The role of three calcineurin subunits and a related transcription factor (Crz1) in conidiation, multistress tolerance and virulence in Beauveria bassiana

Applied Microbiology and Biotechnology

Volumn 99, Issue 2, 2015, Pages 827-840

  Li, Fang ^a   Wang, Zheng Liang ^a,b   Zhang, Long Bin ^a   Ying, Sheng Hua ^a   Feng, Ming Guang ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b CHINA JILIANG UNIVERSITY   (China)

Author keywords

Asexual development; Calcineurin pathway; Entomopathogenic fungi; Functional diversity; Stress response; Virulence

Indexed keywords

DEFECTS; FUNGI; TRANSCRIPTION FACTORS;

ASEXUAL DEVELOPMENT; CALCINEURIN; ENTOMOPATHOGENIC FUNGUS; FUNCTIONAL DIVERSITY; STRESS RESPONSE; VIRULENCE;

TRANSCRIPTION;

CALCINEURIN; CALCINEURIN SUBUNIT A1; CALCINEURIN SUBUNIT A2; CALCINEURIN SUBUNIT B; CALCIUM ION; CARBENDAZIM; CATALASE; MAGNESIUM ION; MANGANESE; MANNITOL; MITOGEN ACTIVATED PROTEIN KINASE; OXIDIZING AGENT; PHOSPHATASE; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR CRZ1; TREHALOSE; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; ZINC ION; BIOLOGICAL CONTROL AGENT; FUNGAL PROTEIN; INSECTICIDE;

CATALYST; ENTOMOPATHOGENIC ORGANISM; ENZYME ACTIVITY; EUKARYOTE; FUNCTIONAL CHANGE; FUNGUS; GROWTH RATE; MUTATION; OSMOSIS; PHENOTYPE; SIGNAL; VIRULENCE;

ARTICLE; BACTERIAL CELL WALL; BEAUVERIA BASSIANA; CELL STRESS; CONIDIUM; CONTROLLED STUDY; DELETION MUTANT; DOWN REGULATION; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FUNGAL GENE; FUNGAL SPORE GERMINATION; FUNGAL VIRULENCE; FUNGUS GROWTH; GENETIC COMPLEMENTATION; GENETIC TRANSCRIPTION; HEAT SHOCK; HOST PATHOGEN INTERACTION; LARVA; NONHUMAN; OSMOLARITY; OSMOTIC STRESS; PHENOTYPE; SIGNAL TRANSDUCTION; SPODOPTERA LITURA; ULTRAVIOLET B RADIATION; WILD TYPE; ANIMAL; BEAUVERIA; BIOLOGICAL CONTROL AGENT; CELL WALL; CHEMISTRY; ESCHERICHIA COLI; GENE DELETION; GENETICS; LD50; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; PATHOGENICITY; PHOSPHORYLATION; PHYSIOLOGICAL STRESS; PHYSIOLOGY; SPODOPTERA; VIRULENCE;

CORDYCEPS BASSIANA; EUKARYOTA; FUNGI; SPODOPTERA LITURA;

ANIMALS; BEAUVERIA; BIOLOGICAL CONTROL AGENTS; CALCINEURIN; CATALASE; CELL WALL; CLONING, MOLECULAR; DOWN-REGULATION; ESCHERICHIA COLI; FUNGAL PROTEINS; GENE DELETION; INSECTICIDES; LARVA; LETHAL DOSE 50; PHENOTYPE; PHOSPHORYLATION; SPODOPTERA; STRESS, PHYSIOLOGICAL; SUPEROXIDE DISMUTASE; TRANSCRIPTION FACTORS; VIRULENCE;

EID: 84921757399     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6124-6     Document Type: Article

References (65)

1. Aramburu J, Rao A, Klee CB (2000) Calcineurin: from structure to function. Curr Top Cell Regul 36:237–295
2. Bader T, Bodendorfer B, Schröppel K, Morschhäuser J (2003) Calcineurin is essential for virulence in Candida albicans. Infect Immun 71:5344–5354
3. Blankenship JR, Heitman J (2005) Calcineurin is required for Candida albicans to survive calcium stress in serum. Infect Immun 73:5767–5774
4. Blankenship JR, Wormley FL, Boyce MK, Schell WA, Filler SG, Perfect JR, Heitman J (2003) Calcineurin is essential for Candida albicans survival in serum and virulence. Eukaryot Cell 2:422–430
5. Cao YQ, Du MJ, Luo S, Xia YX (2014) Calcineurin modulates growth, stress tolerance, and virulence in Metarhizium acridum and its regulatory network. Appl Microbiol Biotechnol 98:8253–8265
6. Cervantes-Chávez JA, Ali S, Bakkeren G (2011) Response to environmental stresses, cell-wall integrity, and virulence are orchestrated through the calcineurin pathway in Ustilago hordei. Mol Plant Microbe Interact 24:219–232
7. Chen YL, Brand A, Morrison EL, Silao FG, Bigol UG, Malbas FF Jr, Nett JE, Andes DR, Solis NV, Filler SG, Averette A, Heitman J (2011) Calcineurin controls drug tolerance, hyphal growth, and virulence in Candida dubliniensis. Eukaryot Cell 10:803–819
8. Choi J, Kim Y, Kim S, Park J, Lee YH (2009) MoCRZ1, a gene encoding a calcineurin-responsive transcription factor, regulates fungal growth and pathogenicity of Magnaporthe oryzae. Fungal Genet Biol 46:243–254
9. Cramer RA Jr, Perfect BZ, Pinchai N, Park S, Perlin DS, Asfaw YG, Heitman J, Perfect JR, Steinbach WJ (2008) Calcineurin target CrzA regulates conidial germination, hyphal growth, and pathogenesis of Aspergillus fumigatus. Eukaryot Cell 7:1085–1097
10. Cruz MC, Sia RA, Olson M, Cox GM, Heitman J (2000) Comparison of the roles of calcineurin in physiology and virulence inserotype D and serotype A strains of Cryptococcus neoformans. Infect Immun 68:982–985
11. Cruz MC, Fox DS, Heitman J (2001) Calcineurin is required for hyphal elongation during mating and haploid fruiting in Cryptococcus neoformans. EMBO J 20:1020–1032
12. 2+ transport in Saccharomyces cerevisiae. J Exp Biol 196:157–166
13. Cyert MS (2003) Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem Biophys Res Commun 311:1143–1150
14. da Silva Ferreira ME, Heinekamp T, Härtl A, Brakhage AA, Semighini CP, Harris SD, Savoldi M, de Gouvêa PF, de Souza Goldman MH, Goldman GH (2007) Functional characterization of the Aspergillus fumigatus calcineurin. Fungal Genet Biol 44:219–230
15. de Faria M, Wraight SP (2007) Mycoinsecticides and Mycoacaricides: a comprehensive list with worldwide coverage and international classification of formulation types. Biol Control 43:237–256
16. 2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 9:1149–1162
17. Elbein AD, Pan YT, Pastuszak I, Carroll D (2003) New insights on trehalose: a multifunctional molecule. Glycobiology 13:17R–27R
18. Fang WG, St Leger RJ (2012) Enhanced UV resistance and improved killing of malaria mosquitoes by photolyase transgenic entomopathogenic fungi. PLoS ONE 7:e43069
19. Fang WG, Zhang YJ, Yang XY, Zheng XL, Duan H, Li Y, Pei Y (2004) Agrobacterium tumefaciens-mediated transformation of Beauveria bassiana using an herbicide resistance gene as a selection marks. J Invertebr Pathol 85:18–24
20. Fox DS, Heitman J (2002) Good fungi gone bad: the corruption of calcineurin. Bioassays 24:894–903
21. Free SJ (2013) Fungal cell wall organization and biosynthesis. Adv Genet 81:33–82
22. Harel A, Bercovich S, Yarden O (2006) Calcineurin is required for sclerotial development and pathogenicity of Sclerotinia sclerotiorum in an oxalic acid-independent manner. Mol Plant Microbe Interact 19:682–693
23. 2+/calcineurin-dependent signaling pathway in the gray mold Botrytis cinerea: the role of calcipressin in modulating calcineurin activity. PLoS ONE 7:e41761. doi:10.1371/journal.pone.0041761
24. Hemenway CS, Heitman J (1999) Lic4, a nuclear phosphoprotein that cooperates with calcineurin to regulate cation homeostasis in Saccharomyces cerevisiae. Mol Gen Genet 261:388–401
25. − homeostasis in fission yeast. Identification of distinct branches of calcineurin signaling pathway in fission yeast. J Biol Chem 278:18078–18084
26. 2+/calmodulin-dependent protein phosphorylation and dephosphorylation. FEMS Microbiol Lett 183:215–219
27. Juvvadi PR, Kuroki Y, Arioka M, Nakajima H, Kitamoto K (2003) Functional analysis of the calcineurin-encoding gene cnaA from Aspergillus oryzae: evidence for its putative role in stress adaptation. Arch Microbiol 179:416–422
28. Juvvadi PR, Fortwendel JR, Rogg LE, Burns KA, Randell SH, Steinbach WJ (2011) Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in Aspergillus fumigatus. Mol Microbiol 82:1235–1259
29. Kashyap RS, Rajan AN, Ramteke SS, Agrawal VS, Kelkar SS, Purohit HJ, Taori GM, Daginawala HF (2007) Diagnosis of tuberculosis in an Indian population by an indirect ELISA protocol based on detection of Antigen 85 complex: a prospective cohort study. BMC Infect Dis 7:74
30. Kim S, Hu J, Oh Y, Park J, Choi J, Lee YH, Dean RA, Mitchell TK (2010) Combining ChIP-chip and expression profiling to model the MoCRZ1 mediated circuit for Ca/calcineurin signaling in the rice blast fungus. PLoS Pathog 6:e1000909
31. Kothe GO, Free SJ (1998) Calcineurin subunit B is required for normal vegetative growth in Neurospora crassa. Fungal Genet Biol 23:248–258
32. Kraus PR, Heitman J (2003) Coping with stress: calmodulin and calcineurin in model and pathogenic fungi. Biochem Biophys Res Commun 311:1151–1157
33. Lee SC, Li A, Calo S, Heitman J (2013) Calcineurin plays key roles in the dimorphic transition and virulence of the human pathogenic Zygomycete Mucor circinelloides. PLoS Genet 9:e1003625. doi:10.1371/journal.ppat.1003625
34. Liu Q, Ying SH, Feng MG, Jiang XH (2009) Physiological implication of intracellular trehalose and mannitol changes in response of entomopathogenic fungus Beauveria bassiana to thermal stress. Antonie Van Leeuwenhoek 95:65–75
35. −ΔΔCt method. Methods 25:402–408
36. Matheos DP, Kingsbury TJ, Ahsan US, Cunningham KV (1997) Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisise. Genes Dev 11:345–3458
37. Miyakawa T, Mizunuma M (2007) Physiological roles of calcineurin in Saccharomyces cerevisiae with special emphasis on its roles in G2/M cell-cycle regulation. Biosci Biotechnol Biochem 71:633–645
38. 2+/calmodulin binding proteins in Aspergillus nidulans cell cycle regulation. Prog Cell Cycle Res 2:217–228
39. Odom A, Muir S, Lim E, Toffaletti DL, Perfect J, Heitman J (1997) Calcineurin is required for virulence of Cryptococcus neoformans. EMBO J 16:2576–2589
40. 2+ gradient. Mol Gen Genet 256:104–114
41. Reedy JL, Filler SG, Heitman J (2010) Elucidating the Candida albicans calcineurin signaling cascade controlling stress response and virulence. Fungal Genet Biol 47:107–116
42. Rispail N, Soanes DM, Ant C, Czajkowski R, Grünler A, Huguet R, Perez-Nadales E, Poli A, Sartorel E, Valiante V, Yang M, Beffa R, Brakhage AA, Gow NAR, Kahmann R, Lebrun MH, Lenasi H, Perez-Martin J, Talbot NJ, Wendland J, Di Pietro A (2009) Comparative genomics of MAP kinase and calcium–calcineurin signaling components in plant and human pathogenic fungi. Fungal Genet Biol 46:287–298
43. Rusnak F, Mertz P (2000) Calcineurin: form and function. Physiol Rev 80:1483–1521
44. Sanglard D, Ischer F, Marchetti O, Entenza J, Bille J (2003) Calcineurin A of Candida albicans: involvement in antifungal tolerance, cell morphogenesis and virulence. Mol Microbiol 48:959–976
45. Santos M, de Larrinoa IF (2005) Functional characterization of the Candida albicans CRZ1 gene encoding a calcineurin-regulated transcription factor. Curr Genet 48:88–100
46. Schumacher J, de Larrinoa IF, Tudzynski B (2008) Calcineurin-responsive zinc finger transcription factor CRZ1 of Botrytis cinerea is required for growth, development and full virulence on bean plants. Eukaryot Cell 7:584–601
47. Seo JA, Guan Y, Yu JH (2006) FluG-dependent asexual development in Aspergillus nidulans occurs via derepression. Genetics 172:1535–1544
48. Song TT, Zhao J, Ying SH, Feng MG (2013) Differential contributions of five ABC transporters to mutidrug resistance, antioxidion and virulence of Beauveria bassiana, an entomopathogenic fungus. PLoS ONE 8:e62179
49. Soriani FM, Malavazi I, da Silva Ferreira ME, Savoldi M, Von Zeska Kress MR, de Souza Glodman MH, Loss O, Bignell E, Goldman GH (2008) Functional characterization of the Aspergillus fumigatus CRZ1 homologue, CrzA. Mol Microbiol 67:1274–1291
50. Soriani FM, Malavazi I, Savoldi M, Espeso E, Dinamarco TM, Bernardes LA, Ferreira ME, Goldman MH, Goldman GH (2010) Identification of possible targets of the Aspergillus fumigatus CRZ1 homologue, CrzA. BMC Microbiol 15:10–12
51. Steinbach WJ, Cramer RA, Perfect BZ, Asfaw YG, Sauer TC, Najvar LK, Kirkpatrick WR, Patterson TF, Benjamin DK, Heitman J, Perfect JR (2006) Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot Cell 5:1091–1103
52. Stie J, Fox D (2008) Calcineurin regulation in fungi and beyond. Eukaryot Cell 7:177–186
53. Viaud M, Brunet-Simon A, Brygoo Y, Pradier JM, Levis C (2003) Cyclophilin A and calcineurin functions investigated by gene inactivation, cyclosporine A inhibition and cDNA arrays approaches in the phytopathogenic fungus Botrytis cinerea. Mol Microbiol 50:1451–1465
54. Wanchoo A, Lewis MW, Keyhani NO (2009) Lectin mapping reveals stage-specific display of surface carbohydrates in in vitro and haemolymph-derived cells of the entomopathogenic fungus Beauveria bassiana. Microbiology SGM 155:3121–3133
55. Wang CS, Feng MG (2014) Advances in fundamental and applied studies in China of fungal biocontrol agents for use against arthropod pests. Biol Control 68:129–135
56. Wang CS, St Leger RJ (2007) The MAD1 adhesin of use of Metarhizium anisopliae links adhesion with blastospore production and virulence to insects, and the MAD2 adhesin enables attachment to plants. Eukaryot Cell 6:808–816
57. Wang ZL, Lu JD, Feng MG (2012) Primary roles of two dehydrogenases in the mannitol metabolism and multi-stress tolerance of entomopathogenic fungus Beauveria bassiana. Environ Microbiol 14:2139–2150
58. Wang ZL, Zhang LB, Ying SH, Feng MG (2013a) Catalases play differentiated roles in the adaptation of a fungal entomopathogen to environmental stresses. Environ Microbiol 15:409–418
59. Wang J, Zhou G, Ying SH, Feng MG (2013b) P-type calcium ATPase functions as a core regulator of Beauveria bassiana growth, conidiation and responses to multiple stressful stimuli through cross-talk with signalling networks. Environ Microbiol 15:967–979
60. West S, Bamborough P, Tully R (1993) Tertiary structure of calcineurin B by homology modeling. J Mol Graph 11:47–52
61. Xiao GH, Ying SH, Zheng P, Wang ZL, Zhang SW, Xie XQ, Shang YF, St Leger RJ, Zhao GP, Wang CS, Feng MG (2012) Genomic perspectives on the evolution of fungal entomopathogenicity in Beauveria bassiana. Sci Rep 2:483
62. Xie XQ, Li F, Ying SH, Feng MG (2012) Additive contributions of two manganese-cored superoxide dismutases (MnSODs) to antioxidation, UV tolerance and virulence of Beauveria bassiana. PLoS ONE 7:e30298
63. Yu JH, Mah JH, Seo JA (2005) Growth and developmental control in the model and pathogenic aspergilli. Eukaryot Cell 5:1577–1584
64. Zhang H, Zhao Q, Liu K, Zhang Z, Wang Y, Zheng X (2009) MgCRZ1, a transcription factor of Magnaporthe grisea, controls growth, development and is involved in full virulence. FEMS Microbiol Lett 293:160–169
65. Zhang SZ, Xia YX, Kim B, Keyhani NO (2011) 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. Mol Microbiol 80:811–826