Tarsiane Mara Carneiro Barbosa

Begomoviruses cause losses in several crops around the world. Whiteflies of the Bemisia tabaci cryptic species MEAM1 and MED are efficient vectors of begomoviruses. MEAM1 has been the predominant species in Brazil since the mid‐1990s. MED was detected in Brazil in 2014, and since then, high insect infestations have been reported, mainly in greenhouse production of solanaceous crops. In this study, we compared the transmission efficiency of the begomoviruses tomato severe rugose virus (ToSRV) and tomato rugose mosaic virus (ToRMV) to tomato ( Solanum lycopersicum ) and bean golden mosaic virus (BGMV) to common bean ( Phaseolus vulgaris ) by a population of MEAM1 and four populations of MED. B . tabaci MEAM1 efficiently transmitted ToSRV and ToRMV to tomato and BGMV to common bean. B . tabaci MED populations did not transmit ToSRV and ToRMV to tomato. Only one population of B . tabaci MED transmitted BGMV with an efficiency of 3%. PCR analysis indicated that B . tabaci MED can acquire ToSRV, ToRMV and BGMV after a 24 h acquisition access period. Furthermore, some greenhouse tomato plantings from São Paulo state were surveyed for the presence of viruses and whiteflies, and B . tabaci MED were predominant, whereas begomoviruses were absent. Our results demonstrate that populations of MED from São Paulo state are inefficient vectors of begomoviruses, being able to acquire the virus but not transmit it to plants. Understanding this interaction is important and suggests that the spread of B . tabaci MED could change the epidemiological scenario of begomoviruses in areas where this insect predominates.

Mixed infection between two or more begomoviruses is commonly found in tomato fields and can affect disease outcomes by increasing symptom severity and viral accumulation compared with single infection. Viruses that affect tomato include tomato severe rugose virus (ToSRV) and tomato rugose mosaic virus (ToRMV). Previous work showed that in mixed infection, ToRMV negatively affects the infectivity and accumulation of ToSRV. ToSRV and ToRMV share a high degree of sequence identity, including cis-elements in the common region (CR) and their specific recognition sites (iteron-related domain, IRD) within the Rep gene. Here, we investigated if divergent sites in the CR and IRD are involved in the interaction between these two begomoviruses. ToSRV clones were constructed containing the same nucleotides as ToRMV in the CR (ToSRV-A_(ToR:CR)), IRD (ToSRV-A_(ToR:IRD)) and in both regions (ToSRV-A_(ToR:CR+IRD)). When plants were co-inoculated with ToRMV and ToSRV-A_(ToR:IRD), the infectivity and accumulation of ToSRV were negatively affected. In mixed inoculation of ToRMV with ToSRV-A_(ToR:CR), high infectivity of both viruses and high DNA accumulation of ToSRV-A_(ToR:CR) were observed. A decrease in viral accumulation was observed in plants inoculated with ToSRV-A_(ToR:CR+IRD). These results indicate that differences in the CR, but not the IRD, are responsible for the negative interference of ToRMV on ToSRV.

Begomoviruses can be found in association with alphasatellites, which are capable of autonomous replication but are dependent on the helper begomovirus for systemic infection, encapsidation and vector transmission. Previous studies suggest that the presence of NW alphasatellites (genus Clecrusatellite) is associated with more severe symptoms. To better understand this interaction, we investigated the effects of two alphasatellites on infectivity, symptom development, viral DNA accumulation and vector transmission of three begomoviruses in three hosts. In tomato and Nicotiana benthamiana, all combinations were infectious. In Leonurus sibiricus, only the ToYSV/ToYSA combination was infectious. The presence of EuYMA increased symptom severity of EuYMV and ToYSV in N. benthamiana, and the presence of ToYSA was associated with more severe symptoms of ToYSV in N. benthamiana and L. sibiricus. EuYMA increased the accumulation of ToYSV in N. benthamiana but reduced the accumulation of EuYMV in tomato and of ToSRV in N. benthamiana. The presence of ToYSA decreased the accumulation of ToYSV in N. benthamiana and L. sibiricus. ToYSA negatively affected transmission of ToSRV by Bemisia tabaci MEAM1. Together, our results indicate that NW alphasatellites can interact with different begomoviruses, increasing symptom severity and interfering in the transmission of the helper begomovirus. Understanding this interaction is important as it may affect the emergence of diseases caused by begomovirus–alphasatellite complexes in the field.