Abstract
Knowledge about the host range and genetic structure of emerging plant viruses provides insights into fundamental ecological and evolutionary processes, and from an applied perspective, facilitates the design and implementation of sustainable disease control measures. Tomato leaf curl New Delhi virus (ToLCNDV) is an emerging whitefly transmitted begomovirus that is rapidly spreading and inciting economically important diseases in cucurbit crops of the Mediterranean basin. Genetic characterization of the ToLCNDV Mediterranean populations has shown that they are monophyletic in cucurbit plants. However, the extent to which other alternative (cultivated and wild) hosts may affect ToLCNDV genetic population structure and virus prevalence remains unknown. In this study a total of 683 samples from 13 cultivated species, and 203 samples from 24 wild species from three major cucurbit-producing areas of Spain (Murcia, Alicante and Castilla-La Mancha) from five cropping seasons (2012–2016) were analyzed for ToLCNDV infection. Except for watermelon, ToLCNDV was detected in all cultivated-cucurbit species as well as in tomato. Among weeds, Ecballium elaterium, Datura stramonium, Sonchus oleraceus, and Solanum nigrum were identified as alternative ToLCNDV plant hosts, which could act as new potential sources of virus inoculum. Furthermore, we performed full-genome deep-sequencing of 80 ToLCNDV isolates from different hosts, location and cropping year. Our phylogenetic analysis supports a Mediterranean virus population that is genetically very homogeneous, with no clustering pattern, and clearly different from Asian virus populations. Additionally, D. stramonium displayed higher levels of within-host genetic diversity than cultivated plants, and this variability appeared to increase with time. These results suggest that the potential ToLCNDV adaptive evolution occurring in wild plant hosts could serve as a source of virus genetic variability, thereby affecting the genetic structure and spatial-temporal dynamics of the viral population.
Highlights
Emerging infectious diseases among cultivated plant species represents a serious threat to food sustainability (Woolhouse et al, 2005; Cleaveland et al, 2007; Jones, 2009)
From the first identification of tomato leaf curl New Delhi virus (ToLCNDV) in cucurbit crops in Spain in 2012, several outbreaks have emerged in cucurbitproducing areas, which have been mainly distributed over greenhouses and open-fields in the South, Central and East areas of Spain
Despite the watermelon plant surveys being conducted in crop fields close to other cucurbit crops with high whitefly populations, that is, under high natural inoculum pressure, ToLCNDV was not detected in any watermelon samples
Summary
Emerging infectious diseases among cultivated plant species represents a serious threat to food sustainability (Woolhouse et al, 2005; Cleaveland et al, 2007; Jones, 2009). These diseases are described as the appearance of an unknown pathogen in a particular plant species, or an already-known pathogen that increases its incidence or arises in a new geographical area often accompanied by drastic reductions in both fruit quality and yield, usually as a consequence of the lack of effective countermeasures (Woolhouse and Gowtage-Sequeria, 2005; Woolhouse et al, 2005; Cleaveland et al, 2007; Woolhouse, 2008; Vurro et al, 2010). It is necessary to determine the range of natural hosts and to examine the genetic diversity and structure of ToLCNDV populations, as this knowledge could help improve the design of an integrated disease management program to reduce the source of the inoculum and the spread of this virus
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