A <scp>TILLING</scp> approach to generate broad‐spectrum resistance to potyviruses in tomato is hampered by <i>eIF4E</i> gene redundancy

Gauffier, Camille; Lebaron, Caroline; Moretti, A.; Constant, Carole; Moquet, Frédéric; Bonnet, Grégori; Caranta, Carole; Gallois, Jean‐Luc

doi:10.1111/tpj.13136

Cited by 80 publications

(107 citation statements)

References 64 publications

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“…In addition, the mRNA expression level of another copy is positively correlated with resistance durability. Taken together these results show that va ‐mediated resistance durability can be explained by redundancy/competition effects between members of the eIF4E gene family, parallel to what was recently shown in tomato (Gauffier et al , ).…”

Section: Introductionsupporting

confidence: 84%

“…A compatible eIF4E isoform is required by potyviruses for their genome translation, replication, stabilization, and intercellular and systemic transport (Contreras‐Paredes et al , ; Robaglia and Caranta, ; Sanfaçon, ; Wang and Krishnaswamy, ). Some potyviruses can also use several eIF4E isoforms in a given host (Gauffier et al , ; Jenner et al , ; Mazier et al , ; Xu et al , ). This suggests that in the absence of a functional eIF4E‐1 in va ‐resistant genotypes, RB PVY variants may use another eIF4E isoform, similar to the situation when TuMV overcomes an eIFiso4E loss‐of‐function in Arabidopsis through VPg mutations allowing recruitment of eIF4E1 (Bastet et al , ; Gallois et al , ).…”

Section: Discussionmentioning

confidence: 99%

“…In tobacco cv Samsun, the depletion of eIF(iso)4E by an antisense down‐regulation strategy resulted in a compensatory increase in eIF4E protein levels (Combe et al , ), while in Brassica rapa , overexpression of an eIFiso4E transgene induces the expression of endogenous eIF4E (Kim et al , ), revealing another regulation mechanism. In tomato, it has also been suggested that protein–protein interactions between eIF4E‐1 and eIF4E‐2 lead to a yet unexplained eIF4E‐2 degradation (Gauffier et al , ). In such a scenario, the deletion of eIF4E‐1 , the loss of eIF4E‐3 and the presence of eIF4E‐ 2‐3 could all contribute, alone or in combination, to the overexpression of eIF4E‐2 .…”

Section: Discussionmentioning

confidence: 99%

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A complex eIF4E locus impacts the durability of va resistance to Potato virus Y in tobacco

Michel

Julio²,

Candresse

et al. 2019

Molecular Plant Pathology

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Summary Many recessive resistances against potyviruses are mediated by eukaryotic translation initiation factor 4E (eIF4E). In tobacco, the va resistance gene commonly used to control Potato virus Y (PVY) corresponds to a large deletion affecting the eIF4E‐1 gene on chromosome 21. Here, we compared the resistance durability conferred by various types of mutations affecting eIF4E‐1 (deletions of various sizes, frameshift or nonsense mutations). The ‘large deletion’ genotypes displayed the broadest and most durable resistance, whereas frameshift and nonsense mutants displayed a less durable resistance, with rapid and frequent apparition of resistance‐breaking variants. In addition, genetic and transcriptomic analyses revealed that resistance durability is strongly impacted by a complex genetic locus on chromosome 14, which contains three other eIF4E genes. One of these, eIF4E‐3 , is rearranged as a hybrid gene between eIF4E‐2 and eIF4E‐3 ( eIF4E‐ 2‐3 ) in the genotypes showing the most durable resistance, while eIF4E‐2 is differentially expressed between the tested varieties. RNA‐seq and quantitative reverse transcriptase‐polymerase chain reaction experiments demonstrated that eIF4E‐2 expression level is positively correlated with resistance durability. These results suggest that besides the nature of the mutation affecting eIF4E‐1 , three factors linked with a complex locus may potentially impact va durability: loss of an integral eIF4E‐3 , presence of eIF4E‐ 2‐3 and overexpression of eIF4E‐2. This latter gene might act as a decoy in a non‐productive virus–plant interaction, limiting the ability of PVY to evolve towards resistance breaking. Taken together, these results show that va resistance durability can in large part be explained by complex redundancy effects in the eIF4E gene family.

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Section: Introductionsupporting

confidence: 84%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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A complex eIF4E locus impacts the durability of va resistance to Potato virus Y in tobacco

Michel

Julio²,

Candresse

et al. 2019

Molecular Plant Pathology

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“…TILLING has been commonly employed in many organisms (McCallum et al, 2000; Meksem et al, 2008; Moens et al, 2008; Dierking and Bilyeu, 2009; Colasuonno et al, 2016; Gauffier et al, 2016; Nida et al, 2016). To perform TILLING, a mutagenized population is developed using a chemical mutagen such as ethyl methanesulfonate (EMS).…”

Section: Introductionmentioning

confidence: 99%

Characterization of the FAD2 Gene Family in Soybean Reveals the Limitations of Gel-Based TILLING in Genes with High Copy Number

et al. 2017

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Soybean seed oil typically contains 18–20% oleic acid. Increasing the content of oleic acid is beneficial for health and biodiesel production. Mutations in FAD2-1 genes have been reported to increase seed oleic acid content. A subset of 1,037 mutant families from a mutagenized soybean cultivar (cv.) Forrest population was screened using reverse genetics (TILLING) to identify mutations within FAD2 genes. Although no fad2 mutants were identified using gel-based TILLING, four fad2-1A and one fad2-1B mutants were identified to have high seed oleic acid content using forward genetic screening and subsequent target sequencing. TILLING has been successfully used as a non-transgenic reverse genetic approach to identify mutations in genes controlling important agronomic traits. However, this technique presents limitations in traits such as oil composition due to gene copy number and similarities within the soybean genome. In soybean, FAD2 are present as two copies, FAD2-1 and FAD2-2. Two FAD2-1 members: FAD2-1A and FAD2-1B; and three FAD2-2 members: FAD2-2A, FAD2-2B, and FAD2-2C have been reported. Syntenic, phylogenetic, and in silico analysis revealed two additional members constituting the FAD2 gene family: GmFAD2-2D and GmFAD2-2E, located on chromosomes 09 and 15, respectively. They are presumed to have diverged from other FAD2-2 members localized on chromosomes 19 (GmFAD2-2A and GmFAD2-2B) and 03 (GmFAD2-2C). This work discusses alternative solutions to the limitations of gel-based TILLING in functional genomics due to high copy number and multiple paralogs of the FAD2 gene family in soybean.

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“…It had been shown that engineering mutations in the host plant eIF4E through the use of the Targeting-Induced Local Lesions in Genome (TILLING) strategy could provide resistance against potyviruses in a range of plants (Julio et al, 2015; Gauffier et al, 2016). The CRISPR-Cas9 sgRNA system has now been used to efficiently inactivate these genes and generate virus-resistant plants (Chandrasekaran et al, 2016; Pyott et al, 2016).…”

Section: Genome Editing Using the Crispr-cas9 System In Plant Virologymentioning

confidence: 99%

Next-Generation Sequencing and Genome Editing in Plant Virology

et al. 2016

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Next-generation sequencing (NGS) has been applied to plant virology since 2009. NGS provides highly efficient, rapid, low cost DNA, or RNA high-throughput sequencing of the genomes of plant viruses and viroids and of the specific small RNAs generated during the infection process. These small RNAs, which cover frequently the whole genome of the infectious agent, are 21–24 nt long and are known as vsRNAs for viruses and vd-sRNAs for viroids. NGS has been used in a number of studies in plant virology including, but not limited to, discovery of novel viruses and viroids as well as detection and identification of those pathogens already known, analysis of genome diversity and evolution, and study of pathogen epidemiology. The genome engineering editing method, clustered regularly interspaced short palindromic repeats (CRISPR)-Cas9 system has been successfully used recently to engineer resistance to DNA geminiviruses (family, Geminiviridae) by targeting different viral genome sequences in infected Nicotiana benthamiana or Arabidopsis plants. The DNA viruses targeted include tomato yellow leaf curl virus and merremia mosaic virus (begomovirus); beet curly top virus and beet severe curly top virus (curtovirus); and bean yellow dwarf virus (mastrevirus). The technique has also been used against the RNA viruses zucchini yellow mosaic virus, papaya ringspot virus and turnip mosaic virus (potyvirus) and cucumber vein yellowing virus (ipomovirus, family, Potyviridae) by targeting the translation initiation genes eIF4E in cucumber or Arabidopsis plants. From these recent advances of major importance, it is expected that NGS and CRISPR-Cas technologies will play a significant role in the very near future in advancing the field of plant virology and connecting it with other related fields of biology.

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A TILLING approach to generate broad‐spectrum resistance to potyviruses in tomato is hampered by eIF4E gene redundancy

Cited by 80 publications

References 64 publications

A complex eIF4E locus impacts the durability of va resistance to Potato virus Y in tobacco

A complex eIF4E locus impacts the durability of va resistance to Potato virus Y in tobacco

Characterization of the FAD2 Gene Family in Soybean Reveals the Limitations of Gel-Based TILLING in Genes with High Copy Number

Next-Generation Sequencing and Genome Editing in Plant Virology

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