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Molecular Breeding

, 38:138 | Cite as

Development of SSR markers linked to QTL reducing leaf hair density and grapevine downy mildew resistance in Vitis vinifera

  • Atsushi Kono
  • Yusuke Ban
  • Nobuhito Mitani
  • Hiroshi Fujii
  • Shusei Sato
  • Koichi Suzaki
  • Akifumi Azuma
  • Noriyuki Onoue
  • Akihiko Sato
Article
  • 34 Downloads

Abstract

Dense leaf hairs of grapevines have been known to act as a preexisting defense structure for preventing the incidence of grapevine downy mildew, because the pathogen, Plasmopara viticola, needs water to invade grapevines, and water is repelled by a hydrophobic surface due to dense leaf hairs. In the present study, we performed regression analyses of downy mildew resistance with leaf hair density using hybrids of Vitis labrusca origin and confirmed the effect of leaf hairs. Reducing the repelling effect of leaf hairs by detergent application canceled the effect of leaf hair, which confirmed the hypothesis. Thereafter, based on QTL analyses in the population of V. vinifera ‘Muscat of Alexandria’ × the interspecific hybrid ‘Campbell Early,’ we identified a major locus in linkage group (LG) 5 of ‘Muscat of Alexandria’ controlling leaf hair density. This locus was previously reported as a small effect QTL for downy mildew resistance, however we found that the locus had high LOD scores explaining 71.9%–78.5% of the phenotypic variance of leaf hairs. Moreover, this locus was detected as a QTL for downy mildew resistance. The effect of this locus was confirmed in two other hybrid populations. Finally, we could successfully identify three traditional V. vinifera table grapes ‘Muscat of Alexandria,’ ‘Katta Kurgan,’ and ‘Parkent’ as the origin of the allele linked to hairlessness by defining the SSR haplotypes. The use of this locus for marker-assisted selections would be a promising strategy for producing grapevines with resistance by preexisting defense structure.

Keywords

DNA marker Grapevine downy mildew Leaf hairs Preexisting defense structure Vitis vinifera Vitis labrusca 

Notes

Acknowledgements

We thank Takeshi Hayashi (NARO, Tsukuba, Japan) for support in Pop AC mapping and manuscript revision, Ryosuke Mochioka (Kagawa University, Kagawa, Japan) and Hino Motosugi (Kyoto Prefectural University, Kyoto, Japan) for providing Japanese wild Vitis species, Natsumaro Kutsuna (LPixel Inc. Tokyo, Japan) for support in imaging analysis, and Technical Support Center Operations Unit 1 in Akitsu for their technical support in vineyards. We are grateful to Mirai Nakahara, Miho Kohata, Tamami Nakasumi, and Sumie Kurokawa (NARO, Hiroshima, Japan) for technical assistance, and to Takao Ito (NARO, Hiroshima, Japan) for critical reading of the manuscript.

Author’s contributions

A. K. wrote the manuscript. A. K., Y. B., K. S., A. A., N. O., and A. S. designed the experiments. A. A. contributed to the experiments using ‘Pinot Meunier.’ A. K. and A. S. contributed to statistical data analyses. A. K. performed the experiments. A. K., Y. B., N. M., and S. S. genotyped Pop AC. Y. B. and N. M. developed populations. H. F. extracted SSRs from the grapevine reference genome.

Funding information

This work was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Genomics for Agricultural Innovation, HOR-2006).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

11032_2018_889_MOESM1_ESM.docx (66 kb)
Supplementary Tables (DOCX 66.4 kb)
11032_2018_889_MOESM2_ESM.docx (5.6 mb)
Supplementary Figs. 1 to 6 (DOCX 5.63 mb)
11032_2018_889_MOESM3_ESM.pdf (244 kb)
Supplementary Fig. 7 (PDF 244 kb)
11032_2018_889_MOESM4_ESM.docx (354 kb)
Supplementary Fig. 8 (DOCX 353 kb)

References

  1. Agrios G (2005) Plant pathology, 5th edn. Academic Press, MassachusettsGoogle Scholar
  2. Bailey LH, Bailey EZ (1930) HORTUS, a concise dictionary of gardening, general horticulture and cultivated plants in North America. The Macmillan Company, New YorkGoogle Scholar
  3. Ban Y, Mitani N, Hayashi T, Sato A, Azuma A, Kono A, Kobayashi S (2014) Exploring quantitative trait loci for anthocyanin content in interspecific hybrid grape (Vitis labruscana × Vitis vinifera). Euphytica 198:101–114.  https://doi.org/10.1007/s10681-014-1087-3 CrossRefGoogle Scholar
  4. Bellin D, Peressotti E, Merdinoglu D, Wiedemann-Merdinoglu S, Adam-Blondon AF, Cipriani G, Morgante M, Testolin R, Di Gaspero G (2009) Resistance to Plasmopara viticola in grapevine ‘Bianca’ is controlled by a major dominant gene causing localized necrosis at the infection site. Theor Appl Genet 120:163–176.  https://doi.org/10.1007/s00122-009-1167-2 CrossRefPubMedGoogle Scholar
  5. Benson G (1999) Tandem repeats finder: a program to analyze DNA sequences. Nucleic Acids Res 27:573–580.  https://doi.org/10.1093/nar/27.2.573 CrossRefPubMedPubMedCentralGoogle Scholar
  6. Cadle-Davidson L (2008) Variation within and between Vitis spp. for foliar resistance to the downy mildew pathogen Plasmopara viticola. Plant Dis 92:1577–1584.  https://doi.org/10.1094/PDIS-92-11-1577 CrossRefGoogle Scholar
  7. Cahoon GA (1998) French hybrid grapes in North America. In: Ferree DC (ed) A history of fruit varieties. Good Fruit Grower Magazine, Washington, pp 152–168Google Scholar
  8. Cipriani G, Spadotto A, Jurman I, Di Gaspero G, Crespan M, Meneghetti S, Frare E, Vignani R, Cresti M, Morgante M, Pezzotti M, Pe E, Policriti A, Testolin R (2010) The SSR-based molecular profile of 1005 grapevine (Vitis vinifera L.) accessions uncovers new synonymy and parentages, and reveals a large admixture amongst varieties of different geographic origin. Theor Appl Genet 121:1569–1585.  https://doi.org/10.1007/s00122-010-1411-9 CrossRefPubMedGoogle Scholar
  9. Crawley MJ (2015) Statistics: an introduction using R, Second edn. John Wiley & Sons Ltd, West SussexGoogle Scholar
  10. Delmotte F, Mestre P, Schneider C, Kassemeyer HH, Kozma P, Richart-Cervera S, Rouxel M, Delière L (2014) Rapid and multiregional adaptation to host partial resistance in a plant pathogenic oomycete: evidence from European populations of Plasmopara viticola, the causal agent of grapevine downy mildew. Infect Genet Evol 27:500–508.  https://doi.org/10.1016/j.meegid.2013.10.017 CrossRefPubMedGoogle Scholar
  11. Di Gaspero G, Copetti D, Coleman C, Castellarin SD, Eibach R, Kozma P, Lacombe T, Gambetta G, Zvyagain A, Cindrić P, Kovács L, Morgante M, Testolin R (2012) Selective sweep at the Rpv3 locus during grapevine breeding for downy mildew resistance. Theor Appl Genet 124:277–286.  https://doi.org/10.1007/s00122-011-1703-8 CrossRefPubMedGoogle Scholar
  12. Divilov K, Wiesner-Hanks T, Barba P, Cadle-Davidson L, Reisch BI (2017) Computer vision for high-throughput quantitative phenotyping: a case study of grapevine downy mildew sporulation and leaf trichomes. Phytopathology 107:1549–1555.  https://doi.org/10.1094/PHYTO-04-17-0137-R CrossRefPubMedGoogle Scholar
  13. Divilov K, Barba P, Cadle-Davidson L, Reisch BI (2018) Single and multiple phenotype QTL analyses of downy mildew resistance in interspecific grapevines. Theor Appl Genet 131:1133–1143.  https://doi.org/10.1007/s00122-018-3065-y CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eibach R, Töpfer R (2014) Progress in grapevine breeding. Acta Hortic (1046):197–209Google Scholar
  15. Eibach R, Zyprian E, Welter L, Töpfer R (2007) The use of molecular markers for pyramiding resistance genes in grapevine breeding. Vitis 46:120–124Google Scholar
  16. Fechter I, Hausmann L, Zyprian E, Daum M, Holtgräwe D, Weisshaar B, Töpfer R (2014) QTL analysis of flowering time and ripening traits suggests an impact of a genomic region on linkage group 1 in Vitis. Theor Appl Genet 127:1857–1872.  https://doi.org/10.1007/s00122-014-2310-2 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Feechan A, Anderson C, Torregrosa L, Jermakow A, Mestre P, Wiedemann-Merdinoglu S, Merdinoglu D, Walker AR, Cadle-Davidson L, Reisch B, Aubourg S, Bentahar N, Shrestha B, Bouquet A, Adam-Blondon AF, Thomas MR, Dry IB (2013) Genetic dissection of a TIR-NB-LRR locus from the wild North American grapevine species Muscadinia rotunidifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine. Plant J 76:661–674.  https://doi.org/10.1111/tpj.12327 CrossRefPubMedGoogle Scholar
  18. Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Töpfer R, Zyprian EM (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108:501–515.  https://doi.org/10.1007/s00122-003-1445-3 CrossRefPubMedGoogle Scholar
  19. Gerrath J, Posluszny U, Melville L (2015) Taming the wild grape. Springer, ChamCrossRefGoogle Scholar
  20. Goto-Yamamoto N, Sawler J, Myles S (2015) Genetic analysis of east Asian grape cultivars suggests hybridization with wild Vitis. PLoS One 10:e0140841.  https://doi.org/10.1371/journal.pone.0140841 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Grattapaglia D, Sederoff R (1994) Genetic linkage maps of Eucalyptus grandis and Eucalyptus urophylla using a pseudo-testcross: mapping strategy and RAPD markers. Genetics 137:1121–1137PubMedPubMedCentralGoogle Scholar
  22. Hedrick UP (1908) The grapes of New York. New York State Agricultural Experimental Station, New YorkGoogle Scholar
  23. Hocquigny S, Pelsy F, Dumas V, Kindt S, Heloir MC, Merdinoglu D (2004) Diversification within grapevine cultivars goes through chimeric states. Genome 47:579–589.  https://doi.org/10.1139/g04-006 CrossRefPubMedGoogle Scholar
  24. Huber F, Röckel F, Schwander F, Maul E, Eibach R, Cousins P, Töpfer R (2016) A view into American grapevine history: Vitis vinifera cv. ‘Sémillon’ is an ancestor of ‘Catawba’ and ‘Concord’. Vitis 55:53–56Google Scholar
  25. IPGRI. 1997. Descriptors for Grapevine (Vitis spp.). https://www.bioversityinternational.org/e-library/publications/detail/descriptors-for-grapevine-vitis-spp/. Accessed 7 March 2018
  26. Jaillon O, Aury JM, Noel B et al (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449:463–468CrossRefGoogle Scholar
  27. Julius Kühn-Institut (2018) Table of loci for traits in grapevine. http://www.vivc.de/docs/dataonbreeding/20180626_Table%20of%20Loci%20for%20Traits%20in%20Grapevine.pdf. Accessed 12 September 2018
  28. Kono A, Ban Y, Sato A, Mitani N (2015a) Evaluation of 17 table grape accessions for foliar resistance to downy mildew. Acta Hortic (1082):207–211.  https://doi.org/10.17660/ActaHortic.2015.1082.28
  29. Kono A, Sato A, Reisch B, Cadle-Davidson L (2015b) Effect of detergent on the quantification of grapevine downy mildew sporangia from leaf discs. HortSci 50:656–660Google Scholar
  30. Kortekamp A, Zyprian E (1999) Leaf hairs as a basic protective barrier against downy mildew of grape. J Phytopathol 147:453–459.  https://doi.org/10.1111/j.1439-0434.1999.tb03850.x CrossRefGoogle Scholar
  31. Kortekamp A, Wind R, Zyprian E (1999) The role of hairs on the wettability of grapevine (Vitis spp.) leaves. Vitis 38:101–105Google Scholar
  32. Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugenics 12:172–175CrossRefGoogle Scholar
  33. Lafon R, Bulit J (1981) Downy mildew of the vine. In: Spencer DM (ed) The downy mildews. Academic Press, London, pp 601–614Google Scholar
  34. Ma ZY, Wen J, Ickert-Bond SM, Chen LQ, Liu XQ (2016) Morphology, structure, and ontogeny of trichomes of the grape genus (Vitis, Vitaceae). Front Plant Sci 7(704).  https://doi.org/10.3389/fpls.2016.00704
  35. Merdinoglu D, Wiedemann-Merdinoglu S, Coste P, Dumas V, Haetty S, Butterlin G, Greif C (2003) Genetic analysis of downy mildew resistance derived from Muscadinia rotundifolia. Acta Hortic 603:451–456CrossRefGoogle Scholar
  36. Moreira FM, Madini A, Marino R, Zulini L, Stefanini M, Velasco R, Kozma P, Grando MS (2011) Genetic linkage maps of two interspecific grape crosses (Vitis spp.) used to localize quantitative trait loci for downy mildew resistance. Tree Genet Genomes 7:153–167.  https://doi.org/10.1007/s11295-010-0322-x CrossRefGoogle Scholar
  37. Parlevliet JE (2002) Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 124:147–156.  https://doi.org/10.1023/A:1015601731446 CrossRefGoogle Scholar
  38. Pauquet J, Bouquet A, This P, Adam-Blondon AF (2001) Establishment of a local map of AFLP markers around the powdery mildew resistance gene Run1 in grapevine and assessment of their usefulness for marker assisted selection. Theor Appl Genet 103:1201–1210.  https://doi.org/10.1007/s001220100664 CrossRefGoogle Scholar
  39. Peressotti E, Wiedemann-Merdinoglu S, Delmotte F, Bellin D, Di Gaspero G, Testoli R, Merdinoglu D, Mestre P (2010) Breakdown of resistance to grapevine downy mildew upon limited deployment of a resistant variety. BMC Plant Biol 10:147.  https://doi.org/10.1186/1471-2229-10-147 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29.  https://doi.org/10.1016/j.tplants.2008.10.006 CrossRefPubMedGoogle Scholar
  41. R Core Team. 2017. R: a language and environment for statistical computing. Vienna, Austria R Foundation for Statistical Computing. https://www.R-project.org/
  42. Reisch BI, Pratt C (1996) Grapes. In: Janick J, Moore JN (eds) Fruit breeding, volume II: vine and small fruits. Wiley & Sons, Inc., New York, pp 297–369Google Scholar
  43. Reisch BI, Owens CL, Cousins PS (2012) Grape. In Badenes M, Byrne DH (eds) Fruit breeding. Springer, Berlin, pp 225–262Google Scholar
  44. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675CrossRefGoogle Scholar
  45. Schuelke M (2000) An economic method for the fluorescent labeling of PCR fragments. Nat Biotechnol 18:233–234.  https://doi.org/10.1038/72708 CrossRefPubMedGoogle Scholar
  46. Schwander F, Eibach R, Fechter I, Hausmann L, Zyprian E, Töpfer R (2012) Rpv10: a new locus from the Asian Vitis gene pool for pyramiding downy mildew resistance loci in grapevine. Theor Appl Genet 124:163–176.  https://doi.org/10.1007/s00122-011-1695-4 CrossRefPubMedGoogle Scholar
  47. Snedecor GW, Cochran WG (1989) Statistical methods, eighth edn. Iowa State Univ. Press, owaGoogle Scholar
  48. St. Clair DA (2010) Quantitative disease resistance and quantitative resistance loci in breeding. Annu Rev Phytopathol 48:247–268CrossRefGoogle Scholar
  49. Stam P (1993) Construction of integrated genetic linkage maps by means of a new computer package: Join Map. Plant J 3:739–744.  https://doi.org/10.1111/j.1365-313X.1993.00739.x CrossRefGoogle Scholar
  50. Staudt G, Kassemeyer HH (1995) Evaluation of downy mildew resistance in various accessions of wild Vitis species. Vitis 34:225–228Google Scholar
  51. Terai Y, Yano R (1977) Varietal resistance to mildew in grapevine. Proceedings of the Kanto-Tosan Plant Protection Society 24:78–79. (in Japanese)Google Scholar
  52. van Ooijen JW (2006) JoinMap 4: software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, WageningenGoogle Scholar
  53. van Ooijen JW (2009) MapQTL® 6, software for the mapping of quantitative trait in experiment population of diploid species. Kyazma BV, WageningenGoogle Scholar
  54. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78.  https://doi.org/10.1093/jhered/93.1.77 CrossRefGoogle Scholar
  55. Welter LJ, Göktürk-Baydar N, Akkurt M, Maul E, Eibach R, Töpfer R, Zyprian EM (2007) Genetic mapping and localization of quantitative trait loci affecting fungal disease resistance and leaf morphology in grapevine (Vitis vinifera L). Mol Breed 20:359–374.  https://doi.org/10.1007/s11032-007-9097-7 CrossRefGoogle Scholar
  56. Yamada M, Sato A (2016) Advances in table grape breeding in Japan. Breed Sci 66:34–45.  https://doi.org/10.1270/jsbbs.66.34 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Yamamura K (1999) Transformation using (x + 0.5) to stabilize the variance of populations. Res Popul Ecol 41:229–234.  https://doi.org/10.1007/s101440050026 CrossRefGoogle Scholar
  58. Yang S, Fresnedo-Ramírez J, Sun Q, Manns DC, Sacks GL, Mansfield AK, Luby JJ, Londo JP, Reisch BI, Fennell AY (2016) Next generation mapping of enological traits in an F2 interspecific grapevine hybrid family. PLoS One 11:e0149560.  https://doi.org/10.1371/journal.pone.014956 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  1. 1.Division of Grape and Persimmon Research, Institute of Fruit Tree and Tea ScienceNational Agriculture and Food Research Organization (NARO)HigashihiroshimaJapan
  2. 2.Division of Lowland Crop ResearchWestern Region Agricultural Research Center, NAROFukuyamaJapan
  3. 3.Division of Fruit Production and Postharvest ScienceInstitute of Fruit Tree and Tea Science, NAROTsukubaJapan
  4. 4.Division of Citrus ResearchInstitute of Fruit Tree and Tea Science, NAROShizuokaJapan
  5. 5.Graduate School of Life SciencesTohoku UniversitySendaiJapan

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