Analysis of the lineage of Phytophthora infestans isolates using mating type assay, traditional markers, and next generation sequencing technologies

English version

Autoři: Ramadan A. Arafa ^aff001; Said M. Kamel ^aff001; Mohamed T. Rakha ^aff003; Nour Elden K. Soliman ^aff004; Olfat M. Moussa ^aff004; Kenta Shirasawa ^aff002
Působiště autorů: Plant Pathology Research Institute, Agricultural Research Center, Giza, Egypt ^aff001; Department of Frontier Research and Development, Kazusa DNA Research Institute, Chiba, Japan ^aff002; Department of Horticulture, Faculty of Agriculture, University of Kafrelsheikh, Kafr El-Sheikh, Egypt ^aff003; Department of Plant Pathology, Faculty of Agriculture, Cairo University, Giza, Egypt ^aff004
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0221604

Souhrn

Phytophthora infestans (Mont.) de Bary, a hemibiotrophic oomycete, has caused severe epidemics of late blight in tomato and potato crops around the world since the Irish Potato Famine in the 1840s. Breeding of late blight resistant cultivars is one of the most effective strategies to overcome this disruptive disease. However, P. infestans is able to break down host resistance and acquire resistance to various fungicides, possibly because of the existence of high genetic variability among P. infestans isolates via sexual and asexual reproduction. Therefore, to manage this disease, it is important to understand the genetic divergence of P. infestans isolates. In this study, we analyzed the genomes of P. infestans isolates collected from Egypt and Japan using various molecular approaches including the mating type assay and genotyping simple sequence repeats, mitochondria DNA, and effector genes. We also analyzed genome-wide single nucleotide polymorphisms using double-digest restriction-site associated DNA sequencing and whole genome resequencing (WGRS). The isolates were classified adequately using high-resolution genome-wide approaches. Moreover, these analyses revealed new clusters of P. infestans isolates in the Egyptian population. Monitoring the genetic divergence of P. infestans isolates as well as breeding of resistant cultivars would facilitate the elimination of the late blight disease.

Klíčová slova:

Data processing – DNA sequencing – Egypt – Genotyping – Microsatellite loci – Mitochondrial DNA – Potato – Tomatoes

Zdroje

1. Martin MD, Vieira FG, Ho SY, Wales N, Schubert M, Seguin-Orlando A, et al. Genomic Characterization of a South American Phytophthora Hybrid Mandates Reassessment of the Geographic Origins of Phytophthora infestans. Mol Biol Evol. 2016;33(2):478–91. Epub 2015/11/19. doi: 10.1093/molbev/msv241 26576850; PubMed Central PMCID: PMC4866541.

2. Gomez-Alpizar L, Carbone I, Ristaino JB. An Andean origin of Phytophthora infestans inferred from mitochondrial and nuclear gene genealogies. Proc Natl Acad Sci U S A. 2007;104(9):3306–11. Epub 2007/03/16. doi: 10.1073/pnas.0611479104 17360643; PubMed Central PMCID: PMC1805513.

3. Goss EM, Tabima JF, Cooke DE, Restrepo S, Fry WE, Forbes GA, et al. The Irish potato famine pathogen Phytophthora infestans originated in central Mexico rather than the Andes. Proc Natl Acad Sci U S A. 2014;111(24):8791–6. Epub 2014/06/04. doi: 10.1073/pnas.1401884111 24889615; PubMed Central PMCID: PMC4066499.

4. Wang S, Boevink PC, Welsh L, Zhang R, Whisson SC, Birch PRJ. Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. New Phytol. 2017;216(1):205–15. Epub 2017/08/02. doi: 10.1111/nph.14696 28758684; PubMed Central PMCID: PMC5601276.

5. Avila-Adame C, Gomez-Alpizar L, Zismann V, Jones KM, Buell CR, Ristaino JB. Mitochondrial genome sequences and molecular evolution of the Irish potato famine pathogen, Phytophthora infestans. Curr Genet. 2006;49(1):39–46. Epub 2005/12/06. doi: 10.1007/s00294-005-0016-3 16328503.

6. Haverkort AJ, Struik PC, Visser RGF, Jacobsen E. Applied Biotechnology to Combat Late Blight in Potato Caused by Phytophthora Infestans. Potato Research. 2009;52(3):249–64. doi: 10.1007/s11540-009-9136-3

7. Turkensteen LJ, Flier WG, Wanningen R, Mulder A. Production, survival and infectivity of oospores of Phytophthora infestans. Plant Pathology. 2000;49(6):688–96. doi: 10.1046/j.1365-3059.2000.00515.x

8. Goodwin S, Fry W. Global migration of Phytophthora infestans. Phytopathology. 1991;82:955–61.

9. Hohl HR, Iselin K. Strains of Phytophthora infestans from Switzerland with A2 mating type behaviour. Transactions of the British Mycological Society. 1984;83(3):529–30. doi: 10.1016/s0007-1536(84)80057-1

10. Kato M, Mizubuti ES, Goodwin SB, Fry WE. Sensitivity to Protectant Fungicides and Pathogenic Fitness of Clonal Lineages of Phytophthora infestans in the United States. Phytopathology. 1997;87(9):973–8. Epub 2008/10/24. doi: 10.1094/PHYTO.1997.87.9.973 18945070.

11. Day JP, Wattier RAM, Shaw DS, Shattock RC. Phenotypic and genotypic diversity in Phytophthora infestans on potato in Great Britain, 1995–98. Plant Pathology. 2004;53(3):303–15. doi: 10.1111/j.0032-0862.2004.01004.x

12. Fry WE, Birch PR, Judelson HS, Grunwald NJ, Danies G, Everts KL, et al. Five Reasons to Consider Phytophthora infestans a Reemerging Pathogen. 2015;105(7):966–81. doi: 10.1094/PHYTO-01-15-0005-FI 25760519.

13. Arafa RA, Shirasawa K. Technical review of molecular markers and next-generation sequencing technology to manage plant pathogenic oomycetes. African Journal of Biotechnology. 2018;17(12):369–79. doi: 10.5897/ajb2017.16304

14. Arafa RA, Moussa OM, Soliman NEK, Shirasawa K, Kamel SM, Rakha MT. Resistance to Phytophthora infestans in tomato wild relatives. African Journal of Agricultural Research. 2017;12(26):2188–96. doi: 10.5897/ajar2017.12422

15. Foolad MR, Merk HL, Ashrafi H. Genetics, Genomics and Breeding of Late Blight and Early Blight Resistance in Tomato. Critical Reviews in Plant Sciences. 2008;27(2):75–107. doi: 10.1080/07352680802147353

16. Chowdappa P, Nirmal Kumar BJ, Madhura S, Mohan Kumar SP, Myers KL, Fry WE, et al. Severe outbreaks of late blight on potato and tomato in South India caused by recent changes in thePhytophthora infestanspopulation. Plant Pathology. 2015;64(1):191–9. doi: 10.1111/ppa.12228

17. Hansen ZR, Knaus BJ, Tabima JF, Press CM, Judelson HS, Grunwald NJ, et al. Loop-mediated isothermal amplification for detection of the tomato and potato late blight pathogen, Phytophthora infestans. J Appl Microbiol. 2016;120(4):1010–20. Epub 2016/01/29. doi: 10.1111/jam.13079 26820117.

18. Rekad FZ, Cooke DEL, Puglisi I, Randall E, Guenaoui Y, Bouznad Z, et al. Characterization of Phytophthora infestans populations in northwestern Algeria during 2008–2014. Fungal Biol. 2017;121(5):467–77. Epub 2017/04/10. doi: 10.1016/j.funbio.2017.01.004 28390504.

19. Yoshida K, Schuenemann VJ, Cano LM, Pais M, Mishra B, Sharma R, et al. The rise and fall of the Phytophthora infestans lineage that triggered the Irish potato famine. Elife. 2013;2:e00731. Epub 2013/06/07. doi: 10.7554/eLife.00731 23741619; PubMed Central PMCID: PMC3667578.

20. Gilroy EM, Breen S, Whisson SC, Squires J, Hein I, Kaczmarek M, et al. Presence/absence, differential expression and sequence polymorphisms between PiAVR2 and PiAVR2-like in Phytophthora infestans determine virulence on R2 plants. New Phytol. 2011;191(3):763–76. Epub 2011/05/05. doi: 10.1111/j.1469-8137.2011.03736.x 21539575.

21. Haas BJ, Kamoun S, Zody MC, Jiang RH, Handsaker RE, Cano LM, et al. Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature. 2009;461(7262):393–8. Epub 2009/09/11. doi: 10.1038/nature08358 19741609.

22. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, et al. A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One. 2011;6(5):e19379. Epub 2011/05/17. doi: 10.1371/journal.pone.0019379 21573248; PubMed Central PMCID: PMC3087801.

23. Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML. Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet. 2011;12(7):499–510. Epub 2011/06/18. doi: 10.1038/nrg3012 21681211.

24. Arafa RA, Soliman NEK, Moussa OM, Kamel SM, Shirasawa K. Characterization of Egyptian Phytophthora infestans population using simple sequence repeat markers. Journal of General Plant Pathology. 2018;84(2):104–7. doi: 10.1007/s10327-018-0763-x

25. Li Y, van der Lee TA, Evenhuis A, van den Bosch GB, van Bekkum PJ, Forch MG, et al. Population dynamics of Phytophthora infestans in the Netherlands reveals expansion and spread of dominant clonal lineages and virulence in sexual offspring. G3 (Bethesda). 2012;2(12):1529–40. Epub 2013/01/01. doi: 10.1534/g3.112.004150 23275876; PubMed Central PMCID: PMC3516475.

26. Knaus BJ, Tabima JF, Shakya SK, Judelson HS, Grünwald NJ. 2019. doi: 10.1101/633701

27. Cooke DE, Cano LM, Raffaele S, Bain RA, Cooke LR, Etherington GJ, et al. Genome analyses of an aggressive and invasive lineage of the Irish potato famine pathogen. PLoS Pathog. 2012;8(10):e1002940. Epub 2012/10/12. doi: 10.1371/journal.ppat.1002940 23055926; PubMed Central PMCID: PMC3464212.

28. Raffaele S, Farrer RA, Cano LM, Studholme DJ, MacLean D, Thines M, et al. Genome evolution following host jumps in the Irish potato famine pathogen lineage. Science. 2010;330(6010):1540–3. Epub 2010/12/15. doi: 10.1126/science.1193070 21148391.

29. Raffaele S, Win J, Cano LM, Kamoun S. Analyses of genome architecture and gene expression reveal novel candidate virulence factors in the secretome of Phytophthora infestans. BMC Genomics. 2010;11:637. Epub 2010/11/18. doi: 10.1186/1471-2164-11-637 21080964; PubMed Central PMCID: PMC3091767.

30. Kim MS, Hohenlohe PA, Kim KH, Seo ST, Klopfenstein NB. Genetic diversity and population structure of Raffaelea quercus-mongolicae, a fungus associated with oak mortality in South Korea. For Pathol. 2016;46(2):164–7. Epub 2016/04/19. doi: 10.1111/efp.12263 27087782; PubMed Central PMCID: PMC4827447.

31. Grewe F, Huang JP, Leavitt SD, Lumbsch HT. Reference-based RADseq resolves robust relationships among closely related species of lichen-forming fungi using metagenomic DNA. Sci Rep. 2017;7(1):9884. Epub 2017/08/31. doi: 10.1038/s41598-017-09906-7 28852019; PubMed Central PMCID: PMC5575168.

32. Grewe F, Lagostina E, Wu H, Printzen C, Lumbsch HT. Population genomic analyses of RAD sequences resolves the phylogenetic relationship of the lichen-forming fungal species Usneaantarctica and Usneaaurantiacoatra. MycoKeys. 2018;(43):91–113. Epub 2018/12/28. doi: 10.3897/mycokeys.43.29093 30588165; PubMed Central PMCID: PMC6300515.

33. Arafa RA, Rakha MT, Soliman NEK, Moussa OM, Kamel SM, Shirasawa K. Rapid identification of candidate genes for resistance to tomato late blight disease using next-generation sequencing technologies. PLoS One. 2017;12(12):e0189951. Epub 2017/12/19. doi: 10.1371/journal.pone.0189951 29253902; PubMed Central PMCID: PMC5734779.

34. Yang L, Wang D, Xu Y, Zhao H, Wang L, Cao X, et al. A New Resistance Gene against Potato Late Blight Originating from Solanum pinnatisectum Located on Potato Chromosome 7. Front Plant Sci. 2017;8:1729. Epub 2017/11/01. doi: 10.3389/fpls.2017.01729 29085380; PubMed Central PMCID: PMC5649132.

35. Cooke L, Zhang R, Wu L, Chen S, Forbes G. Recent developments: late blight in Asia AsiaBlight. EuroBlight workshop. 2017:14–7.

36. Cooke LR, Schepers HTAM, Hermansen A, Bain RA, Bradshaw NJ, Ritchie F, et al. Epidemiology and Integrated Control of Potato Late Blight in Europe. Potato Research. 2011;54(2):183–222. doi: 10.1007/s11540-011-9187-0

37. Runno-Paurson E, Fry WE, Myers KL, Koppel M, Mänd M. Characterisation of Phytophthora infestans isolates collected from potato in Estonia during 2002–2003. European Journal of Plant Pathology. 2009;124(4):565–75. doi: 10.1007/s10658-009-9442-2

38. Griffith GW, Shaw DS. Polymorphisms in phytophthora infestans: four mitochondrial haplotypes are detected after PCR amplification of DNA from pure cultures or from host lesions. Appl Environ Microbiol. 1998;64(10):4007–14. Epub 1998/10/06. 9758833; PubMed Central PMCID: PMC106592.

39. Yang X. Phytophthora mississippiae sp. nov., a New Species Recovered from Irrigation Reservoirs at a Plant Nursery in Mississippi. Journal of Plant Pathology & Microbiology. 2013;04(06). doi: 10.4172/2157-7471.1000180

40. Knapova G, Schlenzig A, Gisi U. Crosses between isolates of Phytophthora infestans from potato and tomato and characterization of F1 and F2 progeny for phenotypic and molecular markers. Plant Pathology. 2002;51(6):698–709. doi: 10.1046/j.1365-3059.2002.00762.x

41. Lees AK, Wattier R, Shaw DS, Sullivan L, Williams NA, Cooke DEL. Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathology. 2006;55(3):311–9. doi: 10.1111/j.1365-3059.2006.01359.x

42. Li Y, Cooke DE, Jacobsen E, van der Lee T. Efficient multiplex simple sequence repeat genotyping of the oomycete plant pathogen Phytophthora infestans. J Microbiol Methods. 2013;92(3):316–22. Epub 2013/01/15. doi: 10.1016/j.mimet.2012.11.021 23313554.

43. van Berloo R. GGT 2.0: versatile software for visualization and analysis of genetic data. J Hered. 2008;99(2):232–6. Epub 2008/01/29. doi: 10.1093/jhered/esm109 18222930.

44. Shirasawa K, Hirakawa H, Isobe S. Analytical workflow of double-digest restriction site-associated DNA sequencing based on empirical and in silico optimization in tomato. DNA Res. 2016;23(2):145–53. Epub 2016/03/05. doi: 10.1093/dnares/dsw004 26932983; PubMed Central PMCID: PMC4833422.

45. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863–4. Epub 2011/02/01. doi: 10.1093/bioinformatics/btr026 21278185; PubMed Central PMCID: PMC3051327.

46. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9. Epub 2012/03/06. doi: 10.1038/nmeth.1923 22388286; PubMed Central PMCID: PMC3322381.

47. Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9. Epub 2009/06/10. doi: 10.1093/bioinformatics/btp352 19505943; PubMed Central PMCID: PMC2723002.

48. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, et al. The variant call format and VCFtools. Bioinformatics. 2011;27(15):2156–8. doi: 10.1093/bioinformatics/btr330 21653522; PubMed Central PMCID: PMC3137218.

49. Shirasawa K, Hirakawa H, Nunome T, Tabata S, Isobe S. Genome-wide survey of artificial mutations induced by ethyl methanesulfonate and gamma rays in tomato. Plant Biotechnol J. 2016;14(1):51–60. Epub 2015/02/18. doi: 10.1111/pbi.12348 25689669; PubMed Central PMCID: PMC5023996.

50. Cingolani P, Platts A, Wang le L, Coon M, Nguyen T, Wang L, et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly (Austin). 2012;6(2):80–92. Epub 2012/06/26. doi: 10.4161/fly.19695 22728672; PubMed Central PMCID: PMC3679285.

51. Xie C, Tammi MT. CNV-seq, a new method to detect copy number variation using high-throughput sequencing. BMC Bioinformatics. 2009;10:80. Epub 2009/03/10. doi: 10.1186/1471-2105-10-80 19267900; PubMed Central PMCID: PMC2667514.

52. Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES. TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics. 2007;23(19):2633–5. Epub 2007/06/26. doi: 10.1093/bioinformatics/btm308 17586829.

Analysis of the lineage of Phytophthora infestans isolates using mating type assay, traditional markers, and next generation sequencing technologies

Souhrn

Klíčová slova:

Zdroje

PLOS One

Současné pohledy na riziko v parodontologii

Svět praktické medicíny 3/2024 (znalostní test z časopisu)

Kardiologické projevy hypereozinofilií

Střevní příprava před kolonoskopií

Aktuální možnosti diagnostiky a léčby litiáz