Whitefly feeding behavior and retention of a foregut‐borne crinivirus exposed to artificial diets with different pH values

Abstract

Transmission of plant viruses by phytophagous hemipteran insects encompasses complex interactions underlying a continuum of processes involved in virus acquisition, retention and inoculation combined with vector feeding behavior. Here, we investigated the effects of dietary pH on whitefly (Bemisia tabaci) feeding behavior and release of Lettuce infectious yellows virus (LIYV) virions retained in the vector's foregut. Electrical penetration graph analysis revealed that variables associated with whitefly probing and ingestion did not differ significantly in pH (4, 7.4, and 9) adjusted artificial diets. To investigate virus retention and release, whiteflies allowed to acquire LIYV virions in a pH 7.4 artificial diet were fed pH 4, 7.4, or 9 virion-free artificial (clearing) diets. Immunofluorescent localization analyses indicated that virions remained bound to the foreguts of approximately 20%-24% of vectors after they fed on each of the 3 pHadjusted clearing diets. When RNA preparations from the clearing diets were analyzed by reverse transcription (RT) nested-PCR and, in some cases, real-time qPCR, successful amplification of LIYV-specific sequence was infrequent but consistently repeatable for the pH 7.4 diet but never observed for the pH 4 and 9 diets, suggesting a weak pH-dependent effect for virion release. Viruliferous vectors that fed on each of the 3 pH-adjusted clearing diets transmitted LIYV to virus-free plants. These results suggest that changes in pH values alone in artificial diet do not result in observable changes in whitefly feeding behaviors, an observation that marks a first in the feeding of artificial diet by whitefly vectors; and that there is a potential causal and contingent relationship between the pH in artificial diet and the release/inoculation of foregut bound virions.

Direct and indirect influences of virus–insect vector–plant interactions on non-circulative, semi-persistent virus transmission

“…In aphids, stylet activity and movement may be guided/influenced by plant cues such as pH, sugar species and concentration, viscosity, and defense components [20,21] (Figure 2). Whether or not similar plant cues are involved in guiding whitefly stylet activity/movement is not known, but we know that the behaviors of whiteflies feeding on artificial diet of different pH values do not differ significantly [22].…”

The promises and challenges of research on plant–insect–microbe interactions

“…By using artificial diet, Zhou et al . () studied the effect of dietary pH ( Bemisia tabaci ) on the feeding behavior and retention/release of Lettuce infectious yellows virus (LIYV) virions. They found that whitefly behavior and virus retention were not significantly influenced, but virus release was weakly affected by dietary pH.…”

“…The acrostyle is presumed to retain viruses but also aphid salivary proteins that might interact with plant host signaling; thus, the characterization of this structure and interaction with various proteins will progress the field of virusinsect-plant interactions. By using artificial diet, Zhou et al (2017) studied the effect of dietary pH (Bemisia tabaci) on the feeding behavior and retention/release of Lettuce infectious yellows virus (LIYV) virions. They found that whitefly behavior and virus retention were not significantly influenced, but virus release was weakly affected by dietary pH.…”

“…For instance, depending on their transmission mode, viruses have evolved specific ways in which they manipulate VOCs and other plants traits to enhance their transmission by insect vectors (Mauck et al, 2012. Understanding the full interplay of how each of these three partners manipulates and responds to the other two in such vectored plant disease systems is perhaps the biggest challenge of all (Webster et al, 2017;Zhou et al, 2017). On top of that, insect endosymbionts have been shown to affect the success of both vector and vectored disease (Tamborindeguy et al, 2017) and hence have become target for manipulation to limit vector-borne diseases (Berasategui et al, 2016).…”

Nuances of Whitefly Vector–Crinivirus Interactions Revealed in the Foregut Retention and Transmission of Lettuce Chlorosis Virus by Two Bemisia tabaci Cryptic Species

“…These observations are further backed by biochemical and molecular data supporting the role of the LIYV CPm in mediating the binding of virions to the vector’s foregut [ 10 , 16 , 17 ]. The mechanism underlying the inoculation of LIYV virions retained in the foregut by NW vectors is not understood but may be influenced by the physical properties in the foregut environment such as the dietary pH [ 19 ].…”