Membrane transporters in self resistance of Cercospora nicotianae to the photoactivated toxin cercosporin

Current Genetics

Volumn 61, Issue 4, 2015, Pages 601-620

  Beseli, Aydin ^a   Amnuaykanjanasin, Alongkorn ^b   Herrero, Sonia ^a,c   Thomas, Elizabeth ^a   Daub, Margaret E ^a  

^a NORTH CAROLINA STATE UNIVERSITY   (United States)

^b NATIONAL SCIENCE AND TECHNOLOGY DEVELOPMENT AGENCY   (Thailand)

^c SYNGENTA BIOTECHNOLOGY INC   (United States)

Author keywords

ABC transporter; CnATR1; CnCFP; CRG1; MFS transporter; Perylenequinone; Photosensitizer resistance; Targeted gene disruption

Indexed keywords

ABC TRANSPORTER; CERCOSPORIN; TOXIN; UNCLASSIFIED DRUG; URACIL; ZINC; ANTIFUNGAL AGENT; CARRIER PROTEIN; CERCOSPORIN TRANSPORTER PROTEIN, CERCOSPORA; FUNGAL PROTEIN; PERYLENE; PHOTOSENSITIZING AGENT; SINGLET OXYGEN;

ARTICLE; CERCOSPORA; CERCOSPORA NICOTIANAE; CONTROLLED STUDY; DNA LIBRARY; GENE; GENE DISRUPTION; GENE EXPRESSION; HOST; INFECTION; MEMBRANE TRANSPORTER GENE; MUTANT; MUTATION; NEUROSPORA CRASSA; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TOXICITY; UPREGULATION; WILD TYPE; ANALOGS AND DERIVATIVES; ANTIFUNGAL RESISTANCE; CLASSIFICATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; METABOLISM; SACCHAROMYCETALES;

ANTIFUNGAL AGENTS; ATP-BINDING CASSETTE TRANSPORTERS; DRUG RESISTANCE, FUNGAL; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE TARGETING; MEMBRANE TRANSPORT PROTEINS; NEUROSPORA CRASSA; PERYLENE; PHOTOSENSITIZING AGENTS; PHYLOGENY; SACCHAROMYCETALES; SINGLET OXYGEN; URACIL; ZINC;

EID: 84944510899     PISSN: 01728083     EISSN: 14320983     Source Type: Journal    
DOI: 10.1007/s00294-015-0486-x     Document Type: Article

References (59)

1. Amnuaykanjanasin A, Daub ME (2009) The ABC transporter ATR1 is necessary for efflux of the toxin cercosporin in the fungus Cercospora nicotianae. Fung Genet Biol 46:146–158
2. 2-resistance genes in resistance to the photoactivated toxin cercosporin. FEMS Microbiol Lett 362:1–7
3. Burge CB (1998) Modeling dependencies in pre-mRNA splicing signals. In: Salzberg S, Searls D, Kasif S (eds) Computational methods in molecular biology, vol 8. Elsevier Science, Amsterdam, pp 127–163
4. Callahan T, Rose M, Meade M, Ehrenshaft M, Upchurch R (1999) CFP, the putative cercosporin transporter of Cercospora kikuchii, is required for wild type cercosporin production, resistance, and virulence on soybean. Mol Plant Microbe Interact 12:901–910
5. Chen HQ, Lee MH, Daub ME, Chung KR (2007a) Molecular analysis of the cercosporin biosynthetic gene cluster in Cercospora nicotianae. Mol Microbiol 64:755–770
6. Chen HQ, Lee MH, Chung KR (2007b) Functional characterization of three genes encoding putative oxidoreductases required for cercosporin toxin biosynthesis in the fungus Cercospora nicotianae. Microbiology 153:2781–2790
7. Choquer M, Lahey KA, Chen HL, Cao L, Ueng PP, Daub ME, Chung KR (2005) The CTB1 gene encoding a fungal polyketide synthase is required for cercosporin toxin biosynthesis and fungal virulence in Cercospora nicotianae. Molec Plant Microbe Interact 18:468–476
8. Choquer M, Lee MH, Bau HJ, Chung KR (2007) Deletion of a MFS transporter-like gene in Cercospora nicotianae reduces cercosporin toxin accumulation and fungal virulence. FEBS Lett 581:489–494
9. Chung KR, Daub ME, Kuchler K, Schaller C (2003) The CRG1 gene required for resistance to the singlet oxygen-generating cercosporin toxin in Cercospora nicotianae encodes a putative fungal transcription factor. Biochem Biophys Res Commun 302:302–310
10. Dahl SG, Sylte I, Ravna AW (2004) Structures and models of transporter proteins. J Pharmacol Exp Ther 309:302–310
11. Daub ME, Chung KR (2009) Photoactivated perylenequinone toxins in plant pathogenesis. In: Deising H (ed) The mycota V plant relationships, 2nd edn. Springer-Verlag, Berlin
12. Daub ME, Leisman GB, Clark RA, Bowden EF (1992) Reductive detoxification as a mechanism of fungal resistance to singlet-oxygen-generating photosensitizers. Proc Natl Acad Sci USA 89:9588–9592
13. Daub ME, Herrero S, Chung KR (2013) Reactive oxygen species in plant pathogenesis: the role of perylenequinone photosensitizers. Antiox Redox Signal 19:970–989
14. De Wit PJ, Van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam KA, Aerts AL, Bahkali AH, Beenen HG, Chettri P, Cox MP, Datema E, De Vries RP, Dhillon B, Ganley AR, Griffiths SA, Guo Y, Hamelin RC, Henrissat B, Kabir MS, Jashni MK, Kema G, Klaubauf S, Lapidus A, Levasseur A, Lindquist E, Mehrabi R, Ohm RA, Owen TJ, Salamov A, Schwelm A, Schijlen E, Sun H, Van den Burg HA, Van Ham RC, Zhang S, Goodwin SB, Grigoriev IV, Collemare J, Bradshaw RE (2012) The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genet. doi:10.1371/journal.pgen.1003088
15. Deininger P (1990) Molecular cloning: a laboratory manual. Anal Biochem 186:182–183
16. Dunnett CW (1955) A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assoc 50:1096–1121
17. Ehrenshaft M, Bilski P, Li M, Chignell CF, Daub ME (1999) A highly conserved sequence is a novel gene involved in denovo vitamin B6 biosynthesis. Proc Natl Acad Sci USA 96:9374–9378
18. Fachin AL, Maffei CM, Martinez-Rossi NM (1996) In vitro susceptibility of Trichophyton rubrum isolates to griseofulvin and tioconazole. Induction and isolation of a resistant mutant to both antimycotic drugs. Mycopathologia 135:141–143
19. Felder T, Bogengruber E, Tenreiro S, Ellinger A, Sá-Correia I, Briza P (2002) Dtr1p, a multidrug resistance transporter of the major facilitator superfamily, plays an essential role in spore wall maturation in Saccharomyces cerevisiae. Eukaryot Cell 1(5):799–810
20. Hayashi K, Schoonbeek HJ, De Waard MA (2002) Bcmfs1, a novel major facilitator superfamily transporter from Botrytis cinerea, provides tolerance towards the natural toxic compounds camptothecin and cercosporin and towards fungicides. Appl Environ Microbiol 68:4996–5004
21. Herrero S, Daub ME (2007) Genetic manipulation of vitamin B-6 biosynthesis in tobacco and fungi uncovers limitations to up-regulation of the pathway. Plant Sci 172:609–620
22. Herrero S, Amnuaykanjanasin A, Daub ME (2007) Identification of genes differentially expressed in the phytopathogenic fungus Cercospora nicotianae between cercosporin toxin-resistant and -susceptible strains. FEMS Microbiol Lett 275:326–337
23. Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
24. Higgins CF (2007) Multiple molecular mechanisms for multidrug resistance transporters. Nature 446:749–757
25. Jacobs M, Stahl U (1995) Gene regulation in mycelial fungi. In: Kueck U (ed) The mycota, II; genetics and biotechnology. Springer-Verlag, New York, pp 155–167
26. Jendzelovsky R, Mikes J, Koval J, Soucek K, Prochazkova J, Kello M, Sackova V, Hofmanova J, Kozubik A, Fedorocko P (2009) Drug efflux transporters, MRP1 and BCRP, affect the outcome of hypericin-mediated photodynamic therapy in HT-29 adenocarcinoma cells. Photochem Photobiol Sci 8:1716–1723
27. Jenns AE, Daub ME (1995) Characterization of mutants of Cercospora-nicotianae sensitive to the toxin cercosporin. Phytopathology 85:906–912
28. Jenns AE, Daub ME, Upchurch RG (1989) Regulation of cercosporin accumulation in culture by medium and temperature manipulation. Phytopathology 79:213–219
29. Jenns AE, Scott DL, Bowden EF, Daub ME (1995) Isolation of mutants of the fungus Cercospora nicotianae altered in their response to singlet-oxygen-generating photosensitizers. Photochem Photobiol Sci 61:488–493
30. Jones PM, George AM (2002) Mechanism of ABC transporters: a molecular dynamics simulation of a well characterized nucleotide-binding subunit. Proc Natl Acad Sci 99:12639–12644
31. Keim M, Williams RS, Harwood AJ (2004) An inverse PCR technique to rapidly isolate the flanking DNA of dictyostelium insertion mutants. Mol Biotechnol 26:221–224
32. Kristensen AS, Andersen J, Jörgensen TN, Sörensen L, Eriksen J, Loland CJ, Strömgaard K, Gether U (2011) SLC6 neurotransmitter transporters: structure, function, and regulation. Pharmacol Rev 63:585–640
33. Lamping E, Baret PV, Holmes AR, Monk BC, Goffeau A, Cannon RD (2010) Fungal PDR transporters:phylogeny, topology, motifs and function. Fung Genet Biol 47:127–142
34. 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 25:402–403
35. Lorang JM, Tuori RP, Martinez JP, Sawyer TL, Redman RS, Rollins JA, Wolpert JT, Johnson KB, Rodriguez RJ, Dickman MB, Ciuffetti LM (2001) Green fluorescent protein is lighting up fungal biology. Appl Environ Microb 67:1987–1994
36. Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Lu S, Marchler GH, Song JS, Thanki N, Yamashita RA, Zhang D, Bryant SH (2011) CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 41:D384–D389
37. Nagao K, Taguchi Y, Arioka M, Kadokura H, Takatsuki A, Yoda K, Yamasaki M (1995) BFR1+, a novel gene of Schizosaccharomyces pombe which confers brefeldin A resistance, is structurally related to the ATP-binding cassette superfamily. J Bacteriol 177:1536–1543
38. Panagiotis M, Kritonas K, Irini NO, Kiriaki C, Nicolaos P, Athanasios T (2007) Expression of the yeast cpd1 gene in tobacco confers resistance to the fungal toxin cercosporin. Biomolec Eng 24:245–251
39. Pantazopoulou A, Diallinas G (2007) Fungal nucleobase transporters. FEMS Microbiol Rev 31:657–675
40. Pao SS, Paulsen IT, Saier MH Jr (1998) Major facilitator superfamily. Microbiol Mol Biol Rev 62:1–34
41. Rockwell NC, Wolfger H, Kuchler K, Thorner J (2009) ABC transporter Pdr10 regulates the membrane microenvironment of Pdr12 in Saccharomyces cerevisiae. J Membr Biol 229:27–52
42. Roohparvar R, De Waard MA, Kema GHJ, Zwiers LH (2007) MgMfs1, a major facilitator superfamily transporter from the fungal wheat pathogen Mycosphaerella graminicola, is a strong protectant against natural toxic compounds and fungicides. Fung Genet Biol 44:378–388
43. Salazar G, Falcon-Perez JM, Harrison R, Faundez V (2009) SLC30A3 (ZnT3) oligomerization by dityrosine bonds regulates its subcellular localization and metal transport capacity. PLoS One 4(6):e5896. doi:10.1371/journalpone0005896
44. Schmittgen TD, Zakrajsek BA, Mills AG, Gorn V, Singer MJ, Reed MW (2000) Quantitative reverse transcription-polymerase chain reaction to study mRNA decay: comparison of endpoint and real-time methods. Anal Biochem 285:194–204
45. Schnabel G, Dai Q, Paradkar MR (2003) Cloning and expression analysis of the ATP binding cassette transporter MFABC1 gene and the alternative oxidase gene MfAOX1 from Monilinia fructicola. Pest Manag Sci 59:1143–1151
46. Servos J, Haase E, Brendel M (1993) Gene SNQ2 of Saccharomyces cerevisiae, which confers resistance to 4-nitroquinoline-N-oxide and other chemicals, encodes a 169 kDa protein homologous to ATP-dependent permeases. Mol Gen Genet 236:214–218
47. Smith KM, Kothe GO, Matsen CB, Khlafallah TK, Adhvaryu KK, Hemphill M, Freitag M, Motamedi MR, Selker EU (2008) The fungus Neurospora crassa displays telomeric silencing mediated by multiple sirtuins and by methylation of histone H3 lysine 9. Epigenet Chromatin 1:5
48. Stefanato F, Abou-Mansour E, Buchala A, Kretschmer M, Mosbach A, Hahn M, Bochet C, Metraux JP, Schoonbeek HJ (2009) The ABC-transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana. Plant J 58:499–510
49. Stoessl A, Abramowski Z, Lester HH, Rock GL, Towers GHN (1990) Further toxic properties of the fungal metabolite dothistromin. Mycopathologia 112:179–186
50. Sweigard J, Chumley F, Carroll A, Farrall L, Valent B (1997) A series of vectors for fungal transformation. Fung Genet Newslett 44:52–53
51. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL-X windows interface. Flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882
52. Toone EJ (2011) Advances in Enzymology and Related Areas of Molecular Biology. In: Barabote D, Thekkiniath J, Strauss RE, Vediyappan G (eds) Xenobiotic efflux in bacteria and fungi: a genomics update. John Wiley and Sons Inc., Hoboken, p 271
53. Ververidis P, Davrazou F, Diallinas G, Georgakopoulos D, Kanellis AK, Panopoulos N (2001) A novel putative reductase (Cpd1p) and the multidrug exporter Snq2p are involved in resistance to cercosporin and other singlet oxygen-generating photosensitizers in Saccharomyces cerevisiae. Curr Genet 39:127–136
54. Vogel HJ (1956) A convenient growth medium for Neurospora (medium N). Microbial Genet Bull 13:42–43
55. Wang H, Qi M, Cutler A (1993) A simple method of preparing plant samples for PCR. Nucleic Acids Res 21:4153–4154
56. Weyand S, Shimamura T, Yajima S, Suzuki S, Mirza O, Krusong K, Carpenter EP, Rutherford NG, Hadden JM, O’Reilly J, Ma P, Saidijam M, Patching SG, Hope RJ, Norbertczak HT, Roach PC, Iwata S, Henderson PJ, Cameron AD (2008) Structure and molecular mechanism of a nucleobase-cation-symport-1 family transporter. Science 322:709–713
57. Winer J (1999) Development and validation of real-time quantitative reverse transcriptase-polymerase chain reaction for monitoring gene expression in cardiac myocytes in vitro. Anal Biochem 270:41–49
58. +/glucose cotransporters (SLC5). Physiology 19:370–376
59. You B, Lee MH, Chung KR (2009) Gene-specific disruption in the filamentous fungus Cercospora nicotianae using a split-marker approach. Arch Microbiol 191:615–622