Accumulation and transmission of alphasatellite, betasatellite and tomato yellow leaf curl virus in susceptible and Ty-1 -resistant tomato plants

Abstract

Begomoviruses (family Geminiviridae) are frequently associated with alphasatellites and betasatellites in the Old World. Tomato yellow leaf curl virus, one of the most damaging begomovirus species worldwide, was recently found associated with betasatellites in the eastern coast of the Mediterranean Sea, and in the Middle East region. Tomato yellow leaf curl virus (TYLCV)/betasatellite associations were shown to increase TYLCV virulence in experimental conditions. The sustainability of TYLCV/satellite associations in tomato was assessed here by estimating accumulation levels of satellites in comparison to TYLCV, vector transmission efficiency, and by testing how far the popular Ty-1 resistance gene used in most TYLCV-resistant tomato cultivars in the Mediterranean Basin is effective against betasatellites. Three satellites previously isolated from okra in Burkina Faso-of the species Cotton leaf curl Gezira betasatellite, Cotton leaf curl Gezira alphasatellite and Okra leaf curl Burkina Faso alphasatellite-were shown to accumulate at levels similar to, or higher than, the helper virus TYLCV-Mld in tomato plants from 32 to 150 days post inoculation (dpi). Cotton leaf curl Gezira betasatellite (CLCuGB) reduced TYLCV-Mld accumulation whereas alphasatellites did not. Transmission tests were performed with B. tabaci from plants infected with TYLCV-Mld/CLCuGB- or TYLCV-Mld/Okra leaf curl Burkina Faso alphasatellite. At 32 dpi, both satellites were transmitted to more than 50% of TYLCV-infected test plants. Betasatellite transmission, tested further with 150 dpi source plants was successful in more than 30% of TYLCV-infected test plants. Ty-1 resistant tomato plants co-infected with TYLCV (-Mld or -IL) and CLCuGB exhibited mild leaf curling and mosaic symptoms at the early stage of infection associated with a positive effect on TYLCV-IL accumulation, while resistant plants infected with TYLCV only, were asymptomatic. Together with previous experimental studies, these results further emphasize the potential risk of betasatellites to tomato cultivation, including with Ty-1 resistant cultivars.

Ty‐1, a universal resistance gene against geminiviruses that is compromised by co‐replication of a betasatellite

“…Recently, Conflon et al () reported on the compromising effect of a co‐replicating betasatellite on Ty‐1 resistance. Ty‐1 tomato lines co‐infected with different TYLCV strains and a cotton leaf curl Gezira betasatellite revealed an increase in disease symptoms, but interestingly titres only increased in the mixed infection case with TYLCV‐Il, while those of TYLCV‐Mld were decreased on addition of the betasatellite.…”

The Global Dimension of Tomato Yellow Leaf Curl Disease: Current Status and Breeding Perspectives

“…In the presence of honeysuckle yellow vein mosaic betasatellite (HYVMVB), TYLCVinfected tomato plants developed more severe stunting symptoms [55]. A recent study showed that co-replication of TYLCV-IL with CLCuGB leads to a significant increase of TYLCV symptoms (Figure 4) [58]. In the Mediterranean basin and the Middle East, which are proposed to be centers of both TYLCV complex origin and diversification, the first betasatellite (i.e., CLCuGB) associated with either TYLCV-IL or TYLCV-Mld in tomato plants was identified very recently in Israel [12,21,59].…”

Frequent occurrence of Mungbean yellow mosaic India virus in tomato leaf curl disease affected tomato in Oman

“…TYLCV has been spread around the world due to the spread of the vector whitefly, the international trade in tomato seedlings and possibly even tomato fruit 4,63,64 . The fear that a disease enhancing, TYLCV-adapted betasatellite such as ToLCB could spread with the virus, has been noted previously 18,65 . The results here raise the additional possibility that other viruses, including viruses not adapted to plants of the Solanaceae such as MYMIV, could be moved around the world as a passenger to TYLCV in tomato.…”