Integration of Ty-1/Ty-3 and Ty-6 confers improved and durable resistance to highly pathogenic begomoviruses in tomato

Abstract

Begomoviruses are among the most destructive pathogens of tomato worldwide, and the introgression of Ty-genes in tomato is a key strategy for disease management. However, a single Ty-gene often provides incomplete protection against highly virulent begomovirus species. Here, commercial tomato cultivars and a series of breeding lines previously developed by the World Vegetable Center (WorldVeg) were inoculated with one of three begomovirus species that differed in virulence. The presence of Ty-1, Ty-2, Ty-3, Ty-3a, ty-5, and Ty-6 was validated using in-gene markers. Tomato plants carrying only Ty-2 were susceptible to all viruses, whereas those with Ty-1 were resistant to a less-virulent begomovirus, but susceptible to more-virulent viruses. Among the seven WorldVeg’s breeding lines, AVTO1919 (Ty-1/Ty-1, Ty-6/Ty-6) and AVTO1920 (Ty-3/Ty-3, Ty-6/Ty-6) were symptomless in most cases and the lowest viral DNA accumulation across all lines tested indicating strong begomovirus resistance. The resistance of AVTO1919 was comparable to or greater than that of AVTO1701, a line homozygous for Ty-2, Ty-3, ty-5, and Ty-6. Furthermore, F₁ plants derived from crosses between AVTO1919 or AVTO1920 and susceptible Moneymaker exhibited reduced disease tolerance, indicating the resistance conferred by Ty-1 or Ty-3 and Ty-6 is incomplete dominance. These results demonstrate that Ty-1/Ty-3 and Ty-6 integration in homozygous states can provide robust and broad-spectrum resistance to begomoviruses and is a valuable strategy for breeding durable resistant tomato cultivars.