PacC and pH-dependent transcriptome of the mycotrophic fungus Trichoderma virens

BMC Genomics

Volumn 14, Issue 1, 2013, Pages

  Trushina, Naomi ^a   Levin, Michal ^a   Mukherjee, Prasun K ^b,c   Horwitz, Benjamin A ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

^b BHABHA ATOMIC RESEARCH CENTRE   (India)

^c CENTRAL INSTITUTE FOR COTTON RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR PACC; TRANSCRIPTOME; UNCLASSIFIED DRUG;

ACIDITY; ALKALINITY; ARTICLE; ATHELIA ROLFSII; BINDING SITE; CONTROLLED STUDY; FUNGAL GENE; FUNGAL STRAIN; FUNGUS GROWTH; GENE DELETION; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; HYPOCREA VIRENS; NONHUMAN; PACC GENE; PH; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION; THANATEPHORUS CUCUMERIS;

ALLELES; BASE SEQUENCE; BASIDIOMYCOTA; BINDING SITES; CLUSTER ANALYSIS; DNA; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE KNOCKOUT TECHNIQUES; GENES, FUNGAL; HYDROGEN-ION CONCENTRATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PLANT DISEASES; RHIZOCTONIA; TRANSCRIPTION FACTORS; TRANSCRIPTOME; TRICHODERMA;

ATHELIA ROLFSII; FUNGI; HYPOCREA VIRENS; THANATEPHORUS CUCUMERIS; TRICHODERMA;

EID: 84874347145     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/1471-2164-14-138     Document Type: Article

References (69)

1. Lamb TM, Xu W, Diamond A, Mitchell AP. Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J Biol Chem 2001, 276(3):1850-1856.
2. Nobile CJ, Solis N, Myers CL, Fay AJ, Deneault JS, Nantel A, Mitchell AP, Filler SG. Candida albicans transcription factor Rim101 mediates pathogenic interactions through cell wall functions. Cell Microbiol 2008, 10(11):2180-2196. 10.1111/j.1462-5822.2008.01198.x, 2701370, 18627379.
3. Peñalva MA, Tilburn J, Bignell E, Arst HN. Ambient pH gene regulation in fungi: making connections. Trends Microbiol 2008, 16(6):291-300. 10.1016/j.tim.2008.03.006, 18457952.
4. Caracuel Z, Roncero MI, Espeso EA, Gonzalez-Verdejo CI, García-Maceira FI, Di Pietro A. The pH signalling transcription factor PacC controls virulence in the plant pathogen Fusarium oxysporum. Mol Microbiol 2003, 48(3):765-779. 10.1046/j.1365-2958.2003.03465.x, 12694620.
5. Caracuel Z, Casanova C, Roncero MI, Di Pietro A, Ramos J. pH response transcription factor PacC controls salt stress tolerance and expression of the P-Type Na+ -ATPase Ena1 in Fusarium oxysporum. Eukaryot Cell 2003, 2(6):1246-1252. 10.1128/EC.2.6.1246-1252.2003, 326653, 14665459.
6. Hervas-Aguilar A, Galindo A, Peñalva MA. Receptor-independent Ambient pH signaling by ubiquitin attachment to fungal arrestin-like PalF. J Biol Chem 2010, 285(23):18095-18102. 10.1074/jbc.M110.114371, 2878570, 20368671.
7. Denison SH, Negrete-Urtasun S, Mingot JM, Tilburn J, Mayer WA, Goel A, Espeso EA, Peñalva MA, Arst HN. Putative membrane components of signal transduction pathways for ambient pH regulation in Aspergillus and meiosis in Saccharomyces are homologous. Mol Microbiol 2001, 39(1):211. 10.1046/j.1365-2958.2001.02254.x, 11123703.
8. Peñalva MA, Arst HN. Recent advances in the characterization of ambient pH regulation of gene expression in filamentous fungi and yeasts. Annu Rev Microbiol 2004, 58:425-451. 10.1146/annurev.micro.58.030603.123715, 15487944.
9. Díez E, Alvaro J, Espeso EA, Rainbow L, Suarez T, Tilburn J, Arst HN, Peñalva MA. Activation of the Aspergillus PacC zinc finger transcription factor requires two proteolytic steps. EMBO J 2002, 21(6):1350-1359. 10.1093/emboj/21.6.1350, 125927, 11889040.
10. Galindo A, Calcagno-Pizarelli AM, Arst HN, Peñalva MA. An ordered pathway for the assembly of fungal ESCRT-containing ambient pH signalling complexes at the plasma membrane. J Cell Sci 2012, 125(Pt 7):1784-1795. 3346829, 22344261.
11. Prusky D, Yakoby N. Pathogenic fungi: leading or led by ambient pH?. Mol Plant Pathol 2003, 4(6):509-516. 10.1046/j.1364-3703.2003.00196.x, 20569410.
12. Miyara I, Shnaiderman C, Meng X, Vargas WA, Díaz-Minguez JM, Thon M, Sherman A, Prusky DB. Role of nitrogen-metabolism genes expressed during pathogenicity of the alkalinizing Colletotrichum gloeosporioides and their differential expression in acidifying pathogens. Mol Plant Microbe Interact 2012, 25(9):1251-1263. 10.1094/MPMI-01-12-0017-R, 22571816.
13. Barad S, Horowitz SB, Moskovitch O, Lichter A, Sherman A, Prusky D. A penicillium expansum glucose oxidase-encoding gene, GOX2, is essential for gluconic acid production and acidification during colonization of deciduous fruit. Mol Plant Microbe Interact 2012, 25(6):779-788. 10.1094/MPMI-01-12-0002, 22352719.
14. Miyara I, Shafran H, Davidzon M, Sherman A, Prusky D. pH Regulation of ammonia secretion by Colletotrichum gloeosporioides and its effect on appressorium formation and pathogenicity. Mol Plant Microbe Interact 2010, 23(3):304-316. 10.1094/MPMI-23-3-0304, 20121452.
15. Alkan N, Davydov O, Sagi M, Fluhr R, Prusky D. Ammonium secretion by Colletotrichum coccodes activates host NADPH oxidase activity enhancing host cell death and fungal virulence in tomato fruits. Mol Plant Microbe Interact 2009, 22(12):1484-1491. 10.1094/MPMI-22-12-1484, 19888814.
16. Alkan N, Fluhr R, Sherman A, Prusky D. Role of ammonia secretion and pH modulation on pathogenicity of Colletotrichum coccodes on tomato fruit. Mol Plant Microbe Interact 2008, 21(8):1058-1066. 10.1094/MPMI-21-8-1058, 18616402.
17. Prusky D, McEvoy JL, Leverentz B, Conway WS. Local modulation of host pH by Colletotrichum species as a mechanism to increase virulence. Mol Plant Microbe Interact 2001, 14(9):1105-1113. 10.1094/MPMI.2001.14.9.1105, 11551075.
18. Rollins JA, Dickman MB. pH signaling in Sclerotinia sclerotiorum: identification of a pacC/RIM1 homolog. Appl Environ Microbiol 2001, 67(1):75-81. 10.1128/AEM.67.1.75-81.2001, 92519, 11133430.
19. Kramer-Haimovich H, Servi E, Katan T, Rollins J, Okon Y, Prusky D. Effect of ammonia production by Colletotrichum gloeosporioides on pelB activation, pectate lyase secretion, and fruit pathogenicity. Appl Environ Microbiol 2006, 72(2):1034-1039. 10.1128/AEM.72.2.1034-1039.2006, 1392887, 16461646.
20. You BJ, Choquer M, Chung KR. The Colletotrichum acutatum gene encoding a putative pH-responsive transcription regulator is a key virulence determinant during fungal pathogenesis on citrus. Mol Plant Microbe Interact 2007, 20(9):1149-1160. 10.1094/MPMI-20-9-1149, 17849717.
21. Rollins JA. The Sclerotinia sclerotiorum pac1 gene is required for sclerotial development and virulence. Mol Plant Microbe Interact 2003, 16(9):785-795. 10.1094/MPMI.2003.16.9.785, 12971602.
22. Li M, Martin SJ, Bruno VM, Mitchell AP, Davis DA. Candida albicans Rim13p, a protease required for Rim101p processing at acidic and alkaline pHs. Eukaryot Cell 2004, 3(3):741-751. 10.1128/EC.3.3.741-751.2004, 420141, 15189995.
23. Martinez-Rossi NM, Persinoti GF, Peres NT, Rossi A. Role of pH in the pathogenesis of dermatophytoses. Mycoses 2012, 55(5):381-387. 10.1111/j.1439-0507.2011.02162.x, 22211778.
24. Bignell E, Negrete-Urtasun S, Calcagno AM, Haynes K, Arst HN, Rogers T. The Aspergillus pH-responsive transcription factor PacC regulates virulence. Mol Microbiol 2005, 55(4):1072-1084.
25. St Leger RJ, Joshi L, Roberts D. Ambient pH is a major determinant in the expression of cuticle-degrading enzymes and hydrophobin by Metarhizium anisopliae. Appl Environ Microbiol 1998, 64(2):709-713. 106106, 9464412.
26. MacCabe AP, Orejas M, Perez-Gonzalez JA, Ramón D. Opposite patterns of expression of two Aspergillus nidulans xylanase genes with respect to ambient pH. J Bacteriol 1998, 180(5):1331-1333. 107024, 9495775.
27. Vankuyk PA, Diderich JA, MacCabe AP, Hererro O, Ruijter GJ, Visser J. Aspergillus niger mstA encodes a high-affinity sugar/H+ symporter which is regulated in response to extracellular pH. Biochem J 2004, 379(Pt 2):375-383. 1224080, 14717659.
28. Eisendle M, Oberegger H, Buttinger R, Illmer P, Haas H. Biosynthesis and uptake of siderophores is controlled by the PacC-mediated ambient-pH Regulatory system in Aspergillus nidulans. Eukaryot Cell 2004, 3(2):561-563. 10.1128/EC.3.2.561-563.2004, 387658, 15075286.
29. Keller NP, Nesbitt C, Sarr B, Phillips TD, Burow GB. pH regulation of sterigmatocystin and aflatoxin biosynthesis in Aspergillus spp. Phytopathology 1997, 87(6):643-648. 10.1094/PHYTO.1997.87.6.643, 18945083.
30. Druzhinina IS, Seidl-Seiboth V, Herrera-Estrella A, Horwitz BA, Kenerley CM, Monte E, Mukherjee PK, Zeilinger S, Grigoriev IV, Kubicek CP. Trichoderma: the genomics of opportunistic success. Nat Rev Microbiol 2011, 9(10):749-759. 10.1038/nrmicro2637, 21921934.
31. Verma M, Brar S, Surampalli R, Valero J. Antagonistic fungi, Trichoderma spp.: panoply of biological control. Biochem Eng J 2007, 37:1-20.
32. Benitez T, Rincón AM, Limón MC, Codón AC. Biocontrol mechanisms of Trichoderma strains. Int Microbiol 2004, 7(4):249-260.
33. Harman GE, Howell CR, Viterbo A, Chet I, Lorito M. Trichoderma species-opportunistic, avirulent plant symbionts. Nat Rev Microbiol 2004, 2(1):43-56. 10.1038/nrmicro797, 15035008.
34. Shoresh M, Harman GE. Differential expression of maize chitinases in the presence or absence of Trichoderma harzianum strain T22 and indications of a novel exo- endo-heterodimeric chitinase activity. BMC Plant Biol 2010, 10:136. 10.1186/1471-2229-10-136, 3017806, 20594307.
35. Moreno-Mateos MA, Delgado-Jarana J, Codón AC, Benitez T. pH and Pac1 control development and antifungal activity in Trichoderma harzianum. Fungal Genet Biol 2007, 44(12):1355-1367. 10.1016/j.fgb.2007.07.012, 17881256.
36. Steyaert JM, Weld RJ, Stewart A. Ambient pH intrinsically influences Trichoderma conidiation and colony morphology. Fungal Biol 2010, 114(2-3):198-208.
37. Gresik M, Kolarova N, Farkaš V. Hyperpolarization and intracellular acidification in Trichoderma viride as a response to illumination. J Gen Microbiol 1991, 137(11):2605-2609.
38. Mukherjee PK, Mukhopadhyay AN, Sarmah DK, Shrestha SM. Comparative antagonistic properties of Gliocladium virens and Trichoderma harzianum on Sclerotium rolfsii and Rhizoctonia solani - its relevance to understanding the mechanisms of biocontrol. J Phytopathology 1995, 143:275-279.
39. Kubicek CP, Herrera-Estrella A, Seidl-Seiboth V, Martinez DA, Druzhinina IS, Thon M, Zeilinger S, Casas-Flores S, Horwitz BA, Mukherjee PK. Comparative genome sequence analysis underscores mycoparasitism as the ancestral life style of Trichoderma. Genome Biol 2011, 12(4):R40. 10.1186/gb-2011-12-4-r40, 3218866, 21501500.
40. Grigoriev I, Nordberg H, Shabalov I, Aerts A, Cantor M, Goodstein D, Kuo A, Minovitsky S, Nikitin R, Ohm R. The genome portal of the department of energy joint genome institute. Nucleic Acids Res 2012, 40(1):D26-32. 10.1093/nar/gkr947, 3245080, 22110030.
41. Espeso EA, Tilburn J, Sanchez-Pulido L, Brown CV, Valencia A, Arst HN, Peñalva MA. Specific DNA recognition by the Aspergillus nidulans three zinc finger transcription factor PacC. J Mol Biol 1997, 274(4):466-480. 10.1006/jmbi.1997.1428, 9417928.
42. Caddick MX, Brownlee AG, Arst HN. Regulation of gene expression by pH of the growth medium in Aspergillus nidulans. Mol Gen Genet 1986, 203(2):346-353. 10.1007/BF00333978, 3016485.
43. Selvig K, Alspaugh JA. pH Response Pathways in Fungi: Adapting to Host-derived and Environmental Signals. Mycobiology 2011, 39(4):249-256. 10.5941/MYCO.2011.39.4.249, 3385132, 22783112.
44. Orejas M, Espeso EA, Tilburn J, Sarkar S, Arst HN, Peñalva MA. Activation of the Aspergillus PacC transcription factor in response to alkaline ambient pH requires proteolysis of the carboxy-terminal moiety. Genes Dev 1995, 9(13):1622-1632. 10.1101/gad.9.13.1622, 7628696.
45. Tilburn J, Sarkar S, Widdick DA, Espeso EA, Orejas M, Mungroo J, Peñalva MA, Arst HN. The Aspergillus PacC zinc finger transcription factor mediates regulation of both acid- and alkaline-expressed genes by ambient pH. EMBO J 1995, 14(4):779-790. 398143, 7882981.
46. Catlett NL, Lee B-N, Yoder O, Turgeon BG. Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet Newsl Online 2003, 50:9-11.
47. Lewis J, Papavizas G. Production of chlamydospores and conidia by Trichoderma spp. in liquid and solid growth media. Soil Biol Biochem 1983, 15:351-357.
48. Lamb TM, Mitchell AP. The transcription factor Rim101p governs ion tolerance and cell differentiation by direct repression of the regulatory genes NRG1 and SMP1 in Saccharomyces cerevisiae. Mol Cell Biol 2003, 23(2):677-686. 10.1128/MCB.23.2.677-686.2003, 151549, 12509465.
49. Bensen ES, Martin SJ, Li M, Berman J, Davis DA. Transcriptional profiling in Candida albicans reveals new adaptive responses to extracellular pH and functions for Rim101p. Mol Microbiol 2004, 54(5):1335-1351. 10.1111/j.1365-2958.2004.04350.x, 15554973.
50. Brakhage AA. Regulation of fungal secondary metabolism. Nat Rev Microbiol 2012, 11(1):21-32.
51. Keller NP, Hohn TM. Metabolic pathway gene clusters in filamentous fungi. Fungal Genet Biol 1997, 21(1):17-29. 10.1006/fgbi.1997.0970, 9073477.
52. Mukherjee PK, Buensanteai N, Moran-Díez ME, Druzhinina IS, Kenerley CM. Functional analysis of non-ribosomal peptide synthetases (NRPSs) in Trichoderma virens reveals a polyketide synthase (PKS)/NRPS hybrid enzyme involved in the induced systemic resistance response in maize. Microbiology 2012, 158(Pt 1):155-165.
53. Bushley KE, Turgeon BG. Phylogenomics reveals subfamilies of fungal nonribosomal peptide synthetases and their evolutionary relationships. BMC Evol Biol 2010, 10:26. 10.1186/1471-2148-10-26, 2823734, 20100353.
54. Kim KH, Cho Y, La Rota M, Cramer RA, Lawrence CB. Functional analysis of the Alternaria brassicicola non-ribosomal peptide synthetase gene AbNPS2 reveals a role in conidial cell wall construction. Mol Plant Pathol 2007, 8(1):23-39. 10.1111/j.1364-3703.2006.00366.x, 20507476.
55. Oide S, Krasnoff SB, Gibson DM, Turgeon BG. Intracellular siderophores are essential for ascomycete sexual development in heterothallic Cochliobolus heterostrophus and homothallic Gibberella zeae. Eukaryot Cell 2007, 6(8):1339-1353. 10.1128/EC.00111-07, 1951124, 17601875.
56. Amich J, Vicentefranqueira R, Leal F, Calera JA. Aspergillus fumigatus survival in alkaline and extreme zinc-limiting environments relies on the induction of a zinc homeostasis system encoded by the zrfC and aspf2 genes. Eukaryot Cell 2010, 9(3):424-437. 10.1128/EC.00348-09, 2837988, 20038606.
57. Serrano R, Martin H, Casamayor A, Ariño J. Signaling alkaline pH stress in the yeast Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway. J Biol Chem 2006, 281(52):39785-39795. 10.1074/jbc.M604497200, 17088254.
58. Plaine A, Walker L, Da Costa G, Mora-Montes HM, McKinnon A, Gow NA, Gaillardin C, Munro CA, Richard ML. Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol 2008, 45(10):1404-1414. 10.1016/j.fgb.2008.08.003, 2649418,2649418, 18765290.
59. Spreghini E, Davis DA, Subaran R, Kim M, Mitchell AP. Roles of Candida albicans Dfg5p and Dcw1p cell surface proteins in growth and hypha formation. Eukaryot Cell 2003, 2(4):746-755. 10.1128/EC.2.4.746-755.2003, 178370, 12912894.
60. Glare T, Caradus J, Gelernter W, Jackson T, Keyhani N, Kohl J, Marrone P, Morin L, Stewart A. Have biopesticides come of age?. Trends Biotechnol 2012, 30(5):250-258. 10.1016/j.tibtech.2012.01.003, 22336383.
61. Longa CMO, Pertot I, Tosi S. Ecophysiological requirements and survival of a Trichoderma atroviride isolate with biocontrol potential. J Basic Microbiol 2008, 48(4):269-277. 10.1002/jobm.200700396, 18720503.
62. Vincent O, Rainbow L, Tilburn J, Arst HN, Peñalva MA. YPXL/I is a protein interaction motif recognized by Aspergillus PalA and its human homologue, AIP1/Alix. Mol Cell Biol 2003, 23(5):1647-1655. 10.1128/MCB.23.5.1647-1655.2003, 151718, 12588984.
63. Gotoh Y, Eguchi Y, Watanabe T, Okamoto S, Doi A, Utsumi R. Two-component signal transduction as potential drug targets in pathogenic bacteria. Curr Opin Microbiol 2010, 13(2):232-239. 10.1016/j.mib.2010.01.008, 20138000.
64. Mukherjee PK, Shrestha SM, Mukhopadhyay AN. Baiting with Sclerotium rolfsii for selective isolation of Gliocladium virens from natural soil. Biocontrol Science and Technology 1993, 3:101-104.
65. Lu S, Lyngholm L, Yang G, Bronson C, Yoder OC, Turgeon BG. Tagged mutations at the Tox1 locus of Cochliobolus heterostrophus by restriction enzyme-mediated integration. Proc Natl Acad Sci USA 1994, 91(26):12649-12653. 10.1073/pnas.91.26.12649, 45496, 7809094.
66. Yu JH, Hamari Z, Han KH, Seo JA, Reyes-Dominguez Y, Scazzocchio C. Double-joint PCR: a PCR-based molecular tool for gene manipulations in filamentous fungi. Fungal Genet Biol 2004, 41(11):973-981. 10.1016/j.fgb.2004.08.001, 15465386.
67. Turgeon BG, Condon B, Liu J, Zhang N. Protoplast transformation of filamentous fungi. Methods Mol Biol 2010, 638:3-19. 10.1007/978-1-60761-611-5_1, 20238257.
68. Levin M, Hashimshony T, Wagner F, Yanai I. Developmental milestones punctuate gene expression in the Caenorhabditis embryo. Dev Cell 2012, 22(5):1101-1108. 10.1016/j.devcel.2012.04.004, 22560298.
69. Yanai I, Peshkin L, Jorgensen P, Kirschner MW. Mapping gene expression in two Xenopus species: evolutionary constraints and developmental flexibility. Dev Cell 2011, 20(4):483-496. 10.1016/j.devcel.2011.03.015, 3118554, 21497761.