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The Significance of Nitrogen Regulation, Source and Availability on the Interaction Between Rice and Rice Blast

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Advances in Genetics, Genomics and Control of Rice Blast Disease

Abstract

Nitrogen regulation in fungi is a tightly controlled process, equipping them with the ability to colonize various ecological niches when preferred nitrogen sources are not available. Genes and pathways controlling this process have been well-defined in model, non-pathogenic fungi such as Aspergillus nidulans and Neurospora crassa. Research is now beginning to elucidate the importance of nitrogen regulation in pathogenicity. In this review, we will explore the regulatory mechanism called nitrogen catabolite repression in fungi and links between this and pathogenicity. We will examine what is currently known regarding nitrogen regulation and plant pathogenic fungi, with a focus on Magnaporthe oryzae, the devastating rice blast pathogen. Transcriptional activators involved in nitrogen catabolite repression are examined and compared among pathogens. We will also outline our own recent results describing a subtilisin serine protease that not only strengthens evidence for a link between nitrogen starved conditions and pathogenicity, but also appears to control expression of an important pathogenicity-related gene, MPG1

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References

  • Andrianopoulos, A., Kourambas, S., Sharp, J. A., Davis, M. A., & Hynes, M. J. (1998). Characterization of the Aspergillus nidulans nmrA gene involved in nitrogen metabolite repression. Journal of Bacteriology, 180(7), 1973–1977.

    PubMed  CAS  Google Scholar 

  • Avila-Adame, C. & Koller W. (2002). Disruption of the alternative oxidase gene in Magnaporthe grisea and its impact on host infection. Molecular Plant-Microbe Interactions, 15(5), 493–500.

    Article  PubMed  CAS  Google Scholar 

  • Bhambra, G. K., Wang, Z. Y., Soanes, D. M., Wakley, G. E., & Talbot, N. J. (2006). Peroxisomal carnitine acetyl transferase is required for elaboration of penetration hyphae during plant infection by Magnaporthe grisea. Molecular Microbiology, 61(1), 46–60.

    Article  PubMed  CAS  Google Scholar 

  • Blodgett, J. T., Herms, D. A., & Bonello, P. (2005). Effects of fertilization on red pine defense chemistry and resistance to Sphaeropsis sapinea. Forest Ecology and Management, 208(1–3), 373–382.

    Article  Google Scholar 

  • Caddick, M. X., Arst, H. N., Taylor, L. H., Johnson, R. I., & Brownlee, A. G. (1986). Cloning of the regulatory gene AREA mediating nitrogen metabolite repression in Aspergillus nidulans. Embo Journal, 5(5), 1087–1090.

    PubMed  CAS  Google Scholar 

  • Chiang, T. Y., & Marzluf, G. A. (1994). DNA recognition by the NIT2 nitrogen regulatory protein - importance of the number, spacing, and orientation of GATA core elements and their flanking sequences upon NIT2 binding. Biochemistry, 33(2), 576–582.

    Article  PubMed  CAS  Google Scholar 

  • Choi, W. B., & Dean, R. A. (1997). The adenylate cyclase gene MAC1 of Magnaporthe grisea controls Appressorium formation and other aspects of growth and development. Plant Cell, 9(11), 1973–1983.

    Article  PubMed  CAS  Google Scholar 

  • Coleman, M., Henricot, B., Arnau, J., & Oliver, R. P. (1997). Starvation-induced genes of the tomato pathogen Cladosporium fulvum are also induced during growth in planta. Molecular Plant-Microbe Interactions, 10(9), 1106–1109.

    Article  PubMed  CAS  Google Scholar 

  • Crawford, N. M., & Arst, H. N. (1993). The molecular-genetics of nitrate assimilation in fungi and plants. Annual Review of Genetics, 27, 115–146.

    Article  PubMed  CAS  Google Scholar 

  • Davis. M. A., & Hynes, M. J. (1987). Complementation of AREA regulatory gene-mutations of Aspergillus nidulans by the heterologous regulatory gene NIT-2 of Neurospora crassa. Proceedings of the National Academy of Sciences of the United States of America, 84(11), 3753–3757.

    Article  PubMed  CAS  Google Scholar 

  • DeZwaan, T. M., Carroll, A. M., Valent, B., & Sweigard, J. A. (1999). Magnaporthe grisea Pth11p is a novel plasma membrane protein that mediates appressorium differentiation in response to inductive substrate cues. Plant Cell, 11(10), 2013–2030.

    Article  PubMed  CAS  Google Scholar 

  • Divon, H. H., & Fluhr, R. (2007). Nutrition acquisition strategies during fungal infection of plants. Fems Microbiology Letters, 266(1), 65–74.

    Article  PubMed  CAS  Google Scholar 

  • Divon, H. H., Ziv, C., Davydov, O., Yarden, O., & Fluhr, R. (2006). The global nitrogen regulator, FNR1, regulates fungal nutrition-genes and fitness during Fusarium oxysporum pathogenesis. Molecular Plant Pathology, 7(6), 485–497.

    Article  CAS  Google Scholar 

  • Donofrio, N. M., Oh, Y., Lundy, R., et al. (2006). Global gene expression during nitrogen starvation in the rice blast fungus, Magnaporthe grisea. Fungal Genetics and Biology, 43(9),605–617.

    Article  PubMed  CAS  Google Scholar 

  • Foster, A. J., Jenkinson, J. M. & Talbot, N. J. (2003). Trehalose synthesis and metabolism are required at different stages of plant infection by Magnaporthe grisea. Embo Journal, 22(2),225–235.

    Article  PubMed  CAS  Google Scholar 

  • Froeliger, E. H., & Carpenter, B. E. (1996). NUT1, a major nitrogen regulatory gene in Magnaporthe grisea, is dispensable for pathogenicity. Molecular & General Genetics, 251(6), 647–656.

    CAS  Google Scholar 

  • Fu, Y. H., & Marzluf, G. A. (1990a). NIT-2, the major positive-acting nitrogen regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. Proceedings of the National Academy of Sciences of the United States of America, 87(14),5331–5335.

    Google Scholar 

  • Fu, Y. H., & Marzluf, G. A. (1990b). Site-directed mutagenesis of the zinc finger DNA-binding domain of the nitrogen regulatory protein NIT2 of Neurospora. Molecular Microbiology, 4(11), 1847–1852.

    Google Scholar 

  • Fukiya, S., Kuge, T., Tanishima, T., Sone, T., Kamakura, T., Yamaguchi, I., & Tomita, F. (2002). Identification of a putative vacuolar serine protease gene in the rice blast fungus, Magnaporthe grisea. Bioscience Biotechnology and Biochemistry, 66(3), 663–666.

    Article  CAS  Google Scholar 

  • Gomez, D., Garcia, I., Scazzocchio, C., & Cubero, B. (2003). Multiple GATA sites: protein binding and physiological relevance for the regulation of the proline transporter gene of Aspergillus nidulans. Molecular Microbiology, 50(1), 277–289.

    Article  PubMed  CAS  Google Scholar 

  • Hensel, M., Arst, H. N., Aufauvre-Brown, A., & Holden, D. W. (1998). The role of the Aspergillus fumigatus are A gene in invasive pulmonary aspergillosis. Molecular and General Genetics, 258(5), 553–557.

    Article  PubMed  CAS  Google Scholar 

  • Jeong, J. S., Mitchell, T. K., & Dean, R. A. (2007). The Magnaporthe grisea snodprot1 homolog, MSPI, is required for virulence. Fems Microbiology Letters, 273(2), 157–165.

    Article  PubMed  CAS  Google Scholar 

  • Lau, G., & Hamer, J. E. (1996). Regulatory genes controlling MPG1 expression and pathogenicity in the rice blast fungus Magnaporthe grisea. Plant Cell, 8(5), 771–781.

    Article  PubMed  CAS  Google Scholar 

  • Long, D. H., Lee, F. N., & TeBeest, D. O. (2000). Effect of nitrogen fertilization on disease progress of rice blast on susceptible and resistant cultivars. Plant Disease, 84(4), 403–409.

    Article  Google Scholar 

  • Marzluf, G. A. (1997). Genetic regulation of nitrogen metabolism in the fungi. Microbiology and Molecular Biology Reviews, 61(1), 17–32.

    PubMed  CAS  Google Scholar 

  • Nam, M. H., Jeong, S. K., Lee, Y. S., Choi, J. M., & Kim, H. G. (2006). Effects of nitrogen, phosphorus, potassium and calcium nutrition on strawberry anthracnose. Plant Pathology, 55(2), 246–249.

    Article  Google Scholar 

  • Neumann, S., Paveley, N. D., Beed, F. D., & Sylvester-Bradley, R. (2004). Nitrogen per unit leaf area affects the upper asymptote of Puccinia striiformis f.sp tritici epidemics in winter wheat. Plant Pathology, 53(6), 725–732.

    Article  Google Scholar 

  • Pageau, K., Reisdorf-Cren, M., Morot-Gaudry, J. F., & Masclaux-Daubresse, C. (2006). The two senescence-related markers, GS1 (cytosolic glutamine synthetase) and GDH (glutamate dehydrogenase), involved in nitrogen mobilization, are differentially regulated during pathogen attack and by stress hormones and reactive oxygen species in Nicotiana tabacum L. leaves. Journal of Experimental Botany, 57(3), 547–557.

    Article  PubMed  CAS  Google Scholar 

  • Pan, H., Feng, B., & Marzluf, G. A. (1997). Two distinct protein-protein interactions between the NIT2 and NMR regulatory proteins are required to establish nitrogen metabolite repression in Neurospora crassa. Molecular Microbiology, 26(4), 721–729.

    Article  PubMed  CAS  Google Scholar 

  • Pellier, A. L., Lauge, R., Veneault-Fourrey, C., & Langin, T. (2003). CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Molecular Microbiology, 48(3), 639–655.

    Article  PubMed  CAS  Google Scholar 

  • Perez-Garcia, A., Snoeijers, S. S., Joosten, M., Goosen, T., & De Wit, P. (2001). Expression of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by the global nitrogen response factor NRF1. Molecular Plant-Microbe Interactions, 14(3),316–325.

    Article  PubMed  CAS  Google Scholar 

  • Ravagnani, A., Gorfinkiel, L., Langdon, T., et al. (1997). Subtle hydrophobic interactions between the seventh residue of the zinc finger loop and the first base of an HGATAR sequence determine promoter-specific recognition by the Aspergillus nidulans GATA factor AreA. Embo Journal, 16(13), 3974–3986.

    Article  PubMed  CAS  Google Scholar 

  • Screen, S., Bailey, A., Charnley, K., Cooper, R., & Clarkson, J. (1998). Isolation of a nitrogen response regulator gene (nrr1) from Metarhizium anisopliae. Gene, 221(1), 17–24.

    Article  PubMed  CAS  Google Scholar 

  • Smith, D. G., Garcia-Pedrajas, M. D., Gold, S. E., & Perlin, M. H. (2003). Isolation and characterization from pathogenic fungi of genes encoding ammonium permeases and their roles in dimorphism. Molecular Microbiology, 50(1), 259–275.

    Article  PubMed  CAS  Google Scholar 

  • Snoeijers, S. S., Perez-Garcia, A., Joosten, M., & De Wit, P. (2000). The effect of nitrogen on disease development and gene expression in bacterial and fungal plant pathogens. European Journal of Plant Pathology, 106(6), 493–506.

    Article  CAS  Google Scholar 

  • Snoeijers, S. S., Vossen, P., Goosen, T., Van den Broek, H. W. J., & De Wit, P. (1999). Transcription of the avirulence gene Avr9 of the fungal tomato pathogen Cladosporium fulvum is regulated by a GATA-type transcription factor in Aspergillus nidulans. Molecular and General Genetics, 261(4–5), 653–659.

    PubMed  CAS  Google Scholar 

  • Solomon, P. S., & Oliver, R. P. (2001). The nitrogen content of the tomato leaf apoplast increases during infection by Cladosporium fulvum. Planta, 213(2), 241–249.

    Article  PubMed  CAS  Google Scholar 

  • Solomon, P. S., Tan, K. C., & Oliver, R. P. (2003). The nutrient supply of pathogenic fungi; a fertile field for study. Molecular Plant Pathology, 4(3), 203–210.

    Article  Google Scholar 

  • Soundararajan, S., Jedd, G., Li, X. L., Ramos-Pamplona, M., Chua, N. H., & Naqvi, N. I. (2004). Woronin body function in Magnaporthe grisea is essential for efficient pathogenesis and for survival during nitrogen starvation stress. Plant Cell, 16(6), 1564–1574.

    Article  PubMed  CAS  Google Scholar 

  • StLeger, R. J., Joshi, L., Bidochka, M. J., & Roberts, D. W. (1996). Construction of an improved mycoinsecticide overexpressing a toxic protease. Proceedings of the National Academy of Sciences of the United States of America, 93(13), 6349–6354.

    Article  CAS  Google Scholar 

  • Talbot, N. J., Ebbole, D. J., & Hamer, J. E. (1993). Identification and characterization of MPG1, a gene involved in pathogenicity from the blast fungus, Magnaporthe grisea. Plant Cell, 5(11), 1575–1590.

    Article  PubMed  CAS  Google Scholar 

  • Talbot, N. J., McCafferty, H. R. K., Ma, M., Moore, K., & Hamer, J. E. (1997). Nitrogen starvation of the rice blast fungus Magnaporthe grisea may act as an environmental cue for disease symptom expression. Physiological and Molecular Plant Pathology, 50(3),179–195.

    Article  CAS  Google Scholar 

  • Tavernier, V., Cadiou, S., Pageau, K., Lauge, R., Reisdorf-Cren, M., Langin, T., & Masclaux-Daubresse, C. (2007). The plant nitrogen mobilization promoted by Colletotrichum lindemuthianum in Phaseolus leaves depends on fungus pathogenicity. Journal of Experimental Botany, 58(12), 3351–3360.

    Article  PubMed  CAS  Google Scholar 

  • Trail, F., Xu, J. R., San Miguel, P., Halgren, R. G., & Kistler, H. C. (2003). Analysis of expressed sequence tags from Gibberella zeae (anamorph Fusarium graminearum). Fungal Genetics and Biology, 38(2), 187–197.

    Article  PubMed  Google Scholar 

  • Tudzynski, B., Homann, V., Feng, B., & Marzluf, G. A. (1999). Isolation, characterization and disruption of the areA nitrogen regulatory gene of Gibberella fujikuroi. Molecular and General Genetics, 261(1), 106–114.

    Article  PubMed  CAS  Google Scholar 

  • Wilson, R. A., Jenkinson, J. M., Gibson, R. P., Littlechild, J. A., Wang, Z. Y., & Talbot, N. J. (2007). Tps1 regulates the pentose phosphate pathway, nitrogen metabolism and fungal virulence. Embo Journal, 26(15), 3673–3685.

    Article  PubMed  CAS  Google Scholar 

  • Yamada, T., Makimura, K., & Abe, S. (2006). Isolation, characterization, and disruption of dnr1, the areA/nit-2-like nitrogen regulatory gene of the zoophilic dermatophyte, Microsporum canis. Medical Mycology, 44(3), 243–252.

    Article  PubMed  CAS  Google Scholar 

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Donofrio, N.M., Mitchell, T.K., Dean, R.A. (2009). The Significance of Nitrogen Regulation, Source and Availability on the Interaction Between Rice and Rice Blast. In: Wang, GL., Valent, B. (eds) Advances in Genetics, Genomics and Control of Rice Blast Disease. Springer, Dordrecht. https://doi.org/10.1007/978-1-4020-9500-9_7

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