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Volume 51 Issue 7
Jul.  2024
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Article Contents

Recombination and repeat-induced point mutation landscapes reveal trade-offs between the sexual and asexual cycles of Magnaporthe oryzae

doi: 10.1016/j.jgg.2024.03.003
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This work was funded by the National Natural Science Foundation of China (32270664 and 32170327), the National Key Research and Development Program of China (2023YFD2200102 and 2023YFD2200104), and Jiangsu Collaborative Innovation Center for Modern Crop Production.

  • Received Date: 2024-01-30
  • Accepted Date: 2024-03-06
  • Rev Recd Date: 2024-03-01
  • Available Online: 2025-06-06
  • Publish Date: 2024-03-13
  • The fungal disease caused by Magnaporthe oryzae is one of the most devastating diseases that endanger many crops worldwide. Evidence shows that sexual reproduction can be advantageous for fungal diseases as hybridization facilitates host-jumping. However, the pervasive clonal lineages of M. oryzae observed in natural fields contradict this expectation. A better understanding of the roles of recombination and the fungi-specific repeat-induced point mutation (RIP) in shaping its evolutionary trajectory is essential to bridge this knowledge gap. Here we systematically investigate the RIP and recombination landscapes in M. oryzae using a whole genome sequencing data from 252 population samples and 92 cross progenies. Our data reveal that the RIP can robustly capture the population history of M. oryzae, and we provide accurate estimations of the recombination and RIP rates across different M. oryzae clades. Significantly, our results highlight a parent-of-origin bias in both recombination and RIP rates, tightly associating with their sexual potential and variations of effector proteins. This bias suggests a critical trade-off between generating novel allelic combinations in the sexual cycle to facilitate host-jumping and stimulating transposon-associated diversification of effectors in the asexual cycle to facilitate host coevolution. These findings provide unique insights into understanding the evolution of blast fungus.
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  • Bailey, T.L., 2021. STREME: accurate and versatile sequence motif discovery. Bioinformatics 37, 2834-2840.
    Bao, J., Chen, M., Zhong, Z., Tang, W., Lin, L., Zhang, X., Jiang, H., Zhang, D., Miao, C., Tang, H., et al., 2017. PacBio sequencing reveals transposable elements as a key contributor to genomic plasticity and virulence variation in Magnaporthe oryzae. Mol. Plant 10, 1465-1468.
    Boeva, V., Zinovyev, A., Bleakley, K., Vert, J.-P., Janoueix-Lerosey, I., Delattre, O., Barillot, E., 2011. Control-free calling of copy number alterations in deep-sequencing data using GC-content normalization. Bioinformatics 27, 268-269.
    Bolger, A.M., Lohse, M., Usadel, B., 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120.
    Cambareri, E.B., Singer, M.J., Selker, E.U., 1991. Recurrence of repeat-induced point mutation (RIP) in Neurospora crassa. Genetics 127, 699-710.
    Danecek, P., Bonfield, J.K., Liddle, J., Marshall, J., Ohan, V., Pollard, M.O., Whitwham, A., Keane, T., McCarthy, S.A., Davies, R.M., et al., 2021. Twelve years of SAMtools and BCFtools. GigaScience 10, giab008.
    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, 980.
    Fang, H., Zhang, F., Zhang, C., Wang, Dan, Shen, S., He, F., Tao, H., Wang, R., Wang, M., Wang, ., et al., 2022. Function of hydroxycinnamoyl transferases for the biosynthesis of phenolamides in rice resistance to Magnaporthe oryzae. J. Genet. Genomics, 49, 776-786.
    Flynn, J.M., Hubley, R., Goubert, C., Rosen, J., Clark, A.G., Feschotte, C., Smit, A.F., 2020. RepeatModeler2 for automated genomic discovery of transposable element families. Proc. Natl. Acad. Sci. 117, 9451-9457.
    Fouche, S., Plissonneau, C., Croll, D., 2018. The birth and death of effectors in rapidly evolving filamentous pathogen genomes. Curr. Opin. Microbiol. 46, 34-42.
    Freitag, M., Williams, R.L., Kothe, G.O., Selker, E.U., 2002. A cytosine methyltransferase homologue is essential for repeat-induced point mutation in Neurospora crassa. Proc. Natl. Acad. Sci. 99, 8802-8807.
    Fu, L., Gu, C., Mochizuki, K., Xiong, J., Miao, W., Wang, G., 2024. The genome-wide meiotic recombination landscape in ciliates and its implications for crossover regulation and genome evolution. J. Genet. Genomics 51, 302-312.
    Galagan, J.E., Calvo, S.E., Borkovich, K.A., Selker, E.U., Read, N.D., Jaffe, D., FitzHugh, W., Ma, L.-J., Smirnov, S., Purcell, S., et al., 2003. The genome sequence of the filamentous fungus Neurospora crassa. Nature 422, 859-868.
    Gessaman, J.D., Selker, E.U., 2017. Induction of H3K9me3 and DNA methylation by tethered heterochromatin factors in Neurospora crassa. Proc. Natl. Acad. Sci. 114, E9598-E9607.
    Gladyshev E. Repeat-induced point mutation and other genome defense mechanisms in fungi 2017.
    Gladyshev, E., Kleckner, N., 2017. DNA sequence homology induces cytosine-to-thymine mutation by a heterochromatin-related pathway in Neurospora. Nat. Genet. 49, 887-894.
    Gladyshev, E., Kleckner, N., 2016. Recombination-independent recognition of DNA homology for repeat-induced point mutation (RIP) is modulated by the underlying nucleotide sequence. PLOS Genet. 12, e1006015.
    Gladyshev, E., Kleckner, N., 2014. Direct recognition of homology between double helices of DNA in Neurospora crassa. Nat. Commun. 5, 3509.
    Goddard, M.R., Godfray, H.C.J., Burt, A., 2005. Sex increases the efficacy of natural selection in experimental yeast populations. Nature 434, 636-640.
    Gomez Luciano, L.B., Tsai, I.J., Chuma, I., Tosa, Y., Chen, Y.-H., Li, J.-Y., Li, M.-Y., Lu, M.-Y.J., Nakayashiki, H., Li, W.-H., 2019. Blast fungal genomes show frequent chromosomal changes, gene gains and losses, and effector gene turnover. Mol. Biol. Evol. 36, 1148-1161.
    Hallgren, J., Tsirigos, K.D., Pedersen, M.D., Armenteros, J.J.A., Marcatili, P., Nielsen, H., Krogh, A., Winther, O., 2022. DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks. bioRxiv. https://www.biorxiv.org/content/10.1101/2022.04.08.487609v1.
    Huang, J., Si, W., Deng, Q., Li, P., Yang, S., 2014. Rapid evolution of avirulence genes in rice blast fungus Magnaporthe oryzae. BMC Genet. 15, 45.
    Ikeda, K., Nakayashiki, H., Kataoka, T., Tamba, H., Hashimoto, Y., Tosa, Y., Mayama, S., 2002. Repeat-induced point mutation (RIP) in Magnaporthe grisea : implications for its sexual cycle in the natural field context. Mol. Microbiol. 45, 1355-1364.
    Inoue, Y., Vy, T.T.P., Yoshida, K., Asano, H., Mitsuoka, C., Asuke, S., Anh, V.L., Cumagun, C.J.R., Chuma, I., Terauchi, R., et al., 2017. Evolution of the wheat blast fungus through functional losses in a host specificity determinant. Science 357, 80-83.
    Koren, S., Walenz, B.P., Berlin, K., Miller, J.R., Bergman, N.H., Phillippy, A.M., 2017. Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation. Genome Res. 27, 722-736.
    Latorre, S.M., Were, V.M., Foster, A.J., Langner, T., Malmgren, A., Harant, A., Asuke, S., Reyes-Avila, S., Gupta, D.R., Jensen, C., et al., 2023. Genomic surveillance uncovers a pandemic clonal lineage of the wheat blast fungus. PLOS Biol. 21, e3002052.
    Letunic, I., Bork, P., 2021. Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res. 49, W293-W296.
    Lewis, Z.A., Honda, S., Khlafallah, T.K., Jeffress, J.K., Freitag, M., Mohn, F., Schubeler, D., Selker, E.U., 2009. Relics of repeat-induced point mutation direct heterochromatin formation in Neurospora crassa. Genome Res. 19, 427-437.
    Li, H., 2013. Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv. http://arxiv.org/abs/1303.3997.
    Li, J., Llorente, B., Liti, G., Yue, J.-X., 2022. RecombineX: a generalized computational framework for automatic high-throughput gamete genotyping and tetrad-based recombination analysis. PLOS Genet. 18, e1010047.
    Liu, H., Huang, J., Sun, X., Li, J., Hu, Y., Yu, L., Liti, G., Tian, D., Hurst, L.D., Yang, S., 2017. Tetrad analysis in plants and fungi finds large differences in gene conversion rates but no GC bias. Nat. Ecol. Evol. 2, 164-173.
    McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., Garimella, K., Altshuler, D., Gabriel, S., Daly, M., et al., 2010. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303.
    Nakamoto, A.A., Joubert, P.M., Krasileva, K.V., 2023. Intraspecific variation of transposable elements reveals differences in the evolutionary history of fungal phytopathogen pathotypes. Genome Biol. Evol. 15, evad206.
    Nakayashiki, H., Nishimoto, N., Ikeda, K., Tosa, Y., Mayama, S., 1999. Degenerate MAGGY elements in a subgroup of Pyricularia grisea: a possible example of successful capture of a genetic invader by a fungal genome. Mol. Gen. Genet. 261, 958-966.
    Naour-Vernet, M.L., Charriat, F., Gracy, J., Cros-Arteil, S., Ravel, S., Veillet, F., Meusnier, I., Padilla, A., Kroj, T., Cesari, S., et al., 2023. Adaptive evolution in virulence effectors of the rice blast fungus Pyricularia oryzae. PLOS Pathog. 19, e1011294.
    Nielsen, H., Tsirigos, K.D., Brunak, S., von Heijne, G., 2019. A brief history of protein sorting prediction. Protein J. 38, 200-216.
    Noor, M.A.F., Grams, K.L., Bertucci, L.A., Almendarez, Y., Reiland, J., Smith, K.R., 2001. The genetics of reproductive isolation and the potential for gene exchange between Drosophila pseudoobscura and D. persimilis via backcross hybrid males. Evolution 55, 512-521.
    Peng, Z., Oliveira-Garcia, E., Lin, G., Hu, Y., Dalby, M., Migeon, P., Tang, H., Farman, M., Cook, D., White, F.F., et al., 2019. Effector gene reshuffling involves dispensable mini-chromosomes in the wheat blast fungus. PLOS Genet. 15, e1008272.
    Pennisi, E., 2010. Armed and dangerous. Science 327, 804-805.
    Price, M.N., Dehal, P.S., Arkin, A.P., 2009. FastTree: computing large minimum evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26, 1641-1650.
    Qi, J., Chen, Y., Copenhaver, G.P., Ma, H., 2014. Detection of genomic variations and DNA polymorphisms and impact on analysis of meiotic recombination and genetic mapping. Proc. Natl. Acad. Sci. 111, 10007-10012.
    Quinlan, A.R., Hall, I.M., 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinforma. Oxf. Engl. 26, 841-842.
    Rahnama, M., Condon, B., Ascari, J.P., Dupuis, J.R., Del Ponte, E.M., Pedley, K.F., Martinez, S., Valent, B., Farman, M.L., 2023. Recent co-evolution of two pandemic plant diseases in a multi-hybrid swarm. Nat. Ecol. Evol. 7, 2055-2066.
    Robinson, J.T., Thorvaldsdottir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., 2011. Integrative genomics viewer. Nat. Biotechnol. 29, 24-26.
    Saha, S., Bridges, S., Magbanua, Z.V., Peterson, D.G., 2008. Empirical comparison of ab initio repeat finding programs. Nucleic Acids Res. 36, 2284-2294.
    Saleh, D., Milazzo, J., Adreit, H., Fournier, E., Tharreau, D., 2014. South-east asia is the center of origin, diversity and dispersion of the rice blast fungus, Magnaporthe oryzae. New Phytol. 201, 1440-1456.
    Saleh, D., Xu, P., Shen, Y., Li, C., Adreit, H., Milazzo, J., Ravigne, V., Bazin, E., Notteghem, J.-L., Fournier, E., Tharreau, D., 2012. Sex at the origin: an asian population of the rice blast fungus Magnaporthe oryzae reproduces sexually. Mol. Ecol. 21, 1330-1344.
    Sanchez-Vallet, A., Fouche, S., Fudal, I., Hartmann, F.E., Soyer, J.L., Tellier, A., Croll, D., 2018. The genome biology of effector gene evolution in filamentous plant pathogens. Annu. Rev. Phytopathol. 56, 21-40.
    Schulze-Lefert, P., Panstruga, R., 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16, 117-125.
    Segurel, L., Wyman, M.J., Przeworski, M., 2014. Determinants of mutation rate variation in the human germline. Annu. Rev. Genomics Hum. Genet. 15, 47-70.
    Seppey, M., Manni, M., Zdobnov, E.M., 2019. BUSCO: assessing genome assembly and annotation completeness, in: Kollmar, M. (Ed.), Gene Prediction: Methods and Protocols, Methods in Molecular Biology. Springer, New York, NY, pp. 227-245.
    Si, W., Yuan, Y., Huang, J., Zhang, X., Zhang, Y., Zhang, Y., Tian, D., Wang, C., Yang, Y., Yang, S., 2015. Widely distributed hot and cold spots in meiotic recombination as shown by the sequencing of rice F2 plants. New Phytol. 206, 1491-1502.
    Sperschneider, J., Dodds, P.N., 2022. EffectorP 3.0: prediction of apoplastic and cytoplasmic effectors in fungi and oomycetes. Mol. Plant-Microbe Interact. 35, 146-156.
    Stergiopoulos, I., de Wit, P.J.G.M., 2009. Fungal effector proteins. Annu. Rev. Phytopathol. 47, 233-263.
    Thierry, M., Charriat, F., Milazzo, J., Adreit, H., Ravel, S., Cros-Arteil, S., Borron, S., Sella, V., Kroj, T., Ioos, R., et al., 2022. Maintenance of divergent lineages of the rice blast fungus Pyricularia oryzae through niche separation, loss of sex and post-mating genetic incompatibilities. PLOS Pathog. 18, e1010687.
    Turgeon, B.G., Yoder, O.C., 2000. Proposed nomenclature for mating type genes of filamentous ascomycetes. Fungal Genet. Biol. 31, 1-5.
    Uchida, M., Konishi, T., Fujigasaki, A., Kita, K., Arie, T., Teraoka, T., Kanda, Y., Mori, M., Arazoe, T., Kamakura, T., 2023. Dysfunctional pro1 leads to female sterility in rice blast fungi. iScience 26, 107020.
    Walker, B.J., Abeel, T., Shea, T., Priest, M., Abouelliel, A., Sakthikumar, S., Cuomo, C.A., Zeng, Q., Wortman, J., Young, S.K., et al., 2014. Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLOS ONE 9, e112963.
    Wang, L., Sun, Y., Sun, X., Yu, L., Xue, L., He, Z., Huang, J., Tian, D., Hurst, L.D., Yang, S., 2020. Repeat-induced point mutation in Neurospora crassa causes the highest known mutation rate and mutational burden of any cellular life. Genome Biol. 21, 142.
    Wang, L., Zhang, Y., Qin, C., Tian, D., Yang, S., Hurst, L.D., 2016. Mutation rate analysis via parent-progeny sequencing of the perennial peach. II. no evidence for recombination-associated mutation. Proc. R. Soc. B Biol. Sci. 283, 20161785.
    Wei, C., Shan, K.-J., Wang, W., Zhang, S., Huan, Q., Qian, W., 2021. Evidence for a mouse origin of the SARS-CoV-2 omicron variant. J. Genet. Genomics 48, 1111-1121.
    Xu, M., Guo, L., Gu, S., Wang, O., Zhang, R., Peters, B.A., Fan, G., Liu, X., Xu, X., Deng, L., et al., 2020. TGS-GapCloser: a fast and accurate gap closer for large genomes with low coverage of error-prone long reads. GigaScience 9, giaa094.
    Yang, S., Li, J., Zhang, X., Zhang, Q., Huang, J., Chen, J.-Q., Hartl, D.L., Tian, D., 2013. Rapidly evolving R genes in diverse grass species confer resistance to rice blast disease. Proc. Natl. Acad. Sci. 110, 18572-18577.
    Zhang, Y., Lu, H.-W., Ruan, J., 2023. GAEP: a comprehensive genome assembly evaluating pipeline. J. Genet. Genomics 50, 747-754.
    Zhong, Z., Chen, M., Lin, L., Han, Y., Bao, J., Tang, W., Lin, L., Lin, Y., et al., 2018. Population genomic analysis of the rice blast fungus reveals specific events associated with expansion of three main clades. ISME J. 12, 1867-1878.
    Zhou, Z.-W., Yu, Z.-G., Huang, X.-M., Liu, J.-S., Guo, Y.-X., Chen, L.-L., Song, J.-M., 2022. GenomeSyn: a bioinformatics tool for visualizing genome synteny and structural variations. J. Genet. Genomics 49, 1174-1176.
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