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.
Similar content being viewed by others
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
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
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
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
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
Castagnone-Sereno P (2002) Genetic variability of nematodes: a threat to the durability of plant resistance genes? Euphytica 124:193–199
Castagnone-Sereno P (2006) Genetic variability and adaptive evolution in parthenogenetic root-knot nematodes. Heredity 96:282–289
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
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
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
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
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
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
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
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
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
Djian-Caporalino C, Védie H, Arrufat A (2009) De nouvelles pistes pour gérer les nématodes à galles. PHM Rev Hortic 515:34–37
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
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
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
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
Fuller VL, Lilley CJ, Urwin PE (2008) Nematode resistance. New Phytol 180:27–44
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
Hare WW (1956) Resistance in pepper to Meloidogyne incognita acrita. Phytopathology 46:98–104
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
Hendy H, Dalmasso A, Cardin MC (1985a) Differences in resistant Capsicum annuum attacked by Meloidogyne species. Nematological 31:72–78
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
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
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
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
Johnson R (1984) A critical analysis of durable resistance. Annu Rev Phytopathol 22:309–330
Kou Y, Wang S (2012) Toward an understanding of the molecular basis of quantitative disease resistance in rice. J Biotech 159:283–290
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
McDonald BA, Linde C (2002) Pathogen population genetics, evolutionary potential, and durable resistance. Annu Rev Phytopathol 40:349–379
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
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
Parlevliet JE (2002) Durability of resistance against fungal, bacterial and viral pathogens; present situation. Euphytica 124:147–156
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
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
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
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
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
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
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
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
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
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
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
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
Trudgill DL, Blok VC (2001) Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Annu Rev Phytopathol 39:53–77
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
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
Williamson VM (1998) Root-knot nematode resistance genes in tomato and their potential for future use. Annu Rev Phytopathol 36:277–293
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
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
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
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.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by C. Gebhardt.
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-013-2235-1