Within-Host Dynamics of the Emergence of Tomato Yellow Leaf Curl Virus Recombinants

Abstract

Tomato yellow leaf curl virus (TYLCV) is a highly damaging begomovirus native to the Middle East. TYLCV has recently spread worldwide, recombining with other begomoviruses. Recent analysis of mixed infections between TYLCV and Tomato leaf curl Comoros begomovirus (ToLCKMV) has shown that, although natural selection preserves certain co-evolved intra-genomic interactions, numerous and diverse recombinants are produced at 120 days post-inoculation (dpi), and recombinant populations from different tomato plants are very divergent. Here, we investigate the population dynamics that lead to such patterns in tomato plants co-infected with TYLCV and ToLCKMV either by agro-inoculation or using the natural whitefly vector Bemisia tabaci. We monitored the frequency of parental and recombinant genotypes independently in 35 plants between 18 and 330 dpi and identified 177 recombinants isolated at different times. Recombinants were detected from 18 dpi and their frequency increased over time to reach about 50% at 150 dpi regardless of the inoculation method. The distribution of breakpoints detected on 96 fully sequenced recombinants was consistent with a continuous generation of new recombinants as well as random and deterministic effects in their maintenance. A severe population bottleneck of around 10 genomes was estimated during early systemic infection–a phenomenon that could account partially for the heterogeneity in recombinant patterns observed among plants. The detection of the same recombinant genome in six of the thirteen plants analysed beyond 30 dpi supported the influence of selection on observed recombination patterns. Moreover, a highly virulent recombinant genotype dominating virus populations within one plant has, apparently, the potential to be maintained in the natural population according to its infectivity, within-host accumulation, and transmission efficiency - all of which were similar or intermediate to those of the parent genotypes. Our results anticipate the outcomes of natural encounters between TYLCV and ToLCKMV.

Distribution and diversity of begomoviruses in tomato and sweet pepper plants in Costa Rica

“…The begomoviruses were highly host‐specific, with different virus species detected in tomato or pepper and a wider diversity observed in tomato (ToLCSiV, TYLCV and ToYMoV) than in sweet pepper (PepGMV) (Table ). Mixed infection of begomoviruses was observed in only one case, in contrast to results obtained from surveys conducted in other countries (Davino et al, ; Urbino et al, ). Thus, only one single mixed infection was detected, with co‐infection of ToLCSiV and ToYMoV in a tomato sample from the Grecia region (Table S1).…”

Environmental nutrient supply alters prevalence and weakens competitive interactions among coinfecting viruses

“…A general framework for understanding the mechanisms governing plant pathogen communities would be an important advance because the interactions among coinfecting pathogens can regulate the vital rates of individual plants, the evolution of populations and the interactions among plant species within a community (Malmstrom et al, 2005b;Borer et al, 2007;Seabloom et al, 2009). In addition, within-host intra-and interspecific parasite interactions can alter pathogen genetic recombination, transmission rates, emergence of new variants or species, host mortality, and virulence evolution (Lal et al, 1994;Miller & Rasochova, 1997;Kamal et al, 2001;Lello et al, 2004;Pedersen & Fenton, 2007;Rigaud et al, 2010;Alizon, 2013;Betancourt et al, 2013;Hall & Little, 2013;Salvaudon et al, 2013;Urbino et al, 2013). A general understanding of the effects of host resource supply on microbial interactions and disease dynamics in plant hosts is particularly relevant given the dramatic increase in the flux of nutrients in global biogeochemical cycles caused by human-induced changes and the increasing use of nutrients in agriculture (Tilman et al, 2001;Rockstrom et al, 2009;V€ or€ osmarty et al, 2010).…”

Mapping genetic determinants of viral traits with FST and quantitative trait locus (QTL) approaches

“…When viruses are prone to recombination as Begomovirus (Martin et al, 2011;Urbino et al, 2013), Caulimovirus (Froissart et al, 2005) or Coronavirus (Baric et al, 1990), a library can be generated in a host co-infected with representatives of two parental species or strains. As selection and genetic drift may reduce the diversity of recombinant genomes, it may be recommended to isolate recombinant genomes as soon as possible after co-infection; for begomoviruses it was reported that 50% of the genomes were recombinant from 120 days post inoculation (Martin et al, 2011;Urbino et al, 2013;García-Andrés et al, 2007). An early isolation of the recombinant genomes may also limit the frequency of random mutations.…”