Pepper yellow leaf curl disease caused by begomoviruses seriously affects pepper (Capsicum spp.) production in a number of regions around the world. Ty genes of tomato, which confer resistance to the tomato yellow leaf curl virus, are the only begomovirus resistance genes cloned to date. In this study, we focused on the identi cation of begomovirus resistance genes in Capsicum annuum. BaPep-5 was identi ed as a novel source of resistance against pepper yellow leaf curl Indonesia virus (PepYLCIV) and pepper yellow leaf curl Aceh virus (PepYLCAV). A single recessive locus, which we named as pepper yellow leaf curl disease virus resistance 1 (pepy-1), responsible for PepYLCAV resistance in BaPep-5 was identi ed on chromosome 5 in an F 2 population derived from a cross between BaPep-5 and the begomovirus susceptible accession BaPep-4. In the target region spanning 34 kb, a single candidate gene, the messenger RNA surveillance factor Pelota, was identi ed. Whole-genome resequencing of BaPep-4 and BaPep-5 and comparison of their genomic DNA sequences revealed a single nucleotide polymorphism (A to G) located at the splice site of the 9th intron of CaPelota in BaPep-5, which caused the insertion of the 9th intron into the transcript, resulting in the addition of 28 amino acids to CaPelota protein without causing a frameshift. Virus-induced gene silencing of CaPelota in the begomovirus susceptible pepper No.218 resulted in the gain of resistance against PepYLCIV, a phenotype consistent with BaPep-5. The DNA marker developed in this study will greatly facilitate marker-assisted breeding of begomovirus resistance in peppers.

Pepper yellow leaf curl disease (PepYLCD) caused by begomoviruses is one of the most devastating diseases affecting pepper (Capsicum spp.) production worldwide. In our previous study, a loss-of-function allele, pepy-1, encoding messenger RNA surveillance factor Pelota was identified as a begomovirus resistance gene from a C. annuum cultivar BaPep-5. In this study, to investigate the effectiveness of pepy-1 conferred resistance against begomovirus in the field, we conducted a three-year evaluation under natural field conditions in Indonesia. The lowest PepYLCD incidence and significantly higher fruit productivity were observed in BaPep-5 when compared to six other commonly cultivated pepper cultivars. The subsequent comparison between BaPep-5 and the susceptible BaPep-4 showed that pepy-1 slowed down the disease onset and progression, resulting in a higher fruit productivity trait in the field. Multiple comparison analyses using an F 2 population obtained by crossing BaPep-5 with BaPep-4 showed that the pepy-1 homozygous individuals had significantly higher fruit productivity, twice than those of the Pepy-1 homozygous or heterozygous individuals. In conclusion, the introgression of pepy-1 is effective to reduce the economic loss of pepper fruit production under natural field infection of begomoviruses.

Pepper yellow leaf curl disease caused by begomoviruses seriously affects pepper (Capsicum spp.) production in a number of regions around the world. Ty genes of tomato, which confer resistance to the tomato yellow leaf curl virus, are the only begomovirus resistance genes cloned to date. In this study, we focused on the identification of begomovirus resistance genes in Capsicum annuum. BaPep-5 was identified as a novel source of resistance against pepper yellow leaf curl Indonesia virus (PepYLCIV) and pepper yellow leaf curl Aceh virus (PepYLCAV). A single recessive locus, which we named as pepper yellow leaf curl disease virus resistance 1 (pepy-1), responsible for PepYLCAV resistance in BaPep-5 was identified on chromosome 5 in an F2 population derived from a cross between BaPep-5 and the begomovirus susceptible accession BaPep-4. In the target region spanning 34 kb, a single candidate gene, the messenger RNA surveillance factor Pelota, was identified. Whole-genome resequencing of BaPep-4 and BaPep-5 and comparison of their genomic DNA sequences revealed a single nucleotide polymorphism (A to G) located at the splice site of the 9th intron of CaPelota in BaPep-5, which caused the insertion of the 9th intron into the transcript, resulting in the addition of 28 amino acids to CaPelota protein without causing a frameshift. Virus-induced gene silencing of CaPelota in the begomovirus susceptible pepper No.218 resulted in the gain of resistance against PepYLCIV, a phenotype consistent with BaPep-5. The DNA marker developed in this study will greatly facilitate marker-assisted breeding of begomovirus resistance in peppers.