Secretome of fungus-infected aphids documents high pathogen activity and weak host response

Fungal Genetics and Biology

Volumn 48, Issue 4, 2011, Pages 343-352

  Grell, Morten N ^a   Jensen, Annette B ^b   Olsen, Peter B ^c   Eilenberg, Jørgen ^b   Lange, Lene ^a  

^a AALBORG UNIVERSITY   (Denmark)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c NOVOZYMES A S   (Denmark)

Author keywords

Aphid; Entomophthorales; Enzyme discovery; Host pathogen interaction; Secretome; Transposon assisted signal trapping

Indexed keywords

COMPLEMENTARY DNA; FUNGAL ENZYME; FUNGAL PROTEIN; SECRETOME; TRIACYLGLYCEROL LIPASE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; APHID; ARTICLE; CUTICLE; DNA LIBRARY; ENTOMOPHTHORA; ENZYME ACTIVITY; FUNGAL STRAIN; GENE; GENE IDENTIFICATION; HEMOLYMPH; HOST PATHOGEN INTERACTION; HYDROLYSIS; IMMUNE RESPONSE; INSECT GENE; MYCOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PANDORA; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN INTERACTION; SPOROGENESIS;

ANIMALS; ENTOMOPHTHORALES; FUNGAL PROTEINS; GENE LIBRARY; HEMIPTERA; HOST-PATHOGEN INTERACTIONS; INSECT PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID;

APHIDIDAE; ENTOMOPHTHORA; ENTOMOPHTHORALES; FUNGI; HEMIPTERA; HEXAPODA; PANDORA (ZYGOMYCETE); SITOBION AVENAE;

EID: 79952039491     PISSN: 10871845     EISSN: 10960937     Source Type: Journal    
DOI: 10.1016/j.fgb.2010.12.003     Document Type: Article

References (50)

1. Aerts A.M., Francois I.E., Cammue B.P., Thevissen K. The mode of antifungal action of plant, insect and human defensins. Cell. Mol. Life Sci. 2008, 65:2069-2079.
2. Altschul S.F., Madden T.L., Schäffer A.A., Zhang J.H., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389-3402.
3. Anisimova M., Gascuel O. Approximate likelihood ratio test for branches: a fast, accurate and powerful alternative. Syst. Biol. 2006, 55:539-552.
4. 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). J. Gen. Microbiol. 1989, 135:489-498.
5. 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 gene libraries. J. Microbiol. Methods 2004, 57:123-133.
6. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
7. Butt T.M., Beckett A., Wilding N. Protoplasts in the in vivo life cycle of Erynia neoaphidis. J. Gen. Microbiol. 1981, 127:417-421.
8. Cabib E., Farkas V., Kosik O., Blanco N., Arroyo J., McPhie P. Assembly of the yeast cell wall. Crh1p and Crh2p act as transglycosylases in vivo and in vitro. J. Biol. Chem. 2008, 283:29859-29872.
9. Cantarel B.L., Coutinho P.M., Rancurel C., Bernard T., Lombard V., Henrissat B. The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res. 2009, 37:D233-D238.
10. Cerenius L., Lee B.L., Söderhäll K. The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008, 29:263-271.
11. Charnley A.K. Fungal pathogens of insects: cuticle degrading enzymes and toxins. Adv. Bot. Res. 2003, 40:241-321.
12. Chevenet F., Brun C., Banuls A.L., Jacq B., Chisten R. TreeDyn: towards dynamic graphics and annotations for analyses of trees. BMC Bioinformat. 2006, 7:439.
13. Dereeper A., Guignon V., Blanc G., Audic S., Buffet S., Chevenet F., Dufayard J.F., Guindon S., Lefort V., Lescot M., Claverie J.M., Gascuel O. Phylogeny.fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Res. 2008, 36:W465-W469.
14. Ewing B., Hillier L.D., Wendl M.C., Green P. Base-calling of automated sequencer traces using phred: I. Accuracy assessment. Genome Res. 1998, 8:175-185.
15. Fan Y.H., Fang W.G., Guo S.J., Pei X.Q., Zhang Y.J., Xiao Y.H., Li D.M., Jin K., Bidochka M.J., Pei Y. Increased insect virulence in Beauveria bassiana strains overexpressing an engineered chitinase. Appl. Environ. Microbiol. 2007, 73:295-302.
16. Fang W.G., Leng B., Xiao Y.H., Jin K., Ma J.C., Fan Y.H., Feng J., Yang X.Y., Zhang Y.J., Pei Y. Cloning of Beauveria bassiana chitinase gene Bbchit1 and its application to improve fungal strain virulence. Appl. Environ. Microbiol. 2005, 71:363-370.
17. Freimoser F.M., Jensen A.B., Tuor U., Aebi M., Eilenberg J. Isolation and in vitro cultivation of the aphid pathogenic fungus Entomophthora planchoniana. Can. J. Microbiol. 2001, 47:1082-1087.
18. Freimoser F.M., Screen S., Hu G., St.Leger R. EST analysis of genes expressed by the zygomycete pathogen Conidiobolus coronatus during growth on insect cuticle. Microbiology 2003, 149:1893-1900.
19. Gerardo N.M., Altincicek B., Anselme C., Atamian H., Barribeau S.M., de Vos M., Duncan E.J., Evans J.D., Gabaldón T., Ghanim M., Heddi A., Kaloshian I., Latorre A., Moya A., Nakabachi A., Parker B.J., Pérez-Brocal V., Pignatelli M., Rahbé Y., Ramsey J.S., Spragg C.J., Tamames J., Tamarit D., Tamborindeguy C., Vincent-Monegat C., Vilcinskas A. Immunity and other defenses in pea aphids, Acyrthosiphon pisum. Genome Biol. 2010, 11:R21.
20. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52:696-704.
21. Hamann T., Lange L. Discovery, cloning and heterologous expression of secreted potato proteins reveal erroneous pre-mRNA splicing in Aspergillus oryzae. J. Biotechnol. 2006, 126:265-276.
22. Hegedus D.D., Khachatourians G.G. Production of an extracellular lipase by Beauveria bassiana. Biotechnol. Lett. 1988, 10:637-642.
23. Hesketh H., Roy H.E., Eilenberg J., Pell J.K., Hails R.S. Challenges in modelling complexity of fungal entomopathogens in semi-natural populations of insects. BioControl 2010, 55:55-73.
24. Hibbett D.S., Binder M., Bischoff J.F., Blackwell M., Canon P.F., Eriksson O.E., Huhndorf S., James T., Kirk P.M., Lücking R., Lumbsch H.T., Lutzoni F., Matheny P.B., McLaughlin D.J., Powell M.J., Redhead S., Schoch C.L., Spatafora J.W., Stalpers J.A., Vilgalys R., Aime M.C., Aptroot A., Bauer R., Begerow D., Benny G.L., Castlebury L.A., Crous P.W., Dai Y.C., Gams W., Geiser D.M., Griffith G.W., Gueidan C., Hawksworth D.L., Hestmark G., Hosaka K., Humber R.A., Hyde K.D., Ironside J.E., Kõljalg U., Kurtzman C.P., Larsson K.H., Lichtwardt R., Longcore J., Miadlikowska J., Miller A., Moncalvo J.M., Mozley-Standridge S., Oberwinkler F., Parmasto E., Reeb V., Rogers J.D., Roux C., Ryvarden L., Sampaio J.P., Schüssler A., Sugiyama J., Thorn R.G., Tibell L., Untereiner W.A., Walker C., Wang Z., Weir A., Weiss M., White M.M., Winka K., Yao Y.J., Zhang N. A higher-level phylogenetic classification of the fungi. Mycol. Res. 2007, 111:509-547.
25. Hountondji F. Lessons from interactions within the cassava green mite fungal pathogen Neozygites tanajoae system and prospects for microbial control using Entomophthorales. Exp. Appl. Acarol. 2008, 46:195-210.
26. Hull-Thompson J., Muffat J., Sanchez D., Walker D.W., Benzer S., Ganfornina M.D., Jasper H. Control of metabolic homeostasis by stress signaling is mediated by the lipocalin NLaz. PLoS Genet. 2009, 5:e1000460.
27. Jensen A.B., Gargas A., Eilenberg J., Rosendahl S. Relationships of the insect-pathogenic order Entomophthorales (Zygomycota, Fungi) based on the phylogenetic analysis of small ribosomal sequences (SSU rDNA). Fungal Genet. Biol. 1998, 24:325-334.
28. Jensen A.B., Thomsen L., Eilenberg J. Value of host range, morphological, and genetic characteristics within the Entomophthora muscae species complex. Mycol. Res. 2006, 110:941-950.
29. 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. Agric. Forest Entomol. 2008, 10:279-290.
30. Kim H.J., Je H.J., Cheon H.M., Kong S.Y., Han J.H., Yun C.Y., Han Y.S., Lee I.H., Kang Y.J., Seo S.J. Accumulation of 23 kDa lipocalin during brain development and injury in Hyphantria cunea. Insect Biochem. Mol. Biol. 2005, 35:1133-1141.
31. 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. J. Insect Physiol. 1995, 41:895-903.
32. Krogh A., Larsson B., von Heijne G., Sonnhammer E.L. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305:567-580.
33. Kutsukake M., Shibao H., Nikoh N., Morioka M., Tamura T., Hoshino T., Ohgiya S., Fukatsu T. Venomous protease of aphid soldier for colony defense. Proc. Natl. Acad. Sci. USA 2004, 101:11338-11343.
34. Lange, L., Schnorr, K., 2004. Discovery of secreted proteins and peptides during fungal-plant interactions. In: Proceedings of the 7th European Conference on Fungal Genetics. Technical University of Denmark (DTU), Denmark, p. 209.
35. Latgé J.P., Beauvais A. Wall composition of the protoplastic Entomophthorales. J. Invertebr. Pathol. 1987, 50:53-57.
36. St.Leger R.J., Joshi L., Bidochka M.J., Roberts D.W. Construction of an improved mycoinsecticide over-expressing a toxic protease. Proc. Natl. Acad. Sci. USA 1996, 93:6349-6354.
37. St.Leger R.J., Joshi L., Bidochka M.J., Rizzo N.W., Roberts D.W. Biochemical characterization and ultrastructural localization of two extracellular trypsins produced by Metarhizium anisopliae in infected cuticles. Appl. Environ. Microbiol. 1996, 62:1257-1264.
38. Marques M., Mojzita D., Amorim M.A., Almeida T., Hohmann S., Moradas-Ferreira P., Costa V. The Pep4p vacuolar proteinase contributes to the turnover of oxidized proteins but PEP4 overexpression is not sufficient to increase chronological lifespan in Saccharomyces cerevisiae. Microbiology 2006, 152:3595-3605.
39. Milner R.J., Holdom D.G., Glare T.R. Diurnal patterns of mortality in aphids infected by entomophthoran fungi. Entomol. Exp. Appl. 1984, 36:37-42.
40. Nakanishi-Shindo Y., Nakayama K., Tanaka A., Toda Y., Jigami Y. Structure of the N-linked oligosaccharides that show the complete loss of α-1, 6-polymannose outer chain from och1, och1 mnn1, and och1 mnn1 alg3 mutants of Saccharomyces cerevisiae. J. Biol. Chem. 1993, 268:26338-26345.
41. Nielsen H., Engelbrecht J., Brunak S., von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 1997, 10:1-6.
42. Nielsen C., Keena M., Hajek A.E. Virulence and fitness of the fungal pathogen Entomophaga maimaiga in its host Lymantria dispar, for pathogen and host strains originating from Asia, Europe, and North America. J. Invertebr. Pathol. 2005, 89:232-242.
43. Notredame C., Higgins D.G., Heringa J. T-Coffee: a novel method for fast and accurate multiple sequence alignment. J. Mol. Biol. 2000, 302:205-217.
44. Paetzel M., Karla A., Strynadka N.C.J., Dalbey R.E. Signal peptidases. Chem. Rev. 2002, 102:4549-4579.
45. Rispe C., Kutsukake M., Doublet V., Hudaverdian S., Legeai F., Simon J.C., Tagu D., Fukatsu T. Large gene family expansion and variable selective pressures for cathepsin B in aphids. Mol. Biol. Evol. 2008, 25:5-17.
46. Roy H.E., Steinkraus D.C., Eilenberg J., Hajek A.E., Pell J.K. Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annu. Rev. Entomol. 2006, 51:331-357.
47. Shaw J.A., Mol P.C., Bowers B., Silverman S.J., Valdivieso M.H., Durán A., Cabib E. The function of chitin synthases 2 and 3 in the Saccharomyces cerevisiae cell cycle. J. Cell. Biol. 1991, 114:111-123.
48. 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. Can. J. Microbiol. 2006, 52:550-559.
49. 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.
50. Zhang Y.J., Feng M.G., Fan Y.H., Luo Z.B., Yang X.Y., Wu D., Pei Y. A cuticle-degrading protease (CDEP-1) of Beauveria bassiana enhances virulence. Biocontrol Sci. Technol. 2008, 18:543-555.