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Abstract: Plants utilize multiple layers of defense mechanisms to fight against the invasion of diverse pathogens. The R gene mediates resistance, in most cases, dependent on the co-existence of its cognate pathogen-derived avirulence (Avr) gene. The rice blast R gene Piz-t corresponds in gene-for-gene fashion to the Magnaporthe oryzae Avr gene AvrPiz-t. In this study, we determined and compared the genomic sequences surrounding the AvrPiz-t gene in both avirulent and virulent isolates, designating as AvrPiz-t-ZB15 and avrPiz-t-70-15 regions, respectively. The sequence of the AvrPiz-t-ZB15 region is 120966 bp whereas avrPiz-t-70-15 is 146292 bp in length. The extreme sequence similarity and good synteny in gene order and content along with the absence of two predicted genes in the avrPiz-t-70-15 region were observed in the predicted protein-coding regions in the AvrPiz-t locus. Nevertheless, frequent presence/absence and highly dynamic organization of transposable elements (TEs) were identified, representing the major variation of the AvrPiz-t locus between different isolates. Moreover, TEs constitute 27.3% and 43.2% of the genomic contents of the AvrPiz-t-ZB15 and avrPiz-t-70-15 regions, respectively, indicating that TEs contribute largely to the organization and evolution of AvrPiz-t locus. The findings of this study suggest that M. oryzae could benefit in an evolutionary sense from the presence of active TEs in genes conferring avirulence and provide an ability to rapidly change and thus to overcome host R genes.

[1]Böhnert, H.U., Fudal, I., Dioh, W., Tharreau, D., Notteghem, J.L., Lebrun, M.H., 2004. A putative polyketide synthase/peptide synthetase from Magnaporthe grisea signals pathogen attack to resistant rice. Plant Cell, 16(9):2499-2513.

[2]Chen, Q.H., Wang, Y.C., Li, A.N., Zhang, Z.G., Zheng, X.B., 2007. Molecular mapping of two cultivar-specific avirulence genes in the rice blast fungus Magnaporthe grisea. Mol. Genet. Genomics, 277(2):139-148.

[3]Collemare, J., Pianfetti, M., Houlle, A.E., Morin, D., Camborde, L., Gagey, M.J., Barbisan, C., Fudal, I., Lebrun, M.H., Böhnert, H.U., 2008. Magnaporthe grisea avirulence gene ACE1 belongs to an infection-specific gene cluster involved in secondary metabolism. New Phytol., 179(1):196-208.

[4]Daboussi, M.J., Capy, P., 2003. Transposable elements in filamentous fungi. Annu. Rev. Microbiol., 57(1):275-299.

[5]Dai, Y., Jia, Y., Correll, J., Wang, X., Wang, Y., 2010. Diversification and evolution of the avirulence gene AVR-Pita1 in field isolates of Magnaporthe oryzae. Fungal Genet. Biol., 47(12):973-980.

[6]Dean, R.A., Talbot, N.J., Ebbole, D.J., Farman, M.L., Mitchell, T.K., Orbach, M.J., Thon, M., Kulkarni, R., Xu, J.R., Pan, H., et al., 2005. The genome sequence of the rice blast fungus Magnaporthe grisea. Nature, 434(7036):980-986.

[7]Dioh, W., Tharreau, D., Notteghem, J.L., Orbach, M., Lebrun, M.H., 2000. Mapping of avirulence genes in the rice blast fungus, Magnaporthe grisea, with RFLP and RAPD markers. Mol. Plant Microbe Interact., 13(2):217-227.

[8]Ewing, B., Green, P., 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res., 8(3):186-194.

[9]Ewing, B., Hillier, L., Wendl, M.C., Green, P., 1998. Base-calling of automated sequencer traces using phred. I. Accuracy assessment. Genome Res., 8(3):175-185.

[10]Farman, M.L., Eto, Y., Nakao, T., Tosa, Y., Nakayashiki, H., Mayama, S., Leong, S.A., 2002. Analysis of the structure of the AVR1-CO39 avirulence locus in virulent rice-infecting isolates of Magnaporthe grisea. Mol. Plant Microbe Interact., 15(1):6-16.

[11]Fu, H., Dooner, H.K., 2002. Intraspecific violation of genetic colinearity and its implications in maize. PNAS, 99(14):9573-9578.

[12]Fudal, I., Böhnert, H.U., Tharreau, D., Lebrun, M.H., 2005. Transposition of MINE, a composite retrotransposon, in the avirulence gene ACE1 of the rice blast fungus Magnaporthe grisea. Fungal Genet. Biol., 42(9):761-772.

[13]Gordon, D., Abajian, C., Green, P., 1998. Consed: a graphical tool for sequence finishing. Genome Res., 8(3):195-202.

[14]Kachroo, P., Leong, S.A., Chattoo, B.B., 1995. Mg-SINE: a short interspersed nuclear element from the rice blast fungus, Magnaporthe grisea. PNAS, 92(24):11125-11129.

[15]Kang, S., Sweigard, J.A., Valent, B., 1995. The PWL host specificity gene family in the blast fungus Magnaporthe grisea. Mol. Plant Microbe Interact., 8(6):939-948.

[16]Kang, S., Lebrun, M.H., Farrall, L., Valent, B., 2001. Gain of virulence caused by insertion of a Pot3 transposon in a Magnaporthe grisea avirulence gene. Mol. Plant Microbe Interact., 14(5):671-674.

[17]Khang, C.H., Park, S.Y., Lee, Y.H., Valent, B., Kang, S., 2008. Genome organization and evolution of the AVR-Pita avirulence gene family in the Magnaporthe grisea species complex. Mol. Plant Microbe Interact., 21(5):658-670.

[18]Lau, G.W., Chao, C.T., Ellingboe, A.H., 1993. Interaction of genes controlling avirulence/virulence of Magnaporthe grisea on rice cultivar Katy. Phytopathology, 83(4):375-382.

[19]Leong, S.A., 2008. The Ins and Outs of Host Recognition of Magnaporthe oryzae. In: Gufstason, J.P., Taylor, J., Stacey, G. (Eds.), The Genomics of Disease. Springer Science+Business Media, New York, p.119-216.

[20]Li, W., Wang, B., Wu, J., Lu, G., Hu, Y., Zhang, X., Zhang, Z., Zhao, Q., Feng, Q., Zhang, H., et al., 2009. The Magnaporthe oryzae avirulence gene AvrPiz-t encodes a predicted secreted protein that triggers the immunity in rice mediated by the blast resistance gene Piz-t. Mol. Plant Microbe Interact., 22(4):411-420.

[21]Liu, J., Wang, X., Mitchell, T., Hu, Y., Liu, X., Dai, L., Wang, G.L., 2010. Recent progress and understanding of the molecular mechanisms of the rice-Magnaporthe oryzae interaction. Mol. Plant Pathol., 11(3):419-427.

[22]Ma, L.J., Ibrahim, A.S., Skory, C., Grabherr, M.G., Burger, G., Butler, M., Elias, M., Idnurm, A., Lang, B.F., Sone, T., et al., 2009. Genomic analysis of the basal lineage fungus Rhizopus oryzae reveals a whole-genome duplication. PLoS Genet., 5(7):e1000549.

[23]Miki, S., Matsui, K., Kito, H., Otsuka, K., Ashizawa, T., Yasuda, N., Fukiya, S., Sato, J., Hirayae, K., Fujita, Y., et al., 2009. Molecular cloning and characterization of the AVR-Pia locus from a Japanese field isolate of Magnaporthe oryzae. Mol. Plant Pathol., 10(3):361-374.

[24]Orbach, M.J., Farrall, L., Sweigard, J.A., Chumley, F.G., Valent, B., 2000. A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell, 12(11):2019-2032.

[25]Saghai-Maroof, M.A., Soliman, K.M., Jorgensen, R.A., Allard, R.W., 1984. Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. PNAS, 81(24):8014-8018.

[26]SanMiguel, P., Tikhonov, A., Jin, Y.K., Motchoulskaia, N., Zakharov, D., Melake-Berhan, A., Springer, P.S., Edwards, K.J., Lee, M., Avramova, Z., et al., 1996. Nested retrotransposons in the intergenic regions of the maize genome. Science, 274(5288):765-768.

[27]Thon, M.R., Martin, S.L., Goff, S., Wing, R.A., Dean, R.A., 2004. BAC end sequences and a physical map reveal transposable element content and clustering patterns in the genome of Magnaporthe grisea. Fungal Genet. Biol., 41(7):657-666.

[28]Thon, M.R., Pan, H., Diener, S., Papalas, J., Taro, A., Mitchell, T.K., Dean, R.A., 2006. The role of transposable element clusters in genome evolution and loss of synteny in the rice blast fungus Magnaporthe oryzae. Genome Biol., 7(2):R16.

[29]Wei, F., Wing, R.A., Wise, R.P., 2002. Genome dynamics and evolution of the Mla (powdery mildew) resistance locus in barley. Plant Cell, 14(8):1903-1917.

[30]Yant, S.R., Wu, X., Huang, Y., Garrison, B., Burgess, S.M., Kay, M.A., 2005. High-resolution genome-wide mapping of transposon integration in mammals. Mol. Cell. Biol., 25(6):2085-2094.

[31]Yasuda, N., Noguchi, M.T., Fujita, Y., 2006. Partial mapping of avirulence genes AVR-Pii and AVR-Pia in the rice blast fungus Magnaporthe oryzae. Can. J. Plant Pathol., 28(3):494-498.

[32]Yoshida, K., Saitoh, H., Fujisawa, S., Kanzaki, H., Matsumura, H., Tosa, Y., Chuma, I., Takano, Y., Win, J., Kamoun, S., et al., 2009. Association genetics reveals three novel avirulence genes from the rice blast fungal pathogen Magnaporthe oryzae. Plant Cell, 21(5):1573-1591.

[33]Zhou, B., Qu, S., Liu, G., Dolan, M., Sakai, H., Lu, G., Bellizzi, M., Wang, G.L., 2006. The eight amino-acid differences within three leucine-rich repeats between Pi2 and Piz-t resistance proteins determine the resistance specificity to Magnaporthe grisea. Mol. Plant Microbe Interact., 19(11):1216-1228.

[34]Zhou, E., Jia, Y., Singh, P., Correll, J.C., Lee, F.N., 2007. Instability of the Magnaporthe oryzae avirulence gene AVR-Pita alters virulence. Fungal Genet. Biol., 44(10):1024-1034.