A Novel Route Controlling Begomovirus Resistance by the Messenger RNA Surveillance Factor Pelota

Abstract

Tomato yellow leaf curl virus (TYLCV) is a devastating disease of tomato (Solanum lycopersicum) that can be effectively controlled by the deployment of resistant cultivars. The TYLCV-resistant line TY172 carries a major recessive locus for TYLCV resistance, designated ty-5, on chromosome 4. In this study, the association between 27 polymorphic DNA markers, spanning the ty-5 locus, and the resistance characteristics of individual plants inoculated with TYLCV in 51 segregating recombinant populations were analyzed. These analyses localized ty-5 into a 425 bp region containing two transversions: one in the first exon of a gene encoding the tomato homolog of the messenger RNA surveillance factor Pelota (Pelo), and a second in its proximal promoter. Analyses of susceptible and resistant lines revealed that the relative transcript level of the gene remained unchanged, regardless of whether the plants were infected with TYLCV or not. This suggests that the polymorphism discovered in the coding region of the gene controls the resistance. Silencing of Pelo in a susceptible line rendered the transgenic plants highly resistant, while in the resistant line TY172 had no effect on symptom development. In addition, over-expression of the susceptible allele of the gene in the resistant TY172 line rendered it susceptible, while over-expression of the resistant allele in susceptible plants had no effect. These results confirm that Pelo is the gene controlling resistance at the ty-5 locus. Pelo, implicated in the ribosome recycling-phase of protein synthesis, offers an alternative route to promote resistance to TYLCV and other viruses.

Fig 1. Association between DNA markers spanning the ty-5 locus and disease severity in representative segregating populations.

In the ruler presented to the left of each analysis: yellow-shaded markers are homozygous for the allele originated from the susceptible line M-82 (SS), red-shaded markers are homozygous for the allele originated from the resistant line TY172 (RR) and gray-shaded markers are heterozygous (SR); the analysis of variance presented at the bottom of each population was carried out with different markers: the marker in red asterisks is the one that was used as an independent variable in each analysis; different superscript letters above means indicate statistically significant difference, P<0.05, between genotypes for each population separately; A-D: four different representative segregating populations; DSI (disease severity index) was determined at 28 DPI (days post inoculation) and at 42 DPI, the DSI values presented is an average of both readings.

Fig 2. Amino-acid sequence of the Pelo gene in the resistant TY172 line compared to the susceptible line M-82.

The substitution of Valine¹⁶ (susceptible lines) to a Glycine (resistant TY172 line) is highlighted with magenta; GenBank accession numbers for TY172 and M-82 are KC447285 and KC447286, respectively.