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Journal of General Plant Pathology

, Volume 85, Issue 3, pp 189–200 | Cite as

Genetic diversity of Phytophthora nicotianae reveals pathogen transmission mode in Japan

  • Auliana AfandiEmail author
  • Ayaka Hieno
  • Arif Wibowo
  • Siti Subandiyah
  • Afandi
  • Haruhisha Suga
  • Koji Tsuchida
  • Koji Kageyama
Fungal Diseases
  • 153 Downloads

Abstract

Phytophthora nicotianae is an important soil-borne pathogen in tropical, subtropical and temperate regions. To clarify the genetic diversity of P. nicotianae and to understand its mode of transmission in Japan, we developed six new microsatellites markers, consisting of six loci and 39 alleles. In a phylogenetic analysis, 138 isolates, including 125 from Japan and 13 from overseas, were shown to differ, even though some were collected from the same host and location, suggesting that there is no geographic or host plant clustering. Population structure analysis also revealed a highly admixed population of P. nicotianae in Japan. Molecular analysis suggested high variance between individuals but no significant differences between populations. Both A1 and A2 mating types were present in the same population, which could be due to high levels of variance between individuals in the population. The absence of geographical structure between populations also suggests that the pathogen is able to migrate from one population to another. We propose that this phenomenon could result from human activities related to the transport of plant and associated agricultural materials.

Keywords

Diversity Microsatellite Phytophthora nicotianae Population genetics Population structure 

Notes

Acknowledgements

The authors acknowledge Mr. Seiji Uematsu, Dr. Hideki Watanabe, Mr. Minoru Inada, Dr. Yuji Kajitani for providing P. nicotianae isolates used in this study.

Supplementary material

10327_2018_836_MOESM1_ESM.xlsx (22 kb)
Supplementary material 1 (XLSX 21 KB)

References

  1. Aguayo J, Adams GC, Halkett F, Catal M, Husson C, Nagy ZÁ, Hansen EM, Marçais B, Frey P (2010) Strong genetic differentiation between North American and European populations of Phytophthora alni subsp. uniformis. Phytopathology 103:190–199CrossRefGoogle Scholar
  2. Asuyama H (1934) New diseases and pathogens reported in the year of 1934 on our cultivated plants in Japan (in Japanese). Jpn J Phytopathol 4:191–197CrossRefGoogle Scholar
  3. Bebber DP, Holmes T, Gurr SJ (2014) The global spread of crop pests and pathogens. Global Ecol Biogeogr 23:1398–1407CrossRefGoogle Scholar
  4. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580CrossRefGoogle Scholar
  5. Biasi A, Martin FN, Cacciola SO, di San Lio GM, Grünwald NJ, Schena L (2016) Genetic analysis of Phytophthora nicotianae populations from different hosts using microsatellite markers. Phytopathology 106:1006–1014CrossRefGoogle Scholar
  6. Bonnet Ph, Lacourt I, Venard P, Ricci P (1994) Diversity in pathogenicity to tobacco and in elicitin production and isolates of Phytophthora parasitica. J Phytopathol 141:25–37CrossRefGoogle Scholar
  7. Bruberg MB, Elameen A, Le VH, Nærstad R, Hermansen A, Lehtinen A, Hannukkala A, Nielsen B, Hansen J, Andersson B, Yuen J (2011) Genetic analysis of Phytophthora infestans populations in the Nordic European countries reveals high genetic variability. Fungal Biol 115:335–342CrossRefGoogle Scholar
  8. Charlesworth B (2015) What use is population genetics? Genetics 200:667–669CrossRefGoogle Scholar
  9. Cline ET, Farr DF, Rossman AY (2008) A synopsis of Phytophthora with accurate scientific names, host range, and geographic distribution. Plant Health Prog.  https://doi.org/10.1094/PHP-2008-0318-01-RS Google Scholar
  10. Colas V, Lacourt I, Ricci P, Vanlerberghe-Masutti F, Poupet A, Panabières F (1998) Diversity of virulence in Phytophthora parasitica on tobacco, as reflected by nuclear RFLPs. Phytopathology 88:205–212CrossRefGoogle Scholar
  11. Earl DA, vonHoldt BM (2012) STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conserv Genet Resour 4:359–361CrossRefGoogle Scholar
  12. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587Google Scholar
  13. Falush D, Stephens M, Pritchard JK (2007) Inference of population structure using multilocus genotype data: dominant markers and null alleles. Mol Ecol Notes 7:574–578CrossRefGoogle Scholar
  14. Horie H (2007) Studies on diagnosis, ecology and control of plant diseases on various horticultural crops in Japan (in Japanese). Jpn J Phytopathol 73:138–140CrossRefGoogle Scholar
  15. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Resour 9:1322–1332CrossRefGoogle Scholar
  16. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806CrossRefGoogle Scholar
  17. Kanto T, Uematsu S, Aino M (2007) Phytophthora blight of poinsettia (Euphorbia pulcherrima Willd. ex Klotzsch.) caused by Phytophthora nicotianae van Breda de Haan (1896) (in Japanese with English summary). Jpn J Phytopathol 73:112–113CrossRefGoogle Scholar
  18. Lees AK, Wattier R, Shaw DS, Sullivan L, Williams NA, Cooke DEL (2006) Novel microsatellite markers for the analysis of Phytophthora infestans populations. Plant Pathol 55:311–319CrossRefGoogle Scholar
  19. Ma L, Ji YJ, Zhang DX (2015) Statistical measures of genetic differentiation of populations: rationales, history and current states. Curr Zool 61:886–897CrossRefGoogle Scholar
  20. Mammella MA, Martin FN, Cacciola SO, Coffey MD, Faedda R, Schena L (2013) Analyses of the population structure in a global collection of Phytophthora nicotianae isolates inferred from mitochondrial and nuclear DNA sequences. Phytopathology 103:610–622CrossRefGoogle Scholar
  21. Matsuzaki M (1988) Distribution of mating types of Phytophthora nicotianae var. parasitica, causal fungus of Phytophthora rot of strawberry, in Saga Prefecture (in Japanese with English summary). Ann Phytopathol Soc Jpn 54:544–547CrossRefGoogle Scholar
  22. Meitz J, Linde C, Thompson A, Langenhoven SD, McLeod A (2010) Phytophthora capsici on vegetable hosts in South Africa: distribution, host range and genetic diversity. Australas Plant Pathol 39:431–439CrossRefGoogle Scholar
  23. Montarry J, Andrividon D, Glais I, Corbiere R, Mialdea G, Delmotte F (2010) Microsatellite markers reveal two admixed genetic groups and an ongoing displacement within the French population of the invasive plant pathogen Phytophthora infestans. Mol Ecol 19:1965–1977CrossRefGoogle Scholar
  24. Morita Y, Tojo M (2007) Modification of PARP medium using fluazinam, miconazole, and nystatin for detection of Pythium spp. in soil. Plant Dis 91:1591–1599CrossRefGoogle Scholar
  25. Nakamura H, Matsuzaki M (1994) Occurrence of Phytophthora rot of limonium caused by Phytophthora nicotianae in Saga Prefecture (Abstract in Japanese). Ann Phytopathol Soc Jpn 60:737Google Scholar
  26. Nath VS, Senthil M, Hegde VM, Jeeva ML, Misra RS, Veena SS, Raj M (2013) Genetic diversity of Phytophthora colocasiae isolates in India based on AFLP analysis. 3 Biotech 3:297–305CrossRefGoogle Scholar
  27. Panabières F, Ali GS, Allagui MB, Dalio RJD, Gudmestad NC, Kuhn ML, Guha Roy S, Schena L, Zampounis A (2016) Phytophthora nicotianae diseases worldwide: new knowledge of a long-recognised pathogen. Phytopathol Mediterr 55:20–40Google Scholar
  28. Parkunan V, Johnson CS, Bowman BC (2010) Population structure, mating type, and mefenoxam sensitivity of Phytophthora nicotianae in Virginia tobacco fields. Plant Dis 94:1361–1365CrossRefGoogle Scholar
  29. Peakall R, Smouse PE (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Resour 6:288–295CrossRefGoogle Scholar
  30. Peakall R, Smouse PE (2012) GenAlEx 6.5: Genetic analysis in Excel. Population genetic software for teaching and research—an update. Bioinformatics 28:2537–2539CrossRefGoogle Scholar
  31. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 7:574–578Google Scholar
  32. Robideau GP, De Cock AW, Coffey MD, Voglmayr H, Brouwer H, Bala K, Chitty DW, Désaulniers N, Eggertson QA, Gachon CM, Hu CH, Küpper FC, Rintoul TL, Sarhan E, Verstappen EC, Zhang Y, Bonants PJ, Ristaino JB, Lévesque CA (2011) DNA barcoding of oomycetes with cytochrome c oxidase subunit I and internal transcribed spacer. Mol Ecol Resour 11:1002–1011CrossRefGoogle Scholar
  33. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  34. San Millán RM, Martínez-Ballesteros I, Rementeria A, Garaizar J, Bikandi J (2013) Online exercise for the design and simulation of PCR and PCR-RFLP experiments. BMC Res Notes 6:513.  https://doi.org/10.1186/1756-0500-6-513 CrossRefGoogle Scholar
  35. Schoebel CN, Stewart J, Gruenwald NJ, Rigling D, Prospero S (2014) Population history and pathways of spread of the plant pathogen Phytophthora plurivora. PLOS One 9:e85368CrossRefGoogle Scholar
  36. Selkoe KA, Toonen RJ (2006) Microsatellites for ecologist: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629CrossRefGoogle Scholar
  37. Sunnucks P (2000) Efficient genetic markers for population biology. Trends Ecol Evol 15:199–203CrossRefGoogle Scholar
  38. Suzui T, Makino T, Ogoshi A (1980) Phytophthora rot of strawberry caused by Phytophthora nicotianae var. parasitica in Shizuoka. Ann Phytopathol Soc Jpn 46:169–178CrossRefGoogle Scholar
  39. Takeuchi J, Horie H (2000) First report of Phytophthora rot of garden pea and Albuca nelsonii in Japan (in Japanese with English summary). Annu Rept Kanto-Tosan Plant Prot Soc 47:45–48Google Scholar
  40. Takeuchi T, Suzuki T (2010) Phytophthora blight (Phytophthora nicotianae) on hydroponically grown Welsh onion (Allium fistulosum L.) and controlling damage with the nutrient solution (in Japanese with English summary). Bull Chiba Agric Res Cent 2:1–6Google Scholar
  41. Takeuchi J, Horie H, Eimori K (2004) First report of Phytophthora rot of New Zealand spinach in Japan (in Japanese with English summary). Annu Rept Kanto-Tosan Plant Prot Soc 51:55–57Google Scholar
  42. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  43. Tashiro N, Uematsu S, Matsuzaki M, Ide Y, Etoh T (2002) Phytophthora palmivora, P. citrophthora and P. nicotianae as causal agents of citrus brown rot (Abstract in Japanese). Jpn J Phytopathol 68:189Google Scholar
  44. Verhoeven KJF, Macel M, Wolfe LM, Biere A (2011) Population admixture, biological invasions and the balance between local adaptation and inbreeding depression. Proc R Soc B 278:2–8CrossRefGoogle Scholar
  45. Watanabe H, Taguchi Y, Hyakumachi M, Kageyama K (2007) Pythium and Phytophthora species associated with root and stem rots of kalanchoe. J Gen Plant Pathol 73:81–88CrossRefGoogle Scholar
  46. Wu M, Li B, Liu P, Weng Q, Zhan J, Chen Q (2017) Genetic analysis of Phytophthora sojae populations in Fujian, China. Plant Pathol 66:1182–1190CrossRefGoogle Scholar
  47. Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinform 13:134CrossRefGoogle Scholar
  48. Yokota S, Oomori T, Nao M, Watanabe T, Kitamoto H (2013) Involvement of Phytophthora rot caused by Phytophthora nicotianae in growth failure of asparagus (Asparagus officinalis L.) in replanted fields in Ehime Prefecture. Soil Microorg 67:77–82Google Scholar

Copyright information

© The Phytopathological Society of Japan and Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  1. 1.The United Graduate School of Agricultural ScienceGifu UniversityGifuJapan
  2. 2.River Basin Research CenterGifu UniversityGifuJapan
  3. 3.Faculty of AgricultureUniversitas Gadjah MadaYogyakartaIndonesia
  4. 4.Faculty of AgricultureUniversitas LampungBandar LampungIndonesia
  5. 5.Life Science Research CenterGifu UniversityGifuJapan
  6. 6.Faculty of Applied Biological ScienceGifu UniversityGifuJapan
  7. 7.Biotechnology Research CenterUniversitas Gadjah MadaYogyakartaIndonesia

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