi. Mycotaxon 2012, 120:477-492.
59. James T.Y., Kauff F., Schoch C.L., Matheny P.B., Hofstetter V., Cox C.J., Vilgalys R. Reconstructing the early evolution of fungi using a six-gene phylogeny. Nature 2006, 443:818-822.
60. Jensen A.B., Dromph K.M. The causal agents of "entomophthoramycosis" belong to two different orders: a suggestion for modification of the clinical nomenclature. Clinical Microbiology and Infection 2005, 11:249-250.
61. Jensen A.B., Eilenberg J. Genetic variation within the insect-pathogenic genus Entomophthora, focusing on the E. muscae complex, using PCR-RFLP of the ITS II and the LSU rDNA. Mycological Research 2001, 105:307-312.
62. Jensen A.B., Eilenberg J.R., Lopez Lastra C. Differential divergences of obligately insect-pathogenic Entomophthora species from fly and aphid hosts. FEMS Microbiology Letters 2009, 300:180-187.
63. Jensen A.B., Gargas A., Eilenberg J., Rosendahl S. Relationships of the insect-pathogenic order Entomophthorales (Zygomycota, Fungi) based on phylogenetic analyses of nuclear small subunit ribosomal DNA sequences (SSU rDNA). Fungal Genetics and Biology 1998, 24:325-334.
64. Jensen A.B., Hansen L.M., Eilenberg J. Grain aphid population structure: no effect of fungal infections in a 2-year field study in Denmark. Agricultural and Forest Entomology 2008, 10:279-290.
65. Jensen A.B., Thomsen L., Eilenberg J. Intraspecific variation and host specificity of Entomophthora muscae sensu stricto isolates revealed by random amplified polymorphic DNA, universal primed PCR, PCR-restriction fragment length polymorphism, and conidial morphology. Journal of Invertebrate Pathology 2001, 78:251-259.
66. Jensen A.B., Thomsen L., Eilenberg J. Value of host range, morphological, and genetic characteristics within the Entomophthora muscae species complex. Mycological Research 2006, 110:941-950.
67. Keeling P.J. Congruent evidence from α-tubulin and β-tubulin gene phylogenies for a zygomycete origin of microsporidia. Fungal Genetics and Biology 2003, 38:298-309.
68. Keller S. Arthropod-pathogenic Entomophthorales of Switzerland. II. Erynia, Eryniopsis, Neozygites, Zoophthora and Tarichium. Sydowia 1991, 43:39-122.
69. Krasnoff S.B., Watson D.W., Gibson D.M., Kwan E.C. Behavioral effects of the entomopathogenic fungus, Entomophthora muscae on its host Musca domestica: postural changes in dying hosts and gated pattern of mortality. Journal of Insect Physiology 1995, 41:895-903.
70. Latgé J.P., Eilenberg J., Beauvais A., Prevost M.C. Morphology of Entomophthora muscae protoplasts grown in vitro. Protoplasma 1988, 146:166-173.
71. Lee T., Yun S.H., Hodge K.T., Humber R.A., Krasnoff S.B., Turgeon G.B., Gibson D.M. Polyketide synthase genes in insect- and nematode-associated fungi. Applied Microbiology and Biotechnology 2001, 56:181-187.
72. Lihme M., Jensen A.B., Rosendahl S. Local scale population genetic structure of Entomophthora muscae epidemics. Fungal Ecology 2009, 2:81-86.
73. Liu X.-Y., Voigt K. Molecular characters of zygomycetous fungi. Molecular identification of fungi 2010, 461-488. Springer Berlin Heidelberg, Berlin, Heidelberg. Y. Gherbawy, K. Voigt (Eds.).
74. Lopez Lastra C.C., Gibson D.M., Hajek A.E. Survival and differential development of Entomophaga maimaiga and Entomophaga aulicae (Zygomycetes: Entomophthorales) in Lymantria dispar hemolymph. Journal of Invertebrate Pathology 2001, 78:201-209.
75. Ma L.-J., Ibrahim A.S., Skory C., Grabherr M.G., Burger G., Butler M., Wickes B.L. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genetics 2009, 5:e1000549.
76. Małagocka J., Grell M.N., Lange L., Eilenberg J., Jensen A.B. Transcriptome of an entomophthoralean fungus (Pandora formicae) shows molecular machinery adjusted for successful host exploitation and transmission. Journal of Invertebrate Pathology 2015, 128:47-56.
77. Manning R.J., Waters S.D., Callaghan A.A. Saprotrophy of Conidiobolus and Basidiobolus in leaf litter. Mycological Research 2007, 111:1437-1449.
78. Martinez D.A., Oliver B.G., Graser Y., Goldberg J.M., Li W., Martinez-Rossi N.M., White T.C. Comparative genome analysis of Trichophyton rubrum and related dermatophytes reveals candidate genes involved in infection. mBio 2012, 3:e00259-e00312.
79. Meerupati T., Andersson K.-M., Friman E., Kumar D., Tunlid A., Ahrén D. Genomic mechanisms accounting for the adaptation to parasitism in nematode-trapping fungi. PLoS Genetics 2013, 9:e1003909.
80. Milne R., Wright T., Welton M., Budau C. Identification and partial purification of a cell-lytic factor from Entomophaga aulicae. Journal of Invertebrate Pathology 1994, 54:253-259.
81. Möbius N., Hertweck C. Fungal phytotoxins as mediators of virulence. Current Opinion in Plant Biology 2009, 12:390-398.
82. Morales-Vidal S., Alatorre-Rosas R., Clark S.J., Pell J.K., Guzmán-Franco A.W. Competition between isolates of Zoophthora radicans co-infecting Plutella xylostella populations. Journal of Invertebrate Pathology 2013, 113:137-145.
83. Murrin F., Holtby J., Noland R.A., Davidson W.S. The genome of Entomophaga aulicae (Entomophthorales, Zygomycetes): base composition and size. Experimental Mycology 1986, 10:67-75.
84. Nagahama T., Sato H., Shimazu M., Sugiyama J. Phylogenetic divergence of the entomophthoralean fungi - evidence from nuclear 18s ribosomal-RNA gene-sequences. Mycologia 1995, 87:203-209.
85. Nielsen C., Milgroom M.G., Hajek A.E. Genetic diversity in the gypsy moth fungal pathogen Entomophaga maimaiga from founder populations in North America and source populations in Asia. Mycological Research 2005, 109:941-950.
86. Olive E.W. Cell and nuclear division in Basidiobolus. Annales Mycologici 1907, 5:404-418.
87. Prabhu R.M., Patel R. Mucormycosis and entomophthoramycosis: a review of the clinical manifestations, diagnosis and treatment. Clinical Microbiology and Infection 2004, 10:31-47.
88. Raffaele S., Kamoun S. Genome evolution in filamentous plant pathogens: why bigger can be better. Nature Reviews Microbiology 2012, 10:417-430.
89. Reddy T.B.K., Thomas A.D., Stamatis D., Bertsch J., Isbandi M., Jansson J., Kyrpides N.C. The Genomes OnLine Database (GOLD) v.5: a metadata management system based on a four level (meta)genome project classification. Nucleic Acids Research 2015, 43:D1099-D1106.
90. Ribes J.A., Vanover-Sams C.L., Baker D.J. Zygomycetes in human disease. Clinical Microbiology Reviews 2000, 13:236-301.
91. Riddle L.W. On the cytology of the Entomophthoraceae. Proceedings of the American Academy of Arts and Sciences 1906, 42:177-198.
92. Robinow C.F. Observations on cell growth, mitosis, and division in the fungus Basidiobolus ranarum. The Journal of Cell Biology 1963, 17:123-152.
93. Rosenblum E.B., Stajich J.E., Maddox N., Eisen M.B. Global gene expression profiles for life stages of the deadly amphibian pathogen Batrachochytrium dendrobatidis. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:17034-17039.
94. Roy H.E., Steinkraus D.C., Eilenberg J., Hajek A.E., Pell J.K. Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology 2006, 51:331-357.
95. Sawyer W.H. The development of Entomophthora sphaerosperma upon Rhopobota vacciniana. Annals of Botany 1933, 47:799-809.
96. Schussler A., Schwarzott D., Walker C. A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycological Research 2001, 105:1413-1421.
97. Scorsetti A.C., Jensen A.B., Lopez Lastra C., Humber R.A. First report of Pandora neoaphidis resting spore formation in vivo in aphid hosts. Fungal Biology 2012, 116:196-203.
98. Shelest E., Voigt K. Genomics to study basal lineage fungal biology: phylogenomics suggests a common origin. Fungal genomics 2014, Vol. 13:31-60. Springer Verlag, Berlin. 2nd ed.
99. Sun N.C., Bowen C.C. Ultrastructural studies of nuclear division in Basidiobolus ranarum Eidam. Caryologia 1972, 25:471-494.
100. Tanabe Y. Molecular phylogeny of parasitic Zygomycota (Dimargaritales, Zoopagales) based on nuclear small subunit ribosomal DNA sequences. Molecular Phylogenetics and Evolution 2000, 16:253-262.
101. Tanabe Y., Saikawa M., Watanabe M.M., Sugiyama J. Molecular phylogeny of Zygomycota based on EF-1α and RPB1 sequences: limitations and utility of alternative markers to rDNA. Molecular Phylogenetics and Evolution 2004, 30:438-449.
102. Thomsen L., Beauvais A. Cloning of two chitin synthase gene fragments from a protoplastic entomophthorale. FEMS Microbiology Letters 1995, 129:115-120.
103. Thomsen L., Jensen A.B. Application of nested-PCR technique to resting spores from the Entomophthora muscae species complex: implications for analyses of host-pathogen population interactions. Mycologia 2002, 94:794-802.
104. Van Houte S., Ros V.I.D., van Oers M.M. Walking with insects: molecular mechanisms behind parasitic manipulation of host behaviour. Molecular Ecology 2013, 22:3458-3475.
105. Vega F.E., Meyling N.V., Luangsa-ard J.J., Blackwell M. Fungal entomopathogens. Insect pathology 2012, 171-220. Elsevier Inc, London. F.E. Vega, H.K. Kaya (Eds.).
106. Vikram H.R., Smilack J.D., Leighton J.A., Crowell M.D., De Petris G. Emergence of gastrointestinal basidiobolomycosis in the United States, with a review of worldwide cases. Clinical Infectious Diseases 2012, 54:1685-1691.
107. Voigt K., Cigelnik E., O'Donnell K. Phylogeny and PCR identification of clinically important zygomycetes based on nuclear ribosomal-DNA sequence data. Journal of Clinical Microbiology 1999, 37:3957-3964.
108. Walsh S.R.A. Development of molecular markers for the detection and differentiation of Entomophaga strains pathogenic for insects 1996, (Ph.D. dissertation), University of Toronto, Canada.
109. Wang C., St.Leger R.J. Genomics of entomopathogenic fungi. The ecological genomics of fungi 2014, 243-260. John Wiley & Sons, Inc, Hoboken. F. Martin (Ed.).
110. Wang J.B., St.Leger R.J., Wang C. Advances in Genomics of Insect Pathogenic Fungi. Advances in Genetics 2016, 94:67-105.
111. Willis J.H. Structural cuticular proteins from arthropods: annotation, nomenclature, and sequence characteristics in the genomics era. Insect Biochemistry and Molecular Biology 2010, 40:189-204.
112. Xu J., Baldwin D., Kindrachuk C., Hegedus D.D. Serine proteases and metalloproteases associated with pathogenesis but not host specificity in the Entomophthoralean fungus Zoophthora radicans. Canadian Journal of Microbiology 2006, 52:550-559.
113. Xu J., Baldwin D., Kindrachuk C., Hegedus D.D. Comparative EST analysis of a Zoophthora radicans isolate derived from Pieris brassicae and an isogenic strain adapted to Plutella xylostella. Microbiology 2009, 155:174-185.
114. Yang J., Wang L., Ji X., Feng Y., Li X., Zou C., Zhang K.Q. Genomic and proteomic analyses of the fungus Arthrobotrys oligospora provide insights into nematode-trap formation. PLoS Pathogens 2011, 7:e1002179.
115. Yendol W.G., Miller E.M., Behnke C.N. Toxic substances from entomophthoraceous fungi. Journal of Invertebrate Pathology 1968, 10:313-319.
116. Zheng P., Xia Y., Xiao G., Xiong C., Hu X., Zhang S., Wang C. Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biology 2011, 12:R116.