Structure-activity relationships delineate how the maize pathogen Cochliobolus heterostrophus uses aromatic compounds as signals and metabolites

Molecular Plant-Microbe Interactions

Volumn 25, Issue 7, 2012, Pages 931-940

  Shalaby, Samer ^a   Horwitz, Benjamin A ^a   Larkov, Olga ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

3 OXOADIPIC ACID; 3-OXOADIPIC ACID; ADIPIC ACID DERIVATIVE; CAFFEIC ACID DERIVATIVE; COUMARIC ACID; ENZYME; FUNGAL PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PHENOL DERIVATIVE; QUINIC ACID; TRANSCRIPTION FACTOR;

ARTICLE; ASCOMYCETES; CHEMISTRY; DRUG EFFECT; GENE DELETION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HOST PATHOGEN INTERACTION; MAIZE; METABOLISM; MICROBIOLOGY; OXIDATION REDUCTION REACTION; PLANT DISEASE; SIGNAL TRANSDUCTION; STRUCTURE ACTIVITY RELATION;

ADIPATES; ASCOMYCOTA; CAFFEIC ACIDS; COUMARIC ACIDS; ENZYMES; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, FUNGAL; GREEN FLUORESCENT PROTEINS; HOST-PATHOGEN INTERACTIONS; OXIDATION-REDUCTION; PHENOLS; PLANT DISEASES; QUINIC ACID; RECOMBINANT FUSION PROTEINS; SEQUENCE DELETION; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; TRANSCRIPTION FACTORS; ZEA MAYS;

COCHLIOBOLUS HETEROSTROPHUS; ZEA MAYS;

EID: 84863303760     PISSN: 08940282     EISSN: None     Source Type: Journal    
DOI: 10.1094/MPMI-01-12-0015-R     Document Type: Article

References (48)

1. Azevedo, D., Tacnet, F., Delaunay, A., Rodrigues-Pousada, C., and Toledano, M. B. 2003. Two redox centers within Yap1 for H2O2 and thiol-reactive chemicals signaling. Free Radic. Biol. Med. 35:889-900. (Pubitemid 37211443)
2. Bandaranayake, P. C., Filappova, T., Tomilov, A., Tomilova, N. B., Jamison-McClung, D., Ngo, Q., Inoue, K., and Yoder, J. I. 2010. A single-electron reducing quinone oxidoreductase is necessary to induce haustorium development in the root parasitic plant Triphysaria. Plant Cell 22:1404-1419.
3. Bennett, R., and Wallsgrove, R. 1994. Secondary metabolites in plant defence mechanisms. New Phytol. 127:617-633. (Pubitemid 2137130)
4. Bhattacharya, A., Sood, P., and Citovsky, V. 2010. The roles of plant phenolics in defence and communication during Agrobacterium and Rhizobium infection. Mol. Plant Pathol. 11:705-719.
5. Bisogno, F., Mascoti, L., Sanchez, C., Garibotto, F., Giannini, F., Kurina-Sanz, M., and Enriz, R. 2007. Structure-antifungal activity relationship of cinnamic acid derivatives. J. Agric. Food Chem. 55:10635-10640.
6. Brencic, A., and Winans, S. C. 2005. Detection of and response to signals involved in host-microbe interactions by plant-associated bacteria. Microbiol. Mol. Biol. Rev. 69:155-194. (Pubitemid 40358070)
7. Brencic, A., Eberhard, A., and Winans, S. C. 2004. Signal quenching, detoxification and mineralization of vir gene-inducing phenolics by the VirH2 protein of Agrobacterium tumefaciens. Mol. Microbiol. 51:1103-1115. (Pubitemid 38270802)
8. Catlett, N. L., Lee, B.-N., Yoder, O., and Turgeon, B. 2003a. Split-marker recombination for efficient targeted deletion of fungal genes. Fungal Genet. Newsl. Online 50:9-11.
9. Catlett, N. L., Yoder, O. C., and Turgeon, B. G. 2003b. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Eukaryot. Cell 2:1151-1161. (Pubitemid 38047225)
10. Charkowski, A. O. 2009. Decaying signals: will understanding bacterialplant communications lead to control of soft rot? Curr. Opin. Biotechnol. 20:178-184.
11. Cook, K. A., and Cain, R. B. 1974. Regulation of aromatic metabolism in the fungi: metabolic control of the 3-oxoadipate pathway in the yeast Rhodotorula mucilaginosa. J. Gen. Microbiol. 85:37-50.
12. Ehrhardt, D. W., Wais, R., and Long, S. R. 1996. Calcium spiking in plant root hairs responding to Rhizobium nodulation signals. Cell 85:673-681.
13. Fisher, R. F., and Long, S. R. 1992. Rhizobium-plant signal exchange. Nature 357:655-660.
14. Ganem, S., Lu, S. W., Lee, B. N., Chou, D. Y., Hadar, R., Turgeon, B. G., and Horwitz, B. A. 2004. G-protein beta subunit of Cochliobolus heterostrophus involved in virulence, asexual and sexual reproductive ability, and morphogenesis. Eukaryot. Cell 3:1653-1663. (Pubitemid 40025122)
15. Giles, N. H., Geever, R. F., Asch, D. K., Avalos, J., and Case, M. E. 1991. The Wilhelmine E. Key 1989 invitational lecture. Organization and regulation of the qa (quinic acid) genes in Neurospora crassa and other fungi. J. Hered. 82:1-7.
16. Gross, S. R., and Tatum, E. L. 1955. Structural specificity of inducers of protocatechuic acid oxidase synthesis in Neurospora. Science 122:1141.
17. Hane, J. K., Lowe, R. G., Solomon, P. S., Tan, K. C., Schoch, C. L., Spatafora, J. W., Crous, P. W., Kodira, C., Birren, B. W., Galagan, J. E., Torriani, S. F., McDonald, B. A., and Oliver, R. P. 2007. Dothideomycete plant interactions illuminated by genome sequencing and EST analysis of the wheat pathogen Stagonospora nodorum. Plant Cell 19:3347-3368.
18. Harwood, C. S., and Parales, R. E. 1996. The beta-ketoadipate pathway and the biology of self-identity. Annu. Rev. Microbiol. 50:553-590.
19. Hess, K. M., Dudley, M. W., Lynn, D. G., Joerger, R. D., and Binns, A. N. 1991. Mechanism of phenolic activation of Agrobacterium virulence genes: development of a specific inhibitor of bacterial sensor/response systems. Proc. Natl. Acad. Sci. U. S. A. 88:7854-7858. (Pubitemid 21915253)
20. Horwitz, B. A., Sharon, A., Lu, S. W., Ritter, V., Sandrock, T. M., Yoder, O. C., and Turgeon, B. G. 1999. A G protein alpha subunit from Cochliobolus heterostrophus involved in mating and appressorium formation. Fungal Genet. Biol. 26:19-32. (Pubitemid 29412608)
21. Igbaria, A., Lev, S., Rose, M. S., Lee, B. N., Hadar, R., Degani, O., and Horwitz, B. A. 2008. Distinct and combined roles of the MAP kinases of Cochliobolus heterostrophus in virulence and stress responses. Mol. Plant-Microbe Interact. 21:769-780. (Pubitemid 351929171)
22. Joubert, P., Beaupere, D., Lelievre, P., Wadouachi, A., Sangwan, R., and Sangwan-Norreel, B. 2002. Effects of phenolic compounds on Agrobacterium vir genes and gene transfer induction-a plausible molecular mechanism of phenol binding protein activation. Plant Sci. 162:733-743. (Pubitemid 34547187)
23. Kim, J. H., Campbell, B. C., Mahoney, N., Chan, K. L., and May, G. S. 2006. Targeting antioxidative signal transduction and stress response system: control of pathogenic Aspergillus with phenolics that inhibit mitochondrial function. J. Appl. Microbiol. 101:181-189. (Pubitemid 43952017)
24. Kim, J. H., Campbell, B. C., Mahoney, N., Chan, K. L., Molyneux, R. J., and May, G. S. 2007. Enhanced activity of strobilurin and fludioxonil by using berberine and phenolic compounds to target fungal antioxidative stress response. Lett. Appl. Microbiol. 45:134-141. (Pubitemid 47094181)
25. Kolattukudy, P. E., Rogers, L. M., Li, D., Hwang, C. S., and Flaishman, M. A. 1995. Surface signaling in pathogenesis. Proc. Natl. Acad. Sci. U. S. A. 92:4080-4087.
26. Kuswandi, K., and Roberts, C. 1992. Genetic control of the protocatechuic acid pathway in Aspergillus nidulans. J. Gen. Microbiol. 138:817-823.
27. Lee, J., Godon, C., Lagniel, G., Spector, D., Garin, J., Labarre, J., and Toledano, M. B. 1999. Yap1 and Skn7 control two specialized oxidative stress response regulons in yeast. J. Biol. Chem. 274:16040-16046.
28. Lev, S., Hadar, R., Amedeo, P., Baker, S. E., Yoder, O. C., and Horwitz, B. A. 2005. Activation of an AP1-like transcription factor of the maize pathogen Cochliobolus heterostrophus in response to oxidative stress and plant signals. Eukaryot. Cell 4:443-454. (Pubitemid 40257143)
29. Li, Y., Peng, Q., Selimi, D., Wang, Q., Charkowski, A. O., Chen, X., and Yang, C. H. 2009. The plant phenolic compound p-coumaric acid represses gene expression in the Dickeya dadantii type III secretion system. Appl. Environ. Microbiol. 75:1223-1228.
30. Lu, S. W., Kroken, S., Lee, B. N., Robbertse, B., Churchill, A. C., Yoder, O. C., and Turgeon, B. G. 2003. A novel class of gene controlling virulence in plant pathogenic ascomycete fungi. Proc. Natl. Acad. Sci. U. S. A. 100:5980-5985. (Pubitemid 36576917)
31. Maeta, K., Nomura, W., Takatsume, Y., Izawa, S., and Inoue, Y. 2007. Green tea polyphenols function as prooxidants to activate oxidativestress- responsive transcription factors in yeasts. Appl. Environ. Microbiol. 73:572-580. (Pubitemid 46147588)
32. Mandal, S. M., Chakraborty, D., and Dey, S. 2010. Phenolic acids act as signaling molecules in plant-microbe symbioses. Plant Signal. Behav. 5:359-368.
33. Maresh, J., Zhang, J., Tzeng, Y. L., Goodman, N. A., and Lynn, D. G. 2007. Rational design of inhibitors of VirA-VirG two-component signal transduction. Bioorg. Med. Chem. Lett. 17:3281-3286. (Pubitemid 46819040)
34. Nicholson, R., and Hammerschmidt, R. 1992. Phenolic compounds and their role in disease resistance. Annu. Rev. Phytopathol. 30:369-389. (Pubitemid 24411041)
35. Oide, S., Liu, J., Yun, S. H., Wu, D., Michev, A., Choi, M. Y., Horwitz, B. A., and Turgeon, B. G. 2010. Histidine kinase two-component response regulator proteins regulate reproductive development, virulence, and stress responses of the fungal cereal pathogens Cochliobolus heterostrophus and Gibberella zeae. Eukaryot. Cell 9:1867-1880.
36. Palmer, A. G., Gao, R., Maresh, J., Erbil, W. K., and Lynn, D. G. 2004. Chemical biology of multi-host/pathogen interactions: chemical perception and metabolic complementation. Annu. Rev. Phytopathol. 42:439-464. (Pubitemid 39308520)
37. Patel, V. B., Schweizer, M., Dykstra, C. C., Kushner, S. R., and Giles, N. H. 1981. Genetic organization and transcriptional regulation in the qa gene cluster of Neurospora crassa. Proc. Natl. Acad. Sci. U. S. A. 78:5783-5787. (Pubitemid 12204444)
38. Robbertse, B., Yoder, O. C., Nguyen, A., Schoch, C. L., and Turgeon, B. G. 2003. Deletion of all Cochliobolus heterostrophus monofunctional catalase-encoding genes reveals a role for one in sensitivity to oxidative stress but none with a role in virulence. Mol. Plant-Microbe Interact. 16:1013-1021. (Pubitemid 37325647)
39. Sethuraman, A., Akin, D., Eisele, J., and Eriksson, K. 1998. Effect of aromatic compounds on growth and ligninolytic enzyme production of two white rot fungi Ceriporiopsis subvermispora and Cyathus stercoreus. Can. J. Microbiol. 44:872-885.
40. Shanmugam, V., Ronen, M., Shalaby, S., Larkov, O., Rachamim, Y., Hadar, R., Rose, M. S., Carmeli, S., Horwitz, B. A., and Lev, S. 2010. The fungal pathogen Cochliobolus heterostrophus responds to maize phenolics: novel small molecule signals in a plant-fungal interaction. Cell Microbiol. 12:1421-1434.
41. Shuen, S., and Buswell, J. 1992. Effect of lignin derived phenols and their methylated derivatives on the growth of Lentinus spp. Lett. Appl. Microbiol. 15:12-14.
42. Tang, X., Dong, W., Griffith, J., Nilsen, R., Matthes, A., Cheng, K. B., Reeves, J., Schuttler, H. B., Case, M. E., Arnold, J., and Logan, D. A. 2011. Systems biology of the qa gene cluster in Neurospora crassa. PLoS One 6:e20671. Published online.
43. Tsai, S. C., and Li, Y. K. 2007. Purification and characterization of a catechol 1, 2-dioxygenase from a phenol degrading Candida albicans TL3. Arch. Microbiol. 187:199-206.
44. Turgeon, B. G., Garber, R. C., and Yoder, O. C. 1987. Development of a fungal transformation system based on selection of sequences with promoter activity. Mol. Cell. Biol. 7:3297-3305.
45. Williams, R. J., Spencer, J. P., and Rice-Evans, C. 2004. Flavonoids: antioxidants or signalling molecules? Free Radic. Biol. Med. 36:838-849. (Pubitemid 38352901)
46. Winans, S. C. 1991. An Agrobacterium two-component regulatory system for the detection of chemicals released from plant wounds. Mol. Microbiol. 5:2345-2350. (Pubitemid 21895965)
47. Wirsel, S., Turgeon, B. G., and Yoder, O. C. 1996. Deletion of the Cochliobolus heterostrophus mating-type (MAT) locus promotes the function of MAT transgenes. Curr. Genet. 29:241-249. (Pubitemid 26055494)
48. Yang, S., Peng, Q., San Francisco, M., Wang, Y., Zeng, Q., and Yang, C. H. 2008. Type III secretion system genes of Dickeya dadantii 3937 are induced by plant phenolic acids PLoS One 3:e2973. Published online.