Advertisement

Molecular Breeding

, 37:145 | Cite as

An integrative AmpSeq platform for highly multiplexed marker-assisted pyramiding of grapevine powdery mildew resistance loci

  • Jonathan Fresnedo-Ramírez
  • Shanshan Yang
  • Qi Sun
  • Linda M. Cote
  • Peter A. Schweitzer
  • Bruce I. Reisch
  • Craig A. Ledbetter
  • James J. Luby
  • Matthew D. Clark
  • Jason P. Londo
  • David M. Gadoury
  • Pál Kozma
  • Lance Cadle-Davidson
Article
  • 476 Downloads

Abstract

Resistance breeding often requires the introgression and tracking of resistance loci from wild species into domesticated backgrounds, typically with the goal of pyramiding multiple resistance genes, to provide durable disease resistance to breeding selections and ultimately cultivars. While molecular markers are commonly used to facilitate these efforts, high genetic diversity and divergent marker technologies can complicate marker-assisted breeding strategies. Here, amplicon sequencing (AmpSeq) was used to integrate SNP markers with dominant presence/absence markers derived from genotyping-by-sequencing and other genotyping technologies, for the simultaneous tracking of five loci for resistance to grapevine powdery mildew. SNP haploblocks defined the loci for REN1, REN2 and REN3, which confer quantitative resistance phenotypes that are challenging to measure via field ratings of natural infections. Presence/absence markers for RUN1 and REN4 were validated to predict qualitative resistance phenotypes and corresponded with previous presence/absence fluorescent electrophoretic assays. Thus, 37 AmpSeq-derived markers were identified for the five loci, and markers for REN1, REN2, REN4 and RUN1 were used for multiplexed screening and selection within diverse breeding germplasm. Poor transferability of SNP markers indicated imperfect marker-trait association in some families. Together, AmpSeq SNP haploblocks and presence/absence markers provide a high-throughput, cost-effective tool to integrate divergent technologies for marker-assisted selection and genetic analysis of introgressed disease resistance loci in grapevine.

Keywords

Marker-assisted breeding Erysiphe necator Uncinula necator Vitis Disease resistance Marker-assisted seedling selection 

Notes

Acknowledgements

We would like to thank Michelle Schaub, Hema Kasinathan, Anna Nowogrodzki, Paige Appleton, Mary Jean Welser and Jackie Lillis for their technical support phenotyping powdery mildew resistance. We thank Steve Luce and Mike Colizzi; Norma Ambriz and Jacob Andresen; and Peter Hemstad from Cornell University, USDA-ARS Parlier, and the University of Minnesota, respectively, for help maintaining the mapping families used in this study. The authors gratefully acknowledge the USDA-NIFA Specialty Crop Research Initiative (award no. 2011-51181-30635) for funding the VitisGen project (http://www.vitisgen.org/) and support for JFR, as well as the National Grape and Wine Initiative for support for SY.

Author contribution statements

JFR, SY, LCD and QS analyzed the data. LMC and PAS carried out sequencing. LCD, BIR, QS, CAL, DWR, JJL, MDC, JPL, PK and DMG developed germplasm and planned the study. JFR, SY and LCD wrote the manuscript. All authors read and approved the final manuscript.

Compliance with ethical standards

This research does not involve human participants or animals.

Conflict of interest

The authors declare that there are no conflicts of interest.

Supplementary material

11032_2017_739_MOESM1_ESM.docx (22 kb)
ESM 1 (DOCX 22 kb)
11032_2017_739_MOESM2_ESM.txt (4 kb)
ESM 2 (TXT 3 kb)
11032_2017_739_MOESM3_ESM.xlsx (2.7 mb)
ESM 3 (XLSX 2770 kb)

References

  1. Akkurt M, Welter L, Maul E, Topfer R, Zyprian E (2007) Development of SCAR markers linked to powdery mildew (Uncinula necator) resistance in grapevine (Vitis vinifera L. and Vitis sp.) Mol Breeding 19(2):103–111.  https://doi.org/10.1007/s11032-006-9047-9 CrossRefGoogle Scholar
  2. Barba P, Cadle-Davidson L, Harriman J, Glaubitz JC, Brooks S, Hyma K, Reisch B (2014) Grapevine powdery mildew resistance and susceptibility loci identified on a high-resolution SNP map. Theor Appl Genet 127(1):73–84.  https://doi.org/10.1007/s00122-013-2202-x CrossRefPubMedGoogle Scholar
  3. Barker CL, Donald T, Pauquet J, Ratnaparkhe MB, Bouquet A, Adam-Blondon AF, Thomas MR, Dry I (2005) Genetic and physical mapping of the grapevine powdery mildew resistance gene, Run1, using a bacterial artificial chromosome library. Theor Appl Genet 111(2):370–377.  https://doi.org/10.1007/s00122-005-2030-8 CrossRefPubMedGoogle Scholar
  4. Blanc S, Wiedemann-Merdinoglu S, Dumas V, Mestre P, Merdinoglu D (2012) A reference genetic map of Muscadinia rotundifolia and identification of Ren5, a new major locus for resistance to grapevine powdery mildew. Theor Appl Genet 125(8):1663–1675.  https://doi.org/10.1007/s00122-012-1942-3 CrossRefPubMedGoogle Scholar
  5. Bolstad BM, Irizarry RA, Astrand M, Speed TP (2003) A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics 19(2):185–193.  https://doi.org/10.1093/bioinformatics/19.2.185 CrossRefPubMedGoogle Scholar
  6. Browning BL, Browning SR (2013) Improving the accuracy and efficiency of identity-by-descent detection in population data. Genetics 194(2):459–471.  https://doi.org/10.1534/genetics.113.150029 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Browning SR, Browning BL (2007) Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. Am J Hum Genet 81(5):1084–1097.  https://doi.org/10.1086/521987 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Cadle-Davidson L, Chicoine DR, Consolie NH (2011) Variation within and among Vitis spp. for foliar resistance to the powdery mildew pathogen Erysiphe necator. Plant Dis 95(2):202–211.  https://doi.org/10.1094/Pdis-02-10-0092 CrossRefGoogle Scholar
  9. Cadle-Davidson L, Gadoury D, Fresnedo-Ramírez J, Yang S, Barba P, Sun Q, Demmings EM, Seem R, Schaub M, Nowogrodzki A, Kasinathan H, Ledbetter C, Reisch BI (2016) Lessons from a phenotyping center revealed by the genome-guided mapping of powdery mildew resistance loci. Phytopathology 106(10):1159–1169.  https://doi.org/10.1094/Phyto-02-16-0080-Fi CrossRefPubMedGoogle Scholar
  10. Coleman C, Copetti D, Cipriani G, Hoffman S, Kozman P, Kovacs L, Morgante M, Testolin R, Di Gaspero G (2009) The powdery mildew resistance gene REN1 co-segregates with an NBS-LRR gene cluster in two central Asian grapevines. BMC Genet 10.  https://doi.org/10.1186/1471-2156-10-89
  11. Dalbó MA (1998) Genetic mapping, QTL analysis, and marker-assisted selection for disease resistance loci in grapes. Cornell University, Ithaca, NYGoogle Scholar
  12. Dalbó MA, Ye GN, Weeden NF, Wilcox WF, Reisch BI (2001) Marker-assisted selection for powdery mildew resistance in grapes. J Am Soc Hortic Sci 126(1):83–89Google Scholar
  13. Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, Grp GPA (2011) The variant call format and VCFtools. Bioinformatics 27(15):2156–2158.  https://doi.org/10.1093/bioinformatics/btr330 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Di Genova A, Almeida AM, Munoz-Espinoza C, Vizoso P, Travisany D, Moraga C, Pinto M, Hinrichsen P, Orellana A, Maass A (2014) Whole genome comparison between table and wine grapes reveals a comprehensive catalog of structural variants. BMC Plant Biol 14.  https://doi.org/10.1186/1471-2229-14-7
  15. Eibach R, Zyprian E, Welter L, Töpfer R (2007) The use of molecular markers for pyramiding resistance genes in grapevine breeding. Vitis 46 (3)Google Scholar
  16. Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6 (5). doi: https://doi.org/10.1371/journal.pone.0019379
  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 rotundifolia identifies paralogous genes conferring resistance to major fungal and oomycete pathogens in cultivated grapevine. Plant J 76(4):661–674.  https://doi.org/10.1111/tpj.12327 CrossRefPubMedGoogle Scholar
  18. Fischer BM, Salakhutdinov I, Akkurt M, Eibach R, Edwards KJ, Topfer R, Zyprian EM (2004) Quantitative trait locus analysis of fungal disease resistance factors on a molecular map of grapevine. Theor Appl Genet 108(3):501–515.  https://doi.org/10.1007/s00122-003-1445-3 CrossRefPubMedGoogle Scholar
  19. Gadoury DM, Cadle-Davidson L, Wilcox WF, Dry IB, Seem RC, Milgroom MG (2012) Grapevine powdery mildew (Erysiphe necator): a fascinating system for the study of the biology, ecology and epidemiology of an obligate biotroph. Mol Plant Pathol 13(1):1–16.  https://doi.org/10.1111/j.1364-3703.2011.00728.x CrossRefPubMedGoogle Scholar
  20. Gao F, Dai R, Pike SM, Qiu WP, Gassmann W (2014) Functions of EDS1-like and PAD4 genes in grapevine defenses against powdery mildew. Plant Mol Biol 86(4–5):381–393.  https://doi.org/10.1007/s11103-014-0235-4 CrossRefPubMedGoogle Scholar
  21. Glaubitz JC, Casstevens TM, Lu F, Harriman J, Elshire RJ, Sun Q, Buckler ES (2014) TASSEL-GBS: a high capacity genotyping by sequencing analysis pipeline. PLoS One 9 (2). doi: https://doi.org/10.1371/journal.pone.0090346
  22. Hoffmann S, Di Gaspero G, Kovacs L, Howard S, Kiss E, Galbacs Z, Testolin R, Kozma P (2008) Resistance to Erysiphe necator in the grapevine 'Kishmish vatkana' is controlled by a single locus through restriction of hyphal growth. Theor Appl Genet 116(3):427–438.  https://doi.org/10.1007/s00122-007-0680-4 CrossRefPubMedGoogle Scholar
  23. Hyma KE, Barba P, Wang MH, Londo JP, Acharya CB, Mitchell SE, Sun Q, Reisch B, Cadle-Davidson L (2015) Heterozygous mapping strategy (HetMappS) for high resolution genotyping-by-sequencing markers: a case study in grapevine. PLoS One 10(8).  https://doi.org/10.1371/journal.pone.0134880
  24. Jaillon O, Aury JM, Noel B, Policriti A, Clepet C, Casagrande A, Choisne N, Aubourg S, Vitulo N, Jubin C, Vezzi A, Legeai F, Hugueney P, Dasilva C, Horner D, Mica E, Jublot D, Poulain J, Bruyere C, Billault A, Segurens B, Gouyvenoux M, Ugarte E, Cattonaro F, Anthouard V, Vico V, Del Fabbro C, Alaux M, Di Gaspero G, Dumas V, Felice N, Paillard S, Juman I, Moroldo M, Scalabrin S, Canaguier A, Le Clainche I, Malacrida G, Durand E, Pesole G, Laucou V, Chatelet P, Merdinoglu D, Delledonne M, Pezzotti M, Lecharny A, Scarpelli C, Artiguenave F, Pe ME, Valle G, Morgante M, Caboche M, Adam-Blondon AF, Weissenbach J, Quetier F, Wincker P, Public F-I (2007) The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 449(7161):463–U465.  https://doi.org/10.1038/nature06148 CrossRefPubMedGoogle Scholar
  25. Luby JJ, Shaw DV (2001) Does marker-assisted selection make dollars and sense in a fruit breeding program? Hortscience 36(5):872–879Google Scholar
  26. Mahanil SB, Lagerholm S, Garris A, Owens C, Ramming D, Cadle-Davidson L (2014) Development of molecular markers for powdery mildew resistance in grapevines. Acta Hortic 1046:91–99CrossRefGoogle Scholar
  27. Mahanil SB, Ramming D, Cadle-Davidson M, Owens C, Garris A, Myles S, Cadle-Davidson L (2012) Development of marker sets useful in the early selection of Ren4 powdery mildew resistance and seedlessness for table and raisin grape breeding. Theor Appl Genet 124(1):23–33.  https://doi.org/10.1007/s00122-011-1684-7 CrossRefPubMedGoogle Scholar
  28. Marcais G, Kingsford C (2011) A fast, lock-free approach for efficient parallel counting of occurrences of k-mers. Bioinformatics 27(6):764–770.  https://doi.org/10.1093/bioinformatics/btr011 CrossRefPubMedPubMedCentralGoogle Scholar
  29. Michelmore RW, Paran I, Kesseli RV (1991) Identification of markers linked to disease-resistance genes by bulked segregant analysis - a rapid method to detect markers in specific genomic regions by using segregating populations. P Natl Acad Sci USA 88(21):9828–9832.  https://doi.org/10.1073/pnas.88.21.9828 CrossRefGoogle Scholar
  30. Migliaro D, Morreale G, Gardiman M, Landolfo S, Crespan M (2012) Direct multiplex PCR for grapevine genotyping and varietal identification. Plant Genet Resour 11(2):182–185.  https://doi.org/10.1017/S1479262112000433 CrossRefGoogle Scholar
  31. Pap D, Riaz S, Dry IB, Jermakow A, Tenscher AC, Cantu D, Olah R, Walker MA (2016) Identification of two novel powdery mildew resistance loci, Ren6 and Ren7, from the wild Chinese grape species Vitis piasezkii. BMC Plant Biol 16. doi: https://doi.org/10.1186/s12870-016-0855-8
  32. Qiu WP, Feechan A, Dry I (2015) Current understanding of grapevine defense mechanisms against the biotrophic fungus (Erysiphe necator), the causal agent of powdery mildew disease. Hortic Res-England 2.  https://doi.org/10.1038/hortres.2015.20
  33. Ramming DW, Gabler F, Smilanick J, Cadle-Davidson M, Barba P, Mahanil S, Cadle-Davidson L (2011) A single dominant locus, Ren4, confers rapid non-race-specific resistance to grapevine powdery mildew. Phytopathology 101(4):502–508.  https://doi.org/10.1094/Phyto-09-10-0237 CrossRefPubMedGoogle Scholar
  34. Reisch BI, Mahanil S, Consolie N, Luce RS, Wallace PG, Cadle-Davidson L (2014) Examination of marker-assisted selection for powdery and downy mildew resistance. Acta Hortic 1046:151–155CrossRefGoogle Scholar
  35. Riaz S, Boursiquot JM, Dangl GS, Lacombe T, Laucou V, Tenscher AC, Walker MA (2013) Identification of mildew resistance in wild and cultivated Central Asian grape germplasm. BMC Plant Biol 13. doi: https://doi.org/10.1186/1471-2229-13-149
  36. Riaz S, Dangl GS, Edwards KJ, Meredith CP (2004) A microsatellite marker based framework linkage map of Vitis vinifera L. Theor Appl Genet 108(5):864–872.  https://doi.org/10.1007/s00122-003-1488-5 CrossRefPubMedGoogle Scholar
  37. Riaz S, Tenscher AC, Ramming DW, Walker MA (2011) Using a limited mapping strategy to identify major QTLs for resistance to grapevine powdery mildew (Erysiphe necator) and their use in marker-assisted breeding. Theor Appl Genet 122(6):1059–1073.  https://doi.org/10.1007/s00122-010-1511-6 CrossRefPubMedGoogle Scholar
  38. Ru S, Main D, Evans K, Peace C (2015) Current applications, challenges, and perspectives of marker-assisted seedling selection in Rosaceae tree fruit breeding. Tree Genet Genomes 11(1).  https://doi.org/10.1007/s11295-015-0834-5
  39. SAS Institute (2015) JMP Pro 12.2. Cary, NCGoogle Scholar
  40. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li WZ, Lopez R, McWilliam H, Remmert M, Soding J, Thompson JD, Higgins DG (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal omega. Mol Syst Biol 7.  https://doi.org/10.1038/msb.2011.75
  41. Teh SL, Fresnedo-Ramirez J, Clark MD, Gadoury DM, Sun Q, Cadle-Davidson L, Luby JJ (2017) Genetic dissection of powdery mildew resistance in interspecific half-sib grapevine families using SNP-based maps. Mol Breeding 37(1).  https://doi.org/10.1007/s11032-016-0586-4
  42. Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG (2012) Primer3-new capabilities and interfaces. Nucleic Acids Res 40(15).  https://doi.org/10.1093/nar/gks596
  43. van Heerden CJ, Burger P, Vermeulen A, Prins R (2014) Detection of downy and powdery mildew resistance QTL in a 'Regent' × 'RedGlobe' population. Euphytica 200(2):281–295.  https://doi.org/10.1007/s10681-014-1167-4 CrossRefGoogle Scholar
  44. Van Ooijen JW (2006) JoinMap(R) 4. Software for the calculation of genetic linkage maps in experimental populations. 4.1 edn., Wageningen, The NetherlandsGoogle Scholar
  45. Van Ooijen JW (2011) Multipoint maximum likelihood mapping in a full-sib family of an outbreeding species. Genet Res 93(5):343–349.  https://doi.org/10.1017/S0016672311000279 CrossRefGoogle Scholar
  46. Velasco R, Zharkikh A, Troggio M, Cartwright DA, Cestaro A, Pruss D, Pindo M, FitzGerald LM, Vezzulli S, Reid J, Malacarne G, Iliev D, Coppola G, Wardell B, Micheletti D, Macalma T, Facci M, Mitchell JT, Perazzolli M, Eldredge G, Gatto P, Oyzerski R, Moretto M, Gutin N, Stefanini M, Chen Y, Segala C, Davenport C, Dematte L, Mraz A, Battilana J, Stormo K, Costa F, Tao QZ, Si-Ammour A, Harkins T, Lackey A, Perbost C, Taillon B, Stella A, Solovyev V, Fawcett JA, Sterck L, Vandepoele K, Grando SM, Toppo S, Moser C, Lanchbury J, Bogden R, Skolnick M, Sgaramella V, Bhatnagar SK, Fontana P, Gutin A, Van de Peer Y, Salamini F, Viola R (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2 (12). doi: https://doi.org/10.1371/journal.pone.0001326
  47. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population-structure. Evolution 38(6):1358–1370.  https://doi.org/10.2307/2408641 PubMedGoogle Scholar
  48. Welter LJ, Gokturk-Baydar N, Akkurt M, Maul E, Eibach R, Topfer 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 Breeding 20(4):359–374.  https://doi.org/10.1007/s11032-007-9097-7 CrossRefGoogle Scholar
  49. Xu C, Ranjbar MRN, Wu Z, DiCarlo J, Wang YX (2017) Detecting very low allele fraction variants using targeted DNA sequencing and a novel molecular barcode-aware variant caller BMC Genomics 18. doi: https://doi.org/10.1186/s12864-016-3425-4
  50. Yang S, Fresnedo-Ramírez J, Sun Q, Manns DC, Sacks GL, Mansfield AK, Luby JJ, Londo JP, Reisch BI, Cadle-Davidson LE, Fennell AY (2016a) Next generation mapping of enological traits in an F2 interspecific grapevine hybrid family. PLoS One 11 (3). doi: https://doi.org/10.1371/journal.pone.0149560
  51. Yang S, Fresnedo-Ramírez J, Wang MH, Cote L, Schweitzer P, Barba P, Takacs EM, Clark M, Luby J, Manns DC, Sacks G, Mansfield AK, Londo J, Fennell A, Gadoury D, Reisch B, Cadle-Davidson L, Sun Q (2016b) A next-generation marker genotyping platform (AmpSeq) in heterozygous crops: a case study for marker-assisted selection in grapevine. Hortic res-England 3. doi: https://doi.org/10.1038/hortres.2016.2
  52. Zarouri B, Vargas AM, Gaforio L, Aller M, de Andrés MT, Cabezas JA (2015) Whole-genome genotyping of grape using a panel of microsatellite multiplex PCRs. Tree Genet Genomes 11(2):17.  https://doi.org/10.1007/s11295-015-0843-4 CrossRefGoogle Scholar
  53. Zendler D, Schneider P, Töpfer R, Zyprian E (2017) Fine mapping of Ren3 reveals two loci mediating hypersensitive response against Erysiphe necator in grapevine. Euphytica 213(3):68.  https://doi.org/10.1007/s10681-017-1857-9 CrossRefGoogle Scholar
  54. Zhao F, McParland S, Kearney F, Du L, Berry DP (2015) Detection of selection signatures in dairy and beef cattle using high-density genomic information. Genet Sel Evol 47(1):49.  https://doi.org/10.1186/s12711-015-0127-3 CrossRefPubMedPubMedCentralGoogle Scholar
  55. Zyprian E, Ochssner I, Schwander F, Simon S, Hausmann L, Bonow-Rex M, Moreno-Sanz P, Grando MS, Wiedemann-Merdinoglu S, Merdinoglu D, Eibach R, Topfer R (2016) Quantitative trait loci affecting pathogen resistance and ripening of grapevines. Mol Gen Genomics 291(4):1573–1594.  https://doi.org/10.1007/s00438-016-1200-5 CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and its text is not subject to copyright protection in the United States; however, its text may be subject to foreign copyright protection 2017

Authors and Affiliations

  • Jonathan Fresnedo-Ramírez
    • 1
  • Shanshan Yang
    • 2
  • Qi Sun
    • 3
  • Linda M. Cote
    • 4
  • Peter A. Schweitzer
    • 4
  • Bruce I. Reisch
    • 5
  • Craig A. Ledbetter
    • 6
  • James J. Luby
    • 7
  • Matthew D. Clark
    • 7
  • Jason P. Londo
    • 8
  • David M. Gadoury
    • 9
  • Pál Kozma
    • 10
  • Lance Cadle-Davidson
    • 8
  1. 1.Department of Horticulture and Crop ScienceThe Ohio State University/OARDCWoosterUSA
  2. 2.Virginia G. Piper Center for Personalized Diagnostics, Biodesign InstituteArizona State UniversityTempeUSA
  3. 3.BRC Bioinformatics Facility, Institute of BiotechnologyCornell UniversityIthacaUSA
  4. 4.BRC Genomics Facility, Institute of BiotechnologyCornell UniversityIthacaUSA
  5. 5.Horticulture Section, School of Integrative Plant Science, New York State Agricultural Experiment StationCornell UniversityGenevaUSA
  6. 6.USDA-ARS San Joaquin Valley Agricultural Sciences CenterParlierUSA
  7. 7.Department of Horticultural ScienceUniversity of MinnesotaSt. PaulUSA
  8. 8.USDA-ARS Grape Genetics Research UnitGenevaUSA
  9. 9.Plant Pathology and Plant-Microbe Biology Section, School of Integrative Plant ScienceCornell UniversityGenevaUSA
  10. 10.Research Institute for Viticulture and Enology, Department of BreedingUniversity of PécsPécsHungary

Personalised recommendations