The Cpc1 regulator of the cross-pathway control of amino acid biosynthesis is required for pathogenicity of the vascular pathogen verticillium longisporum

Molecular Plant-Microbe Interactions

Volumn 26, Issue 11, 2013, Pages 1312-1324

  Timpner, Christian ^a   Braus Stromeyer, Susanna A ^a   Van Tuan, Tran ^a   Braus, Gerhard H ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; FUNGAL PROTEIN; TRANSCRIPTION FACTOR;

AMINO ACID SEQUENCE; ARTICLE; DNA SEQUENCE; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PHYLOGENY; PHYSIOLOGY; PLANT DISEASE; PLANT ROOT; RAPESEED; SEQUENCE ALIGNMENT; TOMATO; VERTICILLIUM; XYLEM;

AMINO ACID SEQUENCE; AMINO ACIDS; BRASSICA NAPUS; CONSERVED SEQUENCE; FUNGAL PROTEINS; GENE EXPRESSION REGULATION, FUNGAL; GENE SILENCING; HOST-PATHOGEN INTERACTIONS; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; MUTATION; PHYLOGENY; PLANT DISEASES; PLANT ROOTS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; VERTICILLIUM; XYLEM;

EID: 84885676904     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-06-13-0181-R     Document Type: Article

References (69)

1. Abad, A., Fernandez-Molina, J. V., Bikandi, J., Ramirez, A., Margareto, J., Sendino, J., Hernando, F. L., Ponton, J., Garaizar, J., and Rementeria, A. 2010. What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev. Iberoam. Micol. 27:155-182.
2. Albrecht, G., Mösch, H. U., Hoffmann, B., Reusser, U., and Braus, G. H. 1998. Monitoring the Gcn4 protein-mediated response in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 273:12696-12702.
3. Braus, G. H. 1991. Aromatic amino acid biosynthesis in the yeast Saccharomyces cerevisiae: A model system for the regulation of a eukaryotic biosynthetic pathway. Microbiol. Rev. 55:349-370.
4. Braus, G. H., Grundmann, O., Brückner, S., and Mösch, H. U. 2003. Amino acid starvation and Gcn4p regulate adhesive growth and FLO11 gene expression in Saccharomyces cerevisiae. Mol. Biol. Cell 14:4272-4284.
5. Carsiotis, M., and Jones, R. F. 1974. Cross-pathway regulation: Tryptophan- mediated control of histidine and arginine biosynthetic enzymes in Neurospora crassa. J. Bacteriol. 119:889-892.
6. Carsiotis, M., Jones, R. F., and Wesseling, A. C. 1974. Cross-pathway regulation: Histidine-mediated control of histidine, tryptophan, and arginine biosynthetic enzymes in Neurospora crassa. J. Bacteriol. 119:893-898.
7. Covert, S. F., Kapoor, P., Lee, M., Briley, A., and Nairn, C. J. 2001. Agrobacterium tumefaciens-mediated transformation of Fusarium circinatum. Mycol. Res. 105:259-264.
8. Daebeler, F., Amelung, D., and Zeise, K. 1988. Verticillium-Welke an winterraps auftreten und bedeutung. nachrichtenblatt Pflanzenschutzdienst DDR 42:71-73.
9. Eckert, S. E., Kubler, E., Hoffmann, B., and Braus, G. H. 2000. The tryptophan synthase-encoding trpB gene of Aspergillus nidulans is regulated by the cross-pathway control system. Mol. Gen. Genet. 263:867-876.
10. Elliott, C. E., Fox, E. M., Jarvis, R. S., and Howlett, B. J. 2011. The crosspathway control system regulates production of the secondary metabolite toxin, sirodesmin PL, in the ascomycete, Leptosphaeria maculans. BMC Microbiol. 11:169.
11. Eynck, C., Koopmann, B., Grunewaldt-Stoecker, G., Karlovsky, P., and von Tiedemann, A. 2007. Differential interactions of Verticillium longisporum and V. dahliae with Brassica napus detected with molecular and histological techniques. Eur. J. Plant Pathol. 118:259-274.
12. Floerl, S., Majcherczyk, A., Possienke, M., Feussner, K., Tappe, H., Gatz, C., Feussner, I., Kues, U., and Polle, A. 2012. Verticillium longisporum infection affects the leaf apoplastic proteome, metabolome, and cell wall properties in Arabidopsis thaliana. PLoS One 7:e31435.Published online.
13. Gibson, D. M., King, B. C., Hayes, M. L., and Bergstrom, G. C. 2011. Plant pathogens as a source of diverse enzymes for lignocellulose digestion. Curr. Opin. Microbiol. 14:264-270.
14. Günzelmann, H., and Paul, V. H. 1990. Zum auftreten und zur bedeutung der verticillium-welke an raps in der bundesrepublik deutschland in 1989. Raps 8:23-25.
15. Heale, J. B., and Karapapa, V. K. 1999. The Verticillium threat to Canada's major oilseed crop: Canola. Can. J. Plant Pathol. 21:1-7.
16. Herzog, B., Streckfuss-Bomeke, K., and Braus, G. H. 2011. A feedback circuit between transcriptional activation and self-destruction of Gcn4 separates its metabolic and morphogenic response in diploid yeasts. J. Mol. Biol. 405:909-925.
17. Hinnebusch, A. G. 1984. Evidence for translational regulation of the activator of general amino acid control in yeast. Proc. Natl. Acad. Sci. U.S.A. 81:6442-6446.
18. Hinnebusch, A. G. 1986. The general control of amino acid biosynthetic genes in the yeast Saccharomyces cerevisiae. CRC Crit. Rev. Biochem. 21:277-317.
19. Hinnebusch, A. G., and Natarajan, K. 2002. Gcn4p, a master regulator of gene expression, is controlled at multiple levels by diverse signals of starvation and stress. Eukaryot. Cell 1:22-32.
20. Hoffmann, B., Wanke, C., Lapaglia, S. K., and Braus, G. H. 2000. c-Jun and RACK1 homologs regulate a control point for sexual development in Aspergillus nidulans. Mol. Microbiol. 37:28-41.
21. Hoffmann, B., Valerius, O., Andermann, M., and Braus, G. H. 2001. Transcriptional autoregulation and inhibition of mRNA translation of amino acid regulator gene cpcA of filamentous fungus Aspergillus nidulans. Mol. Biol. Cell 12:2846-2857.
22. Inderbitzin, P., Davis, R. M., Bostock, R. M., and Subbarao, K. V. 2011. The ascomycete Verticillium longisporum is a hybrid and a plant pathogen with an expanded host range. PLoS One 6:e18260. Published online.
23. Irniger, S., and Braus, G. H. 2003. Controlling transcription by destruction: The regulation of yeast Gcn4p stability. Curr. Genet. 44:8-18.
24. Iven, T., König, S., Singh, S., Braus-Stromeyer, S. A., Bischoff, M., Tietze, L. F., Braus, G. H., Lipka, V., Feussner, I., and Dröge-Laser, W. 2012. Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol. Plant. 5:1389-402.
25. Karapapa, V. K., Bainbridge, B. W., and Heale, J. B. 1997. Morphological and molecular characterization of Verticillium longisporum comb. nov., pathogenic to oilseed rape. Mycol. Res. 101:1281-1293.
26. Kehr, J., Buhtz, A., and Giavalisco, P. 2005. Analysis of xylem sap proteins from Brassica napus. BMC Plant Biol. 5:11.
27. Kilberg, M. S., Shan, J., and Su, N. 2009. ATF4-dependent transcription mediates signaling of amino acid limitation. Trends Endocrin. Met. 20:436-443.
28. King, B. C., Waxman, K. D., Nenni, N. V., Walker, L. P., Bergstrom, G. C., and Gibson, D. M. 2011. Arsenal of plant cell wall degrading enzymes reflects host preference among plant pathogenic fungi. Biotechnol. Biofuels 4:4.
29. Kleinschmidt, M., Grundmann, O., Bluthgen, N., Mösch, H. U., and Braus, G. H. 2005. Transcriptional profiling of Saccharomyces cerevisiae cells under adhesion-inducing conditions. Mol. Genet. Genomics 273:382-393.
30. Klosterman, S. J., Subbarao, K. V., Kang, S., Veronese, P., Gold, S. E., Thomma, B. P., Chen, Z., Henrissat, B., Lee, Y. H., Park, J., Garcia-Pedrajas, M. D., Barbara, D. J., Anchieta, A., de Jonge, R., Santhanam, P., Maruthachalam, K., Atallah, Z., Amyotte, S. G., Paz, Z., Inderbitzin, P., Hayes, R. J., Heiman, D. I., Young, S., Zeng, Q., Engels, R., Galagan, J., Cuomo, C. A., Dobinson, K. F., and Ma, L. J. 2011. Comparative genomics yields insights into niche adaptation of plant vascular wilt pathogens. PLoS Pathog 7:e1002137. Published online.
31. Kolar, M., Punt, P. J., van den Hondel, C. A., and Schwab, H. 1988. Transformation of Penicillium chrysogenum using dominant selection markers and expression of an Escherichia coli lacZ fusion gene. Gene 62:127-134.
32. Krappmann, S., Bignell, E. M., Reichard, U., Rogers, T., Haynes, K., and Braus, G. H. 2004. The Aspergillus fumigatus transcriptional activator CpcA contributes significantly to the virulence of this fungal pathogen. Mol. Microbiol. 52:785-799.
33. Lazo, G. R., Stein, P. A., and Ludwig, R. A. 1991. A DNA transformationcompetent Arabidopsis genomic library in Agrobacterium. Biotechnology 9:963-967.
34. Livak, K. J., and Schmittgen, T. D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-Ct method. Methods 25:402-408.
35. Lopez-Millan, A. F., Morales, F., Abadia, A., and Abadia, J. 2000. Effects of iron deficiency on the composition of the leaf apoplastic fluid and xylem sap in sugar beet. Implications for iron and carbon transport. Plant Physiol 124:873-884.
36. Mösch, H. U., Scheier, B., Lahti, R., Mantsala, P., and Braus, G. H. 1991. Transcriptional activation of yeast nucleotide biosynthetic gene ADE4 by GCN4. J. Biol. Chem. 266:20453-20456.
37. Mullins, E. D., Chen, X., Romaine, P., Raina, R., Geiser, D. M., and Kang, S. 2001. Agrobacterium-mediated transformation of Fusarium oxysporum: An efficient tool for insertional mutagenesis and gene transfer. Phytopathology 91:173-180.
38. Nakayashiki, H. 2005. RNA silencing in fungi: Mechanisms and applications. FEBS Lett 579:5950-5957.
39. Nakayashiki, H., Hanada, S., Nguyen, B.Q., Kadotani, N., Tosa, Y., and Mayama, S. 2005. RNA silencing as a tool for exploring gene function in ascomycete fungi. Fungal Genet. Biol. 42:275-283.
40. Natarajan, K., Meyer, M. R., Jackson, B. M., Slade, D., Roberts, C., Hinnebusch, A. G., and Marton, M. J. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell Biol. 21:4347-4368.
41. Neumann, M. J., and Dobinson, K. F. 2003. Sequence tag analysis of gene expression during pathogenic growth and microsclerotia development in the vascular wilt pathogen Verticillium dahliae. Fungal Genet. Biol. 38:54-62.
42. Oliphant, A. R., Brandl, C. J., and Struhl, K. 1989. Defining the sequence specificity of DNA-binding proteins by selecting binding sites from random-sequence oligonucleotides: Analysis of yeast GCN4 protein. Mol. Cell Biol. 9:2944-2949.
43. Paluh, J. L., Orbach, M. J., Legerton, T. L., and Yanofsky, C. 1988. The cross-pathway control gene of Neurospora crassa, cpc-1, encodes a protein similar to GCN4 of yeast and the DNA-binding domain of the oncogene v-jun-encoded protein. Proc. Natl. Acad. Sci. U.S.A. 85:3728-3732.
44. Piotrowska, M., Kruszewska, A., and Paszewski, A. 1980. Effect of regulatory mutations of sulphur metabolism on the levels of cysteine- and homocysteine- synthesizing enzymes in Neurospora crassa. Acta Biochim. Pol. 27:395-403.
45. Ratzinger, A., Riediger, N., von Tiedemann, A., and Karlovsky, P. 2009. Salicylic acid and salicylic acid glucoside in xylem sap of Brassica napus infected with Verticillium longisporum. J. Plant Res. 122:571-579.
46. Saitou, N., and Nei, M. 1987. The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406-425.
47. Sakuta, C., Oda, A., Yamakawa, S., and Satoh, S. 1998. Root-specific expression of genes for novel glycine-rich proteins cloned by use of an antiserum against xylem sap proteins of cucumber. Plant Cell Physiol. 39:1330-1336.
48. Sasse, C., Bignell, E. M., Hasenberg, M., Haynes, K., Gunzer, M., Braus, G. H., and Krappmann, S. 2008. Basal expression of the Aspergillus fumigatus transcriptional activator CpcA is sufficient to support pulmonary aspergillosis. Fungal Genet. Biol. 45:693-704.
49. Schnathorst, W. C. 1981. Life cycle and epidemiology of Verticillium. Pages 81-111 in: Fungal wilt diseases of plants. M. E. Mace, A. A. Bell, and C. H. Beckmann, eds. Academic Press, New York.
50. Schönig, B., Vogel, S., and Tudzynski, B. 2009. Cpc1 mediates cross-pathway control independently of Mbf1 in Fusarium fujikuroi. Fungal Genet. Biol. 46:898-908.
51. Schürch, A., Miozarri, J., and Hütter, R. 1974. Regulation of tryptophan biosynthesis in Saccharomyces cerevisiae: Mode of action of 5-methyltryptophan and 5-methyl-tryptophan-sensitive mutants J. Bacteriol. 117:1131-1140.
52. Shan, J., Ord, D., Ord, T., and Kilberg, M. S. 2009. Elevated ATF4 expression, in the absence of other signals, is sufficient for transcriptional induction via CCAAT enhancer-binding protein-activating transcription factor response elements. J. Biol. Chem. 284:21241-21248.
53. Shen, W. C., and Ebbole, D. J. 1997. Cross-pathway and pathway-specific control of amino acid biosynthesis in Magnaporthe grisea. Fungal Genet. Biol. 21:40-49.
54. Singh, S., Braus-Stromeyer, S. A., Timpner, C., Tran, V. T., Lohaus, G., Reusche, M., Knufer, J., Teichmann, T., von Tiedemann, A., and Braus, G. H. 2010. Silencing of Vlaro2 for chorismate synthase revealed that the phytopathogen Verticillium longisporum induces the cross-pathway control in the xylem. Appl. Microbiol. Biotechnol. 85:1961-1976.
55. Singh, S., Braus-Stromeyer, S. A., Timpner, C., Valerius, O., von Tiedemann, A., Karlovsky, P., Druebert, C., Polle, A., and Braus, G. H. 2012. The plant host Brassica napus induces in the pathogen Verticillium longisporum the expression of functional catalase peroxidase which is required for the late phase of disease. Mol. Plant-Microbe Interact. 25:569-581.
56. Southern, E. M. 1975. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98:503-517.
57. Struhl, K., Brandl, C. J., Chen, W., Harbury, P. A., Hope, I. A., and Mahadevan, S. 1988. Transcriptional activation by yeast GCN4, a functional homolog to the jun oncoprotein. Cold Spring Harb Symp Quant Biol 53 Pt 2:701-709.
58. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. 2011. MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 28:2731-2739.
59. Tian, C., Kasuga, T., Sachs, M. S., and Glass, N. L. 2007. Transcriptional profiling of cross pathway control in Neurospora crassa and comparative analysis of the Gcn4 and CPC1 regulons. Eukaryot. Cell 6:1018-1029.
60. Tilsner, J., Kassner, N., Struck, C., and Lohaus, G. 2005. Amino acid contents and transport in oilseed rape (Brassica napus L.) under different nitrogen conditions. Planta 221:328-338.
61. Tran, V. T., Braus-Stromeyer, S. A., Timpner, C., and Braus, G. H. 2013. Molecular diagnosis to discriminate pathogen and apathogen species of the hybrid Verticillium longisporum on the oilseed crop Brassica napus. Appl. Microbiol. Biotechnol. 97:4467-4483.
62. Tripathi, G., Wiltshire, C., Macaskill, S., Tournu, H., Budge, S., and Brown, A. J. 2002. Gcn4 co-ordinates morphogenetic and metabolic responses to amino acid starvation in Candida albicans. EMBO (Eur. Mol. Biol. Organ.) J 21:5448-5456.
63. Valerius, O., Kleinschmidt, M., Rachfall, N., Schulze, F., Lopez Marin, S., Hoppert, M., Streckfuss-Bomeke, K., Fischer, C., and Braus, G. H. 2007. The Saccharomyces homolog of mammalian RACK1, Cpc2/Asc1p, is required for FLO11-dependent adhesive growth and dimorphism. Mol. Cell Proteomics 6:1968-1979.
64. Wanke, C., Eckert, S., Albrecht, G., van Hartingsveldt, W., Punt, P. J., van den Hondel, C. A., and Braus, G. H. 1997. The Aspergillus niger GCN4 homolog, cpcA, is transcriptionally regulated and encodes an unusual leucine zipper. Mol. Microbiol. 23:23-33.
65. Zeise, K., and Seidel, D. 1990. Zur entwicklung und schadwirkung der Verticillium welkekrankheit am winterraps. Raps 8:20-22.
66. Zeise, K., and von Tiedemann, A. 2001. Morphological and physiological differentiation among vegetative compatibility groups of Verticillium dahliae in relation to V. longisporum. J. Phytopathol. 149:469-475.
67. Zeise, K., and von Tiedemann, A. 2002a. Host Specialization among Vegetative Compatibility Groups of Verticillium dahliae in relation to Verticillium longisporum. J Phytopathology 150:112-119.
68. Zeise, K., and von Tiedemann, A. 2002b. Application of RAPD-PCR for virulence type analysis within Verticillium dahliae and V. longisporum J. Phytopathology 150:557-563.
69. Zhou, L., Hu, Q., Johannson, A., and Dixelius, C. 2006. Verticillium longisporum and Verticillium dahliae: Infection and disease in Brassica napus. Plant Pathol 55:137-144.