Differential expression of insect and plant specific adhesin genes, Mad1 and Mad2, in Metarhizium robertsii

Fungal Biology

Volumn 115, Issue 11, 2011, Pages 1174-1185

  Barelli, Larissa ^a   Padilla Guerrero, Israel Enrique ^a,b   Bidochka, Michael J ^a  

^a BROCK UNIVERSITY   (Canada)

^b UNIVERSITY OF GUANAJUATO   (Mexico)

Author keywords

Adhesin; Mad2; Metarhizium robertsii; Starvation; STRE; Stress

Indexed keywords

FUNGAL PROTEIN;

ENTOMOPATHOGENIC ORGANISM; EXUDATION; FRUIT; FUNGUS; GENE EXPRESSION; HEAT SHOCK; INSECT; MOLECULAR ANALYSIS; PATHOGENICITY; RHIZOSPHERE; ROOT COLONIZATION; STARVATION; SUBSTRATE;

ANIMAL; ARTICLE; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INSECT; METABOLISM; METARHIZIUM; MICROBIOLOGY; PLANT;

ANIMALS; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; INSECTS; METARHIZIUM; PLANTS;

BLATTARIA; FUNGI; HEXAPODA; LYCOPERSICON ESCULENTUM; MANDUCA SEXTA; METARHIZIUM; PLUTELLA XYLOSTELLA;

EID: 80955142748     PISSN: 18786146     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.funbio.2011.08.003     Document Type: Article

References (62)

1. Anderson S.O., Roepstorff P. Phenolic compounds released by mild acid hydrolysis from sclerotized cuticle: purification, structure, and possible origin from cross-links. Insect Biochemistry 1978, 8:99-104.
2. Badis G., Chan E.T., van Bakel H., Pena-Castillo L., Tillo D., Tsui K., et al. A library of yeast transcription factor motifs reveals a widespread function for Rsc3 in targeting nucleosome exclusion at promoters. Molecular Cell 2008, 32:878-887.
3. Bais H.P., Weir T.L., Perry L.G., Gilroy S., Vivanco J.M. The role of root exudates in rhizosphere interactions with plants and other organisms. Annual Review of Plant Biology 2006, 57:233-266.
4. Bischoff J.F., Rehner S.A., Humber R.A. A multilocus phylogeny of the Metarhizium anisopliae lineage. Mycologia 2009, 101:512-530.
5. Boorstein W.R., Craig E.A. Regulation of a yeast HSP70 gene by a cAMP responsive transcriptional control element. The EMBO Journal 1990, 9:2543-2553.
6. Buxton E.W. Root exudates for banana and their relationship to strains of the Fusarium causing Panama wilt. Annals of Applied Biology 1962, 50:269-282.
7. Carlson M. Glucose repression in yeast. Current Opinion in Microbiology 1999, 2:202-207.
8. Choquer M., Boccara M., Vidal-Cros A. A semi-quantitative RT-PCR method to readily compare expression levels within Botrytis cinerea multigenic families in vitro and in planta. Current Genetics 2003, 43:303-309.
9. Ciriacy M. Genetics of alcohol dehydrogenase in Saccharomyces cerevisiae. II. Two loci controlling synthesis of the glucose-repressible ADH II. Molecular and General Genetics 1975, 138:157-164.
10. Coffman J.A., Rai R., Cunningham T., Svetlov V., Cooper T.G. Gat1p, a GATA family protein whose production is sensitive to nitrogen catabolite repression, participates in transcriptional activation of nitrogen-catabolic genes in Saccharomyces cerevisiae. Molecular Cell Biology 1996, 16:847-858.
11. Czarnota M.A., Rimando A.M., Weston L.A. Evaluation of root exudates of seven sorghum accessions. Journal of Chemical Ecology 2003, 29:2073-2083.
12. Estruch F. Stress-controlled transcription factors, stress-induced genes and stress tolerance in budding yeast. FEMS Microbiology Letters 2000, 24:469-486.
13. Fang W., Bidochka M.J. Expression of genes involved in germination, conidiogenesis and pathogenesis in Metarhizium anisopliae using quantitative real-time RT-PCR. Mycological Research 2006, 110:1165-1171.
14. 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.
15. Farré D., Roset R., Huerta M., Adsuara J.E., Roselló L., Albà M.M., Messeguer X. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Research 2003, 31:3651-3653.
16. Fernandes L., Rodrigues-Pousada C., Struhl K. Yap, a novel family of eight bZIP proteins in Saccharomyces cerevisiae with distinct biological functions. Molecular and Cellular Biology 1997, 17:6982-6993.
17. Freimoser F.M., Screen S., Bagga S., Hu G., St. Leger R.J. Expressed sequence tag (EST) analysis of two subspecies of Metarhizium anisopliae reveals a plethora of secreted proteins with potential activity in insect hosts. Microbiology 2005, 149:239-247.
18. Gancedo J.M. Yeast carbon catabolite repression. Microbiology and Molecular Biology Reviews 1998, 62:334-361.
19. Goettel M.S., St. Leger R.J., Bhairi S., Jung M.K., Oakley B.R., Roberts D.W., Staples R.C. Pathogenicity and growth of Metarhizium anisopliae stable transformed to benomyl resistance. Current Genetics 1990, 17:129-132.
20. Görner W., Durchschlag E., Martinez-Pastor M.T., Estruch F., Ammerer G., Hamilton B., et al. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes and Development 1998, 12:586-597.
21. Hancock J.G. Soluble metabolites in intercellular regions of squash hypocotyl tissues: implications for exudation. Plant and Soil 1977, 47:103-112.
22. Hildebrandt U., Ouziad F., Marner F.J., Bothe H. The bacterium Paenibacillus validus stimulates growth of the arbuscular mycorrhizal fungus Glomus intraradices up to the formation of fertile spores. FEMS Microbiology Letters 2006, 254:258-267.
23. Holder D.J., Keyhani N.O. Adhesion of the entomopathogenic fungus Beauveria bassiana to substrata. Applied and Environmental Microbiology 2005, 71:5260-5266.
24. 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.
25. Jalali B., Suryanarayana D. Shift in the carbohydrate spectrum of the root exudates of wheat in relation to its root-rot disease. Plant and Soil 1971, 34:261-267.
26. Jones K.D., Kompala D.S. Cybernetic model of the growth dynamics of Saccharomyces cerevisiae in batch and continuous cultures. Journal of Biotechnology 1999, 71:105-131.
27. Kendrick B. The Fifth Kingdom 2000, Focus Publishing, Newburyport, MA. 3rd edn.
28. Liu K., Ding X., Deng B., Chen W. Isolation and characterization of endophytic taxol-producing fungi from Taxus chinensis. Journal of Industrial Microbiology and Biotechnology 2009, 36:1171-1177.
29. Madrigal Pulido J., Padilla Guerrero I., Magaña Martínez I.D., Cacho Valadez B., Torres Guzman J.C., Salazar Solis E., Felix Gutierrez Corona J., Schrank A., Jiménez Bremont F., González Hernandez A. Isolation, characterization and expression analysis of the ornithine decarboxylase gene (ODC1) of the entomopathogenic fungus, Metarhizium anisopliae. Microbiological Research 2011 January 13.
30. Marchler G., Schuller C., Adam G., Ruis H. A Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. The EMBO Journal 1993, 12:1997-2003.
31. Martinez-Pastor M.T., Marchler G., Schuller C., Marchler-Bauer A., Ruis H., Estruch F. The Saccharomyces cerevisiae UAS element controlled by protein kinase A activates transcription in response to a variety of stress conditions. The EMBO Journal 1996, 15:2227-2235.
32. Messenguy F., Vierendeels F., Scherens B., Dubois E. In Saccharomyces cerevisiae, expression of arginine catabolic genes CAR1 and CAR2 in response to exogenous nitrogen availability is mediated by the Ume6 (CargRI)-Sin3 (CargRII)-Rpd3 (CargRIII) complex. Journal of Bacteriology 2000, 182:3158-3164.
33. Morales-Hernandez C.E., Padilla-Guerrero I.E., González-Hernandez G.A., Salazar-Solis E., Torres-Guzman J.C. Catalase overexpression reduces the germination time and increases the pathogenicity of the fungus Metarhizium anisopliae. Applied Microbiology and Biotechnology 2010, 87:1033-1044.
34. Natarajan K., Meyer M.R., Jackson B.M., Slade D., Roberts C., Hinnebusch A.G., Marton M.J. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Molecular Cell Biology 2001, 21:4347-4368.
35. Padilla-Guerrero I.E., Barelli L., González-Hernandez, Torres-Guzman J.C., Bidochka M.J. Flexible metabolism in Metarhizium anisopliae and Beauveria bassiana: role of the glyoxylate cycle during insect pathogenesis. Microbiology 2011, 157:199-208.
36. Pall M.L., Brunelli J.P. A series of six compact fungal transformation vectors containing polylinkers with multiple unique restriction sites. Fungal Genetics Newsletter 1993, 40:59-62.
37. Pava-Ripoll M., Angelini C., Fang W., 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 2010, 157:47-55.
38. Pedruzzi I., Burckert N., Egger P., De Virgilio C. Saccharomyces cerevisiae Ras/cAMP pathway controls post-diauxic shift element-dependent transcription through the zinc finger protein Gis1. The EMBO Journal 2000, 19:2569-2579.
39. Rangel D.E.N., Anderson A.J., Roberts D.W. Growth of Metarhizium anisopliae on non-preferred carbon sources yields conidia with increased UV-B tolerance. Journal of Invertebrate Pathology 2006, 93:127-134.
40. Rangel D.E.N., Anderson A.J., Roberts D.W. Evaluating physical and nutritional stress during mycelial growth as inducers of tolerance to heat and UV-B radiation in Metarhizium anisopliae conidia. Mycological Research 2008, 112:1362-1372.
41. Rath A.C., Carr C.J., Graham B.R. Characterization of Metarhizium anisopliae strains by carbohydrate utilization (API50CH). Journal of Invertebrate Pathology 1995, 96:152-161.
42. Rovira A.D. Plant root exudates and their influence upon soil microorganisms. Ecology of Soil-borne Plant Pathogens: Prelude to Biological Control 1965, 170-186. University of California Press, Berkeley, Los Angeles. K.F. Baker, W.C. Snyder (Eds.).
43. Rovira A.D. Plant root exudates. The Botanical Review 1969, 35:35-57.
44. Scervino J.M., Ponce M.A., Erra-Bassells R., Vierheilig H., Ocampo J.A., Godeas A. Arbuscular mycorrhizal colonization of tomato by Gigaspora and Glomus species in the presence of root flavonoids. Journal of Plant Physiology 2005, 162:625-633.
45. Schüller H.J. Transcriptional control of nonfermentative metabolism in the yeast. Saccharomyces cerevisiae. Current Genetics 2003, 43:139-160.
46. Small C.L.N., Bidochka M.J. Up-regulation of Pr1, a subtilisin-like protein, during conidiation in the insect pathogen Metarhizium anisopliae. Mycological Research 2005, 109:307-313.
47. St. Leger R.J., Butt T.M., Staples R.C., Roberts D.W. Synthesis of proteins including a cuticle-degrading protease during differentiation of the entomopathogenic fungus Metarhizium anisopliae. Experimental Mycology 1989, 13:253-262.
48. 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 entomopathogenic fungus, Metarhizium anisopliae. Gene 1992, 120:119-124.
49. Todd R.B., Andrianopoulos A., Davis M.A., Hynes M.J. FacB, the Aspergillus nidulans activator of acetate utilization genes, binds dissimilar DNA sequences. The EMBO Journal 1998, 17:2042-2054.
50. Tyler B.M., de la Serna I., Cujec T., Ballica R. Mechanism of coordinate regulation of ribosomal genes by nutrition and growth in Neurospora. Nucleic Acid Research 1991, 19:6511-6517.
51. Uren N.C. Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. The Rhizosphere: Biochemistry and Organic Substances at the Soil-Plant Interface 2007, 1-21. CRC Press, Boca Raton, Florida. R. Pinton, Z. Varanini, P. Nannipieri (Eds.).
52. Uyar E.O., Hamamci H., Türke S. Effect of different stresses on trehalose levels in Rhizopus oryzae. Journal of Basic Microbiology 2010, 50:368-372.
53. Vancura V., Stanek M. Root exudates of plants. V. Kinetics of exudates from bean roots as related to the presence of reserve compounds in cotyledons. Plant and Soil 1975, 43:547-559.
54. 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.
55. Wang C., Skrobek A., Butt T.M. Investigations on the destruxin production of the entomopathogenic fungus Metarhizium anisopliae. Journal of Invertebrate Pathology 2004, 85:168-174.
56. 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.
57. 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.
58. Wu C. Heat shock transcription factors: structure and regulation. Annual Review of Cell and Developmental Biology 1995, 11:441-469.
59. Wyrebek M, Huber C, Sasan RK, Bidochka MJ, 2011. Three sympatrically occurring species of Metarhizium show plant rhizosphere specificity. Microbiology, doi:10.1099/mic.0.051102-0.
60. Young E.T., Dombek K.M., Tachibana C., Ideker T. Multiple pathways are co-regulated by the protein kinase Snf1 and the transcription factors Adr1 and Cat8. Journal of Biology and Chemisty 2003, 278:26146-26158.
61. Yu J.H., Hamari Z., Han K.H., Seo J.A., Reyes-Dominguez Y., Scazzocchio C. Double-joint PCR: a PCR based molecular tool for gene manipulations in filamentous fungi. Fungal Genetics and Biology 2004, 41:973-981.
62. 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 entomopathogenic fungus, Beauveria bassiana. Molecular Microbiology 2011, 80:811-826.