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The plant genetic background affects the efficiency of the pepper major nematode resistance genes Me1 and Me3

Theoretical and Applied Genetics volume 127, pages 499–507 (2014)Cite this article

Abstract

Key message

The plant genetic background influences the efficiency of major resistance genes to root-knot nematodes in pepper and has to be considered in breeding strategies.

Abstract

Root-knot nematodes (RKNs), Meloidogyne spp., are extremely polyphagous plant parasites worldwide. Since the use of most chemical nematicides is being prohibited, genetic resistance is an efficient alternative way to protect crops against these pests. However, nematode populations proved able to breakdown plant resistance, and genetic resources in terms of resistance genes (R-genes) are limited. Sustainable management of these valuable resources is thus a key point of R-gene durability. In pepper, Me1 and Me3 are two dominant major R-genes, currently used in breeding programs to control M. arenaria, M. incognita and M. javanica, the three main RKN species. These two genes differ in the hypersensitive response induced by nematode infection. In this study, they were introgressed in either a susceptible or a partially resistant genetic background, in either homozygous or heterozygous allelic status. Challenging these genotypes with an avirulent M. incognita isolate demonstrated that (1) the efficiency of the R-genes in reducing the reproductive potential of RKNs is strongly affected by the plant genetic background, (2) the allelic status of the R-genes has no effect on nematode reproduction. These results highlight the primary importance of the choice of both the R-gene and the genetic background into which it is introgressed during the selection of new elite cultivars by plant breeders.

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References

  • Ammati M, Thomason IJ, McKinney HE (1986) Retention of resistance to Meloidogyne incognita in Lycopersicon genotypes at high soil temperature. J Nematol 18:491–495

    CAS  PubMed Central  PubMed  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 ultrastructural changes upon nematode infection. Plant Sci 133:79–90

    CAS  Article  Google Scholar 

  • Bost SC, Triantaphyllou AC (1982) Genetic basis of the epidemiologic effects of resistance to Meloidogyne incognita in the tomato cultivar small fry. J Nematol 14:540–544

    CAS  PubMed Central  PubMed  Google Scholar 

  • Brun H, Chevre AM, Fitt BD, Powers S, Besnard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard M, Andrivon D (2010) Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 185:285–299

    PubMed  Article  Google Scholar 

  • Cap GB, Roberts PA, Thomason IJ (1993) Inheritance of heat-stable resistance to Meloidogyne incognita in Lycopersicon peruvianum and its relationship to the Mi gene. Theor Appl Genet 85:777–783

    CAS  PubMed  Google Scholar 

  • Castagnone-Sereno P (2002) Genetic variability of nematodes: a threat to the durability of plant resistance genes? Euphytica 124:193–199

    CAS  Article  Google Scholar 

  • Castagnone-Sereno P (2006) Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96:282–289

    CAS  PubMed  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 

  • Castro AJ, Capettini F, Corey AE, Filichkina T, Hayes PM, Kleinhofs A, Kudrna D, Richardson K, Sandoval-Islas S, Rossi C, Vivar H (2003) Mapping and pyramiding of qualitative and quantitative resistance to stripe rust in barley. Theor Appl Genet 107:922–930

    CAS  PubMed  Article  Google Scholar 

  • Chintamanani S, Multani DS, Ruess H, Johal GS (2008) Distinct mechanisms govern the dosage-dependent and developmentally regulated resistance conferred by the maize Hm2 gene. Mol Plant Microbe Interact 21:79–86

    CAS  PubMed  Article  Google Scholar 

  • Collmer CW, Marston MF, Taylor JC, Jahn M (2000) The I gene of bean: a dosage-dependent allele conferring extreme resistance, hypersensitive resistance, or spreading vascular necrosis in response to the potyvirus Bean common mosaic virus. Mol Plant Microbe Interact 13:1266–1270

    CAS  PubMed  Article  Google Scholar 

  • Cortada L, Javier Sorribas F, Ornat C, Fe Andres M, Verdejo-Lucas S (2009) Response of tomato rootstocks carrying the Mi-resistance gene to populations of Meloidogyne arenaria, M. incognita and M. javanica. Eur J of Plant Pathol 124:337–343

    Article  Google Scholar 

  • Dalmasso A, Berge JB (1978) Molecular polymorphism and phylogenetic relationship in some Meloidogyne spp.: application to the taxonomy of Meloidogyne. J Nematol 10:323–332

    CAS  PubMed Central  PubMed  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Januel A, Lefebvre V, Daubèze A, Palloix A, Dalmasso A, Abad P (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

    CAS  PubMed  Article  Google Scholar 

  • Djian-Caporalino C, Pijarowski L, Fazari A, Samson M, Gaveau L, O’Byrne C, Lefebvre V, Caranta C, Palloix A, Abad P (2001) High-resolution genetic mapping of the pepper (Capsicum annuum L.) resistance loci Me 3 and Me 4 conferring heat-stable resistance to root-knot nematodes (Meloidogyne spp.). Theor Appl Genet 103:592–600

    CAS  Article  Google Scholar 

  • Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, VandeCasteele C, Faure I, Brunoud G, Pijarowski L, Palloix A, Lefebvre V, Abad P (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

    CAS  PubMed  Article  Google Scholar 

  • Djian-Caporalino C, Védie H, Arrufat A (2009) De nouvelles pistes pour gérer les nématodes à galles. PHM Rev Hortic 515:34–37

    Google Scholar 

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

    Article  Google Scholar 

  • Dumas de Vaulx R, Chambonnet D, Pochard E (1981) Culture in vitro d’anthères de piment (Capsicum annuum): amélioration des taux d’obtention de plantes chez différents génotypes par des traitements à +35°C. Agronomie 1:859–864

    Article  Google Scholar 

  • Fazari A, Palloix A, Wang L, Hua MY, Sage-Palloix A-M, 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

    CAS  Article  Google Scholar 

  • Fournet S, Kerlan MC, Renault L, Dantec JP, Rouaux C, Montarry J (2012) Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence. Plant Pathol 62:184–193

    Article  Google Scholar 

  • Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44

    CAS  PubMed  Article  Google Scholar 

  • Fulton TM, Chunwongse J, Tanksley SD (1995) Microprep protocol for extraction of DNA from tomato and other herbaceous plants. Plant Mol Biol Rep 13:207–209

    CAS  Article  Google Scholar 

  • Hare WW (1956) Resistance in pepper to Meloidogyne incognita acrita. Phytopathology 46:98–104

    Google Scholar 

  • Hendy H (1984) Contribution à l’étude des relations hôte-parasite chez les nématodes phytophages du genre Meloidogyne. Génétique et mécanismes de la résistance chez Capsicum spp. Thèse de Doctorat, USTL Montpellier, France, p 157

    Google Scholar 

  • Hendy H, Dalmasso A, Cardin MC (1985a) Differences in resistant Capsicum annuum attacked by Meloidogyne species. Nematological 31:72–78

    Article  Google Scholar 

  • Hendy H, Pochard E, Dalmasso A (1985b) Transmission héréditaire de la résistance aux Meloidogyne portée par deux lignées de Capsicum annuum: études de descendances d’homozygotes issues d’androgénèse. Agronomie 5:93–100

    Article  Google Scholar 

  • Jacquet M, Bongiovanni M, Martinez M, Verschave P, Wajnberg E, Castagnone-Sereno P (2005) Variation in resistance to the root-knot nematode Meloidogyne incognita in tomato genotypes bearing the Mi gene. Plant Pathol 54:93–99

    Article  Google Scholar 

  • Jahier J, Chain F, Barloy D, Tanguy A-M, Lemoine J, Riault G, Margalé E, Trottet M, Jacquot E (2009) Effect of combining two genes for partial resistance to Barley yellow dwarf virus-PAV (BYDV-PAV) derived from Thinopyrum intermedium in wheat. Plant Pathol 58:807–814

    Article  Google Scholar 

  • Jarquin-Barberena H, Dalmasso A, de Guiran G, Cardin MC (1991) Acquired virulence in the plant parasitic nematode Meloidogyne incognita. 1. Biological analysis of the phenomenon. Rev Nématol 14:299–303

    Google Scholar 

  • Johnson R (1984) A critical analysis of durable resistance. Annu Rev Phytopathol 22:309–330

    Article  Google Scholar 

  • Kou Y, Wang S (2012) Toward an understanding of the molecular basis of quantitative disease resistance in rice. J Biotech 159:283–290

    CAS  Article  Google Scholar 

  • López-Pérez J-A, Le Strange M, Kaloshian I, Ploeg AT (2006) Differential response of Mi gene-resistant tomato rootstocks to root-knot nematodes (Meloidogyne incognita). Crop Prot 25:382–388

    Article  Google Scholar 

  • McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379

    CAS  PubMed  Article  Google Scholar 

  • Paillard S, Trotoux-Verplancke G, Perretant M-R, Mohamadi F, Leconte M, Coedel S, de Vallavieille-Pope C, Dedryver F (2012) Durable resistance to stripe rust is due to three specific resistance genes in French bread wheat cultivar Apache. Theor Appl Genet 125:955–965

    CAS  PubMed  Article  Google Scholar 

  • Palloix A, Ayme V, Moury B (2009) Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol 183:190–199

    CAS  PubMed  Article  Google Scholar 

  • Parlevliet JE (2002) Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 124:147–156

    CAS  Article  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. Phytopathology 95:158–165

    CAS  PubMed  Article  Google Scholar 

  • 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

    CAS  PubMed  Article  Google Scholar 

  • Richardson KL, Vales MI, Kling JG, Mundt CC, Hayes PM (2006) Pyramiding and dissecting disease resistance QTL to barley stripe rust. Theor Appl Genet 113:485–495

    CAS  PubMed  Article  Google Scholar 

  • Riedel C, Habekuss A, Schliephake E, Niks R, Broer I, Ordon F (2011) Pyramiding of Ryd2 and Ryd3 conferring tolerance to a German isolate of Barley yellow dwarf virus-PAV (BYDV-PAV-ASL-1) leads to quantitative resistance against this isolate. Theor Appl Genet 123:69–76

    CAS  PubMed  Article  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 Central  PubMed  Google Scholar 

  • Rossi C, Cuesta-Marcos A, Vales I, Gomez-Pando L, Orjeda G, Wise R, Sato K, Hori K, Capettini F, Vivar H, Chen X, Hayes P (2006) Mapping multiple disease resistance genes using a barley mapping population evaluated in Peru, Mexico, and the USA. Mol Breed 18:355–366

    Article  Google Scholar 

  • Tan MYA, Alles R, Hutten RCB, Visser RGF, van Eck HJ (2009) Pyramiding of Meloidogyne hapla resistance genes in potato does not result in an increase of resistance. Potato Res 52:331–340

    CAS  Article  Google Scholar 

  • Tan MYA, Hutten RCB, Visser RGF, van Eck HJ (2010) The effect of pyramiding Phytophthora infestans resistance genes R Pi-mcd1 and R Pi-ber in potato. Theor Appl Genet 121:117–125

    PubMed Central  PubMed  Article  Google Scholar 

  • Thies JA, Fery RL (1998) Modified expression of the N gene for southern root-knot nematode resistance in pepper at high soil temperatures. J Am Soc Hortic Sci 123:1012–1015

    CAS  Google Scholar 

  • Thies JA, Fery RL (2000) Characterization of resistance conferred by the N gene to Meloidogyne arenaria Races 1 and 2, M. hapla, and M. javanica in two sets of isogenic lines of Capsicum annuum L. J Am Soc Hortic Sci 125:71–75

    Google Scholar 

  • Thies JA, Fery RL (2002) Heat stability of resistance to southern root-knot nematode in bell pepper genotypes homozygous and heterozygous for the N gene. J Am Soc Hortic Sci 127:371–375

    CAS  Google Scholar 

  • Triantaphyllou AC (1985) Cytogenetics, cytotaxonomy and phylogeny of root-knot nematodes. In: Sasser JN, Carter CC (eds) An advanced treatise on Meloidogyne, vol 1. North Carolina State University Graphics, Raleigh, pp 113–126

    Google Scholar 

  • Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77

    CAS  PubMed  Article  Google Scholar 

  • Tzortzakakis EA, Trudgill DL, Phillips MS (1998) Evidence for a dosage effect of the Mi gene on partially virulent isolates of Meloidogyne javanica. J Nematol 30:76–80

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang C, Ulloa M, Roberts PA (2008) A transgressive segregation factor (RKN2) in Gossypium barbadense for nematode resistance clusters with gene rkn1 in G. hirsutum. Mol Genet Genomics 279:41–52

    CAS  PubMed  Article  Google Scholar 

  • Williamson VM (1998) Root-knot nematode resistance genes in tomato and their potential for future use. Annu Rev Phytopathol 36:277–293

    CAS  PubMed  Article  Google Scholar 

  • Williamson VM, Roberts PA (2009) Mechanisms and genetics of resistance. In: Perry RN, Moens M, Starr JL (eds) Root-knot nematodes. CAB International, Wallingford, pp 301–325

    Chapter  Google Scholar 

  • Zhou Y, Cao Y, Huang Y, Xie W, Xu C, Li X, Wang S (2009) Multiple gene loci affecting genetic background-controlled disease resistance conferred by R gene Xa3/Xa26 in rice. Theor Appl Genet 120:127–138

    CAS  PubMed  Article  Google Scholar 

  • Zijlstra C, Donkers-Venne DTHM, Fargette M (2000) Identification of Meloidogyne incognita, M. javanica and M. arenaria using sequence characterised amplified region (SCAR) based PCR assays. Nematology 2:847–853

    CAS  Article  Google Scholar 

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Acknowledgments

We thank Anne-Marie Sage-Palloix, Ghislaine Nemouchi and Bruno Savio for plant breeding and for providing BC1-S1 and BC2-S1 seeds. We also acknowledge the seed companies Gautier Semences, Rijk Zwaan France, Sakata Vegetables Europe, Syngenta Seeds, Takii France and Vilmorin, & Cie, and ANRT (Association Nationale de la Recherche Technologique) foundation for their financial support.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

The authors declare that the experiments comply with the current laws of the country in which they were performed.

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Affiliations

  1. INRA, UMR1355 Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

    A. Barbary, A. Fazari, N. Marteu, P. Castagnone-Sereno & C. Djian-Caporalino

  2. UNS, UMR Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

    A. Barbary, A. Fazari, N. Marteu, P. Castagnone-Sereno & C. Djian-Caporalino

  3. CNRS, UMR7254 Institut Sophia Agrobiotech, 06903, Sophia Antipolis, France

    A. Barbary, A. Fazari, N. Marteu, P. Castagnone-Sereno & C. Djian-Caporalino

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

    A. Palloix

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  1. A. Barbary
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  2. A. Palloix
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  3. A. Fazari
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  4. N. Marteu
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  5. P. Castagnone-Sereno
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  6. C. Djian-Caporalino
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Correspondence to A. Barbary.

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Communicated by C. Gebhardt.

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Barbary, A., Palloix, A., Fazari, A. et al. The plant genetic background affects the efficiency of the pepper major nematode resistance genes Me1 and Me3 . Theor Appl Genet 127, 499–507 (2014). https://doi.org/10.1007/s00122-013-2235-1

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  • DOI: https://doi.org/10.1007/s00122-013-2235-1

Keywords

  • Nematode Population
  • Nematode Reproduction
  • Homozygous Resistant
  • Pepper Genotype
  • Yolo Wonder