Pyramiding, alternating or mixing: Comparative performances of deployment strategies of nematode resistance genes to promote plant resistance efficiency and durability

BMC Plant Biology

Volumn 14, Issue 1, 2014, Pages

  Djian Caporalino, Caroline ^a   Palloix, Alain ^b   Fazari, Ariane ^a   Marteu, Nathalie ^a   Barbary, Arnaud ^a   Abad, Pierre ^a   Sage Palloix, Anne Marie ^b   Mateille, Thierry ^c   Risso, Sabine ^d   Lanza, Roger ^d   Taussig, Catherine ^e   Castagnone Sereno, Philippe ^a  

^a Institut Sophia Agrobiotech   (France)

^b Researches Center of Avignon   (France)

^c CENTRE DE BIOLOGIE ET DE GESTION DES POPULATIONS   (France)

^d Chambre d'Agriculture des Alpes Maritimes   (France)

^e APREL   (France)

Author keywords

Breeding strategy; Capsicum spp; Meloidogyne spp; Resistance gene deployment; Root knot nematodes; Sustainable crop protection; Virulence emergence

Indexed keywords

VEGETABLE PROTEIN;

ANIMAL; ARTICLE; GENETICS; LETTUCE; METABOLISM; NEMATODE; PARASITOLOGY; PATHOGENICITY; PEPPER; PLANT DISEASE;

ANIMALS; CAPSICUM; LETTUCE; NEMATODA; PLANT DISEASES; PLANT PROTEINS;

EID: 84897688788     PISSN: None     EISSN: 14712229     Source Type: Journal    
DOI: 10.1186/1471-2229-14-53     Document Type: Article

References (64)

1. Starr JL, Bridge J, Cook R. Resistance to plant-parasitic nematodes: history, current use and future potential. Plant Resistance to Parasitic Nematodes 2002, 1-22. Wallingford: CAB International, Starr JL, Cook R, Bridge J.
2. McDonald BA, Linde C. Pathogen population genetics and the durability of resistance. Euphytica 2002, 124:163-180.
3. García-Arenal F, McDonald BA. An analysis of the durability of resistance to plant viruses. Phytopathology 2003, 93:941-952. 10.1094/PHYTO.2003.93.8.941, 18943860.
4. Gallun RL. Genetic interrelationships between host plants and Insects. J Environ Qual 1972, 1:259-265.
5. Castagnone-Sereno P. Genetic variability of nematodes: a threat to the durability of plant resistance genes?. Euphytica 2002, 124:193-199.
6. Johnson R. Durable resistance: definition of, genetic control & attainment in plant breeding. Phytopathology 1981, 71:567-568.
7. Lecoq H, Moury B, Desbiez C, Palloix A, Pitrat M. Durable virus resistance in plants through conventional approaches: a challenge. Virus Res 2004, 100:31-39. 10.1016/j.virusres.2003.12.012, 15036833.
8. Brun H, Chèvre AM, Fitt BD, Powers S, Besnard AL, Ermel M, Huteau V, Marquer B, Eber F, Renard M, Andrivon D. Quantitative resistance increases the durability of qualitative resistance to Leptosphaeria maculans in Brassica napus. New Phytol 2010, 185:285-299. 10.1111/j.1469-8137.2009.03049.x, 19814776.
9. Palloix A, Ayme V, Moury B. Durability of plant major resistance genes to pathogens depends on the genetic background, experimental evidence and consequences for breeding strategies. New Phytol 2009, 183:190-199. 10.1111/j.1469-8137.2009.02827.x, 19344475.
10. Nelson RR. Stabilizing racial populations of plant pathogens by use of resistance genes. J Environ Qual 1972, 1:220-227.
11. Gallun RL, Khush GS. Genetic factors affecting expression and stability of resistance. Breeding Plant Resistance to Insects 1980, 63-68. New York: Wiley, Maxwell FG, Jennings PR.
12. Liu J, Liu D, Tao W, Li W, Wang Chen P, Cheng S, Gao D. Molecular marker-facilitated pyramiding of different genes for powdery mildew resistance in wheat. Plant Breed 2000, 119:21-24.
13. Huang N, Angeles ER, Domingo J, Magpantay G, Singh S, Zhang G, Kumaravadivel N, Bennett J, Khush GS. Pyramiding of bacterial blight resistance genes in rice: marker-assisted selection using RFLP and PCR. Theor Appl Genet 2004, 95:313-320.
14. Hittalmani S, Parco A, Mew TV, Zeigler RS, Huang N. Fine mapping and DNA marker-assisted pyramiding of three major genes for blast resistance in rice. Theor Appl Genet 2000, 100:1121-1128.
15. Kiyosawa S. Genetics and epidemiological modeling of breakdown of plant-disease resistance. Annu Rev Phytopathol 1982, 20:93-117.
16. Finckh MR, Gacek ES, Goyeau H, Lannou C, Merz U, Mundt CC, Munk L, Nadziak J, Newton AC, De Vallavieille-Pope C, Wolfe MS. Cereal variety and species mixtures in practice, with emphasis on disease resistance. Agronomie 2000, 20:813-837.
17. Lindhout P. The perspectives of polygenic resistance in breeding for durable disease resistance. Euphytica 2002, 124:217-226.
18. Delourme R, Chèvre AM, Brun H, Rouxel T, Balesdent MH, Dias JS, Salisbury P, Renard M, Rimmer SR. Major gene and polygenic resistance to Leptosphaeria maculans in oilseed rape (Brassica napus). Eur J Plant Pathol 2006, 114:41-52.
19. Stuthman DD, Leonard JJ, Miller-Garvin J. Breeding crops for durable resistance to disease. Adv Agron 2007, 95:319-367.
20. Wolfe MS, Barrett JA. Can we lead the pathogen astray?. Plant Dis 1980, 70:148-155.
21. Mundt CC, Cowger C, Garrett KA. Relevance of integrated disease management to resistance durability. Euphytica 2002, 124:245-252.
22. Zhu Y, Chen H, Fan J, Wang Y, Li Y, Chen J, Fan JX, Yang S, Hu L, Leung H, Mew TW, Teng PS, Wang Z, Mundt CC. Genetic diversity and disease control in rice. Nature 2000, 406:718-722. 10.1038/35021046, 10963595.
23. Gould F. Simulation models for predicting durability of insect-resistant germplasm: a deterministic diploid, two locus model. Environ Entomol 1986, 15:1-23.
24. Van den Bosch F, Gilligan CA. Measures of durability of resistance. Phytopathology 2003, 93:616-625. 10.1094/PHYTO.2003.93.5.616, 18942985.
25. Fabre F, Rousseau E, Mailleret L, Moury B. Durable strategies to deploy plant resistance in agricultural landscapes. New Phytol 2012, 193:1064-1075. 10.1111/j.1469-8137.2011.04019.x, 22260272.
26. Wang J, Chapmanb SC, Bonnettc DG, Rebetzkec GJ, Croucha J. Application of population genetic theory and simulation models to efficiently pyramid multiple genes via marker-assisted selection. Crop Sci 2007, 47:582-588.
27. Consortium REX. Heterogeneity of selection and the evolution of resistance. Trends Ecol Evol 2012, 28:110-118.
28. Chitwood DJ. Nematicides. Encyclopedia of Agrochemicals, Volume 3 2003, 1104-1115. New York: John Wiley & Sons, Plimmer JR, http://naldc.nal.usda.gov/download/43874/PDF.
29. Sasser JN. Worlwide dissemination and importance of the root-knot nematode, Meloidogyne spp. J Nematol 1977, 22:585-589.
30. EC Directive1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Counci. Directives 79/117/EEC and 91/414/EEC. Official Journal of the European Union, 24.11.2009, L 309/1-50 (in French, abstract available in English at http://eur-lex.europa.eu/LexUriServ/LexUriServ.do?uri=OJ:L:2009:309:0001:0050:EN:PDF).
31. UNEP (United Nations Environment Programme) Ninth edition of the Handbook for the Montreal Protocol on Substances that Deplete the Ozone Layer 2012, Nairobi, Kenya: UNON Publishing Section Services, Secretariat for The Vienna Convention for the Protection of the Ozone Layer & The Montreal Protocol on Substances that Deplete the Ozone Layer. United Nations Environment Programme, http://ozone.unep.org/, UNEP (United Nations Environment Programme).
32. Williamson VM, Kumar A. Nematode resistance in plants: the battle underground. Trends Genet 2006, 22:396-403. 10.1016/j.tig.2006.05.003, 16723170.
33. Djian-Caporalino C, Pijarowski L, Januel A, Lefebvre V, Daubeze A, Palloix A, Dalmasso A, Abad P. Spectrum of resistance to root-knot nematodes and inheritance of heat-stable resistance in pepper (Capsicum annuum L.). Theor Appl Genet 1999, 99:496-502. 10.1007/s001220051262, 22665183.
34. Djian-Caporalino C, Pijarowski L, Fazari A, Samson M, Gaveau L, O'Byrne C, Lefebvre V, Caranta C, Palloix A, Abad P. 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 2001, 103:592-600.
35. Djian-Caporalino C, Fazari A, Arguel MJ, Vernie T, VandeCasteele C, Faure I, Brunoud G, Pijarowski L, Palloix A, Lefebvre V, Abad P. Root-knot nematode (Meloidogyne spp.) Me resistance genes in pepper (Capsicum annuum L.) are clustered on the P9 chromosome. Theor Appl Genet 2007, 114:473-486. 10.1007/s00122-006-0447-3, 17136373.
36. Castagnone-Sereno P, Bongiovanni M, Palloix A, Dalmasso A. Selection for Meloidogyne incognita virulence against resistance genes from tomato and pepper and specificity of the virulence/resistant determinants. Eur J Plant Pathol 1996, 102:585-590.
37. Djian-Caporalino C, Molinari S, Palloix A, Ciancio A, Fazari A, Marteu N, Ris N, Castagnone-Sereno P. 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 2011, 131:431-440.
38. Castagnone-Sereno P, Bongiovanni M, Djian-Caporalino C. New data on the specificity of the root-knot nematode resistance genes Me1 and Me3 in pepper. Plant Breed 2001, 120:429-433.
39. Hendy H, Dalmasso A, Cardin MC. Differences in resistant Capsicum annuum attacked by different Meloidogyne species. Nematologica 1985, 31:72-78.
40. Bleve-Zacheo T, Bongiovanni M, Melillo MT, Castagnone-Sereno P. The pepper resistance genes Me1 et Me3 induce differential penetration rates and temporal sequences of root cell ultrastructural changes upon nematode infection. Plant Sci 1998, 133:79-90.
41. Barbary A, Palloix A, Fazari A, Marteu N, Castagnone-Sereno P, Djian-Caporalino C. The plant genetic background affects the efficiency of the pepper major nematode resistance genes Me1 and Me3. Theor Appl Genet 2014, 127:499-507. 10.1007/s00122-013-2235-1, 24258389.
42. Lyngkjær MF, Newton AC, Atzema JL, Baker SJ. The Barley mlo-gene: an important powdery mildew resistance source. Agronomie 2000, 20:745-756.
43. Rouxel T, Penaud A, Pinochet X, Brun H, Gout L, Delourme R, Schmit J, Balesdent MH. A 10-year survey of populations of Leptosphaeria maculans in France indicates a rapid adaptation towards the Rlm1 resistance gene of oilseed rape. Eur J Plant Pathol 2003, 109:871-881.
44. Fournet S, Kerlan MC, Renault L, Dantec JP, Rouaux C, Montarry J. Selection of nematodes by resistant plants has implications for local adaptation and cross-virulence. Plant Pathol 2013, 62:184-193.
45. Palloix A, Quenouille J, Paulhiac E, Moury B. Quantitative trait loci from the host genetic background modulates the durability of a resistance gene: a rational basis for sustainable resistance breeding in plants. Heredity in press.
46. Castagnone-Sereno P, Bongiovanni M, Wajnberg E. Selection and parasite evolution: a reproductive fitness cost associated with virulence in the parthenogenetic nematode Meloidogyne incognita. Evolutionary Ecology 2007, 21:259-270.
47. Pink DAC. Strategies using genes for non-durable resistance. Euphytica 2002, 1:227-236.
48. Mundt CC. Probability of mutation to multiple virulence and durability of resistance gene pyramids. Phytopathology 1990, 80:221-223.
49. López-Pérez JA, Le Strange M, Kaloshian I, Ploeg AT. Differential response of Mi gene-resistant tomato rootstocks to root-knot nematodes (Meloidogyne incognita). Crop Prot 2006, 25:382-388.
50. Wang C, Ulloa M, Roberts PA. A transgressive segregation factor (RKN2) in Gossypium barbadense for nematode resistance clusters with gene rkn1 in G. hirsutum. Mol Genet Genomics 2008, 279:41-52. 10.1007/s00438-007-0292-3, 17940800.
51. Zhou Y, Cao Y, Huang Y, Xie W, Xu C, Li X, Wang S. Multiple gene loci affecting genetic background-controlled disease resistance conferred by R gene Xa3/Xa26 in rice. Theor Appl Genet 2009, 120:127-138. 10.1007/s00122-009-1164-5, 19826775.
52. Christie JR. Root-knot nematodes. Plant Nematodes, Their bionomic and Control 1959, 69-70. Gainesville, FL, USA: Agricultural Experiment Stations, University of Florida, Christie JR.
53. Djian-Caporalino C, Bourdy G, Cayrol JC, Regnault-Roger C, Philogène B, Vincent C. Nematicidal and nematode-resistant plants. Biopesticides of Plant Origin 2005, 173-224. Londres, Paris, New York: Editions Tec & Doc.
54. Cadet P. Recherches de méthodes culturales de lutte contre les nématodes parasites de la canne à sucre en Afrique de l'Ouest. Revue Nématol 1985, 8:377-382.
55. Margarida D, Isabel C, Isabel A, Maria C. Solanum sisymbriifolium - a new approach for the management of plant-parasitic nematodes. Eur J Plant Pathol 2012, 133:171.
56. Wehner TC, Walters SA, Barker KR. Resistance to root-knot nematodes in cucumber and horned cucumber. J Nematol 1991, 23:611-614. 2619209, 19283171.
57. Cuadra R, Cruz X, Fajardo JL. Cultivos de ciclo corto como plantas trampas para el control del nematodo agallador. Nematropica 2000, 30:241-246.
58. Ferris H. Cover crops and nematode management. Nemaplex (Nematode-Plant Expert Information System) 2003, http://plpnemweb.ucdavis.edu/nemaplex/nemaplex.htm, http://plpnemweb.ucdavis.edu/nemaplex/Mangmnt/Covercrops.htm.
59. Fazari A, Palloix A, Wang LH, Hua MY, Sage-Palloix AM, Zhang BX, Djian-Caporalino C. The root-knot nematode resistance N-gene co-localizes in the Me-genes cluster on the pepper (Capsicum annuum L.) P9 chromosome. Plant Breed 2012, 131:665-673.
60. Jarquin-Barberena H, Dalmasso A, de Guiran G, Cardin MC. Acquired virulence in the plant parasitic nematode Meloidogyne incognita. I. Biological analysis of the phenomenon. Rev Nématol 1991, 14:299-303.
61. Dalmasso A, Bergé JB. Molecular polymorphism and phylogenetic relationship in some Meloidogyne spp.: application to the taxonomy of Meloidogyne. J Nematol 1978, 10:323-332. 2617902, 19305862.
62. Zijlstra C, Donkers-Venne THM, Fargette M. Identification of Meloidogyne incognita, M. javanica and M. arenaria using sequence characterised amplified region (SCAR) based PCR assays. J Nematol 2000, 2:847-853.
63. Roberts PA, Dalmasso A, Cap GB, Castagnone-Sereno P. Resistance in Lycopersicon peruvianum to isolates of Mi gene-compatible Meloidogyne populations. J Nematol 1990, 22:585-589. 2619063, 19287762.
64. Zeck WM. A rating scheme for field evaluation of root-knot nematode infestations. Pflanzenschutz-Nachrichten 1971, 24:141-144.