Begomovirus populations in single plants are complex and may include both well-adapted and poorly-adapted viruses.

Begomoviruses (single-stranded DNA plant viruses transmitted by whiteflies) are economically important pathogens causing epidemics worldwide. Tomato-infecting begomoviruses emerged in Brazil in the 1990's following the introduction of Bemisia tabaci Middle East-Asia Minor 1. It is believed that these viruses evolved from indigenous viruses infecting non-cultivated hosts. However, tomato-infecting viruses are rarely found in non-cultivated hosts, and vice-versa. It is possible that viral populations in a given host are composed primarily of viruses which are well adapted to this host, but also include a small proportion of poorly adapted viruses. Following transfer to a new host, the composition of the viral population would shift rapidly, with the viruses which are better adapted to the new host becoming predominant. To test this hypothesis, we collected tomato and Sida plants growing next to each other at two locations in 2014 and 2018. Total DNA was extracted from tomato and Sida samples from each location and year and used as a template for high-throughput sequencing. Reads were mapped following a highly stringent set of criteria. For the 2014 samples, >98% of the Sida reads mapped to Sida micrantha mosaic virus (SiMMV), but 0.1% of the reads mapped to tomato severe rugose virus (ToSRV). Conversely, >99% of the tomato reads mapped to ToSRV, with 0.18% mapping to SiMMV. For the 2018 samples, 41% of the Sida reads mapped to three Sida-adapted viruses and 0.1% of the reads mapped to ToSRV, while 99.9% of the tomato reads mapped to ToSRV. These results are consistent with the hypothesis that viral populations in a single plant are composed primarily of the virus that is better adapted to the host but also include a small proportion of viruses that are poorly adapted.

Evolutionary dynamics of bipartite begomoviruses revealed by complete genome analysis.

Several key evolutionary events marked the evolution of geminiviruses, culminating with the emergence of divided (bipartite) genomes represented by viruses classified in the genus Begomovirus. This genus represents the most abundant group of multipartite viruses, contributing significantly to the observed abundance of multipartite species in the virosphere. Although aspects related to virus-host interactions and evolutionary dynamics have been extensively studied, the bipartite nature of these viruses has been little explored in evolutionary studies. Here, we performed a parallel evolutionary analysis of the DNA-A and DNA-B segments of New World begomoviruses. A total of 239 full-length DNA-B sequences obtained in this study, combined with 292 DNA-A and 76 DNA-B sequences retrieved from GenBank, were analysed. The results indicate that the DNA-A and DNA-B respond differentially to evolutionary processes, with the DNA-B being more permissive to variation and more prone to recombination than the DNA-A. Although a clear geographic segregation was observed for both segments, differences in the genetic structure between DNA-A and DNA-B were also observed, with cognate segments belonging to distinct genetic clusters. DNA-B coding regions evolve under the same selection pressures than DNA-A coding regions. Together, our results indicate an interplay between reassortment and recombination acting at different levels across distinct subpopulations and segments.

Transmission of the Bean-Associated Cytorhabdovirus by the Whitefly Bemisia tabaci MEAM1.

The knowledge of genomic data of new plant viruses is increasing exponentially; however, some aspects of their biology, such as vectors and host range, remain mostly unknown. This information is crucial for the understanding of virus-plant interactions, control strategies, and mechanisms to prevent outbreaks. Typically, rhabdoviruses infect monocot and dicot plants and are vectored in nature by hemipteran sap-sucking insects, including aphids, leafhoppers, and planthoppers. However, several strains of a potentially whitefly-transmitted virus, papaya cytorhabdovirus, were recently described: (i) bean-associated cytorhabdovirus (BaCV) in Brazil, (ii) papaya virus E (PpVE) in Ecuador, and (iii) citrus-associated rhabdovirus (CiaRV) in China. Here, we examine the potential of the Bemisia tabaci Middle East-Asia Minor 1 (MEAM1) to transmit BaCV, its morphological and cytopathological characteristics, and assess the incidence of BaCV across bean producing areas in Brazil. Our results show that BaCV is efficiently transmitted, in experimental conditions, by B. tabaci MEAM1 to bean cultivars, and with lower efficiency to cowpea and soybean. Moreover, we detected BaCV RNA in viruliferous whiteflies but we were unable to visualize viral particles or viroplasm in the whitefly tissues. BaCV could not be singly isolated for pathogenicity tests, identification of the induced symptoms, and the transmission assay. BaCV was detected in five out of the seven states in Brazil included in our study, suggesting that it is widely distributed throughout bean producing areas in the country. This is the first report of a whitefly-transmitted rhabdovirus.

Discovery of the first maize-infecting mastrevirus in the Americas using a vector-enabled metagenomics approach.

The genus Mastrevirus (family Geminiviridae) is composed of single-stranded DNA viruses that infect mono- and dicotyledonous plants and are transmitted by leafhoppers. In South America, there have been only two previous reports of mastreviruses, both identified in sweet potatoes (from Peru and Uruguay). As part of a general viral surveillance program, we used a vector-enabled metagenomics (VEM) approach and sampled leafhoppers (Dalbulus maidis) in Itumbiara (State of Goiás), Brazil. High-throughput sequencing of viral DNA purified from the leafhopper sample revealed mastrevirus-like contigs. Using a set of abutting primers, a 2746-nt circular genome was recovered. The circular genome has a typical mastrevirus genome organization and shares <63% pairwise identity with other mastrevirus isolates from around the world. Therefore, the new mastrevirus was tentatively named "maize striate mosaic virus". Seventeen maize leaf samples were collected in the same field as the leafhoppers, and ten samples were found to be positive for this mastrevirus. Furthermore, the ten genomes recovered from the maize samples share >99% pairwise identity with the one from the leafhopper. This is the first report of a maize-infecting mastrevirus in the Americas, the first identified in a non-vegetatively propagated mastrevirus host in South America, and the first mastrevirus to be identified in Brazil.