Genomic analyses and transcriptional profiles of the glycoside hydrolase family 18 genes of the entomopathogenic fungus Metarhizium anisopliae

PLoS ONE

Volumn 9, Issue 9, 2014, Pages

  Junges, Ângela ^a   Boldo, Juliano Tomazzoni ^a   Souza, Bárbara Kunzler ^a   Guedes, Rafael Lucas Muniz ^b   Sbaraini, Nicolau ^a   Kmetzsch, Lívia ^a   Thompson, Claudia Elizabeth ^a   Staats, Charley Christian ^a   De Almeida, Luis Gonzaga Paula ^b   De Vasconcelos, Ana Tereza Ribeiro ^b   Vainstein, Marilene Henning ^a   Schrank, Augusto ^a  

^a FEDERAL UNIVERSITY OF RIO GRANDE DO SUL   (Brazil)

^b LABORATÓRIO NACIONAL DE COMPUTAÇÃO CIENTÍFICA   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLGLUCOSAMINIDASE; CHITIN; CHITINASE; GLYCOSIDASE; GLYCOSIDASE FAMILY 18; UNCLASSIFIED DRUG; FUNGAL PROTEIN; TRANSCRIPTOME;

AMINO ACID SEQUENCE; ARTICLE; CHI2 GENE; CHI3 GENE; CHIT1 GENE; DEGLYCOSYLATION; FUNGAL GENE; FUNGAL GENETICS; FUNGAL STRAIN; FUNGAL VIRULENCE; FUNGUS CULTURE; INTRON; METARHIZIUM ANISOPLIAE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PHYLOGENY; POLYMERASE CHAIN REACTION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN HYDROLYSIS; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; QUANTITATIVE ANALYSIS; RNA EXTRACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; TRANSCRIPTION INITIATION; UNINDEXED SEQUENCE; DNA SEQUENCE; ENZYMOLOGY; FUNGAL GENOME; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; METARHIZIUM;

FUNGI; METARHIZIUM ANISOPLIAE;

CHITINASE; FUNGAL PROTEINS; GENOME, FUNGAL; METARHIZIUM; PHYLOGENY; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84907200769     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0107864     Document Type: Article

References (75)

1. Merzendorfer H (2011) The cellular basis of chitin synthesis in fungi and insects: common principles and differences. Eur J Cell Biol 90: 759-769.
2. Tharanathan RN, Kittur FS (2003) Chitin-the undisputed biomolecule of great potential. Crit Rev Food Sci Nutr 43: 61-87.
3. Duo-Chuan L (2006) Review of fungal chitinases. Mycopathologia 161: 345-360.
4. Seidl V (2008) Chitinases of filamentous fungi: a large group of diverse proteins with multiple physiological functions. Fungal Biology Reviews 22: 36-42.
5. Cantarel BL, Coutinho PM, Rancurel C, Bernard T, Lombard V, et al. (2009) The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics. Nucleic Acids Res 37: D233-238.
6. Patil RS, Ghormade VV, Deshpande MV (2000) Chitinolytic enzymes: an exploration. Enzyme Microb Technol 26: 473-483.
7. van Munster JM, van der Kaaij RM, Dijkhuizen L, van der Maarel MJ (2012) Biochemical characterization of Aspergillus niger CfcI, a glycoside hydrolase family 18 chitinase that releases monomers during substrate hydrolysis. Microbiology 158: 2168-2179.
8. Eijsink V, Hoell I, Vaaje-Kolstada G (2010) Structure and function of enzymes acting on chitin and chitosan. Biotechnol Genet Eng Rev 27: 331-366.
9. Vaaje-Kolstad G, Horn SJ, Sorlie M, Eijsink VG (2013) The chitinolytic machinery of Serratia marcescens-a model system for enzymatic degradation of recalcitrant polysaccharides. FEBS J 280: 3028-3049.
10. Henrissat B (1991) A classification of glycosyl hydrolases based on amino acid sequence similarities. Biochem J 280 (Pt 2): 309-316.
11. Truong NH, Park SM, Nishizawa Y, Watanabe T, Sasaki T, et al. (2003) Structure, heterologous expression, and properties of rice (Oryza sativa L.) family 19 chitinases. Biosci Biotechnol Biochem 67: 1063-1070.
12. Ueda M, Kojima M, Yoshikawa T, Mitsuda N, Araki K, et al. (2003) A novel type of family 19 chitinase from Aeromonas sp. No.10S-24. Cloning, sequence, expression, and the enzymatic properties. Eur J Biochem 270: 2513-2520.
13. Honda Y, Taniguchi H, Kitaoka M (2008) A reducing-end-acting chitinase from Vibrio proteolyticus belonging to glycoside hydrolase family 19. Appl Microbiol Biotechnol 78: 627-634.
14. Geng J, Plenefisch J, Komuniecki PR, Komuniecki R (2002) Secretion of a novel developmentally regulated chitinase (family 19 glycosyl hydrolase) into the perivitelline fluid of the parasitic nematode, Ascaris suum. Mol Biochem Parasitol 124: 11-21.
15. Funkhouser JD, Aronson NN Jr. (2007) Chitinase family GH18: evolutionary insights from the genomic history of a diverse protein family. BMC Evol Biol 7: 96.
16. Gruber S, Seidl-Seiboth V (2012) Self versus non-self: fungal cell wall degradation in Trichoderma. Microbiology 158: 26-34.
17. Seidl V, Huemer B, Seiboth B, Kubicek CP (2005) A complete survey of Trichoderma chitinases reveals three distinct subgroups of family 18 chitinases. FEBS J 272: 5923-5939.
18. Karlsson M, Stenlid J (2009) Evolution of family 18 glycoside hydrolases: diversity, domain structures and phylogenetic relationships. J Mol Microbiol Biotechnol 16: 208-223.
19. Gao Q, Jin K, Ying SH, Zhang Y, Xiao G, et al. (2011) Genome sequencing and comparative transcriptomics of the model entomopathogenic fungi Metarhizium anisopliae and M. acridum. PLoS Genet 7: e1001264.
20. Zheng P, Xia Y, Xiao G, Xiong C, Hu X, et al. (2011) Genome sequence of the insect pathogenic fungus Cordyceps militaris, a valued traditional Chinese medicine. Genome Biol 12: R116.
21. Schrank A, Vainstein MH (2010) Metarhizium anisopliae enzymes and toxins. Toxicon 56: 1267-1274.
22. Bowman SM, Free SJ (2006) The structure and synthesis of the fungal cell wall. Bioessays 28: 799-808.
23. Hartl L, Zach S, Seidl-Seiboth V (2012) Fungal chitinases: diversity, mechanistic properties and biotechnological potential. Appl Microbiol Biotechnol 93: 533-543.
24. Gruber S, Vaaje-Kolstad G, Matarese F, Lopez-Mondejar R, Kubicek CP, et al. (2011) Analysis of subgroup C of fungal chitinases containing chitin-binding and LysM modules in the mycoparasite Trichoderma atroviride. Glycobiology 21: 122-133.
25. Boldo JT, Junges A, do Amaral KB, Staats CC, Vainstein MH, et al. (2009) Endochitinase CHI2 of the biocontrol fungus Metarhizium anisopliae affects its virulence toward the cotton stainer bug Dysdercus peruvianus. Curr Genet 55: 551-560.
26. Staats CC, Kmetzsch L, Lubeck I, Junges A, Vainstein MH, et al. (2013) Metarhizium anisopliae chitinase CHIT30 is involved in heat-shock stress and contributes to virulence against Dysdercus peruvianus. Fungal Biol 117: 137-144.
27. Shin KS, Kwon NJ, Kim YH, Park HS, Kwon GS, et al. (2009) Differential roles of the ChiB chitinase in autolysis and cell death of Aspergillus nidulans. Eukaryot Cell 8: 738-746.
28. Jaques AK, Fukamizo T, Hall D, Barton RC, Escott GM, et al. (2003) Disruption of the gene encoding the ChiB1 chitinase of Aspergillus fumigatus and characterization of a recombinant gene product. Microbiology 149: 2931-2939.
29. Carsolio C, Gutierrez A, Jimenez B, Van Montagu M, Herrera-Estrella A (1994) Characterization of ech-42, a Trichoderma harzianum endochitinase gene expressed during mycoparasitism. Proc Natl Acad Sci U S A 91: 10903-10907.
30. Tzelepis GD, Melin P, Stenlid J, Jensen DF, Karlsson M (2014) Functional analysis of the C-II subgroup killer toxin-like chitinases in the filamentous ascomycete Aspergillus nidulans. Fungal Genet Biol 64: 58-66.
31. Bogo MR, Rota CA, Pinto H Jr., Ocampos M, Correa CT, et al. (1998) A chitinase encoding gene (chit1 gene) from the entomopathogen Metarhizium anisopliae: isolation and characterization of genomic and full-length cDNA. Curr Microbiol 37: 221-225.
32. Baratto CM, Dutra V, Boldo JT, Leiria LB, Vainstein MH, et al. (2006) Isolation, characterization, and transcriptional analysis of the chitinase chi2 Gene (DQ011663) from the biocontrol fungus Metarhizium anisopliae var. anisopliae. Curr Microbiol 53: 217-221.
33. da Silva MV, Santi L, Staats CC, da Costa AM, Colodel EM, et al. (2005) Cuticle-induced endo/exoacting chitinase CHIT30 from Metarhizium anisopliae is encoded by an ortholog of the chi3 gene. Res Microbiol 156: 382-392.
34. Lubeck I, Arruda W, Souza BK, Stanisçuaski F, Carlini CR, et al. (2008) Evaluation of Metarhizium anisopliae strains as potential biocontrol agents of the tick Rhipicephalus (Boophilus) microplus and the cotton stainer Dysdercus peruvianus. Fungal Ecology 1: 78-88.
35. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41: 95-98.
36. Boraston AB, Bolam DN, Gilbert HJ, Davies GJ (2004) Carbohydrate-binding modules: fine-tuning polysaccharide recognition. Biochem J 382: 769-781.
37. Zdobnov EM, Apweiler R (2001) InterProScan-an integration platform for the signature-recognition methods in InterPro. Bioinformatics 17: 847-848.
38. Yin Y, Mao X, Yang J, Chen X, Mao F, et al. (2012) dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res 40: W445-451.
39. Marchler-Bauer A, Anderson JB, Chitsaz F, Derbyshire MK, De Weese-Scott C, et al. (2009) CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37: D205-210.
40. Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
41. Eisenhaber B, Schneider G, Wildpaner M, Eisenhaber F (2004) A sensitive predictor for potential GPI lipid modification sites in fungal protein sequences and its application to genome-wide studies for Aspergillus nidulans, Candida albicans, Neurospora crassa, Saccharomyces cerevisiae and Schizosaccharomyces pombe. J Mol Biol 337: 243-253.
42. Bjellqvist B, Basse B, Olsen E, Celis JE (1994) Reference points for comparisons of two-dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophoresis 15: 529-539.
43. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, et al. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
44. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30: 2725-2729.
45. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406-425.
46. Li L, Stoeckert CJ Jr., Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13: 2178-2189.
47. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, et al. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37: e45.
48. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
49. Reich M, Liefeld T, Gould J, Lerner J, Tamayo P, et al. (2006) Gene Pattern 2.0. Nat Genet 38: 500-501.
50. Karlsson M, Stenlid J (2008) Comparative evolutionary histories of the fungal chitinase gene family reveal non-random size expansions and contractions due to adaptive natural selection. Evol Bioinform Online 4: 47-60.
51. Stals I, Samyn B, Sergeant K, White T, Hoorelbeke K, et al. (2010) Identification of a gene coding for a deglycosylating enzyme in Hypocrea jecorina. FEMS Microbiol Lett 303: 9-17.
52. Synstad B, Gaseidnes S, Van Aalten DM, Vriend G, Nielsen JE, et al. (2004) Mutational and computational analysis of the role of conserved residues in the active site of a family 18 chitinase. Eur J Biochem 271: 253-262.
53. Bateman A, Bycroft M (2000) The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol 299: 1113-1119.
54. Fuglsang CC, Berka RM, Wahleithner JA, Kauppinen S, Shuster JR, et al. (2000) Biochemical analysis of recombinant fungal mutanases. A new family of alpha1,3-glucanases with novel carbohydrate-binding domains. J Biol Chem 275: 2009-2018.
55. Nielsen H, Engelbrecht J, Brunak S, von Heijne G (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
56. Hegde RS, Bernstein HD (2006) The surprising complexity of signal sequences. Trends Biochem Sci 31: 563-571.
57. Hamaguchi T, Ito T, Inoue Y, Limpaseni T, Pongsawasdi P, et al. (2010) Purification, characterization and molecular cloning of a novel endo-beta-Nacetylglucosaminidase from the basidiomycete, Flammulina velutipes. Glycobiology 20: 420-432.
58. Tzelepis G, Hosomi A, Hossain TJ, Hirayama H, Dubey M, et al. (2014) Endobeta-N-acetylglucosamidases (ENGases) in the fungus Trichoderma atroviride: Possible involvement of the filamentous fungi-specific cytosolic ENGase in the ERAD process. Biochem Biophys Res Commun 449: 256-261.
59. Boldo JT, do Amaral KB, Junges A, Pinto PM, Staats CC, et al. (2010) Evidence of alternative splicing of the chi2 chitinase gene from Metarhizium anisopliae. Gene 462: 1-7.
60. Zhao Z, Liu H, Wang C, Xu JR (2014) Correction: Comparative analysis of fungal genomes reveals different plant cell wall degrading capacity in fungi. BMC Genomics 15: 6.
61. Peterson ME, Chen F, Saven JG, Roos DS, Babbitt PC, et al. (2009) Evolutionary constraints on structural similarity in orthologs and paralogs. Protein Sci 18: 1306-1315.
62. Pinto AdS, Barreto CC, Vainstein MH, Schrank A, Ulhoa CJ (1997) Purification and characterization of an extracellular chitinase from the entomopathogen Metarhizium anisopliae. Canadian Journal of Microbiology 43: 322-327.
63. Liu ZH, Yang Q, Hu S, Zhang JD, Ma J (2008) Cloning and characterization of a novel chitinase gene (chi46) from Chaetomium globosum and identification of its biological activity. Appl Microbiol Biotechnol 80: 241-252.
64. St. Leger RJ, Staples RC, Roberts DW (1993) Entomopathogenic Isolates of Metarhizium anisopliae, Beauveria bassiana, and Aspergillus flavus Produce Multiple Extracellular Chitinase Isozymes. Journal of Invertebrate Pathology 61: 81-84.
65. Kruszewska JS, Perlinska-Lenart U, Gorka-Niec W, Orlowski J, Zembek P, et al. (2008) Alterations in protein secretion caused by metabolic engineering of glycosylation pathways in fungi. Acta Biochim Pol 55: 447-456.
66. Barreto CC, Staats CC, Schrank A, Vainstein MH (2004) Distribution of chitinases in the entomopathogen Metarhizium anisopliae and effect of Nacetylglucosamine in protein secretion. Curr Microbiol 48: 102-107.
67. Santi L, Silva WO, Pinto AF, Schrank A, Vainstein MH (2010) Metarhizium anisopliae host-pathogen interaction: differential immunoproteomics reveals proteins involved in the infection process of arthropods. Fungal Biol 114: 312-319.
68. Santi L, Silva WO, Pinto AF, Schrank A, Vainstein MH (2009) Differential immunoproteomics enables identification of Metarhizium anisopliae proteins related to Rhipicephalus microplus infection. Res Microbiol 160: 824-828.
69. Nielsen CB, Friedman B, Birren B, Burge CB, Galagan JE (2004) Patterns of intron gain and loss in fungi. PLoS Biol 2: e422.
70. Yamazaki H, Tanaka A, Kaneko J, Ohta A, Horiuchi H (2008) Aspergillus nidulans ChiA is a glycosylphosphatidylinositol (GPI)-anchored chitinase specifically localized at polarized growth sites. Fungal Genet Biol 45: 963-972.
71. Alcazar-Fuoli L, Clavaud C, Lamarre C, Aimanianda V, Seidl-Seiboth V, et al. (2011) Functional analysis of the fungal/plant class chitinase family in Aspergillus fumigatus. Fungal Genet Biol 48: 418-429.
72. Nei M, Rooney AP (2005) Concerted and birth-and-death evolution of multigene families. Annu Rev Genet 39: 121-152.
73. Fan Y, Zhang Y, Yang X, Pei X, Guo S, et al. (2007) Expression of a Beauveria bassiana chitinase (Bbchit1) in Escherichia coli and Pichia pastoris. Protein Expr Purif 56: 93-99.
74. Kong LA, Yang J, Li GT, Qi LL, Zhang YJ, et al. (2012) Different chitin synthase genes are required for various developmental and plant infection processes in the rice blast fungus Magnaporthe oryzae. PLoS Pathog 8: e1002526.
75. Deising HB, Werner S, Wernitz M (2000) The role of fungal appressoria in plant infection. Microbes Infect 2: 1631-1641.