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. 2023 Apr 29;26(5):106752.
doi: 10.1016/j.isci.2023.106752. eCollection 2023 May 19.

A sucrose-specific receptor in Bemisia tabaci and its putative role in phloem feeding

Ofer Aidlin Harari  1 , Amir Dekel  1 , Dor Wintraube  1 , Yuri Vainer  1 , Rita Mozes-Koch  1 , Esther Yakir  1 , Osnat Malka  1 , Shai Morin  1 , Jonathan D Bohbot  1
Affiliations

A sucrose-specific receptor in Bemisia tabaci and its putative role in phloem feeding

Ofer Aidlin Harari et al. iScience. .

Abstract

In insects, specialized feeding on the phloem sap (containing mainly the sugar sucrose) has evolved only in some hemipteran lineages. This feeding behavior requires an ability to locate feeding sites buried deeply within the plant tissue. To determine the molecular mechanism involved, we hypothesized that the phloem-feeding whitefly Bemisia tabaci relies on gustatory receptor (GR)-mediated sugar sensing. We first conducted choice assays, which indicated that B. tabaci adults consistently choose diets containing higher sucrose concentrations. Next, we identified four GR genes in the B. tabaci genome. One of them, BtabGR1, displayed significant sucrose specificity when expressed in Xenopus oocytes. Silencing of BtabGR1 significantly interfered with the ability of B. tabaci adults to discriminate between non-phloem and phloem concentrations of sucrose. These findings suggest that in phloem feeders, sugar sensing by sugar receptors might allow tracking an increasing gradient of sucrose concentrations in the leaf, leading eventually to the location of the feeding site.

Keywords: Biological sciences; Molecular biology; Molecular mechanism of behavior.

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Conflict of interest statement

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Figures

None
Graphical abstract
Figure 1
Figure 1
B. tabaci adults can sense, discriminate, and choose between different concentrations of sucrose (A) The B. tabaci stylets encounter increasing apoplastic sucrose concentrations,, on their way to the phloem sieve elements located deep within the leaf. Sucrose concentrations in the phloem sap are from Hayashi and Chino and Fink et al., (B) The dual-choice assay consists of two feeding sites in the lid that subject adults of B. tabaci to two diets. (C) The percentage (mean ± SEM) of B. tabaci adults choosing a one diet over the other (68 mM of an amino acid cocktail mimicking the Arabidopsis thaliana phloem sap, H2O, changing concentrations of sucrose) after 24 h (n > 30 in all experiments, details on the statistical analysis are provided in the ‘STAR Methods’ section).
Figure 2
Figure 2
A unique clade of sugar receptors has emerged in sternorrhynchans (A) A phylogenetic tree of insect sugar GRs suggests two main lineages, the GR43a and the Gr5/61/64 groups, and the presence of a distinct clade within the Gr5/61/64 group that harbors only sweet GRs belonging to species from the Sternorrhyncha suborder of Hemiptera. Insect orders are marked by different branch colors. The four identified B. tabaci GRs are marked with solid white circles (complete coding sequence) or square (partial coding sequence) shapes. (B) Amino acid sequence alignment of representative sweet GRs from the GR61/64/5 lineages (Figure S3). The indicated pairwise amino acid sequence identity (ID) is to the BtabGR1sequence.
Figure 3
Figure 3
BtabGR1 is a sucrose receptor (A) Haworth projections of sucrose, maltose, glucose, and fructose. Sucrose is composed of glucose and fructose subunits. (B) Representative current traces of BtabGR1 and water-injected Xenopus oocytes in response to 100 mM of 14 sugar molecules. Black arrows indicate sugar delivery. (C) BtabGR1 is narrowly tuned to sucrose (kurtosis value = 13.65). The mean current responses (±SEM, n = 6) to 100 mM of 14 sweeteners were normalized to sucrose (one-way ANOVA; ∗∗∗∗p < 0.0001). (D) Representative current traces of BtabGR1 in response to 10-fold serial dilutions of sucrose, maltose, glucose, and fructose. (E) Sucrose was the most efficacious (two-way ANOVA followed by Tukey’s post-hoc test; ∗∗∗∗p < 0.0001) and most potent ligand (one-way ANOVA; ∗∗p = 0.0033, data are represented as mean ± SEM). (F) Representative current trace of BtabGR1 in response to low millimolar sucrose concentrations. (G) Concentration-response relationship between BtabGR1 current responses and low sucrose concentrations (two-way ANOVA followed by Tukey’s post-hoc test).
Figure 4
Figure 4
Silencing of BtabGR1 interferes with the ability to discriminate between sucrose concentrations (A) The percentage (mean ± SEM) of B. tabaci adults choosing 300 mM over 50 mM sucrose after 72 h of feeding on dsBtabGR1 (n = 50) or dsGFP (n = 46) containing diets (details on the statistical analysis are provided in the ‘STAR Methods’ section). (B) An RT-PCR assay indicating a significant reduction in the expression (mean 2−ΔΔCt ± SEM) of the BtabGR1 gene in whole body homogenates of dsBtabGR1- versus dsGFP-fed insects (p = 0.0008, n = 4).
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