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

Abstract

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.

Persistent, circulative transmission of begomoviruses by whitefly vectors

“…Begomoviruses, such as TYLCV, directly manipulate the settling, probing, feeding behavior and host preference of their whitefly vector in a way that enhance virus transmission efficiency and spread. Such results imply cooperative and/ or neutral co-evolutionary relationships between the virus and its insect vector [79][80][81][82][83] [82] demonstrated that TYLCV-infected and TYLCCNV-infected plants had no or only marginal effects on the development, survival and fecundity of the MEAM1. On the other hand, the latter group reported that survival and fecundity rates were reduced on virusinfected plants, compared to those on uninfected plants in the Asia II3 (formerly termed ZHJ1 biotype) B. tabaci species [82].…”

Plant Virus Ecology: A Glimpse of Recent Accomplishments

“…Direct changes occur when the virus remain inside the insect for its whole life span. For example, in tomato TYLCV (Tomato yellow leaf curl virus) remained in the body of white fly thus influencing vector settling, probing and feeding (Moreno-Delafuente et al, 2013). Further research revealed that the interaction between virus and vector was mutually beneficial for each other specifically for the biotype Q only (Pan et al, 2013).…”

Diversity of Plant Virus Populations: A Valuable Tool for Epidemiological Studies

“…More complex interaction among viruses, hosts and vectors may also play a role in selection for transmission. For instance, plant viruses may have mutualistic interactions with their vectors, so that infected plants become more attractive for transmission vectors [54], viruliferous vectors increase their fecundity by partial suppression of plant defense mechanisms against feeding vectors [55] and some circulative-propagative viruses seem to modify their vectors' feeding behavior to increase their transmission rate [56,57].…”