Tree genotype modulates the effects of water deficit on a plant-manipulating aphid

• We study how poplar genotype mediates water deficit effects on a gall-inducing aphid.
• Three irrigation levels were applied to a susceptible and a resistant host genotype.
• For both genotypes, water deficit affected plant growth and gall anatomy.
• The effect of water deficit on aphid performance differed according to host genotype.
• The medium irrigation level favored aphid development on the resistant host.

Successful plant manipulation by herbivores requires a reconfiguration of the primary and secondary metabolisms of the host-plant. Water deficit is generally predicted to negatively affect the development of gall-inducing insects, by impairing their ability to remodel the primary metabolism of their host. We assessed whether host genotype could modulate water deficit effects on a gall-inducing aphid, Phloeomyzus passerinii, developing on poplars, which are known to be among the most susceptible trees to water deficit. Stem-cuttings of two poplar genotypes, with a different resistance level to P. passerinii, were grown under three irrigation treatments, and subsequently infested with the same aphid clone. Plant growth parameters and aphid colonies development were recorded, and the development and organization of the pseudogall induced by the aphid was observed using histological investigations. The three irrigation treatments resulted in three levels of water deficit. Mean predawn leaf water potential reached −0.10, −0.49 and −0.75 MPa in the optimal, intermediate and low irrigation treatments respectively. In both genotypes, growth, architecture and photosynthesis were similarly affected. The severe water deficit reduced the development of aphids on both genotypes, which is in agreement with the general prediction for gall-inducing insects. Nonetheless, while the intermediate water deficit did not affect the development of aphids on the susceptible genotype, it enhanced their development on the resistant one. This latter observation contradicts the prediction for gall-inducing insects, but is in agreement with the plant stress hypothesis for sucking insects. The size of the pseudogall induced by the aphids in the bark of their host progressively diminished when water deficit increased. Lignification, believed to be an important component of poplar resistance to P. passerinii, also progressively decreased with water deficit. The involvement of physiological and architecture modifications due to water deficit on the development of aphids is discussed. The results demonstrate that host genotype can modulate water deficit effects on the development of a galling aphid, thereby compromising predictions on the outcome of droughts on stand resistance to plant-manipulating herbivores.