Revealing the Complexity of Sweepovirus-Deltasatellite–Plant Host Interactions: Expanded Natural and Experimental Helper Virus Range and Effect Dependence on Virus-Host Combination

Abstract

Sweepoviruses are begomoviruses (genus Begomovirus, family Geminiviridae) with ssDNA genomes infecting sweet potato and other species of the family Convolvulaceae. Deltasatellites (genus Deltasatellite, family Tolecusatellitidae) are small-size non-coding DNA satellites associated with begomoviruses. In this study, the genetic diversity of deltasatellites associated with sweepoviruses infecting Ipomoea indica plants was analyzed by further sampling the populations where the deltasatellite sweet potato leaf curl deltasatellite 1 (SPLCD1) was initially found, expanding the search to other geographical areas in southern continental Spain and the Canary Islands. The sweepoviruses present in the samples coinfected with deltasatellites were also fully characterized by sequencing in order to define the range of viruses that could act as helper viruses in nature. Additionally, experiments were performed to assess the ability of a number of geminivirids (the monopartite tomato leaf deformation virus and the bipartite NW begomovirus Sida golden yellow vein virus, the bipartite OW begomovirus tomato leaf curl New Delhi virus, and the curtovirus beet curly top virus) to transreplicate SPLCD1 in their natural plant hosts or the experimental host Nicotiana benthamiana. The results show that SPLCD1 can be transreplicated by all the geminivirids assayed in N. benthamiana and by tomato leaf curl New Delhi virus in zucchini. The presence of SPLCD1 did not affect the symptomatology caused by the helper viruses, and its effect on viral DNA accumulation depended on the helper virus–host plant combination.

Insights into Emerging Begomovirus–Deltasatellite Complex Diversity: The First Deltasatellite Infecting Legumes

“…Known examples are the New World Sida golden yellow vein virus (SiGYVV)/Sida golden yellow vein deltasatellite 1 (SiGYVD1) and tomato yellow leaf distortion virus/tomato yellow leaf distortion deltasatellite 2 (ToYLDD2) both in the natural malvaceous host plants and the experimental host N. benthamiana, and tomato leaf deformation virus (ToLDeV)/SiGYVD1 and ToLDeV/ToYLDD2 in N. benthamiana [40]. The same has been observed in coinfections of sweet potato leaf curl deltasatellite 1 (SPLCD1) and the bipartite Old World begomovirus tomato leaf curl New Delhi virus (ToLCNDV), the bipartite New World begomovirus SiGYVV, the monopartite New World begomovirus ToYLDeV or the curtovirus beet curly top virus in N. benthamiana; SPLCD1 and ToLCNDV in zucchini; and SPLCD1 and the sweepovirus sweet potato leaf curl virus (SPLCV) in most natural host plants [41]. Exceptions include the slight decrease in symptomatology of SPLCD1 and SPLCV observed in Ipomoea setosa and I. nil and SPLCD1 and tomato yellow leaf curl virus or tomato yellow leaf curl Sardinia virus in N. benthamiana and tomato.…”

“…The same has been observed in coinfections of sweet potato leaf curl deltasatellite 1 (SPLCD1) and the bipartite Old World begomovirus tomato leaf curl New Delhi virus (ToLCNDV), the bipartite New World begomovirus SiGYVV, the monopartite New World begomovirus ToYLDeV or the curtovirus beet curly top virus in N. benthamiana; SPLCD1 and ToLCNDV in zucchini; and SPLCD1 and the sweepovirus sweet potato leaf curl virus (SPLCV) in most natural host plants [41]. Exceptions include the slight decrease in symptomatology of SPLCD1 and SPLCV observed in Ipomoea setosa and I. nil and SPLCD1 and tomato yellow leaf curl virus or tomato yellow leaf curl Sardinia virus in N. benthamiana and tomato.…”

“…The most well-characterized deltasatellites have been naturally associated with (i) a monopartite Old World begomovirus infecting tomato in Australia [ 39 ]; (ii) bipartite begomoviruses infecting three wild malvaceous plant species in Cuba [ 35 ]; (iii) monopartite Old World begomoviruses infecting sweet potato ( Ipomoea batatas ) and I. indica (sweepoviruses) in Spain and Portugal [ 21 ]; and (iv) a sweepovirus infecting Merremia dissecta in Venezuela [ 21 ]. In some cases, deltasatellites reduce or increase the accumulation of the helper begomovirus, but rarely modify the symptoms caused by them [ 40 , 41 ].…”

High-Throughput Sequencing Identified Distinct Bipartite and Monopartite Begomovirus Variants Associated with DNA-Satellites from Tomato and Muskmelon Plants in Saudi Arabia

“…This could be a reason that in mixed infections between monopartite and bipartite begomoviruses, the DNA-B component cannot be well trans-replicated by the monopartite begomovirus genome [ 59 ]. Monopartite begomovirus associated DNA-satellites either harbor their Rep protein (alphasatellites), or are flexible in their trans-replication by the helper begomovirus, i.e., betasatellites [ 61 , 62 , 63 ].…”

Begomoviruses: what is the secret(s) of their success?

“…In most cases, deltasatellites do not affect the symptoms caused by the helper begomoviruses [57][58][59][60][61]. However, it is not unusual that they influence accumulation of the helper virus.…”