title: A TILLING approach to generate broad-spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy.
abstract: Genetic resistance to pathogens is important for sustainable maintenance of crop yields. Recent biotechnologies offer alternative approaches to generate resistant plants by compensating for the lack of natural resistance. Tomato (Solanum lycopersicum) and related species offer a model in which natural and TILLING-induced potyvirus resistance alleles may be compared. For resistance based on translation initiation factor eIF4E1, we confirm that the natural allele Sh-eIF4E1(PI24)-pot1, isolated from the wild tomato species Solanum habrochaites, is associated with a wide spectrum of resistance to both potato virus Y and tobacco etch virus isolates. In contrast, a null allele of the same gene, isolated through a TILLING strategy in cultivated tomato S. lycopersicum, is associated with a much narrower resistance spectrum. Introgressing the null allele into S. habrochaites did not extend its resistance spectrum, indicating that the genetic background is not responsible for the broad resistance. Instead, the different types of eIF4E1 mutations affect the levels of eIF4E2 differently, suggesting that eIF4E2 is also involved in potyvirus resistance. Indeed, combining two null mutations affecting eIF4E1 and eIF4E2 re-establishes a wide resistance spectrum in cultivated tomato, but to the detriment of plant development. These results highlight redundancy effects within the eIF4E gene family, where regulation of expression alters susceptibility or resistance to potyviruses. For crop improvement, using loss-of-function alleles to generate resistance may be counter-productive if they narrow the resistance spectrum and limit growth. It may be more effective to use alleles encoding functional variants similar to those found in natural diversity.
authors: INRA-UR 1052, GAFL Domaine St Maurice, CS 60094, F-84143, Montfavet, France.
authors: Camille
authors: C
authors: Gauffier
authors: INRA-UR 1052, GAFL Domaine St Maurice, CS 60094, F-84143, Montfavet, France.
authors: Caroline
authors: C
authors: Lebaron
authors: INRA-UR 1052, GAFL Domaine St Maurice, CS 60094, F-84143, Montfavet, France.
authors: André
authors: A
authors: Moretti
authors: Sakata Vegetables Europe, Domaine de Sablas Rue du Moulin, F-30620, Uchaud, France.
authors: Carole
authors: C
authors: Constant
authors: Gautier Semences, Route d'Avignon, F-13630, Eyragues, France.
authors: Frédéric
authors: F
authors: Moquet
authors: Syngenta, 346 Route des Pasquiers, F-84260, Sarrians, France.
authors: Grégori
authors: G
authors: Bonnet
authors: INRA-UR 1052, GAFL Domaine St Maurice, CS 60094, F-84143, Montfavet, France.
authors: Carole
authors: C
authors: Caranta
authors: INRA-UR 1052, GAFL Domaine St Maurice, CS 60094, F-84143, Montfavet, France.
authors: Jean-Luc
authors: JL
authors: Gallois
mesh_terms: D060467:Disease Resistance / Q000235:genetics; D039561:Eukaryotic Initiation Factor-4E / Q000235:genetics* / Q000378:metabolism; D018506:Gene Expression Regulation, Plant; D055786:Gene Knockout Techniques; D005799:Genes, Dominant; D023281:Genomics / Q000379:methods*; D018551:Solanum lycopersicum / Q000235:genetics* / Q000254:growth & development / Q000821:virology; D005810:Multigene Family; D009154:Mutation; D010935:Plant Diseases / Q000235:genetics / Q000821:virology*; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D030821:Plants, Genetically Modified; D017800:Potyvirus / Q000472:pathogenicity*
chemical_list: D039561:Eukaryotic Initiation Factor-4E; D010940:Plant Proteins
keywords: Solanum lycopersicum; TILLING; eIF4E; natural variation; potato virus Y; potyvirus; tobacco etch virus