Development of virulence to Meloidogyne incognita on resistant pepper rootstocks

  • C. Ros Ibáñez Dept. Biotecnología y Protección de Cultivos. IMIDA. Mayor s/n, 30150 La Alberca (Murcia)
  • Lee Robertson Dept. Biodiversidad y Biología Evolutiva. Museo Nacional de Ciencias Naturales (MNCN-CSIC), C/José Gutiérrez Abascal, 2. 28006 Madrid
  • Maria del Carmen Martinez-Lluch Dept. Biotecnología y Protección de Cultivos. IMIDA. Mayor s/n, 30150 La Alberca (Murcia)
  • Ana Cano-García SSVV. Consejería de Agricultura y Agua. Mayor s/n, 30150 La Alberca (Murcia)
  • Alfredo Lacasa-Plasencia Dept. Biotecnología y Protección de Cultivos. IMIDA. Mayor s/n, 30150 La Alberca (Murcia)
Keywords: Capsicum annum, nematode, pot experiment, greenhouse experiment, grafting


The root-knot nematode (RKN) Meloidogyne incognita is a major soil parasite of pepper crops in greenhouses in Southeast Spain. Due to the limitations of the use of soil fumigants, grafting plants on resistant rootstocks (R-rootstocks) has become an important alternative to chemical nematicides. The repeated use of R-rootstocks can bring about the selection of virulent populations capable of overcoming resistance. We carried out a six-year investigation on resistant rootstocks in a naturally M. incognita infested greenhouse, and found that two successive years of growing plants grafted on R-rootstocks Atlante (ATL) were sufficient to overcome resistance (galling index 1.5 and 5.6 in the first and second years respectively). A large variability was observed between several R-rootstocks. Two R-rootstocks (C19 and Snooker) behaved like ATL while two others (Terrano and DRO 8801) were not infected by RKN. Laboratory studies with the same R-rootstocks, inoculated with two nematode isolates (avirulent and virulent against ATL) confirmed the greenhouse results, indicating that some rootstocks may be infested by virulent populations and others may not. It suggests that different R-genes, which are differentially overcome by RKN, have been introgressed into the rootstocks. This may have consequences for the management of resistant rootstocks in the field.


Download data is not yet available.

Author Biography

Maria del Carmen Martinez-Lluch, Dept. Biotecnología y Protección de Cultivos. IMIDA. Mayor s/n, 30150 La Alberca (Murcia)
Departamento de biotecnología y Protección de Cultivos.

Agricultural Technical Engineer


Bello A, Escuer M, Sanz R, López-Pérez JA, Guirao P, 1997. Biofumigación, nematodos y bromuro de metilo en el cultivo de pimiento. In: Posibilidad de alternativas viables al bromuro de metilo en pimiento de invernadero (López A, Mora JA, eds.) Consejería de Medioambiente, Agricultura y Agua, Murcia, Espa-a, pp: 67-108.

Bello A, López-Pérez JA, García Álvarez A, Arcos, SC, Ros C, Guerrero MM, Guirao P, Lacasa A, 2004. Biofumigación con solarización para el control de nematodos en cultivo de pimiento. In: Desinfección de suelos en invernaderos de pimiento (Lacasa A, Guerrero MM, Oncina M, Mora JA, eds.). Consejería de Agricultura, Agua y Medio Ambiente. Región de Murcia, Espa-a, pp: 129-208.l 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.

Bridge JS, Page LJ, 1980. Estimation of root-knot nematodes infestation levels on roots using a rating chart. Trop Pest Manage 26: 296-298.

Castagnone-Sereno P, 1999. Limites de l'utilisation de la résistance aux nématodes à galles chez la tomate. Des risques nouveaux liés au développement de populations virulentes du parasite. Phytoma 522: 61-63.

Castagnone-Sereno P, 2006. Genetic variability and adaptive in parthenogenetic root-knot nematodes. Heredity 96: 282-289.

Castagnone-Sereno P, 2012. Meloidogyne enterolobii (=M. mayaguensis): profile of an emerging, highly pathogenic, root-knot nematode species. Nematology 14: 133-138.

Castagnone-Sereno P, Piotte C, Abad P, Bongiovanni M, Dalmasso A, 1991. Isolation of a repeated DNA probe showing polymorphism among Meloidogyne incognita populations. J Nematol 23 (3): 316-320.

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.

Castagnone-Sereno P, Bongiovanni M, Dijan-Caporalino C, 2001. New data of the root-knot nematode resistance genes Me1 and Me3 in pepper. Plant Breeding 120: 429-433.

Djian-Caporalino C, Pijarowski L, Januel A, Lefebvre V, Daubeze 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, Berthou F, Fazari A, Lefebvre A, Palloix A, Pergard A, Pijarowski, L, 2004. Genetic, cytological and molecular bases of the resistance to root-knot nematodes (Meloidogyne spp.) in pepper (Capsicum annum L). Proc 12th Eucarpia Meeting on Genetics and Breeding of Capsicum and Eggplants, 17-19 May, Noordwijkerhout, The Netherlands. p: 180.

Djian-Caporalino C, Fazari A, Arguel MJ, Vemie 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 annum L.) are clusted on P9 chromosome. Theor Appl Genet 114: 473-486.

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 31: 431-440.

Fazari A, Palloix A, Wang LW, 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 Breeding 131 (5): 665-673.

Fery RL, Dukes PD, Thies JA, 1998. "Carolina Wonder" and "Charleston Belle": Southern root-knot nematode resistant bell peppers. HortScience 33: 900-902.

Flegg JJM, 1967. Extraction of Xiphinema and Longidorus species from soil by modification of Cobb’s decanting sieving technique. Ann Appl Biol 60: 429-437.

Giné A, Bonmatí M, Sarro A, Stchiegel M, Valero J, Ornat C, Fernández C, Sorribas FJ, 2013. Natural occurrence of fungal egg parasites of root-knot nematodes, Meloidogyne spp. in organic and integrated vegetable production systems in Spain. BioControl 58: 407-416.

Goodey JB, Franklin MT, Hooper DJ, 1965. The nematode parasites of plant catalogued under their host. Commonwealth Agricultural Bureaux, Farnham Royal, UK. 214pp.

Hartman KM, Sasser JN, 1985. Identification of Meloidogyne species on the basis of differential host test and perineal pattern morphology. In: Advanced treatise on Meloidogyne, Vol. II, Methodology (Barker KR, Carter CC, Sasser, JN, eds). North Carolina State University Graphics, Raleigh, NC, USA, pp: 69–77.

Hendy H, Pochard E, Damalso A, 1985. Transmission héréditaire de la résistance aux nématodes Meloidogyne Chitwood (Tylenchida) portée par 2 lignés de Capsicum Nahum L.: étude de descendances homozygotes sigues d`androgenése. Agronomie 5 (2): 93-100.

Hussey RS, Barker KR, 1973. A comparison of methods of collecting inocula on Meloidogyne spp. including a new technique. Plant Dis Rep 57: 1025-1028.

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

Lamberti F, 1981. Plant nematode problems in the Mediterranean region. Helmintol Abstr Ser B Plant Nematol CAB 50: 145-166.

López-Pérez JA, Escuer M, Díez-Rojo M, Robertson L, Piedra-Buena A, López-Cepero J, Bello A, 2011. Host range of Meloidogyne arenaria (Neal, 1889) Chitwood, 1949 (nematoda: Meloidogynae) in Spain. Nematropica 41 (1): 130-139.

Omwega C O, Thomason IJ, Roberts PA, 1988. A nondestructive technique for screening bean germ plasm for resistance to Meloidogyne incognita. Plant Dis 72: 970-972.

Ornat C, Verdejo-Lucas S, Sorribas FJ, 2001. A population of Meloidogyne javanica in Spain virulent to the Mi resistance gene in tomato. Plant Dis 85 (3): 271-276.

Ozarslandan A, Devran Z, Mutlu N, 2009. First report of Columbia root-knot nematode (Meloidogyne chitwoodi) in potato in Turkey. Plant Dis 93: 3.

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.

Robertson L, López-Pérez JA, Bello A, Díez-Rojo MA, Escuer M, Piedra-Buena A, Ros C, Martínez C, 2006. Characterization of Meloidogyne incognita, M. arenaria and M hapla populations from Spain and Uruguay parasitizing pepper (Capsicum annuum). Crop Prot 25: 440-445.

Ros C, Guerrero MM, Lacasa A, Guirao P, González A, Bello A, López-Pérez JA, Martínez MA, 2004. El injerto en pimiento. Comportamiento de patrones frente a hongos y nematodos. In: Desinfección de suelos en invernaderos de pimiento (Lacasa A, Guerrero MM, Oncina M, Mora JA, eds). Consejería de Agricultura, Agua y Medio Ambiente. Región de Murcia, Espa-a, pp: 279-312.

Ros C, Guerrero MM, Martínez MA, Barceló N, Martínez MC, Rodríguez I, Guirao P, Bello A, Lacasa A, 2005. Resistant sweet pepper rootstocks integrated into the management of soilborne pathogens in greenhouse. Acta Horticulturae 698: 305-310.

Ros C, Guerrero MM, Martínez MA, Lacasa A, Bello A, 2006. Integrated management of Meloidogyne resistance in sweet pepper in greenhouses. Bull IOBC-WPRS 29 (4): 319-324.

Sasser JN, Freckman DW, 1987. A world perspective on Nematology: The Rrole of society. In: Vistas on Nematology (Veech JA & Dickerson DW, eds). Society of Nematologists, Hyattsville, MD, USA. pp: 7-14.

Talavera M, Verdejo-Lucas S, Ornat C, Torres J, Vela MD, Macias FJ, Cortada L, Arias DJ, Valero J, Sorribas FJ, 2009. Crop rotations with Mi gene resistant and susceptible tomato cultivars for management of root-knot nematodes in plastic houses. Crop Prot 28: 662-667.

Thies JA, Fery RL, 2002. Heat stability of resistance to souther root-knot in nematode in bell pepper genotypes homozygous and heterozygous for the N gene. J Am Soc Hortic Sci 127 (3): 371-375.

Trudgill DL, Blok VC, 2001. Apomictic, polyphagous root-knot nematodes: exceptionally successful and damaging biotrophic root pathogens. Ann 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 (1): 76-80.

Verdejo-Lucas S, Ornat C, Sorribas FJ, Stchiegel A, 2002. Species of rootknot nematodes and fungal egg parasites recovered from vegetables in Almería and Barcelona. J Nematol 34: 405-408.

Verdejo-Lucas S, Cortada L, Sorribas FJ, Ornat C, 2009. Selection of virulent populations of Meloidogyne javanica by repeated cultivation of Mi resistance gene tomato rootstocks under field conditions. Plant Pathol 58: 990-998.

Verdejo-Lucas S, Talavera M, Andrés MF, 2012. Virulence response to the Mi 1 gene of Meloidogyne populations from tomato in greenhouses. Crop Prot 39: 97-105.

Wesemael WML, Viaene N, Moens M, 2011. Root-knot nematodes (Meloidogyne spp.) in Europe. Nematology 13: 3-16.

How to Cite
Ros IbáñezC., RobertsonL., Martinez-LluchM. del C., Cano-GarcíaA., & Lacasa-PlasenciaA. (2014). Development of virulence to Meloidogyne incognita on resistant pepper rootstocks. Spanish Journal of Agricultural Research, 12(1), 225-232.
Plant protection