Skip to main content
SpringerLink
Log in

Fine mapping of the root-knot nematode resistance gene Me1 in pepper (Capsicum annuum L.) and development of markers tightly linked to Me1

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

Root-knot nematodes (RKNs) can severely damage crops, including peppers, worldwide. The application of resistance genes identified in the Capsicum annuum genome may represent a safe and economically relevant strategy for controlling RKNs. Among the Me genes (Me1, Me3, Me7, and N) that have been mapped to a cluster on chromosome P9, Me1 confers a heat-stable and broad-spectrum resistance that is difficult for virulent RKNs to overcome. In this study, we developed several closely linked kompetitive allele-specific PCR (KASPar) markers, simple sequence repeat (SSR) markers, sequence characterized amplified region (SCAR) markers, and high-resolution melting (HRM) markers for the mapping of RKN-resistance genes. Analyses of 948 individuals (BC1 and F2 progenies) revealed that Me1 was located between SCAR marker 16880-1-V2 and HRM marker 16830-H-V2, with 13 and 0 recombination events with Me1, respectively. These markers were localized to a 132-kb interval, which included six genes. The development of several PCR-based markers closely linked to Me1 will be useful for the marker-assisted selection of RKN resistance in pepper cultivars. Among these markers, 16830-H-V2 and 16830-CAPS are present in the CA09g16830 gene, which is predicted to be a putative late blight resistance protein homolog R1A-3 gene. This gene appears to be a suitable Me1 candidate gene.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Ahn YK, Tripathi S, Kim JH, Cho YI, Lee HE, Kim DS (2014) Transcriptome analysis of Capsicum annuum varieties mandarin and black cluster: assembly, annotation and molecular marker discovery. Gene 533:494–499

    Article  CAS  PubMed  Google Scholar 

  • Ashrafi H, Hill T, Stoffel K, Kozik A, Yao J, Chin-Wo SR (2012) De novo assembly of the pepper transcriptome (Capsicum annuum): a benchmark for in silico discovery of snps, ssrs and candidate genes. BMC Genomics 13:571

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bleve-Zacheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P (1998) The pepper resistance genes Me1 and Me3 induce differential penetration rates and temporal sequences of root cell ultra structural changes upon nematode infection. Plant Sci 133:79–90

    Article  CAS  Google Scholar 

  • Bucki P, Paran I, Ganot L, Ozalvo R, Iberkleid I, Miyara SB (2017) Pathogenic variability of Meloidogyne incognita populations occurring in pepper-production greenhouses in Israel toward Me1, Me3 and N pepper resistance genes. Plant Dis 101:1391–1401. https://doi.org/10.1094/PDIS-11-16-1667-RE

    Article  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Palloix A, Dalmasso A (1996) Selection for Meloidogyne incognita, virulence against resistance genes from tomato and pepper and specificity of the virulence resistance determinants. Eur J Plant Pathol 102:585–590

    Article  Google Scholar 

  • Castagnone-Sereno P, Bongiovanni M, Djian-Caporalino C (2001) New data on the specificity of the root-knot nematode resistance genes Me1 and Me3 in pepper. Plant Breed 120:429–433

    Article  CAS  Google Scholar 

  • Celik I, Sogut MA, Ozkaynak E, Doganlar S, Frary A (2016) Physical mapping of NBS-coding resistance genes to the Me-gene cluster on chromosome P9 reveals markers tightly linked to the N gene for root-knot nematode resistance in pepper. Mol Breed 36:137

    Article  Google Scholar 

  • Chen C, Zhuang M, Li KN, Liu YM, Yang LM, Zhang YY, Cheng F, Sun PT, Fang ZY (2010) Development and utility of EST-SSR marker in cabbage. Acta Horticulturae Sinica 37:221–228

    Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Januel A, Lefebvre V, Daubèze A, Palloix A (1999) Spectrum of resistance to root-knot nematodes and inheritance of heat-stable resistance in pepper (Capsicum annuum L.) Theor Appl Genet 99:496–502

    Article  CAS  PubMed  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Fazari A, Samson M, Gaveau L, O’Byrne C (2001) High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me3 and Me4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.) Theor Appl Genet 103:592–600

    Article  CAS  Google Scholar 

  • Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, Vandecasteele C, Faure I (2007) Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 114:473–486

    Article  CAS  PubMed  Google Scholar 

  • Djian-Caporalino C, Molinari S, Palloix A, Ciancio A, Fazari A, Marteu N (2011) The reproductive potential of the root-knot nematode Meloidogyne incognitais affected by selection for virulence against major resistance genes from tomato and pepper. Eur J Plant Pathol 131:431–440

    Article  Google Scholar 

  • Djian-Caporalino C, Palloix A, Fazari A, Marteu N, Barbary A, Abad P (2014) Pyramiding, alternating or mixing: comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability. BMC Plant Biol 14:53

    Article  PubMed  PubMed Central  Google Scholar 

  • Eisenback JD, Triantaphyllou HH (1991) Root-knot nematodes: Meloidogyne species and races. In: Nickle WR (ed) Manual of agricultural nematology. Marcel Dekker, Inc., New York, pp 191–274

    Google Scholar 

  • Ernst K, Kumar A, Kriseleit D, Kloos DU, Phillips MS, Ganal MW (2002) The broad-spectrum potatocyst nematode resistance gene (Hero) from tomato is the only member of a large gene family of NBS-LRR genes with an unusual amino acid repeat in the LRR region. Plant J 31:127–136

    Article  CAS  PubMed  Google Scholar 

  • Fazari A, Palloix A, Wang L, Hua MY, Sage-Palloix AM, Zhang BX, Djian-Caporalino C (2012) The root-knot nematode resistance N-gene co-localizes in the Me-genes cluster on the pepper (Capsicum annuum L.) P9 chromosome. Plant Breed 131:665–673

    Article  CAS  Google Scholar 

  • Fery RL, Dukes PD (1996) The inheritance of resistance to the southern root-knot nematode in ‘Carolina Hot’ cayenne pepper. J Am Soc Hort Sci 121:1024–1027

    Google Scholar 

  • Fery RL, Dukes PD, Thies JA (1998) ‘Carolina Wonder’ and ‘Charleston Belle’: southern root knot nematode-resistant bell peppers. Hort Sci 33:900–902

    Google Scholar 

  • Hare WW (1957) Inheritance of resistance to root-knot nematodes in pepper. Phytopathology 47:455–459

    Google Scholar 

  • Hendy H, Dalmasso A, Cardin C (1985) Differences inresistant Capsicum annuum attacked by different Meloidogy nespecies. Nematologica 31:72–78

    Article  Google Scholar 

  • Huang H, Zhang Z, Zhang Z, Mao S, Wang L, Zhang B (2011) Analysis of SSRs information in Capsicum spp. from EST database. Agric Sci China 10:1532–1536

    Article  CAS  Google Scholar 

  • Jupe F, Pritchard L, Etherington GJ, Mackenzie K, Cock PJ, Wright F, Sharma SK, Bolser D, Bryan GJ, Jones JD, Hein I (2012) Identification and localisation of the NBS-LRR gene family within the potato genome. BMC Genomics 13:75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim S, Park M, Yeom S, Kim YM, Lee JM, Lee HA, Seo E, Choi J, Cheong K, Kim KT, Jung K, Lee GW, Oh SK, Bae C, Kim S, Lee HY, Kim SY, Kim MS, Kang BC, Jo YD, Yang HB, Jeong HJ, Kang WH, Kwon JK, Shin C, Lim JY, Park JH, Huh JH, Kim JS, Kim BD, Cohen O, Paran I, Suh MC, Lee SB, Kim YK, Shin Y, Noh SJ, Park J, Seo YS, Kwon SY, Kim HA, Park JM, Kim HJ, Choi SB, Bosland PW, Reves G, Jo SH, Lee BW, Cho HT, Choi HS, Lee MS, Yu Y, Choi YD, Park BS, Deynze A, Ashrafi H, Hill T, Kim WT, Pai HS, Ahn HK, Yeam I, Giovannoni JJ, Rose JKC, Sørensen I, Lee SJ, Kim RW, Choi IY, Choi BS, Lim JS, Lee YH, Choi D (2014) Genome sequence of the hot pepper provides insights into the evolution of pungency in Capsicum species. Nat Genet 46:270–278

    Article  CAS  PubMed  Google Scholar 

  • Kosambi DD (1944) The estimation of map distances from recombination values. Ann Eugenics 12:172–175

    Article  Google Scholar 

  • Kumpatla SP, Mukhopadhyay S (2005) Mining and survey of simple sequence repeats in expressed sequence tags of dicotyledonous species. Genome 48:985–998

    Article  CAS  PubMed  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Baarlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181

    Article  CAS  PubMed  Google Scholar 

  • Lefebvre V, Goffinet B, Chauvet JC, Caromel B, Signoret P, Brand R (2001) Evaluation of genetic distances between pepper inbred lines for cultivar protection purposes: comparison of AFLP, RAPD and phenotypic data. Theor Appl Genet 102:741–750

    Article  CAS  Google Scholar 

  • Lincoln SE, Daly MJ, Lander ES (1993) Construction of a genetic linkage map with Mapmaker/Exp v3.0: a tutorial and reference manual. Technical report, Whitehead Institute, Cambridge

  • Liu F, Xie L, Mi B, Ouyang X, Mao Z, Zou X, Xie B (2014) SNP Mining in pepper transcriptome and the polymorphism analysis. Acta Horticulturae Sinica 41:343–348

    CAS  Google Scholar 

  • Milligan SB, Bodeau J, Yaghoobi J, Kaloshian I, Zabel P, Williamson VM (1998) The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10:1307–1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Paal J, Henselewski H, Muth J, Meksem K, Menéndez CM, Salamini F, Ballvora A, Gebhardt C (2004) Molecular cloning of the potato Gro1-4 gene conferring resistance to pathotype Ro1 of the root cyst nematode Globodera rostochiensis, based on a candidate gene approach. Plant J 38:285–297

    Article  CAS  PubMed  Google Scholar 

  • Pegard A, Brizzard G, Fazari A, Soucaze O, Abad P, Djian-Caporalino C (2005) Histological characterization of resistance to different root-knot nematode species related to phenolics accumulation in Capsicum annuum L. Phytopathology 95:158–165

    Article  CAS  PubMed  Google Scholar 

  • Piedra BA, Diez-Rojo MA, Bello A, Robertson L, Lopez-Perez JA, Escuer M, Leon L (2005) Comportamiento de Meloidogyne incognita sobre tomate pimiento resistente en Uruguay. Nematropica 51:10–15

    Google Scholar 

  • Qin C, Yu C, Shen Y, Fang X, Chen L, Min J, Cheng J, Zhao S, Xu M, Luo Y, Yang Y, Wu Z, Mao L, Wu H, Ling-Hu C, Zhou H, Lin H, González-Morales S, Trejo-Saavedra D, Tian H, Tang X, Zhao M, Huang Z, Zhou A, Yao X, Cui J, Li W, Chen Z, Feng Y, Niu Y, Bi S, Yang X, Li W, Cai H, Luo X, Montes-Hernández S, Leyva-González M, Xiong Z, He X, Bai L, Tan S, Tang X, Liu D, Liu J, Zhang S, Chen M, Zhang L, Zhang L, Zhang Y, Liao W, Zhang Y, Wang M, Lv X, Wen B, Liu H, Luan H, Zhang Y, Yang S, Wang X, Xu J, Li X, Li S, Wang J, Palloix A, Bosland P, Li Y, Krogh A, Rivera-Bustamante R, Herrera-Estrella L, Yin Y, Yu J, Hu K, Zhang Z (2014) Whole-genome sequencing of cultivated and wild peppers provides insights into Capsicum domestication and specialization. PANS 111:5135–5140

    Article  CAS  Google Scholar 

  • Roberts PA, Dalmasso A, Cap GB, Castagnone-Sereno P (1990) Resistance in Lycopersicum peruvianum to isolates of Mi gene-compatible Meloidogyne populations. J Nematol 22:585–589

    CAS  PubMed  PubMed Central  Google Scholar 

  • Sanguinetti CJ, Dias-Neto E, Simpson AJG (1994) Rapid silver staining and recovery of PCR products separated on polyacrylamide gels. Bio Tech 17:915–919

    Google Scholar 

  • Sasser JN (1980) Root-knot nematodes: a globe. Plant Dis 64:37

    Article  Google Scholar 

  • Starr JL, Bridge J, Cook R (2002) Resistance to plant-parasitic nematodes: history, current use and future potential. In: Starr JL, Cook R, Bridge J (eds) Plant resistance to parasitic nematodes. CABI Publishing, Wallingford, pp 1–22

    Chapter  Google Scholar 

  • Thies JA, Ariss JJ (2009) Comparison between the N and Me3 genes conferring resistance to the root-knot nematode (Meloidogyne incognita) in genetically different pepper lines (Capsicum annuum). Eur J Plant Pathol 125:545–550

    Article  CAS  Google Scholar 

  • Uncu AT, Celik I, Devran Z, Ozkaynak E, Frary A, Frary A, Doganlar S (2015) Development of a SNP-based CAPS assay for the Me1 gene conferring resistance to root knot nematodes in pepper. Euphytica 206:393–399

    Article  CAS  Google Scholar 

  • Vossen EAG, Voort JNAMR, Kanyuka K, Bendahmane A, Sandbrink H, Baulcombe DC, Bakker J, Stiekema WJ, Klein-Lankhorst RM (2000) Homologues of a single resistance-gene cluster in potato confer resistance to distinct pathogens: a virus and a nematode. Plant J 23:567–576

    Article  PubMed  Google Scholar 

  • Wang L, Gu X, Hua M, Mao S, Zhang Z, Peng D, Yun X, Zhang B (2009) A SCAR marker linked to the N gene for resistance to root knot nematodes (Meloidogyne spp.) in pepper (Capsicum annuum L.) Sci Hortic 122:318–322

    Article  CAS  Google Scholar 

  • Williamson VM (1999) Plant nematode resistance genes. Curr Opin Plant Biol 2:327–331

    Article  CAS  PubMed  Google Scholar 

  • Williamson VW, Hussey RS (1996) Nematode pathogenesis and resistance in plants. Plant Cell 8:1735–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Liwen Bianji, Edanz Editing China (www.liwenbianji.cn/ac) for editing the English text of a draft of this manuscript.

Funding

This work was funded by the National Natural Science Foundation of China (31572121), the China National Key Technology Research and Development Program (2011BAZ01732), the Project of the China Ministry of Agriculture (CARS-25), the Core Research Budget of the Non-Profit Governmental Research Institute (ICS, CAAS; 1610032011011), and the Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (CAAS-ASTIP-IVFCAAS).

Author information

Author notes

  1. Carolina Djian-Caporalino and Lihao Wang contributed equally to this work.

Authors and Affiliations

  1. Institute of Vegetables and Flowers, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Xueying Wang, Yacong Cao, Zhenghai Zhang, Shengli Mao, Baoxi Zhang & Lihao Wang

  2. INRA PACA, UMR1301 INRA/UNSA/CNRS, Interactions Biotiques et Santé Végétale, BP167, 06903, Sophia Antipolis, France

    Ariane Fazari & Caroline Djian-Caporalino

  3. INRA-PACA, UR1052, Génétique et Amélioration des Fruits et Légumes, CS 60094, 84140, Montfavet Cedex, France

    Alain Palloix

Authors
  1. Xueying Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ariane Fazari
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yacong Cao
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhenghai Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Alain Palloix
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shengli Mao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Baoxi Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Caroline Djian-Caporalino
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Lihao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lihao Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Alain Palloix is deceased.

Electronic supplementary material

ESM 1

(XLSX 24 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Fazari, A., Cao, Y. et al. Fine mapping of the root-knot nematode resistance gene Me1 in pepper (Capsicum annuum L.) and development of markers tightly linked to Me1. Mol Breeding 38, 39 (2018). https://doi.org/10.1007/s11032-018-0793-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11032-018-0793-2

Keywords

Search

Navigation