Insect Pathogenic Fungi as Endophytes

Advances in Genetics

Volumn 94, Issue , 2016, Pages 107-135

  Moonjely, S ^a   Barelli, L ^a   Bidochka, M J ^a  

^a BROCK UNIVERSITY   (Canada)

Author keywords

Beauveria; Endophyte; Host switching; Insect pathogen; Metarhizium; Pathogen evolution

Indexed keywords

BIOLOGICAL CONTROL AGENT;

ANIMAL; BEAUVERIA; BIOLOGICAL CONTROL AGENT; ENDOPHYTE; EVOLUTION; FUNGUS; GENETICS; INSECT; METARHIZIUM; MICROBIOLOGY; PATHOGENICITY; PHYSIOLOGY; PLANT; SECONDARY METABOLISM; SYMBIOSIS;

ANIMALS; BEAUVERIA; BIOLOGICAL CONTROL AGENTS; BIOLOGICAL EVOLUTION; ENDOPHYTES; FUNGI; INSECTS; METARHIZIUM; PLANTS; SECONDARY METABOLISM; SYMBIOSIS;

EID: 84958268068     PISSN: 00652660     EISSN: None     Source Type: Book Series    
DOI: 10.1016/bs.adgen.2015.12.004     Document Type: Article

References (144)

1. Ahmad J.S., Baker R. Rhizosphere competence of Trichoderma harzianum. Phytopathology 1987, 77:182-189.
2. Alam S.M. Nutrient uptake by plants under stress conditions. Handbook of plant and crop stress 1999, 285-314. Marcel Dekker, New York. M. Pessakakli (Ed.).
3. Aly A.H., Debbab A., Proksch P. Fungal endophytes: unique plant inhabitants with great promises. Applied Microbiology and Biotechnology 2011, 90:1829-1845.
4. Bagga S., Hu G., Screen S.E., St.Leger R.J. Reconstructing the diversification of subtilisins in the pathogenic fungus Metarhizium anisopliae. Gene 2004, 324:159-169.
5. Behie S.W., Bidochka M.J. Ubiquity of insect-derived nitrogen transfer to plants by endophytic insect-pathogenic fungi: an additional branch of the soil nitrogen cycle. Science 2014, 80:1553-1560.
6. Behie S.W., Jones S.J., Bidochka M.J. Plant tissue localization of the endophytic insect pathogenic fungi Metarhizium and Beauveria. Fungal Ecology 2015, 13:112-119.
7. Behie S.W., Padilla-Guerrero I.E., Bidochka M.J. Nutrient transfer to plants by phylogenetically diverse fungi suggests convergent evolutionary strategies in rhizospheric symbionts. Communicative and Integrative Biology 2013, 6:e22321.
8. Behie S.W., Zelisko P.M., Bidochka M.J. Endophytic insect-parasitic fungi translocate nitrogen directly from insects to plants. Science 2012, 336:1576-1577.
9. Berg G., Faithfull I.G., Powell K.S., Bruce R.J., Williams D.G., Yen A.L. Biology and management of the redheaded pasture cockchafer Adoryphorus couloni (Burmeister)(Scarabaeidae: Dynastinae) in Australia: a review of current knowledge. Austral Entomology 2014, 53:144-158.
10. 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.
11. Bidochka, M. J., St. Leger, R. J., Roberts, D. W. (1997). Mechanisms of deuteromycete fungal infections in grasshoppers and locusts: an overview. In M. S. Goettel & D. L. Johnson (Eds.), Microbial control of grasshoppers and locusts. Memoirs of the Entomological Society of Canada, 171, 213-224.
12. Blanford S., Chan B.H.K., Jenkins N., Sim D., Turner R.J., Read A.F., Thomas M.B. Fungal pathogen reduces potential for malaria transmission. Science 2005, 308:1638-1641.
13. Bonfante P., Genre A. Mechanisms underlying beneficial plant-fungus interactions in mycorrhizal symbiosis. Nature Communications 2010, 1:48.
14. Boucias D.G., Pendland J.C., Latge J.P. Nonspecific factors involved in attachment of entomopathogenic deuteromycetes to host insect cuticle. Applied and Environmental Microbiology 1988, 54:1795-1805.
15. Carollo C.A., Calil A.L.A., Schiave L.A., Guaratini T., Roberts D.W., Lopes N.P., Braga G.U. Fungal tyrosine betaine, a novel secondary metabolite from conidia of insect pathogenic Metarhizium spp. fungi. Fungal Biology 2010, 114:473-480.
16. Castrillo L.A., Griggs M.H., Ranger C.M., Reding M.E., Vandenberg J.D. Virulence of commercial strains of Beauveria bassiana and Metarhizium brunneum (Ascomycota: Hypocreales) against adult Xylosandrus germanus (Coleoptera: Curculionidae) and impact on brood. Biological Control 2011, 58:121-126.
17. Donzelli B.G.G., Krasnoff S.B. Molecular Genetics of Secondary Chemistry in Metarhizium Fungi. Advances in Genetics 2016, 94:365-436.
18. Elena G.J., Beatriz P.J., Alejandro P., Lecuona R.E. Metarhizium anisopliae (Metschnikoff) Sorokin promotes growth and has endophytic activity in tomato plants. Advanced Biomedical Research 2011, 5:22-27.
19. Fan Y., Borovsky D., Hawkings C., Ortiz-Urquiza A., Keyhani N.O. Exploiting host molecules to augment mycoinsecticide virulence. Nature Biotechnology 2012, 30:35-37.
20. Fan Y.H., Fang W.G., Guo S.J., Pei X.Q., Zhang Y.J., Xiao Y.H., Pei Y. Increased insect virulence in Beauveria bassiana strains over expressing an engineered chitinase. Applied and Environmental Microbiology 2007, 73:295-302.
21. Fan Y.H., Pei X.Q., Guo S.J., Zhang Y.J., Luo Z.B., Liao X.G., Pei Y. Increased virulence using engineered protease-chitin binding domain hybrid expressed in the insect pathogenic fungus Beauveria bassiana. Microbial Pathogenesis 2010, 49:376-380.
22. Fang W.G., Feng J., Fan Y.H., Zhang Y.J., Bidochka M.J., Leger R.J.S., Pei Y. Expressing a fusion protein with protease and chitinase activities increases the virulence of the insect pathogen Beauveria bassiana. Journal of Invertebrate Pathology 2009, 102:155-159.
23. Fang W., Lu H.L., King G.F., St.Leger R.J. Construction of a hypervirulent and specific mycoinsecticide for locust control. Scientific Reports 2014, 4.
24. Fang W., Pava-Ripoll M., Wang S., Leger R.S. Protein kinase A regulates production of virulence determinants by the entomopathogenic fungus, Metarhizium anisopliae. Fungal Genetics and Biology 2009, 46:277-285.
25. Fang W., Pei Y., Bidochka M.J. A regulator of a G protein signalling (RGS) gene, cag8, from the insect-pathogenic fungus Metarhizium anisopliae is involved in conidiation, virulence and hydrophobin synthesis. Microbiology 2007, 153:1017-1025.
26. Fang W., 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.
27. Fang W., St.Leger R.J. Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi. PLoS One 2012, 7(8):e43069. 10.1371/journal.pone.0043069.
28. Faria M.R., Wraight S.P. Mycoinsecticides and mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biological Control 2007, 43:237-256.
29. Fellbaum C.R., Gachomo E.W., Beesetty Y., Choudhari S., Strahan G.D., Pfeffer P.E., Bücking H. Carbon availability triggers fungal nitrogen uptake and transport in arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:2666-2671.
30. Fujii Y., Tani H., Ichinoe M., Nakajima H. Zygosporin D and two new cytochalasins produced by the fungus Metarhizium anisopliae. Journal of Natural Products 2000, 63:132-135.
31. Gao Q., Jin K., Ying S.H., Zhang Y., Xiao G., Shang Y., Wang C. Genome sequencing and comparative transcriptomics of the model insect pathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genetics 2011, 10.1371/journal.pgen.1001264.
32. Garyali S., Reddy M.S. Taxol production by an endophytic fungus, Fusarium redolens, isolated from Himalayan yew. Journal of Microbiology and Biotechnology 2013, 23:1372-1380.
33. Geremia R.A., Goldman G.H., Jacobs D., Ardiles W., Vila S.B., Van Montagu M., Herrera-Estrella A. Molecular characterization of the proteinase-encoding gene, prbl, related to mycoparasitism by Trichoderma harzianum. Molecular Microbiology 1993, 8:603-613.
34. Gibson D.M., Donzelli B.G., Krasnoff S.B., Keyhani N.O. Discovering the secondary metabolite potential encoded within insect pathogenic fungi. Natural Product Reports 2014, 31:1287-1305.
35. Gómez-Vidal S., Salinas J., Tena M., Lopez-Llorca L.V. Proteomic analysis of date palm (Phoenix dactylifera L.) responses to endophytic colonization by entomopathogenic fungi. Electrophoresis 2009, 30:2996-3005.
36. Govindarajulu M., Pfeffer P.E., Jin H., Abubaker J., Douds D.D., Allen J.W., Shachar-Hill Y. Nitrogen transfer in the arbuscular mycorrhizal symbiosis. Nature 2005, 435:819-823.
37. Grogan G.J., Holland H.L. The biocatalytic reactions of Beauveria spp. Journal of Molecular Catalysis B: Enzymatic 2000, 9:1-32.
38. Guether M., Neuhäuser B., Balestrini R., Dynowski M., Ludewig U., Bonfante P. A mycorrhizal-specific ammonium transporter from Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiology 2009, 150:73-83.
39. Gupta S., Krasnoff S.B., Renwick J.A.A., Roberts D.W., Steiner J.R., Clardy J. Viridoxins A and B: novel toxins from the fungus Metarhizium flavoviride. Journal of Organic Chemistry 1993, 58:1062-1067.
40. Harman G.E. Overview of mechanisms and uses of Trichoderma spp. Phytopathology 2006, 96:190-194.
41. Harman G.E., Howell C.R., Viterbo A., Chet I., Lorito M. Trichoderma species-opportunistic, avirulent plant symbionts. Nature Reviews Microbiology 2004, 2:43-56.
42. 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.
43. 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.
44. 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.
45. Hu X., Zhang Y., Xiao G, Zheng P., XIA Y., Zhang X Genome survey uncovers the secrets of sex and lifestyle in caterpillar fungus. Chinese Science Bulletin 2013, 58:2846-2854.
46. Huang W., Shang Y., Chen P., Cen K., Wang C. Regulation of bZIP transcription factor MBZ1 on cell wall integrity, spore adherence, and virulence in Metarhizium robertsii. Journal of Biological Chemistry 2015, 10.1074/jbc.M114.630939.
47. Huang W., Shang Y., Chen P., Gao Q., Wang C. MrpacC regulates sporulation, insect cuticle penetration and immune evasion in Metarhizium robertsii. Environmental Microbiology 2015, 17:994-1008.
48. Humber R.A. Evolution of insect pathogenicity in fungi. Journal of Invertebrate Pathology 2008, 98:262-266.
49. Iannone L.J., Cabral D. Effects of the Neotyphodium endophyte status on plant performance of Bromus auleticus, a wild native grass from South America. Symbiosis 2006, 41:61-69.
50. Jackson M.A., Dunlap C.A., Jaronski S.T. Ecological considerations in producing and formulating fungal insect pathogens for use in insect biocontrol. The ecology of fungal insect pathogens 2010, 129-145. Springer, Netherlands.
51. Jaeger C.H., Lindow S.E., Miller W., Clark E., Firestone M.K. Mapping of sugar and amino acid availability in soil around roots with bacterial sensors of sucrose and tryptophan. Applied and Environmental Microbiology 1999, 65:2685-2690.
52. Jakobsen I., Abbott L.K., Robson A.D. External hyphae of vesicular-arbuscular mycorrhizal fungi associated with Trifolium subterraneum L. 1. Spread of hyphae and phosphorus inflow into roots. New Phytologist 1992, 120:371-379.
53. Jha M.N., Jha S., Chourasia S.K. Agroecology and agromicrobes. Agroecology, ecosystems, and sustainability 2015, 81-102. CRC Press, Boca Raton, FL. N. Benkeblia (Ed.).
54. Jin K., Ming Y., Xia Y.X. MaHog1, a Hog1-type mitogen-activated protein kinase gene, contributes to stress tolerance and virulence of the insect pathogenic fungus Metarhizium acridum. Microbiology Sgm 2012, 158:2987-2996.
55. Kawaguchi M., Minamisawa Plant-microbe communications for symbiosis. Plant and Cell Physiology 2010, 51:1377-1380.
56. Khan A.L., Hamayun M., Khan S.A., Kang S.M., Shinwari Z.K., Kamran M., Lee I.J. Pure culture of Metarhizium anisopliae LHL07 reprograms soybean to higher growth and mitigates salt stress. World Journal of Microbiology and Biotechnology 2012, 28:1483-1494.
57. Kiers E.T., Duhamel M., Beesetty Y., Mensah J.A., Franken A., Verbruggen E., Bücking H. Reciprocal rewards stabilize cooperation in the mycorrhizal symbiosis. Science 2011, 333:880-882.
58. Kim J.S., Roh J.Y., Choi J.Y., Shin S.C., Jeon M.J., Je Y.H. Insecticidal activity of Paecilomyces fumosoroseus SFP-198 as a multi-targeting biological control agent against the greenhouse whitefly and the two-spotted spider mite. International Journal of Industrial Entomology 2008, 17:181-187.
59. Kosuta S., Chabaud M., Lougnon G., Gough C., Dénarié J., Barker D.G., Bécard G. A diffusible factor from arbuscular mycorrhizal fungi induces symbiosis-specific MtENOD11 expression in roots of Medicago truncatula. Plant Physiology 2003, 131:952-962.
60. Krasnoff S.B., Keresztes I., Gillilan R.E., Szebenyi D.M., Donzelli B.G., Churchill A.C., Gibson D.M. Serinocyclins A and B, cyclic heptapeptides from Metarhizium anisopliae. Journal of Natural Products 2007, 70:1919-1924.
61. Krasnoff S.B., Sommers C.H., Moon Y.S., Donzelli B.G., Vandenberg J.D., Churchill A.C., Gibson D.M. Production of mutagenic metabolites by Metarhizium anisopliae. Journal of Agricultural and Food Chemistry 2006, 54:7083-7088.
62. Kuboki H., Tsuchida T., Wakazono K., Isshiki K., Kumagai H., Yoshioka T. Mer-f3, 12-hydroxy-ovalicin, produced by Metarhizium sp. f3. Journal of Antibiotics 1999, 52:590-593.
63. Kuc J., Strobel N.E. Induced resistance using pathogens and nonpathogens. Biological control of plant diseases 1992, 295-303. Springer, US.
64. Lee S.Y., Kinoshita H., Ihara F., Igarashi Y., Nihira T. Identification of novel derivative of helvolic acid from Metarhizium anisopliae grown in medium with insect component. Journal of Bioscience and Bioengineering 2008, 105:476-480.
65. Liao X., Lu H.L., Fang W., St Leger R.J. Overexpression of a Metarhizium robertsii HSP25 gene increases thermotolerance and survival in soil. Applied Microbiology and Biotechnology 2013, 98:777-783.
66. Liao X., O'Brien T.R., Fang W., St.Leger R.J. The plant beneficial effects of Metarhizium species correlate with their association with roots. Applied Microbiology and Biotechnology 2014, 98:7089-7096.
67. Liu B.L., Tzeng Y.M. Development and applications of destruxins: a review. Biotechnology Advances 2012, 30:1242-1254.
68. Liu Q., Ying S.H., Li J.G., Tian C.G., Feng M.G. Insight into the transcriptional regulation of Msn2 required for conidiation, multi-stress responses and virulence of two insect pathogenic fungi. Fungal Genetics and Biology 2013, 54:42-51.
69. Li J., Yu L., Yang J., Dong L., Tian B., Yu Z., Zhang K. New insights into the evolution of subtilisin-like serine protease genes in Pezizomycotina. BMC Evolutionary Biology 2010, 10:68.
70. Luo S., He M., Cao Y., Xia Y. The tetraspanin gene MaPls1 contributes to virulence by affecting germination, appressorial function and enzymes for cuticle degradation in the insect pathogenic fungus, Metarhizium acridum. Environmental Microbiology 2013, 15:2966-2979.
71. Luo X.D., Keyhani N.O., Yu X.D., He Z.J., Luo Z.B., Pei Y., Zhang Y.J. The MAP kinase Bbslt2 controls growth, conidiation, cell wall integrity, and virulence in the insect pathogenic fungus Beauveria bassiana. Fungal Genetics and Biology 2012, 49:544-555.
72. Luo Z.B., Qin Y.Q., Pei Y., Keyhani N.O. Ablation of the creA regulator results in amino acid toxicity, temperature sensitivity, pleiotropic effects on cellular development and loss of virulence in the filamentous fungus Beauveria bassiana. Environmental Microbiology 2014, 16:1122-1136.
73. Maillet F., Poinsot V., André O., Puech-Pagès V., Haouy A., Gueunier M., Dénarié J. Fungal lipochitooligosaccharide symbiotic signals in arbuscular mycorrhiza. Nature 2011, 469:58-63.
74. Mehrabi R., Zhao X., Kim Y., Xu J.-R. The cAMP signaling and MAP kinase pathways in plant pathogenic fungi. The Micota 2009, vol V:157-172. Springer-Verlag. 2nd ed. H. Deising (Ed.).
75. Miller T.C., Gubler W.D., Laemmlen F.F., Geng S., Rizzo D.M. Potential for using Lecanicillium lecanii for suppression of strawberry powdery mildew. Biocontrol Science and Technology 2004, 14:215-220.
76. Moraes C.K., Schrank A., Vainstein M.H. Regulation of extracellular chitinases and proteases in the insect pathogen and acaricide Metarhizium anisopliae. Current Microbiology 2003, 46:205-210.
77. Nahar P., Ghormade V., Deshpande M.V. The extracellular constitutive production of chitin deacetylase in Metarhizium anisopliae: possible edge to insect pathogenic fungi in the biological control of insect pests. Journal of Invertebrate Pathology 2004, 85:80-88.
78. Oldroyd G.E.D., Harrison M.J., Paszkowski U. Reprogramming plant cells for endosymbiosis. Science 2009, 324:753-754.
79. Ortiz-Urquiza A., Keyhani N.O. Action on the surface: insect pathogenic fungi versus the insect cuticle. Insects 2013, 4:357-374.
80. Ortiz-Urquiza A., Keyhani N.O. Stress response signaling and virulence: insights from insect pathogenic fungi. Current Genetics 2015, 61:239-249.
81. Ortiz-Urquiza A., Luo Z., Keyhani N.O. Improving mycoinsecticides for insect biological control. Applied Microbiology and Biotechnology 2015, 99:1057-1068.
82. Ownley B.H., Griffin M.R., Klingeman W.E., Gwinn K.D., Moulton J.K., Pereira R.M. Beauveria bassiana: endophytic colonization and plant disease control. Journal of Invertebrate Pathology 2008, 98:267-270.
83. Ownley B.H., Gwinn K.D., Vega F.E. Endophytic fungal insect pathogens with activity against plant pathogens: ecology and evolution. BioControl 2010, 55:113-128.
84. Patrick M., Adlard M.W., Keshavarz T. Production of an indolizidine alkaloid, swainsonine by the filamentous fungus, Metarhizium anisopliae. Biotechnology Letters 1993, 15:997-1000.
85. Pava-Ripoll M., Angelini C., Fang W., Wang S., Posada F.J., St.Leger R.J. The rhizosphere-competent insect pathogen Metarhizium anisopliae expresses a specific subset of genes in plant root exudate. Microbiology 2011, 157:47-55.
86. Pedrini N., Crespo R., Juárez M.P. Biochemistry of insect epicuticle degradation by entomopathogenic fungi. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology 2007, 146:124-137.
87. Pekrul S., Grula E.A. Mode of infection of the corn earworm (Heliothis zea) by Beauveria bassiana as revealed by scanning electron microscopy. Journal of Invertebrate Pathology 1979, 34:238-247.
88. Peng G.X., Xia Y.X. Expression of scorpion toxin LqhIT2 increases the virulence of Metarhizium acridum towards Locusta migratoria manilensis. Journal of Industrial Microbiology and Biotechnology 2014, 41(11):1659-1666.
89. Pickles B.J., Pither J. Still scratching the surface: how much of the 'black box' of soil ectomycorrhizal communities remains in the dark?. New Phytologist 2014, 201:1101-1105.
90. Pilat M.V. Permeability of the chitin of insects to entomogenous fungi. Lenin Academy of Agricultural Sciences (Medicine) Russia 1938, 73-75.
91. Pospelov V.P. Methods of infecting insects with entomogenous fungi. Lenin Academy of Agricultural Sciences Russia 1938, 64-67.
92. Quesada-Moraga E., Herrero N., Zabalgogeazcoa I. Insect pathogenic and nematophagous fungal endophytes. Advances in endophytic research 2014, 85-99. Springer, New Delhi, India. V.C. Verma, A.C. Gange (Eds.).
93. Reddy P.V., Lam C.K., Belanger F.C. Mutualistic fungal endophytes express a proteinase that is homologous to proteases suspected to be important in fungal pathogenicity. Plant Physiology 1996, 111:1209-1218.
94. Rodriguez R.J., Redman R.S., Henson J.M. Symbiotic lifestyle expression by fungal endophytes and the adaptation of plants to stress: unraveling the complexities of intimacy. Mycology Series 2005, 23:683.
95. Rose J.K., Ham K.S., Darvill A.G., Albersheim P. Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counter defense mechanism by plant pathogens. Plant Cell 2002, 14:1329-1345.
96. Rovira A.D. Plant root exudates. Botanical Review 1969, 35:35-57.
97. Ruijter G.J.G., Bax M., Patel H., Flitter S.J., van de Vondervoort P.J.I., de Vries R.P., Visser J. Mannitol is required for stress tolerance in Aspergillus niger conidiospores. Eukaryotic Cell 2003, 2:690-698.
98. Santi L., da Silva W.O.B., Berger M., Guimarães J.A., Schrank A., Vainstein M.H. Conidial surface proteins of Metarhizium anisopliae: source of activities related with toxic effects, host penetration and pathogenesis. Toxicon 2010, 55:874-880.
99. Sasan R.K., Bidochka M.J. The insect-pathogenic fungus Metarhizium robertsii (Clavicipitaceae) is also an endophyte that stimulates plant root development. American Journal of Botany 2012, 99:101-107.
100. Sasan R.K., Bidochka M.J. Antagonism of the endophytic insect pathogenic fungus Metarhizium robertsii against the bean plant pathogen Fusarium solani f. sp. phaseoli. Canadian Journal of Plant Pathology 2013, 35:288-293.
101. Scharf D.H., Heinekamp T., Brakhage A.A. Human and plant fungal pathogens: the role of secondary metabolites. PLoS Pathogens 2014, 10.1371/journal.ppat.1003859.
102. Scholte E.J., Knols B.G., Takken W. Infection of the malaria mosquito Anopheles gambiae with the entomopathogenic fungus Metarhizium anisopliae reduces blood feeding and fecundity. Journal of Invertebrate Pathology 2006, 91:43-49.
103. Schrank A., Vainstein M.H. Metarhizium anisopliae enzymes and toxins. Toxicon 2010, 56:1267-1274.
104. Screen S.E., St.Leger R.J. Cloning, expression, and substrate specificity of a fungal chymotrypsin - evidence for lateral gene transfer from an actinomycete bacterium. Journal of Biological Chemistry 2000, 275:6689-6694.
105. Sevim A., Donzelli B.G., Wu D., Demirbag Z., Gibson D.M., Turgeon B.G. Hydrophobin genes of the entomopathogenic fungus, Metarhizium brunneum, are differentially expressed and corresponding mutants are decreased in virulence. Current Genetics 2012, 58:79-92.
106. Shakeri J., Foster H.A. Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzyme and Microbial Technology 2007, 40:961-968.
107. Small C.L.N., Bidochka M.J. Up-regulation of Pr1, a subtilisin-like protease, during conidiation in the insect pathogen Metarhizium anisopliae. Mycological Research 2005, 109:307-313.
108. Spatafora J.W., Sung G.H., Sung H.M., Hywel-Jones L., White J.F. Phylogenetic evidence for an animal pathogen origin of ergot and the grass endophytes. Molecular Ecology 2007, 16:1701-1711.
109. Srivastava C.N., Maurya P., Sharma P., Mohan L. Prospective role of insecticides of fungal origin: Review. Entomological Research 2009, 39:341-355.
110. St Leger R.J. The role of cuticle-degrading proteases in fungal pathogenesis of insects. Canadian Journal of Botany 1995, 73:S1119-S1125.
111. St.Leger R.J., Charnley A.K., Cooper R.M. Characterization of cuticle-degrading proteases produced by the entomopathogen Metarhizium anisopliae. Archives of Biochemistry and Biophysics 1987, 253:221-232.
112. St.Leger R.J., Joshi L., Bidochka M.J., Rizzo N.W., Roberts D.W. Characterization and ultrastructural localization of chitinases from Metarhizium anisopliae, M. flavoviride, and Beauveria bassiana during fungal invasion of host (Manduca sexta) cuticle. Applied and Environmental Microbiology 1996, 62:907-912.
113. St.Leger R.J., Nelson J.O., Screen S.E. The insect pathogenic fungus Metarhizium anisopliae alters ambient pH, allowing extracellular protease production and activity. Microbiology 1999, 145:2691-2699.
114. St.Leger R.J., Staples R.C., Roberts D.W. Cloning and regulatory analysis of starvation-stress gene, ssgA, encoding a hydrophobin-like protein from the insect pathogenic fungus, Metarhizium anisopliae. Gene 1992, 120:119-124.
115. St.Leger R.J., Wang C., Fang W. New perspectives on insect pathogens. Fungal Biology Reviews 2011, 25:84-88.
116. Tunlid A., Rosen S.E.B., Rask L. Purification and characterization of an extracellular serine protease from the nematode trapping fungus Arthrobotrys oligospora. Microbiology 1994, 140:1687-1695.
117. Ujjan A.A., Shahzad S. Insecticidal potential of Beauveria bassiana strain PDRL1187 and imidacloprid to mustard aphid (Lipaphis erysimi) under field conditions. Pakistan Journal of Zoology 2014, 46:1277-1281.
118. Vega F.E. Insect pathology and fungal endophytes. Journal of Invertebrate Pathology 2008, 98:277-279.
119. Vega F.E., Goettel M.S., Blackwell M., Chandler D., Jackson M.A., Keller S., Roy H.E. Fungal entomopathogens: new insights on their ecology. Fungal Ecology 2009, 2:149-159.
120. Wagner B.L., Lewis L.C. Colonization of corn, Zea mays, by the insect pathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology 2000, 66:3468-3473.
121. Wang J.B., St.Leger R.J., Wang C. Advances in Genomics of Insect Pathogenic Fungi. Advances in Genetics 2016, 94:67-105.
122. Wang S., Fang W., Wang C., St.Leger R.J. Insertion of an esterase gene into specific locust pathogen (Metarhizium acridum) enables it to infect caterpillars. PLoS Pathogens 2011, 7(6):e1002097.
123. Wang C., 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.
124. Wang C., St.Leger R.J. Developmental and transcriptional responses to host and nonhost cuticles by the specific locust pathogen Metarhizium anisopliae var. acridum. Eukaryotic Cell 2005, 4:937-947.
125. 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.
126. Wang C., 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.
127. 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.
128. Wang C., St Leger R.J. A scorpion neurotoxin increases the potency of a fungal insecticide. Nature Biotechnology 2007, 25:1455-1456.
129. Wang C., St.Leger R.J. Genomics of entomopathogenic fungi. The ecological genomics of fungi 2014, 243-260. John Wiley & Sons, Inc. F. Martin (Ed.).
130. Wang Q., Xu L. Beauvericin, a bioactive compound produced by fungi: a short review. Molecules 2012, 17:2367-2377.
131. Wang J., Zhou G., Ying S.H., Feng M.G. Adenylate cyclase orthologues in two filamentous insect pathogens contribute differentially to growth, conidiation, pathogenicity, and multistress responses. Fungal Biology 2014, 118:422-431.
132. Whiteford J.R., Spanu P.D. Hydrophobins and the interactions between fungi and plants. Molecular Plant Pathology 2002, 3:391-400.
133. White J.F., Sullivan R.F., Balady G.A., Gianfagna T., Yue Q., Meyer W. A fungal endosymbiont of the grass Bromus setifolius: distribution in some Andean populations, identification and examination of beneficial properties. Symbiosis 2001, 31:241-257.
134. Wyrebek M., Bidochka M.J. Variability in the insect and plant adhesins, Mad1 and Mad2, within the fungal genus Metarhizium suggest plant adaptation as an evolutionary force. PLoS One 2013, 10.1371/journal.pone.0059357.
135. Wyrebek M., Huber C., Sasan R.K., Bidochka M.J. Three sympatrically occurring species of Metarhizium show plant rhizosphere specificity. Microbiology 2011, 157:2904-2911.
136. Xiao G., Ying S.H., Zheng P., Wang Z.L., Zhang S., Xie Q., Feng M.G. Genomic perspectives on the evolution of fungal insect pathogenicity in Beauveria bassiana. Scientific Reports 2012, 2:1-10.
137. Ying S.H., Feng M.G., Keyhani N.O. A carbon responsive G-protein coupled receptor modulates broad developmental and genetic networks in the insect pathogenic fungus, Beauveria bassiana. Environmental Microbiology 2013, 15:2902-2921.
138. Ying S.H., Ji X.P., Wang X.X., Feng M.G., Keyhani N.O. The transcriptional co-activator multiprotein bridging factor 1 from the fungal insect pathogen, Beauveria bassiana, mediates regulation of hyphal morphogenesis, stress tolerance and virulence. Environmental Microbiology 2014, 16:1879-1897.
139. Zhang S., Xia Y.X., Kim B., Keyhani N.O. Two hydrophobins are involved in fungal spore coat rodlet layer assembly and each play distinct roles in surface interactions, development and pathogenesis in the insect pathogenic fungus, Beauveria bassiana. Molecular Microbiology 2011, 80:811-826.
140. Zhang Y., Xu L., Zhang S., Liu X., An Z., Wang M., Guo Y. Genetic diversity of Ophiocordyceps sinensis, a medicinal fungus endemic to the Tibetan Plateau: implications for its evolution and conservation. BMC Evolutionary Biology 2009, 9:290.
141. Zhang Y.J., Zhang J.Q., Jiang X.D., Wang G.J., Luo Z.B., Fan Y.H., Pei Y. Requirement of a mitogen-activated protein kinase for appressorium formation and penetration of insect cuticle by the insect pathogenic fungus Beauveria bassiana. Applied and Environmental Microbiology 2010, 76:2262-2270.
142. Zhang Y.J., Zhao J.H., Fang W.G., Zhang J.Q., Luo Z.B., Zhang M., Pei Y. Mitogen-activated protein kinase hog1 in the insect pathogenic fungus Beauveria bassiana regulates environmental stress responses and virulence to insects. Applied and Environmental Microbiology 2009, 75:3787-3795.
143. Zhao H., Lovett B., Fang W. Genetically Engineering Entomopathogenic Fungi. Advances in Genetics 2016, 94:137-163.
144. Zhong X., Peng Q.Y., Li S.S., Chen H., Sun H.X., Zhang G.R., Liu X. Detection of Ophiocordyceps sinensis in the roots of plants in alpine meadows by nested-touchdown polymerase chain reaction. Fungal Biology 2014, 118:359-363.