Dual nematode infection in Brassica nigra affects shoot metabolome and aphid survival in distinct contrast to single-species infection.

Previous studies showed that aphid performance was compromised on Brassica nigra infected by root-lesion nematodes (Pratylenchus penetrans, Pp), but less, or positively influenced by root-knot nematode (Meloidogyne spp.) infection. These experiments were on single-species nematode infections, but roots can be infected naturally with several nematode species simultaneously. We performed greenhouse assays to assess the effects of single [Meloidogyne incognita (Mi) or Pp] and concurrent (MP) nematode infections on aphid performance. Using targeted and untargeted profiling of leaf and phloem metabolomes, we examined how single and concurrent nematode infections affect shoot metabolomes, and elucidated the possible consequences for aphid performance. We found that the metabolic response to double-infection is different from that to single-species infections. Moreover, Mi and Pp infections triggered discrete changes in B. nigra leaf and phloem metabolic profiles. Both Pp and MP infections reduced aphid survival, suggesting that the biological effect could primarily be dominated by Pp-induced changes. This concurred with increased indole glucosinolates and hydroxycinnamic acid levels in the leaves, in particular the putative involvement of salicylic acid-2-O-β-d-glucoside. This study provides evidence that concurrent infection by different nematode species, as is common in natural environments, is associated with distinct changes in aboveground plant metabolomes, which are linked to differences in the survival of an aboveground herbivore.