The Plant Pathology Journal

The Korean Society of Plant Pathology (한국식물병리학회)
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Whole Genome Enabled Phylogenetic and Secretome Analyses of Two Venturia nashicola Isolates

  • Prokchorchik, Maxim (Department of Life Sciences, Pohang University of Science and Technology) ;
  • Won, Kyungho (National Institute of Horticultural and Herbal Science (NIHHS), Rural Development Administration (RDA)) ;
  • Lee, Yoonyoung (Department of Life Sciences, Pohang University of Science and Technology) ;
  • Segonzac, Cecile (Department of Plant Science, Plant Genomics and Breeding Institute and Research Institute of Agriculture and Life Sciences, College of Agriculture and Life Sciences, Seoul National University) ;
  • Sohn, Kee Hoon (Department of Life Sciences, Pohang University of Science and Technology)
  • Received : 2019.10.11
  • Accepted : 2019.12.10
  • Published : 2020.02.01
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Abstract

Venturia nashicola is a fungal pathogen causing scab disease in Asian pears. It is particularly important in the Northeast Asia region where Asian pears are intensively grown. Venturia nashicola causes disease in Asian pear but not in European pear. Due to the highly restricted host range of Venturia nashicola, it is hypothesized that the small secreted proteins deployed by the pathogen are responsible for the host determination. Here we report the whole genome based phylogenetic analysis and predicted secretomes for V. nashicola isolates. We believe that our data will provide a valuable information for further validation and functional characterization of host determinants in V. nashicola.

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References

  1. Ahmed, M. B., Santos, K. C. G. D., Sanchez, I. B., Petre, B., Lorrain, C., Plourde, M. B., Duplessis, S., Desgagne-Penix, I. and Germain, H. 2018. A rust fungal effector binds plant DNA and modulates transcription. Sci. Rep. 8:14718. https://doi.org/10.1038/s41598-018-32825-0
  2. Bock, C. H., Chen, C., Yu, F., Stevenson, K. L. and Wood, B. W. 2016. Draft genome sequence of Fusicladium effusum, cause of pecan scab. Stand. Genomic Sci. 11:36. https://doi.org/10.1186/s40793-016-0161-y
  3. Bouvier, L., Bourcy, M., Boulay, M., Tellier, M., Guerif, P., Denance, C., Durel, C.-E. and Lespinasse, Y. 2012. A new pear scab resistance gene Rvp1 from the European pear cultivar 'Navara' maps in a genomic region syntenic to an apple scab resistance gene cluster on linkage group 2. Tree Genet. Genomes 8:53-60. https://doi.org/10.1007/s11295-011-0419-x
  4. Bowen, J. K., Mesarich, C. H., Bus, V. G. M., Beresford, R. M., Plummer, K. M. and Templeton, M. D. 2011. Venturia inaequalis: the causal agent of apple scab. Mol. Plant Pathol. 12:105-122. https://doi.org/10.1111/j.1364-3703.2010.00656.x
  5. Bus, V. G. M., Rikkerink, E. H. A., Caffier, V., Durel, C.-E. and Plummer, K. M. 2011. Revision of the nomenclature of the differential host-pathogen interactions of Venturia inaequalis and Malus. Annu. Rev. Phytopathol. 49:391-413. https://doi.org/10.1146/annurev-phyto-072910-095339
  6. Chen, C., Bock, C. H. and Wood, B. W. 2017. Draft genome sequence of Venturia carpophila, the causal agent of peach scab. Stand. Genomic Sci. 12:68. https://doi.org/10.1186/s40793-017-0280-0
  7. de Jonge, R., van Esse, H. P., Maruthachalam, K., Bolton, M. D., Santhanam, P., Saber, M. K., Zhang, Z., Usami, T., Lievens, B., Subbarao, K. V. and Thomma, B. P. 2012. Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proc. Natl. Acad. Sci. U. S. A. 109:5110-5115. https://doi.org/10.1073/pnas.1119623109
  8. Delcher, A. L., Phillippy, A., Carlton, J. and Salzberg, S. L. 2002. Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res. 30:2478-2483. https://doi.org/10.1093/nar/30.11.2478
  9. Deng, C. H., Plummer, K. M., Jones, D. A. B., Mesarich, C. H., Shiller, J., Taranto, A. P., Robinson, A. J., Kastner, P., Hall, N. E., Templeton, M. D. and Bowen, J. K. 2017. Comparative analysis of the predicted secretomes of Rosaceae scab pathogens Venturia inaequalis and V. pirina reveals expanded effector families and putative determinants of host range. BMC Genomics 18:339. https://doi.org/10.1186/s12864-017-3699-1
  10. Emanuelsson, O., Brunak, S., von Heijne, G. and Nielsen, H. 2007. Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2:953-971. https://doi.org/10.1038/nprot.2007.131
  11. Gonzalez-Dominguez, E., Armengol, J. and Rossi, V. 2017. Biology and epidemiology of Venturia species affecting fruit crops: a review. Front. Plant Sci. 8:1496. https://doi.org/10.3389/fpls.2017.01496
  12. Huo, L., Zhang, H., Huo, X., Yang, Y., Li, X. and Yin, Y. 2017. pHMM-tree: phylogeny of profile hidden Markov models. Bioinformatics 33:1093-1095.
  13. Ishii, H. 2012. Resistance in Venturia nashicola to benzimidazoles and sterol demethylation inhibitors. In: Fungicide resistance in crop protection: risk and management, ed. by T. S. Thind, pp. 21-31. CAB International, Wallingford, UK.
  14. Ishii, H. and Yanase, H. 2000. Venturia nashicola, the scab fungus of Japanese and Chinese pears: a species distinct from V. pirina. Mycol. Res. 104:755-759. https://doi.org/10.1017/S0953756299001720
  15. Johnson, S., Jones, D., Thrimawithana, A. H., Deng, C. H., Bowen, J. K., Mesarich, C. H., Ishii, H., Won, K., Bus, V. G. M. and Plummer, K. M. 2019. Whole genome sequence resource of the Asian pear scab pathogen Venturia nashicola. Mol. Plant-Microbe Interact. 32:1463-1467. https://doi.org/10.1094/MPMI-03-19-0067-A
  16. Jones, J. D. G. and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. https://doi.org/10.1038/nature05286
  17. Joshi, S. G., Schaart, J. G., Groenwold, R., Jacobsen, E., Schouten, H. J. and Krens, F. A. 2011. Functional analysis and expression profiling of HcrVf1 and HcrVf2 for development of scab resistant cisgenic and intragenic apples. Plant Mol. Biol. 75:579-591. https://doi.org/10.1007/s11103-011-9749-1
  18. Karanyi, Z., Holb, I., Hornok, L., Pocsi, I. and Miskei, M. 2013. FSRD: fungal stress response database. Database (Oxford) 2013:bat037.
  19. Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E. L. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580. https://doi.org/10.1006/jmbi.2000.4315
  20. Krzywinski, M., Schein, J., Birol, I., Connors, J., Gascoyne, R., Horsman, D., Jones, S. J. and Marra, M. A. 2009. Circos: an information aesthetic for comparative genomics. Genome Res. 19:1639-1645. https://doi.org/10.1101/gr.092759.109
  21. Kwak, Y., Min, J., Song, J., Kim, M., Lee, H. and Kim, H. T. 2017. Relationship of resistance to benzimidazole fungicides with mutation of ${\beta}$-tubulin gene in Venturia nashicola. Res. Plant Dis. 23:150-158 (in Korean). https://doi.org/10.5423/RPD.2017.23.2.150
  22. Li, L., Stoeckert, C. J. Jr. and Roos, D. S. 2003. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 13:2178-2189. https://doi.org/10.1101/gr.1224503
  23. MacHardy, W. E. 1996. Apple scab: biology, epidemiology, and management. American Phytopathological Society, St. Paul, MN, USA. 570 pp.
  24. Minkin, I., Patel, A., Kolmogorov, M., Vyahhi, N. and Pham, S. 2013. Sibelia: a scalable and comprehensive synteny block generation tool for closely related microbial genomes. In: Lecture notes in computer science, Vol. 8126. Algorithms in bioinformatics. 13th International workshop, WABI 2013, eds. by A. Darling and J. Stoye, pp. 215-229. Springer-Verlag Berlin Heidelberg, Berlin, Heidelberg, Germany.
  25. Mistry, J., Finn, R. D., Eddy, S. R., Bateman, A. and Punta, M. 2013. Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 41:e121. https://doi.org/10.1093/nar/gkt263
  26. Nattestad, M. and Schatz, M. C. 2016. Assemblytics: a web analytics tool for the detection of variants from an assembly. Bioinformatics 32:3021-3023. https://doi.org/10.1093/bioinformatics/btw369
  27. Nguyen Ba, A. N., Pogoutse, A., Provart, N. and Moses, A. M. 2009. NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction. BMC Bioinformatics 10:202. https://doi.org/10.1186/1471-2105-10-202
  28. Nielsen, H. 2017. Predicting secretory proteins with SignalP. In: Methods in molecular biology, Vol. 1611. Protein function prediction, ed. by D. Kihara, pp. 59-73. Humana Press, New York, NY, USA.
  29. Park, P., Ishii, H., Adachi, Y., Kanematsu, S., Ieki, H. and Umemoto, S. 2000. Infection behavior of Venturia nashicola, the cause of scab on Asian pears. Phytopathology 90:1209-1216. https://doi.org/10.1094/PHYTO.2000.90.11.1209
  30. Passey, T. A. J., Armitage, A. D. and Xu, X. 2018. Annotated draft genome sequence of the apple scab pathogen Venturia inaequalis. Microbiol. Resour. Announc. 7:e01062-18.
  31. Prokchorchik, M., Won, K., Lee, Y., Choi, E. D., Segonzac, C. and Sohn, K. H. 2019. High contiguity whole genome sequence and gene annotation resource for two Venturia nashicola isolates. Mol. Plant-Microbe Interact. 32:1091-1094. https://doi.org/10.1094/MPMI-03-19-0072-A
  32. Schouten, H. J., Brinkhuis, J., van der Burgh, A., Schaart, J. G., Groenwold, R., Broggini, G. A. L. and Gessler, C. 2014. Cloning and functional characterization of the Rvi15 (Vr2) gene for apple scab resistance. Tree Genet. Genomes 10:251-260. https://doi.org/10.1007/s11295-013-0678-9
  33. Seemann, T. 2015. Snippy: rapid haploid variant calling and core genome alignment. URL https://github.com/tseemann/snippy [11 October 2019].
  34. Selin, C., de Kievit, T. R., Belmonte, M. F. and Fernando, W. G. D. 2016. Elucidating the role of effectors in plant-fungal interactions: progress and challenges. Front. Microbiol. 7:600.
  35. Shiller, J., Van de Wouw, A. P., Taranto, A. P., Bowen, J. K., Dubois, D., Robinson, A., Deng, C. H. and Plummer, K. M. 2015. A large family of AvrLm6-like genes in the apple and pear scab pathogens, Venturia inaequalis and Venturia pirina. Front. Plant Sci. 6:980.
  36. Sivanesan, A. 1977. Bibliotheca mycologica, Vol. 59. The taxonomy and pathology of Venturia species. J. Cramer, Vaduz, Germany. 139 pp.
  37. Sonah, H., Deshmukh, R. K. and Bélanger, R. R. 2016. Computational prediction of effector proteins in fungi: opportunities and challenges. Front. Plant Sci. 7:126.
  38. Song, J. and Seo, H.-J. 2018. Antifungal activity of agro-materials against pear scab (Venturia nashicola) and pear rust (Gymnosporangium asiaticum) fungi. Res. Plant Dis. 24:33-40 (in Korean). https://doi.org/10.5423/RPD.2018.24.1.33
  39. Sperschneider, J., Dodds, P. N., Gardiner, D. M., Singh, K. B. and Taylor, J. M. 2018. Improved prediction of fungal effector proteins from secretomes with EffectorP 2.0. Mol. Plant Pathol. 19:2094-2110. https://doi.org/10.1111/mpp.12682
  40. Tanaka, S. and Yamamoto, S. 1964. Studies on pear scab II. Taxonomy of the causal fungus of Japanese pear scab. Jpn. J. Phytopathol. 29:128-136 (in Japanese). https://doi.org/10.3186/jjphytopath.29.128
  41. Uhse, S. and Djamei, A. 2018. Effectors of plant-colonizing fungi and beyond. PLoS Pathog. 14:e1006992. https://doi.org/10.1371/journal.ppat.1006992
  42. Urban, M., Cuzick, A., Rutherford, K., Irvine, A., Pedro, H., Pant, R., Sadanadan, V., Khamari, L., Billal, S., Mohanty, S. and Hammond-Kosack, K. E. 2017. PHI-base: a new interface and further additions for the multi-species pathogen-host interactions database. Nucleic Acids Res. 45:D604-D610. https://doi.org/10.1093/nar/gkw1089
  43. Vargas, W. A., Sanz-Martin, J. M., Rech, G. E., Armijos-Jaramillo, V. D., Rivera, L. P., Echeverria, M. M., Diaz-Minguez, J. M., Thon, M. R. and Sukno, S. A. 2016. A fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development. Mol. Plant-Microbe Interact. 29:83-95. https://doi.org/10.1094/MPMI-09-15-0209-R
  44. Vinatzer, B. A., Patocchi, A., Gianfranceschi, L., Tartarini, S., Zhang, H. B., Gessler, C. and Sansavini, S. 2001. Apple contains receptor-like genes homologous to the Cladosporium fulvum resistance gene family of tomato with a cluster of genes cosegregating with Vf apple scab resistance. Mol. Plant-Microbe Interact. 14:508-515. https://doi.org/10.1094/MPMI.2001.14.4.508
  45. Won, K., Bastiaanse, H., Kim, Y. K., Song, J. H., Kang, S. S., Lee, H. C., Cho, K. H., Brewer, L., Singla, G., Gardiner, S. E., Chagne, D. and Bus, V. G. M. 2014. Genetic mapping of polygenic scab (Venturia pirina) resistance in an interspecific pear family. Mol. Breed. 34:2179-2189. https://doi.org/10.1007/s11032-014-0172-6
  46. Yun, Y. H., Yoon, S. K., Son, S. Y. and Kim, S. H. 2013. Homology of scytalone dehydratase melanin gene in Venturia nashicola. Korean J. Mycol. 41:200-204 (in Korean). https://doi.org/10.4489/KJM.2013.41.3.200
  47. Zhao, P., Kakishima, M., Uzuhashi, S. and Ishii, H. 2012. Multigene phylogenetic analysis of inter- and intraspecific relationships in Venturia nashicola and V. pirina. Eur. J. Plant Pathol. 132:245-258. https://doi.org/10.1007/s10658-011-9869-0