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Gene Expression Modulation of Two Biosynthesis Pathways via Signal Transduction in Cochliobolus heterostrophus

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DOI: 10.4236/abb.2014.54042    2,828 Downloads   3,982 Views   Citations
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ABSTRACT

G-protein-linked pathways have evolved to allow responses to extracellular agonists (hormones, neurotransmitters, odors, chemoattractants, light and nutrients) in eukaryotic cells, ranging from simpler systems, including yeasts, filamentous fungi and slime molds, to more complex organisms, such as mammals. Although the role of G-protein and mitogen-activated protein kinase (MAPK) in filamentous fungi has been studied for over a decade, downstream elements are less known, and the study of target genes has evolved mainly in recent years. Here, we examined the involvement of G-protein subunits and MAPK in controlling the expression of two distinct target genes. These genes were selected from an array database according to their unique expression profile and the role of closely related genes found in other Ascomycetes. One of these genes is BPH, which encodes the enzyme responsible for cytochrome P450-dependent benzoate hydroxylation in microsomes. The other gene is CIPA, which encodes isoflavone reductase (IfR), an enzyme involved in the synthesis of phytoalexin, which catalyzes an intermediate step in pisatin biosynthesis. The expression profile of these two genes was determined in a series of signaling deficiency mutants that were grown on different media using a DNA microarray. Comparison of the expression profile in the two wild type strains and mutants deficient in the G-protein α or β subunits or in MAPK, revealed a unique control mechanism for the BPH and CIPA genes. The two genes are highly expressed during the infection of the host plant leaves and may associate with the fungal response to the host. Signaling via G-protein or MAPK was shown to be related to cascades that altered the expression of these genes in response to the growth condition. This work demonstrates that signal transduction pathways are controlling genes that, although sharing an environmental dependent response, participate in distinct biosynthesis pathways. Moreover, the transcriptional profile may point to distinct and shared roles of the signaling components.

Conflicts of Interest

The authors declare no conflicts of interest.

Cite this paper

Degani, O. (2014) Gene Expression Modulation of Two Biosynthesis Pathways via Signal Transduction in Cochliobolus heterostrophus. Advances in Bioscience and Biotechnology, 5, 340-352. doi: 10.4236/abb.2014.54042.

References

[1] Degani, O., Maor, R., Hadar, R., Sharon, A. and Horwitz, B.A. (2004) Host Physiology and Pathogenic Variation of Cochliobolus heterostrophus Strains with Mutations in the G Protein Alpha Subunit, CGA1. Applied and Environmental Microbiology, 70, 5005-5009. http://dx.doi.org/10.1128/AEM.70.8.5005-5009.2004
[2] 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. http://dx.doi.org/10.1128/EC.3.6.1653-1663.2004
[3] 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 Genetics and Biology, 26, 19-32. http://dx.doi.org/10.1006/fgbi.1998.1094
[4] Lev, S., Sharon, A., Hadar, R., Ma, H. and Horwitz, B.A. (1999) A Mitogen-Activated Protein Kinase of the Corn Leaf Pathogen Cochliobolus heterostrophus Is Involved in Conidiation, Appressorium Formation, and Pathogenicity: Diverse Roles for Mitogen-Activated Protein Kinase Homologs in Foliar Pathogens. Proceedings of the National Academy of Sciences of the United States of America, 96, 13542-13547. http://dx.doi.org/10.1073/pnas.96.23.13542
[5] Degani, O. (2013) Cochliobolus heterostrophus G-Protein Alpha and Beta Subunit Double Mutant Reveals Shared and Distinct Roles in Development and Virulence. Physiological and Molecular Plant Pathology, 82, 35-45.
http://dx.doi.org/10.1016/j.pmpp.2013.01.004
[6] Degani, O. (2013) Construction of a Constitutively Activated Gα Mutant in the Maize Pathogen Cochliobolus heterostrophus. American Journal of Plant Sciences, 4, 2394-2399. http://dx.doi.org/10.4236/ajps.2013.412296
[7] Clapham, D. and Neer, E.J. (1993) New Roles for G Protein Betagamma Dimers in Transmembrane Signalling. Nature, 365, 403-406. http://dx.doi.org/10.1038/365403a0
[8] Crespo, P., Xu, N., Simonds, W.F. and Gutkind, J.S. (1994) Ras-Dependent Activation of MAP Kinase Pathway Mediated by G-Protein Beta Gamma Subunits. Nature, 369, 418-420. http://dx.doi.org/10.1038/369418a0
[9] Gudermann, T. (2001) Multiple Pathways of ERK Activation by G Protein-Coupled Receptors. Novartis Foundation Symposia, 239, 68-84. http://dx.doi.org/10.1002/0470846674.ch7
[10] Degani, O. (2014) G Protein and MAPK Signaling Pathways Control the Ability of Cochliobolus heterostrophus to Exploit Different Carbon Sources. Advances in Biological Chemistry, 4, 40-50.
http://dx.doi.org/10.4236/abc.2014.41007
[11] Lev, S. and Horwitz, B.A. (2003) A Mitogen-Activated Protein Kinase Pathway Modulates the Expression of Two Cellulase Genes in Cochliobolus heterostrophus during Plant Infection. Plant Cell, 15, 835-844.
http://dx.doi.org/10.1105/tpc.010546
[12] Degani, O., Lev, S. and Ronen, M. (2013) Hydrophobin Gene Expression in the Maize Pathogen Cochliobolus heterostrophus. Physiological and Molecular Plant Pathology, 83, 25-34. http://dx.doi.org/10.1016/j.pmpp.2013.03.003
[13] Eliahu, N., Igbaria, A., Rose, M.S., Horwitz, B.A. and Lev, S. (2007) Melanin Biosynthesis in the Maize Pathogen Cochliobolus heterostrophus Depends on Two Mitogen-Activated Protein Kinases, Chk1 and Mps1, and the Transcription Factor Cmr1. Eukaryotic Cell, 6, 421-429. http://dx.doi.org/10.1128/EC.00264-06
[14] Dixon, R.A., Dey, P.M. and Lamb, C.J. (1983) Phytoalexins: Enzymology and Molecular Biology. Advances in Enzymology and Related Areas of Molecular Biology, 55, 1-136.
[15] Dixon, R.A. (2001) Natural Products and Plant Disease Resistance. Nature, 411, 843-847.
http://dx.doi.org/10.1038/35081178
[16] Wu, Q. and VanEtten, H.D. (2004) Introduction of Plant and Fungal Genes into Pea (Pisum sativum L.) Hairy Roots Reduces Their Ability to Produce Pisatin and Affects Their Response to a Fungal Pathogen. Molecular Plant-Microbe Interactions, 17, 798-804. http://dx.doi.org/10.1094/MPMI.2004.17.7.798
[17] Agrios, G.N. (2005) Plant Pathology Academic Press Inc., London.
[18] Dewick, P.M. (1988) Isoflavonoids. The Flavonoids. Advances in Research since 1980, Chapman and Hall, New York.
http://dx.doi.org/10.1007/978-1-4899-2913-6_5
[19] Oommen, A., Dixon, R.A. and Paiva, N.L. (1994) The Elicitor-Inducible Alfalfa Isoflavone Reductase Promoter Confers Different Patterns of Developmental Expression in Homologous and Heterologous Transgenic Plants. Plant Cell, 6, 1789-1803.
[20] Paiva, N.L., Edwards, R., Sun, Y.J., Hrazdina, G. and Dixon, R.A. (1991) Stress Responses in Alfalfa (Medicago sativa L.) 11. Molecular Cloning and Expression of Alfalfa Isoflavone Reductase, a Key Enzyme of Isoflavonoid Phytoalexin Biosynthesis. Plant Molecular Biology, 17, 653-667. http://dx.doi.org/10.1007/BF00037051
[21] Tiemann, K., Inze, D., Van Montagu, M. and Barz, W. (1991) Pterocarpan Phytoalexin Biosynthesis in Elicitor-Challenged Chickpea (Cicer arietinum L.) Cell Cultures. Purification, Characterization and cDNA Cloning of NADPH: Isoflavone Oxidoreductase. European Journal of Biochemistry, 200, 751-757.
http://dx.doi.org/10.1111/j.1432-1033.1991.tb16241.x
[22] Paiva, N.L., Oommen, A., Harrison, M.J. and Dixon, R.A. (1994) Regulation of Isoflavonoid Metabolism in Alfalfa. Plant Cell, Tissue and Organ Culture, 38, 213-220. http://dx.doi.org/10.1007/BF00033879
[23] Melin, P., Schnurer, J. and Wagner, E.G. (2002) Proteome Analysis of Aspergillus nidulans Reveals Proteins Associated with the Response to the Antibiotic Concanamycin A, Produced by Streptomyces Species. Molecular Genetics and Genomics, 267, 695-702. http://dx.doi.org/10.1007/s00438-002-0695-0
[24] Hong, Y.M., Park, S.W. and Choi, S.Y. (1998) Expression of the CIP1 Gene Induced under Cadmium Stress in Candida sp. Molecules and Cells, 8, 84-89.
[25] Nelson, D.R., Koymans, L., Kamataki, T., Stegeman, J.J., Feyereisen, R., Waxman, D.J., Waterman, M.R., Gotoh, O., Coon, M.J., Estabrook, R.W., Gunsalus, I.C. and Nebert, D.W. (1996) P450 Superfamily: Update on New Sequences, Gene Mapping, Accession Numbers and Nomenclature. Pharmacogenetics, 6, 1-42.
http://dx.doi.org/10.1097/00008571-199602000-00002
[26] Omura, T. (1999) Forty Years of Cytochrome P450. Biochemical and Biophysical Research Communications, 266, 690-698. http://dx.doi.org/10.1006/bbrc.1999.1887
[27] Nelson, D.R. (1999) Cytochrome P450 and the Individuality of Species. Archives of Biochemistry and Biophysics, 369, 1-10. http://dx.doi.org/10.1006/abbi.1999.1352
[28] Gonzalez, F.J. (1990) Molecular Genetics of the P-450 Superfamily. Pharmacology and Therapeutics, 45, 1-38.
http://dx.doi.org/10.1016/0163-7258(90)90006-N
[29] Graham, S.E. and Peterson, J.A. (1999) How Similar Are P450s and What Can Their Differences Teach Us? Archives of Biochemistry and Biophysics, 369, 24-29. http://dx.doi.org/10.1006/abbi.1999.1350
[30] Fujii, T., Nakamura, K., Shibuya, K., Tanase, S., Gotoh, O., Ogawa, T. and Fukuda, H. (1997) Structural Characterization of the Gene and Corresponding cDNA for the Cytochrome P450rm from Rhodotorula minuta Which Catalyzes Formation of Isobutene and 4-Hydroxylation of Benzoate. Molecular and General Genetics, 256, 115-120.
http://dx.doi.org/10.1007/s004380050552
[31] Van den Brink, J.M., Punt, P.J., van Gorcom, R.F. and van den Hondel, C.A. (2000) Regulation of Expression of the Aspergillus niger Benzoate Para-Hydroxylase Cytochrome P450 System. Molecular and General Genetics, 263, 601-609. http://dx.doi.org/10.1007/s004380051207
[32] Fraser, J.A., Davis, M.A. and Hynes, M.J. (2002) The Genes gmdA, Encoding an Amidase, and bzuA, Encoding a Cytochrome P450, Are Required for Benzamide Utilization in Aspergillus nidulans. Fungal Genetics and Biology, 35, 135-146. http://dx.doi.org/10.1006/fgbi.2001.1307
[33] Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic Local Alignment Search Tool. Journal of Molecular Biology, 215, 403-410.
[34] Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. and Higgins, D.G. (1997) The CLUSTAL_X Windows Interface: Flexible Strategies for Multiple Sequence Alignment Aided by Quality Analysis Tools. Nucleic Acids Research, 25, 4876-4882. http://dx.doi.org/10.1093/nar/25.24.4876
[35] Boschloo, J.G., Moonen, E., van Gorcom, R.F., Hermes, H.F. and Bos, C.J. (1991) Genetic Analysis of Aspergillus niger Mutants Defective in Benzoate-4-Hydroxylase Function. Current Genetics, 19, 261-264.
http://dx.doi.org/10.1007/BF00355052
[36] Van Gorcom, R.F., Boschloo, J.G., Kuijvenhoven, A., Lange, J., van Vark, A.J., Bos, C.J., van Balken, J.A., Pouwels, P.H. and van den Hondel, C.A. (1990) Isolation and Molecular Characterisation of the Benzoate-Para-Hydroxylase Gene (bphA) of Aspergillus niger: A Member of a New Gene Family of the Cytochrome P450 Superfamily. Molecular and General Genetics, 223, 192-197.
[37] Bolker, M. (1998) Sex and Crime: Heterotrimeric G Proteins in Fungal Mating and Pathogenesis. Fungal Genetics and Biology, 25, 143-156. http://dx.doi.org/10.1006/fgbi.1998.1102
[38] Staskawicz, B.J., Ausubel, F.M., Baker, B.J., Ellis, J.G. and Jones, J.D. (1995) Molecular Genetics of Plant Disease Resistance. Science, 268, 661-667. http://dx.doi.org/10.1126/science.7732374
[39] Harrison, M.J. and Dixon, R.A. (1993) Isoflavonoid Accumulation and Expression of Defense Gene Transcripts during the Establishment of Vesicular-Arbuscular Mycorrhizal Associations in Roots of Medicago truncatula. Molecular Plant-Microbe Interactions, 6, 643-654. http://dx.doi.org/10.1094/MPMI-6-643
[40] Volpin, H., Phillips, D.A., Okon, Y. and Kapulnik, Y. (1995) Suppression of an Isoflavonoid Phytoalexin Defense Response in Mycorrhizal Alfalfa Roots. Plant Physiology, 108, 1449-1454.
[41] Jakobek, J.L., Smith, J.A. and Lindgren, P.B. (1993) Suppression of Bean Defense Responses by Pseudomonas syringae. Plant Cell, 5, 57-63.
[42] Rao, J.R. and Cooper, J.E. (1994) Rhizobia Catabolize Nod Gene-Inducing Flavonoids via C-Ring Fission Mechanisms. Journal of Bacteriology, 176, 5409-5413.
[43] Funnell, D.L., Matthews, P.S. and Van Etten, H.D. (2002) Identification of New Pisatin Demethylase Genes (PDA5 and PDA7) in Nectria haematococca and Non-Mendelian Segregation of Pisatin Demethylating Ability and Virulence on Pea Due to Loss of Chromosomal Elements. Fungal Genetics and Biology, 37, 121-133.
http://dx.doi.org/10.1016/S1087-1845(02)00503-0
[44] Matthews, D.E. and Van Etten, H.D. (1983) Detoxification of the Phytoalexin Pisatin by a Fungal Cytochrome P-450. Archives of Biochemistry and Biophysics, 224, 494-505. http://dx.doi.org/10.1016/0003-9861(83)90237-0
[45] Palumbo, J.D., Kado, C.I. and Phillips, D.A. (1998) An Isoflavonoid-Inducible Efflux Pump in Agrobacterium tumefaciens Is Involved in Competitive Colonization of Roots. Journal of Bacteriology, 180, 3107-3113.
[46] Dixon, R.A., Harrison, M.J. and Paiva, N.L. (1995) The Isoflavonoid Phytoalexin Pathway: From Enzymes to Genes to Transcription Factors. Physiologia Plantarum, 93, 385-392. http://dx.doi.org/10.1111/j.1399-3054.1995.tb02243.x
[47] Dixon, R.A., Dey, P.M. and Lamb, C.J. (1983) Advances in Enzymology and Related Areas in Molecular Biology. John Wiley & Sons, New York.
[48] Babiychuk, E., Kushnir, S., Belles-Boix, E., Van Montagu, M. and Inzé, D. (1995) Arabidopsis thaliana NADPH Oxidoreductase Homologs Confer Tolerance of Yeasts toward the Thiol-Oxidizing Drug Diamide. Journal of Biological Chemistry, 270, 26224-26231. http://dx.doi.org/10.1074/jbc.270.44.26224
[49] Petrucco, S., Bolchi, A., Foroni, C., Percudani, R., Rossi, G.L. and Ottonello, S. (1996) A Maize Gene Encoding an NADPH Binding Enzyme Highly Homologous to Isoflavone Reductases Is Activated in Response to Sulfur Starvation. Plant Cell, 8, 69-80.
[50] Lers, A., Burd, S., Lomaniec, E., Droby, S. and Chalutz, E. (1998) The Expression of a Grapefruit Gene Encoding an Isoflavone Reductase-Like Protein Is Induced in Response to UV Irradiation. Plant Molecular Biology, 36, 847.
http://dx.doi.org/10.1023/A:1005996515602
[51] Kim, S.T., Cho, K.S., Kim, S.G., Kang, S.Y. and Kang, K.Y. (2003) A Rice Isoflavone Reductase-Like Gene, OsIRL, Is Induced by Rice Blast Fungal Elicitor. Molecules and Cells, 16, 224-231.
[52] Booth, I.R., Kroll, R.G. and Gould, G.W. (1989) The Preservation of Foods by Low pH. Mechanisms of Action of Food Preservation Procedures, Elsevier Applied Science, Elsevier Science Publishers Ltd. London, 119-160.
[53] Pearce, A.K., Booth, I.R. and Brown, A.J. (2001) Genetic Manipulation of 6-Phosphofructo-1-Kinase and Fructose 2,6-Bisphosphate Levels Affects the Extent to Which Benzoic Acid Inhibits the Growth of Saccharomyces cerevisiae. Microbiology, 147, 403-410.
[54] Chong, J., Pierrel, M.A., Atanassova, R., Werck-Reichhart, D., Fritig, B. and Saindrenan, P. (2001) Free and Conjugated Benzoic Acid in Tobacco Plants and Cell Cultures. Induced Accumulation upon Elicitation of Defense Responses and Role as Salicylic Acid Precursors. Plant Physiology, 125, 318-328. http://dx.doi.org/10.1104/pp.125.1.318
[55] Shah, Y. and Klessig, D.F. (1999) Salicylic Acid: Signal Perception and Transduction. Elsevier Science, Amsterdam.

  
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