Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons
Abstract 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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-05-01
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| Series: | BMC Plant Biology |
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| Online Access: | https://doi.org/10.1186/s12870-023-04248-1 |
| _version_ | 1827952791997382656 |
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| author | Pierre Sadon Marie-Noëlle Corre Raphael Lugan Nathalie Boissot |
| author_facet | Pierre Sadon Marie-Noëlle Corre Raphael Lugan Nathalie Boissot |
| author_sort | Pierre Sadon |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-09T14:03:11Z |
| format | Article |
| id | doaj.art-4a83f64c66b24edca1a6e7760165ec8a |
| institution | Directory Open Access Journal |
| issn | 1471-2229 |
| language | English |
| last_indexed | 2024-04-09T14:03:11Z |
| publishDate | 2023-05-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Plant Biology |
| spelling | doaj.art-4a83f64c66b24edca1a6e7760165ec8a2023-05-07T11:10:00ZengBMCBMC Plant Biology1471-22292023-05-0123111410.1186/s12870-023-04248-1Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melonsPierre Sadon0Marie-Noëlle Corre1Raphael Lugan2Nathalie Boissot3Génétique et Amélioration des Fruits et Légumes, National Institute for Agriculture, Food and Environment, INRAEGénétique et Amélioration des Fruits et Légumes, National Institute for Agriculture, Food and Environment, INRAEPlantes et Systèmes de cultures Horticoles, National Institute for Agriculture, Food and Environment, INRAEGénétique et Amélioration des Fruits et Légumes, National Institute for Agriculture, Food and Environment, INRAEAbstract 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.https://doi.org/10.1186/s12870-023-04248-1NLRPlant resistanceSpecialized metabolitesPrimary metabolitesVat melon |
| spellingShingle | Pierre Sadon Marie-Noëlle Corre Raphael Lugan Nathalie Boissot Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons BMC Plant Biology NLR Plant resistance Specialized metabolites Primary metabolites Vat melon |
| title | Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons |
| title_full | Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons |
| title_fullStr | Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons |
| title_full_unstemmed | Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons |
| title_short | Aphid adaptation to cucurbits: sugars, cucurbitacin and phloem structure in resistant and susceptible melons |
| title_sort | aphid adaptation to cucurbits sugars cucurbitacin and phloem structure in resistant and susceptible melons |
| topic | NLR Plant resistance Specialized metabolites Primary metabolites Vat melon |
| url | https://doi.org/10.1186/s12870-023-04248-1 |
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