Knock-out mutation of eukaryotic initiation factor 4E2 (eIF4E2) confers resistance to pepper veinal mottle virus in tomato

Moury, Benoît; Lebaron, Caroline; Szadkowski, Marion; Khalifa, M. Ben; Girardot, Gregory; Bi, Bolou Antoine Bolou; Koné, Daouda; Nitiema, Léon W.; Fakhfakh, H.; Gallois, Jean‐Luc

doi:10.1016/j.virol.2019.09.015

Cited by 24 publications

(18 citation statements)

References 37 publications

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“…The 1INS and 3DEL alleles significantly reduced the susceptibility to PVY N but not to PVY O (Figure 2). These results can be interpreted on the basis of previous studies in which eIF4E1 and eIF4E2 were individually or doubly knocked out or down in tomato (Mazier et al, 2011;Gauffier et al, 2016;Bastet et al, 2017;Moury et al, 2020). The previous studies indicated that PVY primarily uses eIF4E1, but most PVY strains can alternatively use eIF4E2 to promote infection when eIF4E1 is knocked out or down.…”

Section: Discussionsupporting

confidence: 58%

“…Natural antiviral alleles of eIF4E1 have been identified as pot1 and pot1 2 on chromosome 3 in tomato relatives (Ruffel et al, 2005;Lebaron et al, 2016). A knockout mutant of eIF4E2 on chromosome 2 confers resistance to pepper veinal mottle virus (Piron et al, 2010;Moury et al, 2020). Interestingly, pot1 shows a wider spectrum of resistance to members of the Potyvirus genus than does a knockout mutant of eIF4E1; in addition, it shows a similar spectrum to that of eIF4E1 and eIF4E2 double-knockout, without the growth defect seen in the double-knockout plant (Gauffier et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

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Artificially Edited Alleles of the Eukaryotic Translation Initiation Factor 4E1 Gene Differentially Reduce Susceptibility to Cucumber Mosaic Virus and Potato Virus Y in Tomato

et al. 2020

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Eukaryotic translation initiation factors, including eIF4E, are susceptibility factors for viral infection in host plants. Mutation and double-stranded RNA-mediated silencing of tomato eIF4E genes can confer resistance to viruses, particularly members of the Potyvirus genus. Here, we artificially mutated the eIF4E1 gene on chromosome 3 of a commercial cultivar of tomato (Solanum lycopersicum L.) by using CRISPR/Cas9. We obtained three alleles, comprising two deletions of three and nine nucleotides (3DEL and 9DEL) and a single nucleotide insertion (1INS), near regions that encode amino acid residues important for binding to the mRNA 5' cap structure and to eIF4G. Plants homozygous for these alleles were termed 3DEL, 9DEL, and 1INS plants, respectively. In accordance with previous studies, inoculation tests with potato virus Y (PVY; type member of the genus Potyvirus) yielded a significant reduction in susceptibility to the N strain (PVYN), but not to the ordinary strain (PVYO), in 1INS plants. 9DEL among three artificial alleles had a deleterious effect on infection by cucumber mosaic virus (CMV, type member of the genus Cucumovirus). When CMV was mechanically inoculated into tomato plants and viral coat accumulation was measured in the non-inoculated upper leaves, the level of viral coat protein was significantly lower in the 9DEL plants than in the parental cultivar. Tissue blotting of microperforated inoculated leaves of the 9DEL plants revealed significantly fewer infection foci compared with those of the parental cultivar, suggesting that 9DEL negatively affects the initial steps of infection with CMV in a mechanically inoculated leaf. In laboratory tests, viral aphid transmission from an infected susceptible plant to 9DEL plants was reduced compared with the parental control. Although many pathogen resistance genes have been discovered in tomato and its wild relatives, no CMV resistance genes have been used in practice. RNA silencing of eIF4E expression has previously been reported to not affect susceptibility to CMV in tomato. Our findings suggest that artificial gene editing can introduce additional resistance to that achieved with mutagenesis breeding, and that edited eIF4E alleles confer an alternative way to manage CMV in tomato fields.

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Section: Discussionsupporting

confidence: 58%

Section: Introductionmentioning

confidence: 99%

Artificially Edited Alleles of the Eukaryotic Translation Initiation Factor 4E1 Gene Differentially Reduce Susceptibility to Cucumber Mosaic Virus and Potato Virus Y in Tomato

et al. 2020

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“…Owing to the loss-of-function of the eIF4E protein, the plant lacks one of its most important interaction partners for bymoviruses (Wang and Krishnaswamy, 2012). That mechanism has been reported to confer broad resistance to several bymoviruses in a number of dicotyledonous plants as, for instance, cucumber, tomato and Arabidopsis (Chandrasekaran et al, 2016;Pyott et al, 2016;Atarashi et al, 2020;Moury et al, 2020). However, in a temperate cereal such as barley, the full knock-out of EIF4E was rather expected to be lethal; Yang et al (2016) screened over 2,900 wild and domesticated barley accessions and identified 65 haplotypes for HvEIF4E, of which 19 were associated with resistance to bymoviruses.…”

Section: Discussionmentioning

confidence: 99%

Targeted Knockout of Eukaryotic Translation Initiation Factor 4E Confers Bymovirus Resistance in Winter Barley

et al. 2021

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The Eukaryotic Translation Initiation Factor 4E (EIF4E) is a well-known susceptibility factor for potyvirus infections in many plant species. The barley yellow mosaic virus disease, caused by the bymoviruses Barley yellow mosaic virus (BaYMV) and Barley mild mosaic virus (BaMMV), can lead to yield losses of up to 50% in winter barley. In autumn, the roots of young barley plants are infected by the soil-borne plasmodiophoraceous parasite Polymyxa graminis L. that serves as viral vector. Upon viral establishment and systemic spreading into the upper parts of the plants, yellow mosaics occur as first symptoms on leaves. In the further course of plant development, the disease entails leaf necrosis and increased susceptibility to frost damage. Thanks to the rym4 and rym5 allelic variants of the HvEIF4E gene, more than two thirds of current European winter barley cultivars are resistant to BaYMV and BaMMV. However, several strains of BaYMV and BaMMV have already overcome rym4- and rym5-mediated resistance. Accordingly, new resistance-conferring alleles are needed for barley breeding. Therefore, we performed targeted mutagenesis of the EIF4E gene by Cas9 endonuclease in BaMMV/BaYMV-susceptible winter barley cv. “Igri”. Small insertions were generated, resulting in a shift of the translational reading frame, thereby causing the loss-of-function of EIF4E. The mutations occurred in the homozygous state already in the primary mutants. Their progeny proved invariably homozygous and fully resistant to mechanical inoculation with BaMMV. EIF4E knockout plants showed normal growth habit and produced grains, yet exhibited a yield penalty.

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“…The recognition of eIF4E as a major susceptibility factor for potyviruses led research groups to develop resistance strategies by targeting this protein factor. eIF4E mediated virus resistance has been shown in tomato (Gauffier et al, 2016;Moury et al, 2020), melon (Rodríguez-Hernández et al, 2012), plum (Wang et al, 2013), peanut (Xu et al, 2017), lettuce (Tavert-Roudet et al, 2012), potato (Cavatorta et al, 2011), peas (Bruun-Rasmussen et al, 2007 and soybean (Gao et al, 2020). Since potyviruses also interact with eIFiso4E, this protein has also been targeted for virus resistance.…”

Section: Eif4e and Virusesmentioning

confidence: 99%

“…Natural or introduced mutations in eIF4E have conferred viral resistance (Dinkova et al, 2016;Leonard, 2004;Moury et al, 2020;Nicaise et al, 2003;. Mutations on eIF4E were designed based on the recessive resistance observations in the PTE-Ta4E model and natural eIF4E resistance in pea, melon, and lettuce (German-Retana et al, 2008).…”

Section: Wheat Eif4e Mutation Designmentioning

confidence: 99%

Decoding the translation initiation mechanism of maize chlorotic mottle virus

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Knock-out mutation of eukaryotic initiation factor 4E2 (eIF4E2) confers resistance to pepper veinal mottle virus in tomato

Cited by 24 publications

References 37 publications

Artificially Edited Alleles of the Eukaryotic Translation Initiation Factor 4E1 Gene Differentially Reduce Susceptibility to Cucumber Mosaic Virus and Potato Virus Y in Tomato

Artificially Edited Alleles of the Eukaryotic Translation Initiation Factor 4E1 Gene Differentially Reduce Susceptibility to Cucumber Mosaic Virus and Potato Virus Y in Tomato

Targeted Knockout of Eukaryotic Translation Initiation Factor 4E Confers Bymovirus Resistance in Winter Barley

Decoding the translation initiation mechanism of maize chlorotic mottle virus

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