Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons

BACKGROUND: Aphis gossypii, a strictly phloemophagaous aphid, colonize hundreds of plant families, and a group of clones formed a cucurbit-specialised host-race. Cucurbits are unique in having evolved a specific extra-fascicular phloem (EFP), which carries defence-related metabolites such as cucurbitacin, whereas the fascicular phloem (FP) is common to all higher plants and carries primary metabolites, such as raffinose-family oligosaccharides (RFOs). Both cucurbitacins (in the EFP) and galactinol (in the FP) have been suggested to be toxic to aphids. We investigated these hypotheses in cucurbit-specialized A. gossypii fed on melon plants with or without aphid-resistance conferred by the NLR gene Vat. We selected a plant-aphid system with (i) Vat-mediated resistance not triggered, (ii) Vat-mediated resistance triggered by an aphid clone adapted to the presence of Vat resistant alleles and (iii) Vat-mediated resistance triggered by a non-adapted aphid clone. RESULTS: We quantified cucurbitacin B, its glycosylated derivative, and sugars, in melon plants and aphids that fed on. The level of cucurbitacin in plants was unrelated to both aphid infestation and aphid resistance. Galactinol was present at higher quantities in plants when Vat-mediated resistance was triggered, but its presence did not correlate with aphid performance. Finally, we showed that cucurbit-specialized A. gossypii fed from the FP but could also occasionally access the EFP without sustainably feeding from it. However, the clone not adapted to Vat-mediated resistance were less able to access the FP when the Vat resistance was triggered. CONCLUSION: We concluded that galactinol accumulation in resistant plants does not affect aphids, but may play a role in aphid adaptation to fasting and that Cucurbitacin in planta is not a real threat to Aphis gossypii. Moreover, the specific phloem of Cucurbits is involved neither in A. gossypii cucurbit specialisation nor in adaptation to Vat-dependent resistance. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12870-023-04248-1.