Tree Genetics & Genomes

, 14:47 | Cite as

Genetic analyses of resistance to the peach root-knot nematode (Meloidogyne floridensis) using microsatellite markers

  • Mary Ann D. Maquilan
  • Mercy A. Olmstead
  • James W. Olmstead
  • Donald W. Dickson
  • José X. Chaparro
Original Article
Part of the following topical collections:
  1. Disease Resistance


Most commercially important rootstocks for peach [Prunus persica (L.) Batsch] had been selected for resistance to one or more of the root-knot nematode (RKN) species: Meloidogyne incognita, M. arenaria, and M. javanica. The peach root-knot nematode, M. floridensis (MF), is a relatively newly discovered threat to peach and is not controlled by resistance genes in “Nemared,” “Nemaguard,” and “Okinawa.” The “Flordaguard” peach seedling rootstock, conventionally bred to provide resistance to MF, has solely been used for low-chill peach production in Florida for over 20 years and has already shown signs of resistance breakdown. A source of high resistance to the pathogenic MF isolate (“MFGnv14”) was identified from wild peach Prunus kansuensis Rehder (Kansu peach), thereby suggesting the potential for broadening spectrum and increasing durability of resistance in peach rootstocks through interspecific hybridization with P. kansuensis. Using 12 F2 and BC1F1 populations derived from crosses between Okinawa or Flordaguard peach and P. kansuensis populations, we examined the genetic control for MF resistance by identifying associated microsatellite markers and determining genomic location of the resistance locus. One microsatellite marker (UDP98-025) showed strong and consistent association with resistance based on root-galling index. The resistance locus was mapped on the subtelomeric region of linkage group 2, co-localizing with other previously reported RKN resistance genes in Prunus. Segregation of gall-index-based resistance observed in F2 and BC1F1 populations is compatible with the involvement of a multiallelic locus wherein a dominant (Mf1) or recessive (mf3) resistance allele is inherited from P. kansuensis, and susceptibility alleles (mf2) from peach.


Nematode resistance Prunus kansuensis Microsatellite Peach rootstocks Meloidogyne floridensis Genetic linkage 


Data archiving statement

(Peach × P. kansuensis linkage maps to be submitted to the Genome Database for Rosaceae. Accession numbers will be provided once available.)

Funding information

This study was funded in part by the Florida Department of Agriculture and Consumer Services under the Specialty Crop Block Grant Nos. 18004 and 20727.

Supplementary material

11295_2018_1260_MOESM1_ESM.docx (29 kb)
ESM 1. Figure S2 Microsatellite SSR markers screened for polymorphism and selected for mapping the Mf resistance locus on each of the eight linkage groups (LG1-LG8) of the ‘Texas’ almond x ‘Earlygold’ (TxE) peach reference map. Marker names and positions (Kosambi map distances, cM) are indicated on the right and left side of bars, respectively. Markers selected for linkage analyses are denoted by bold, uppercase letters. Three markers (colored red and green) in LG 4 and LG5 were mapped to other interspecific Prunus linkage maps at distances beyond the length of the TxE map. Non-selected markers denoted by lowercase letters are characterized by one of the following: 1) non-polymorphic (enclosed in parentheses), 2) polymorphic but are spaced at very close intervals (bold letters), and 3) polymorphic but are difficult to score (italicized letters) (DOCX 29 kb)
11295_2018_1260_MOESM2_ESM.xlsx (36 kb)
ESM 2. File S4 Microsatellite allele configurations and genotype cross combinations for F2 and BC1F1 peach x P. kansuensis interspecific progenies inferred from segregation patterns of marker band and electropherogram data (XLSX 35 kb)
11295_2018_1260_MOESM3_ESM.docx (20 kb)
ESM 3. Figure S5 Combined SSR linkage map based on two F2 mapping populations derived from ‘Flordaguard’ (FG) x Prunus kansuensis (PK). Microsatellite markers were assigned into eight linkage groups (LG1-LG8) and ordered in accordance with the ‘Texas’ almond x ‘Earlygold’ peach linkage map. Numbers to the left side of the bars represent the estimated genetic distances (centiMorgan) of the microsatellite markers (DOCX 20 kb)
11295_2018_1260_MOESM4_ESM.docx (20 kb)
ESM 4. Combined SSR linkage map based on five F2 mapping populations derived from ‘Okinawa’ (OK) x Prunus kansuensis (PK). Microsatellite markers were assigned into eight linkage groups (LG1-LG8) and ordered in accordance with the ‘Texas’ almond x ‘Earlygold’ peach linkage map. Numbers to the left side of the bars represent the estimated genetic distances (centiMorgan) of the microsatellite markers (DOCX 20 kb)
11295_2018_1260_MOESM5_ESM.docx (20 kb)
ESM 5. Figure S7 Combined SSR linkage map based on three BC1 mapping populations derived from peach (‘Flordaguard’ [FG] and ‘UFSharp’ [SH]) x F1 (‘Okinawa’ [OK] x Prunus kansuensis [PK]). Microsatellite markers were assigned into eight linkage groups (LG1-LG8) and ordered in accordance with the ‘Texas’ almond x ‘Earlygold’ peach linkage map. Numbers to the left side of the bars represent the estimated genetic distances (centiMorgan) of the microsatellite markers (DOCX 20 kb)
11295_2018_1260_MOESM6_ESM.docx (21 kb)
ESM 6. Figure S8 Combined SSR linkage map based on two BC1 mapping populations derived from peach (‘UFSharp’ [SH]) x F1 (‘Flordaguard’ [FG] x Prunus kansuensis [PK]). Microsatellite markers were assigned into eight linkage groups (LG1-LG8) and ordered in accordance with the ‘Texas’ almond x ‘Earlygold’ peach linkage map. Numbers to the left side of the bars represent the estimated genetic distances (centiMorgan) of the microsatellite markers (DOCX 20 kb)
11295_2018_1260_MOESM7_ESM.docx (22 kb)
ESM 7. Table S1 Origins of the microsatellite markers tested for polymorphism and number of markers included in the linkage maps (DOCX 21 kb)
11295_2018_1260_MOESM8_ESM.docx (22 kb)
ESM 8. Table S3 Characteristics of the polymorphic microsatellite markers used to map the Mf resistance locus in peach x Prunus kansuensis interspecific progenies (DOCX 22 kb)
11295_2018_1260_MOESM9_ESM.docx (14 kb)
ESM 9. Table S9 Combined linkage map based on five F2 mapping populations derived from crosses between ‘Okinawa’ x Prunus kansuensis (OK x PK) compared with Prunus ‘Texas’ x ‘Earlygold’ (TxE) reference map (DOCX 14 kb)
11295_2018_1260_MOESM10_ESM.docx (15 kb)
Table S10 Combined linkage map based on two F2 mapping populations derived from crosses between ‘Flordaguard’ x Prunus kansuensis (FG x PK) compared with Prunus ‘Texas’ x ‘Earlygold’ (TxE) reference map (DOCX 14 kb)
11295_2018_1260_MOESM11_ESM.docx (14 kb)
Table S11 Combined linkage map based on three BC1 mapping populations of peach (‘Flordaguard’ or ‘UFSharp’) x F1 (‘Okinawa’ x Prunus kansuensis) (FG/SH x [OK x PK]) compared with Prunus ‘Texas’ x ‘Earlygold’ (TxE) reference map (DOCX 14 kb)
11295_2018_1260_MOESM12_ESM.docx (15 kb)
Table S12 Combined linkage map based on two BC1 mapping populations of peach (‘UFSharp’) x F1 (‘Flordaguard’ x Prunus kansuensis) (SH x [FG x PK]) compared with Prunus ‘Texas’ x ‘Earlygold’ (TxE). (DOCX 14 kb)


  1. Aranzana MJ, Carbo J, Arus P (2003a) Microsatellite variability in peach [Prunus persica (L.) Batsch]: cultivar identification, marker mutation, pedigree inferences and population structure. Theor Appl Genet 106:1341–1352. CrossRefPubMedGoogle Scholar
  2. Aranzana MJ, Garcia-Mas J, Carbo J, Arus P (2002) Development and variability analysis of microsatellite markers in peach. Plant Breed 121:87–92. CrossRefGoogle Scholar
  3. Aranzana MJ, Pineda A, Cosson P, Dirlewanger E, Ascasibar J, Cipriani G, Ryder CD, Testolin R, Abbott A, King GJ, Iezzoni AF, Arus P (2003b) A set of simple-sequence repeat (SSR) markers covering the Prunus genome. Theor Appl Genet 106:819–825. CrossRefPubMedGoogle Scholar
  4. Bus VGM, Esmenjaud D, Buck E, Laurens F (2009) Application of genetic markers in rosaceous crops. In: Folta KM, Gardiner SE (eds) Genetics and genomics of rosaceae. Springer, New York, pp 563–599CrossRefGoogle Scholar
  5. Cao K, Wang LR, Zhao P, Zhu GR, Fang WC, Chen CW, Wang XW (2014) Identification of a candidate gene for resistance to root-knot nematode in a wild peach and screening of its polymorphisms. Plant Breed 133:530–535. CrossRefGoogle Scholar
  6. Cao K, Wang LR, Zhu GR, Fang WC, Chen CW, Zhao P (2011) Construction of a linkage map and identification of resistance gene analog markers for root-knot nematodes in wild peach, Prunus kansuensis. J Am Soc Hortic Sci 136:190–197Google Scholar
  7. Castagnone-Sereno P (2006) Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96:282–289. CrossRefPubMedGoogle Scholar
  8. Chaparro JX, Sherman WB (2006) ‘UFSharp’ peach. J Amer Pomolog Soc 60:95–96Google Scholar
  9. Chaparro JX, Werner DJ, Omalley D, Sederoff RR (1994) Targeted mapping and linkage analysis of morphological isozyme, and RAPD markers in peach. Theor Appl Genet 87:805–815. CrossRefPubMedGoogle Scholar
  10. Charcosset A, Moreau L (2004) Use of molecular markers for the development of new cultivars and the evaluation of genetic diversity. Euphytica 137:81–94. CrossRefGoogle Scholar
  11. Chavez DJ, Chaparro JX (2011) Identification of markers linked to seedlessness in Citrus kinokuni hort. ex Tanaka and its progeny using bulked segregant analysis. HortScience 46:693–697Google Scholar
  12. Chu Y, Wu CL, Holbrook CC, Tillman BL, Person G, Ozias-Akins P (2011) Marker-assisted selection to pyramid nematode resistance and the high oleic trait in peanut. Plant Genome 4:110–117. CrossRefGoogle Scholar
  13. Clarke LA, Rebelo CS, Gonçalves J, Boavida MG, Jordan P (2001) PCR amplification introduces errors into mononucleotide and dinucleotide repeat sequences. J Clin Pathol: Mol Pathol 54:351–353. CrossRefGoogle Scholar
  14. Claverie M, Bosselut N, Lecouls AC, Voisin R, Lafargue B, Poizat C, Kleinhentz M, Laigret F, Dirlewanger E, Esmenjaud D (2004) Location of independent root-knot nematode resistance genes in plum and peach. Theor Appl Genet 108:765–773. CrossRefPubMedGoogle Scholar
  15. Claverie M, Dirlewanger E, Bosselut N, Van Ghelder C, Voisin R, Kleinhentz M, Lafargue B, Abad P, Rosso MN, Chalhoub B, Esmenjaud D (2011) The Ma gene for complete-spectrum resistance to Meloidogyne species in Prunus is a TNL with a huge repeated C-terminal post-LRR region. Plant Physiol 156:779–792. CrossRefPubMedPubMedCentralGoogle Scholar
  16. Concibido V, Diers B, Arelli R (2004) A decade of QTL mapping for cyst nematode resistance in soybean. Crop Sci 44:1121–1131CrossRefGoogle Scholar
  17. DeWoody JA, Nason JD, Hipkins VD (2006) Mitigating scoring errors in microsatellite data from wild populations. Mol Ecol Notes 6:951–957. CrossRefGoogle Scholar
  18. Dirlewanger E, Cosson P, Boudehri K, Renaud C, Capdeville G, Tauzin Y, Laigret F, Moing A (2007) Development of a second-generation genetic linkage map for peach [Prunus persica (L.) Batsch] and characterization of morphological traits affecting flower and fruit. Tree Genet Genomes 3:1–13. CrossRefGoogle Scholar
  19. Dirlewanger E, Cosson P, Howad W, Capdeville G, Bosselut N, Claverie M, Voisin R, Poizat C, Lafargue B, Baron O, Laigret F, Kleinhentz M, Arus P, Esmenjaud D (2004a) Microsatellite genetic linkage maps of myrobalan plum and an almond-peach hybrid - location of root-knot nematode resistance genes. Theor Appl Genet 109:827–838. CrossRefPubMedGoogle Scholar
  20. Dirlewanger E, Graziano E, Joobeur T, Garriga-Calder F, Cosson P, Howad W, Arus P (2004b) Comparative mapping and marker-assisted selection in Rosaceae fruit crops. PNAS 101:9891–9896. CrossRefPubMedGoogle Scholar
  21. Duval H, Hoerter M, Polidori J, Confolent C, Masse M, Moretti A, Van Ghelder C, Esmenjaud D (2014) High-resolution mapping of the RMia gene for resistance to root-knot nematodes in peach. Tree Genet Genomes 10:297–306. CrossRefGoogle Scholar
  22. Esmenjaud D, Minot JC, Voisin R, Bonnet A, Salesses G (1996) Inheritance of resistance to the root-knot nematode Meloidogyne arenaria in Myrobalan plum. Theor Appl Genet 92:873–879. CrossRefPubMedGoogle Scholar
  23. Esmenjaud D, Minot JC, Voisin R, Pinochet J, Salesses G (1994) Inter- and intraspecific resistance variability in Myrobalan plum, peach, and peach-almond rootstock using 22 root-knot nematode populations. J Am Soc Hortic Sci 119:94–100Google Scholar
  24. Fan S, Bielenberg DG, Zhebentyayeva TN, Reighard GL, Okie WR, Holland D, Abbott AG (2010) Mapping quantitative trait loci associated with chilling requirement, heat requirement and bloom date in peach (Prunus persica). New Phytol 185:917–930. CrossRefPubMedGoogle Scholar
  25. Flint-Garcia SA, Thornsberry JM, Buckler ES (2003) Structure of linkage disequilibrium in plants. Annu Rev Plant Biol 54:357–374. CrossRefPubMedGoogle Scholar
  26. Handoo ZA, Nyczepir AP, Esmenjaud D, van der Beek JG, Castagnone-Sereno P, Carta LK, Skantar AM, Higgins JA (2004) Morphological, molecular, and differential-host characterization of Meloidogyne floridensis n. sp. (Nematoda : Meloidogynidae), a root-knot nematode parasitizing peach in Florida. J Nematol 36:20–35PubMedPubMedCentralGoogle Scholar
  27. Hansen CJ, Lownsbery BF, Hesse CO (1956) Nematode resistance in peaches. Calif Agric 10:5–11Google Scholar
  28. Hospital F (2005) Selection in backcross programmes. Philos Trans R Soc B 360:1503–1511. CrossRefGoogle Scholar
  29. Jenkins JN, McCarty JC, Wubben MJ, Hayes R, Gutierrez OA, Callahan F, Deng D (2012) SSR markers for marker assisted selection of root-knot nematode (Meloidogyne incognita) resistant plants in cotton (Gossypium hirsutum L). Euphytica 183:49–54. CrossRefGoogle Scholar
  30. Joobeur T, Viruel MA, de Vicente MC, Jauregui B, Ballester J, Dettori MT, Verde I, Truco MJ, Messeguer R, Batlle I, Quarta R, Dirlewanger E, Arus P (1998) Construction of a saturated linkage map for Prunus using an almond x peach F2 progeny. Theor Appl Genet 97:1034–1041.
  31. Khallouk S, Voisin R, Portier U, Polidori J, Van Ghelder C, Esmenjaud D (2013) Multiyear evaluation of the durability of the resistance conferred by Ma and RMia genes to Meloidogyne incognita in Prunus under controlled conditions. Phytopathology 103:833–840. CrossRefPubMedGoogle Scholar
  32. Kochba J, Spiegel-Roy P (1975) Inheritance of resistance to the root-knot nematode (Meloidogyne javanica Chitwood) in bitter almond progenies. Euphytica 24:453–457. CrossRefGoogle Scholar
  33. Lalli DA, Decroocq V, Blenda AV, Schurdi-Levraud V, Garay L, Le Gall O, Damsteegt V, Reighard GL, Abbott AG (2005) Identification and mapping of resistance gene analogs (RGAs) in Prunus: a resistance map for Prunus. Theor Appl Genet 111:1504–1513.
  34. Lu ZX, Reighard GL, Nyczepir AP, Beckman TG, Ramming DW (2000) Inheritance of resistance to root-knot nematodes (Meloidogyne sp.) in Prunus rootstocks. HortScience 35:1344–1346Google Scholar
  35. Lu ZX, Sossey-Alaoui K, Reighard GL, Baird WV, Abbott AG (1999) Development and characterization of a codominant marker linked to root-knot nematode resistance, and its application to peach rootstock breeding. Theor Appl Genet 99:115–122. CrossRefGoogle Scholar
  36. Mackay TFC, Stone EA, Ayroles JF (2009) The genetics of quantitative traits: challenges and prospects. Nat Rev Genet 10:565–577. CrossRefPubMedGoogle Scholar
  37. Maquilan MAD (2017) Rootstock breeding for resistancce to the peach root-knot nematode (Meloidogyne floridensis). Dissertation, University of FloridaGoogle Scholar
  38. Miah G, Rafii MY, Ismail MR, Puteh AB, Rahim HA, Islam KN, Latif MA (2013) A review of microsatellite markers and their applications in rice breeding programs to improve blast disease resistance. Int J Mol Sci 14:22499–22528. CrossRefPubMedPubMedCentralGoogle Scholar
  39. Mnejja M, Garcia-Mas J, Audergon JM, Arus P (2010) Prunus microsatellite marker transferability across rosaceous crops. Tree Genet Genomes 6:689–700. CrossRefGoogle Scholar
  40. Okie WR, Beckman TG, Nyczepir AP, Reighard GL, Newall WC, Zehr EI (1994) BY520-9, a peach rootstock for the southeastern United States that increases scion longevity. HortScience 29:705–706Google Scholar
  41. Olmstead M, Chaparro J, Ferguson J (2015) Rootstocks for Florida stone fruit. HS1110. Gainesville: University of Florida Institute of Food and Agricultural Sciences. Accessed 15 January 2016
  42. Ramming DW, Tanner O (1983) ‘Nemared’ peach rootstock. HortScience 18:376Google Scholar
  43. Reighard G, Loreti F (2008) Rootstock development. p. 193–220. In: Layne, D. and Bassi, D. (eds) The peach: botany, production and uses. CABI publishing, WallingfordGoogle Scholar
  44. Rubio-Cabetas MJ, Lecouls AC, Salesses G, Bonnet A, Minot JC, Voisin R, Esmenjaud D (1998) Evidence of a new gene for high resistance to Meloidogyne spp. in Myrobalan plum, Prunus cerasifera. Plant Breed 117:567–571. CrossRefGoogle Scholar
  45. Sharpe R (1967) Root-knot nematode populations on peaches in Florida. Proc Fla State Hort Soc 80:342–344Google Scholar
  46. Sharpe RH (1957) Okinawa peach shows promising resistance to root-knot nematodes. Fla Agric Exp 657:320–322Google Scholar
  47. Sherman WB, Lyrene PM, Sharpe RH (1991) Flordaguard peach rootstock. HortScience 26:427–428Google Scholar
  48. Tautz D (1989) Hypervariability of simple sequences as a general source for polymorphic DNA markers. Nucleic Acids Res 17:6463–6471. CrossRefPubMedPubMedCentralGoogle Scholar
  49. Taylor AL, Sasser JN (1978) Biology, identification and control of root-knot nematodes (Meloidogyne species). N.C. State Univ. Dep. Plant Path. and USAID, Raleigh, p 111pGoogle Scholar
  50. Van Ghelder C, Esmenjaud D (2016) TNL genes in peach: insights into the post-LRR domain. BMC Genomics 17:317. CrossRefPubMedPubMedCentralGoogle Scholar
  51. Van Ghelder C, Lafargue B, Dirlewanger E, Ouassa A, Voisin R, Polidori J, Kleinhentz M, Esmenjaud D (2010) Characterization of the RMja gene for resistance to root-knot nematodes in almond: spectrum, location, and interest for Prunus breeding. Tree Genet Genomes 6:503–511. CrossRefGoogle Scholar
  52. Van Ooijen J (2006) JoinMap 4.1, software for the calculation of genetic linkage maps in experimental populations of diploid species. Kyazma B. V, WageningenGoogle Scholar
  53. Van Ooijen J (2009) MapQTL 6, software for the mapping of quantitative trait loci in experimental populations of diploid species. Kyazma B. V, WageningenGoogle Scholar
  54. Verde I, Abbott AG, Scalabrin S, Jung S, Shu S, Marroni F, Zhebentyayeva T, Dettori MT, Grimwood J, Cattonaro F (2013) The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 45:487–496. CrossRefPubMedGoogle Scholar
  55. Verde I, Bassil N, Scalabrin S, Gilmore B, Lawley CT, Gasic K, Micheletti D, Rosyara UR, Cattonaro F, Vendramin E, Main D, Aramini V, Blas AL, Mockler TC, Bryant DW, Wilhelm L, Troggio M, Sosinski B, Aranzana MJ, Arús P, Iezzoni A, Morgante M, Peace C (2012) Development and evaluation of a 9K SNP array for peach by internationally coordinated SNP detection and validation in breeding germplasm. PLoS One 7:e35668. CrossRefPubMedPubMedCentralGoogle Scholar
  56. Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78. CrossRefPubMedGoogle Scholar
  57. Yamamoto T, Shimada T, Imai T, Yaegaki H, Haji T, Matsuta N, Yamaguchi M, Hayashi T (2001) Characterization of morphological traits based on a genetic linkage map in peach. Breed Sci 51:271–278. CrossRefGoogle Scholar
  58. Yamamoto T, Yamaguchi M, Hayashi T (2005) An integrated genetic linkage map of peach by SSR, STS, AFLP and RAPD. J Japan Soc Hort Sci 74:204–213. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Mary Ann D. Maquilan
    • 1
  • Mercy A. Olmstead
    • 1
  • James W. Olmstead
    • 1
  • Donald W. Dickson
    • 2
  • José X. Chaparro
    • 1
  1. 1.Horticultural Sciences DepartmentUniversity of FloridaGainesvilleUSA
  2. 2.Entomology and Nematology DepartmentUniversity of FloridaGainesvilleUSA

Personalised recommendations