Direct and indirect effects of a thrips‐transmitted <i><scp>T</scp>ospovirus</i> on the preference and fitness of its vector, <i><scp>F</scp>rankliniella fusca</i>

Shrestha, Anita; Srinivasan, Rajagopalbabu; Riley, David G.; Culbreath, A. K.

doi:10.1111/eea.12011

Cited by 69 publications

(59 citation statements)

References 71 publications

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“…Our work and other recent findings [24], [26] suggest that the transmission mechanisms shape pathogens effects on host-vector interactions. We conclude that TYLCV, a circulative phloem-restricted begomovirus, has evolved to manipulate the settling, probing and feeding behavior of its vector, B. tabaci in a manner that facilitates its own transmission.…”

Section: Discussionsupporting

confidence: 82%

“…Relatively little research has explored solely the direct effects of plant pathogens on their vectors when they are ingested and circulate through their body. In fact, most of the studies have concentrated on the indirect effects mediated by the plant when a virus induces changes in vector performance and behavior or in the preference for its plant host after infection [19]–[23], or the mixed effects (direct plus indirect effects) [24], [25]. Evaluating the indirect effects, from the pathogen stand point, the virus will benefit when the attractiveness of the infected host plant is maximum until the vector lands and probes on the plant.…”

Section: Introductionmentioning

confidence: 99%

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A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread

et al. 2013

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Plant viruses can produce direct and plant-mediated indirect effects on their insect vectors, modifying their life cycle, fitness and behavior. Viruses may benefit from such changes leading to enhanced transmission efficiency and spread. In our study, female adults of Bemisia tabaci were subjected to an acquisition access period of 72 h in Tomato yellow leaf curl virus (TYLCV)-infected and non-infected tomato plants to obtain viruliferous and non-viruliferous whiteflies, respectively. Insects that were exposed to virus-infected plants were checked by PCR to verify their viruliferous status. Results of the Ethovision video tracking bioassays indicated that TYLCV induced an arrestant behavior of B. tabaci, as viruliferous whitefly adults remained motionless for more time and moved slower than non-viruliferous whiteflies after their first contact with eggplant leaf discs. In fact, Electrical Penetration Graphs showed that TYLCV-viruliferous B. tabaci fed more often from phloem sieve elements and made a larger number of phloem contacts (increased number of E1, E2 and sustained E2 per insect, p<0.05) in eggplants than non-viruliferous whiteflies. Furthermore, the duration of the salivation phase in phloem sieve elements (E1) preceding sustained sap ingestion was longer in viruliferous than in non-viruliferous whiteflies (p<0.05). This particular probing behavior is known to significantly enhance the inoculation efficiency of TYLCV by B. tabaci. Our results show evidence that TYLCV directly manipulates the settling, probing and feeding behavior of its vector B. tabaci in a way that enhances virus transmission efficiency and spread. Furthermore, TYLCV-B. tabaci interactions are mutually beneficial to both the virus and its vector because B. tabaci feeds more efficiently after acquisition of TYLCV. This outcome has clear implications in the epidemiology and management of the TYLCV-B. tabaci complex.

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Section: Discussionsupporting

confidence: 82%

Section: Introductionmentioning

confidence: 99%

A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread

et al. 2013

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“…The settling, probing, and feeding behavior of whiteflies transmitting Tomato leaf curl virus has also been shown to be conditional on the infection status of tobacco and whether the vector was viruliferous (Moreno-Delafuente et al 2013). Similarly, other recent studies demonstrated that feeding behavior or preference of thrips vectors of Tospoviruses change after virus acquisition by the vector (Stafford et al 2011, Shrestha et al 2012). These conditional preferences would be expected to lead to increased virus spread and suggest that some viruses may have evolved to manipulate the settling, probing and feeding behavior of their vectors to enhance transmission, although the mechanisms responsible have not been identified.…”

Section: Introductionmentioning

confidence: 92%

“…, Shrestha et al. ). These conditional preferences would be expected to lead to increased virus spread and suggest that some viruses may have evolved to manipulate the settling, probing and feeding behavior of their vectors to enhance transmission, although the mechanisms responsible have not been identified.…”

Section: Introductionmentioning

confidence: 99%

Vector population growth and condition‐dependent movement drive the spread of plant pathogens

Shaw

Peace

Power

et al. 2017

Ecology

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Plant viruses, often spread by arthropod vectors, impact natural and agricultural ecosystems worldwide. Intuitively, the movement behavior and life history of vectors influence pathogen spread, but the relative contribution of each factor has not been examined. Recent research has highlighted the influence of host infection status on vector behavior and life history. Here, we developed a model to explore how vector traits influence the spread of vector-borne plant viruses. We allowed vector life history (growth rate, carrying capacity) and movement behavior (departure and settlement rates) parameters to be conditional on whether the plant host is infected or healthy and whether the vector is viruliferous (carrying the virus) or not. We ran simulations under a wide range of parameter combinations and quantified the fraction of hosts infected over time. We also ran case studies of the model for Barley yellow dwarf virus, a persistently transmitted virus, and for Potato virus Y, a non-persistently transmitted virus. We quantified the relative importance of each parameter on pathogen spread using Latin hypercube sampling with the statistical partial rank correlation coefficient technique. We found two general types of mechanisms in our model that increased the rate of pathogen spread. First, increasing factors such as vector intrinsic growth rate, carrying capacity, and departure rate from hosts (independent of whether these factors were condition-dependent) led to more vectors moving between hosts, which increased pathogen spread. Second, changing condition-dependent factors such as a vector's preference for settling on a host with a different infection status than itself, and vector tendency to leave a host of the same infection status, led to increased contact between hosts and vectors with different infection statuses, which also increased pathogen spread. Overall, our findings suggest that vector population growth rates had the greatest influence on rates of virus spread, but rates of vector dispersal from infected hosts and from hosts of the same infection status were also very important. Our model highlights the importance of simultaneously considering vector life history and behavior to better understand pathogen spread. Although developed for plant viruses, our model could readily be utilized with other vector-borne pathogen systems.

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“…To efficiently transmit from plant to plant, viruses induce chemical and physical changes in the host, affecting vector-host interactions (Eigenbrode et al 2002;Hurd 2003;Belliure et al 2005). In addition, plant viruses can modify the feeding preferences or feeding behaviour of their insect vector to enhance transmission efficiency and spread (Stafford et al 2011;Ingwell et al 2012;Shrestha et al 2012;Moreno-Delafuente et al 2013).…”

Section: Introductionmentioning

confidence: 99%

Preference of the vector thrips Frankliniella occidentalis for plants infected with thrips‐non‐transmissible Tomato spotted wilt virus

Tomitaka

Abe

Sakurai

et al. 2014

J Applied Entomology

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The effect of a thrips-non-transmissible Tomato spotted wilt virus (TSWV) on insect-host interactions between thrips and Arabidopsis thaliana was analysed. A wild-type TSWV virulent isolate and a TSWV isolate that induces mild symptoms on inoculated plants (TSWV-Mo) were used in this study, and TSWV-Mo isolate was obtained by single local lesion isolation using Petunia x hybrid after several passages on Nicotiana rustica plants. In transmission test, although wild-type TSWV (TSWV-wt) was transmitted by two thrips species (transmission ratio; Frankliniella occidentalis, 25%; Thrips tabaci, 10%; and T. palmi, 0%), none of the thrips transmitted TSWV-Mo. Feeding damage by F. occidentalis in A. thaliana plants was more extensive on TSWV-wt-infected plants than on TSWV-Mo-infected plants, despite comparable preference. Among the markers of plant defences, salicylic acid-regulated genes were upregulated threefold to sixfold by TSWV-wt or TSWV-Mo infection. In contrast, jasmonate-regulated genes and jasmonate/ethylene-regulated genes were not affected by the infections. Pull assays showed that adjacent TSWV-Mo-infected plants were preferred over uninfected plants. In conclusion, our results showed that the transmissibility by thrips of TSWV is not related to preference of vector thrips and suggested that TSWV-Mo-infected plants may be used as attractants for behaviour control of thrips.

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Direct and indirect effects of a thrips‐transmitted Tospovirus on the preference and fitness of its vector, Frankliniella fusca

Cited by 69 publications

References 71 publications

A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread

A Plant Virus Manipulates the Behavior of Its Whitefly Vector to Enhance Its Transmission Efficiency and Spread

Vector population growth and condition‐dependent movement drive the spread of plant pathogens

Preference of the vector thrips Frankliniella occidentalis for plants infected with thrips‐non‐transmissible Tomato spotted wilt virus

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