Entry of bunyaviruses into plants and vectors

Chen, Yuting; Dessau, Moshe; Rotenberg, Dorith; Rasmussen, David A.; Whitfield, Anna E.

doi:10.1016/bs.aivir.2019.07.001

Cited by 21 publications

(23 citation statements)

References 140 publications

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“…Although one might expect to see similar bottlenecks within thrips as the virus must traverse through the midgut to the salivary glands before transmission can occur 28 , we found that genetic diversity tended to increase slightly in thrips, although not to a statistically significant level. We may have failed to detect bottlenecks in thrips as multiple insects were sampled and then pooled at a single time point to obtain enough RNA for sequencing.…”

Section: Discussioncontrasting

confidence: 56%

Evolutionary dynamics of Tomato spotted wilt virus within and between alternate plant hosts and thrips

Ruark-Seward

Bonville

Kennedy

et al. 2020

Sci Rep

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Tomato spotted wilt virus (TSWV) is a generalist pathogen with one of the broadest known host ranges among RNA viruses. To understand how TSWV adapts to different hosts, we experimentally passaged viral populations between two alternate hosts, Emilia sochifolia and Datura stramonium, and an obligate vector in which it also replicates, western flower thrips (Frankliniella occidentalis). Deep sequencing viral populations at multiple time points allowed us to track the evolutionary dynamics of viral populations within and between hosts. High levels of viral genetic diversity were maintained in both plants and thrips between transmission events. Rapid fluctuations in the frequency of amino acid variants indicated strong host-specific selection pressures on proteins involved in viral movement (NSm) and replication (RdRp). While several genetic variants showed opposing fitness effects in different hosts, fitness effects were generally positively correlated between hosts indicating that positive rather than antagonistic pleiotropy is pervasive. These results suggest that high levels of genetic diversity together with the positive pleiotropic effects of mutations have allowed TSWV to rapidly adapt to new hosts and expand its host range.

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Section: Discussioncontrasting

confidence: 56%

Evolutionary dynamics of Tomato spotted wilt virus within and between alternate plant hosts and thrips

Ruark-Seward

Bonville

Kennedy

et al. 2020

Sci Rep

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“…Orthotospoviruses are transmitted by thrips in a persistent, propagative manner and can replicate in both plant hosts and thrips vectors. Bunyaviruses, as well as reoviruses and rhabdoviruses that are transmitted in a propagative manner, can replicate in organisms belonging to two kingdoms [58], and they are hypothesized to have originated from animal-infecting viruses that acquired the ability to infect plants via the acquisition of "movement proteins", the key proteins necessary for virus cell-to-cell movement in plants [59]. This evolutionary history and the longer association of thrips and orthotospoviruses [10] could explain why a narrower bottleneck is constituted by thrips transmission, as well as the fact that viruses need to pass more barriers in insects to arrive to the salivary glands than in plants, where each cell is equally available for acquisition and transmission.…”

Section: Discussionmentioning

confidence: 99%

“…This evolutionary history and the longer association of thrips and orthotospoviruses [10] could explain why a narrower bottleneck is constituted by thrips transmission, as well as the fact that viruses need to pass more barriers in insects to arrive to the salivary glands than in plants, where each cell is equally available for acquisition and transmission. Interestingly, TSWV enters through the thrips epithelial cells of the midgut anterior region [60], but how virions reach the salivary glands remains unknown [58].…”

Section: Discussionmentioning

confidence: 99%

Thrips as the Transmission Bottleneck for Mixed Infection of Two Orthotospoviruses

Zhao

Rosa

2020

Plants

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Mixed infections provide opportunities for viruses to increase genetic diversity by facilitating genomic reassortment or recombination, and they may lead to the emergence of new virus species. Mixed infections of two economically important orthotospoviruses, Tomato spotted wilt orthotospovirus (TSWV) and Impatiens necrotic spot orthotospovirus (INSV), were found in recent years, but no natural reassortants between INSV and TSWV were ever reported. The goal of this study was to establish how vector preferences and the ability to transmit INSV and TSWV influence transmission and establishment of mixed infections. Our results demonstrate that thrips prefer to oviposit on TSWV and INSV mixed-infected plants over singly infected or healthy plants, providing young nymphs with the opportunity to acquire both viruses. Conversely, we observed that thrips served as a bottleneck during transmission and favored transmission of one of the two viruses over the second one, or over transmission of both viruses simultaneously. This constraint was relaxed in plants, when transmission of TSWV and INSV occurred sequentially, demonstrating that plants serve as orthotospovirus permissive hosts, while thrips serve as a bottleneck. Viral fitness, as measured by virus replication, transmission, and competition with other viral strains, is not well studied in mixed infection. Our study looks at the success of transmission during mixed infection of orthotopoviruses, enhancing the understanding of orthotospovirus epidemiology and evolution.

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“…Although TSWV moves systemically through plants, only a subset of the viral population may undergo long-distance transport to new leaves, resulting in distinct founder populations with lower diversity. One might expect to see similar bottlenecks within thrips as the virus must traverse through the midgut to the salivary glands before transmission can occur (Chen et al ., 2019). We may have failed to detect bottlenecks in thrips as multiple insects were sampled and then pooled at a single time point to obtain enough RNA for sequencing.…”

Section: Discussionmentioning

confidence: 99%

“…Like many other plant viruses, TSWV is considered to be a plant host generalist but a vector specialist (Lefeuvre et al ., 2019). Indeed, only 9 of more than 7,000 described thrips species are known to be competent vectors of TSWV (Jones et al , 2005;Chen et al ., 2019), and particular genetic isolates of TSWV appear to be intimately adapted to local thrips populations (Jacobson and Kennedy, 2013). Future work by our group will therefore look at differences in absolute fitness between hosts and whether it is more difficult for TSWV to adapt to new plant hosts or new vector species.…”

Section: Discussionmentioning

confidence: 99%

Evolutionary dynamics ofTomato spotted wilt viruswithin and between alternate plant hosts and thrips

Ruark-Seward

Bonville

Kennedy

et al. 2020

Preprint

Self Cite

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Tomato spotted wilt virus (TSWV) is a generalist pathogen with one of the broadest known host ranges among RNA viruses. To understand how TSWV adapts to different hosts, we experimentally passaged viral populations between two alternate hosts, Emilia sochifolia and Datura stramonium , and an obligate vector in which it also replicates, western flower thrips ( Frankliniella occidentalis ). Deep sequencing viral populations at multiple time points allowed us to track the evolutionary dynamics of viral populations within and between hosts. High levels of viral genetic diversity were maintained in both plants and thrips between transmission events.Rapid fluctuations in the frequency of amino acid variants indicated strong host-specific selection pressures on proteins involved in viral movement (NSm) and replication (RdRp). While several genetic variants showed opposing fitness effects in different hosts, fitness effects were generally positively correlated between hosts indicating that positive rather than antagonistic pleiotropy is pervasive. These results suggest that high levels of genetic diversity together with the positive pleiotropic effects of mutations have allowed TSWV to rapidly adapt to new hosts and expand its host range.

show abstract

Entry of bunyaviruses into plants and vectors

Cited by 21 publications

References 140 publications

Evolutionary dynamics of Tomato spotted wilt virus within and between alternate plant hosts and thrips

Evolutionary dynamics of Tomato spotted wilt virus within and between alternate plant hosts and thrips

Thrips as the Transmission Bottleneck for Mixed Infection of Two Orthotospoviruses

Evolutionary dynamics ofTomato spotted wilt viruswithin and between alternate plant hosts and thrips

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