Root infection by the nematode Meloidogyne incognita modulates leaf antiherbivore defenses and plant resistance to Spodoptera exigua depending on the nematode's infection cycle

Studies on plant-mediated interactions between root parasitic nematodes and aboveground herbivores are rapidly increasing. However, the outcomes for the interacting organisms vary, and the mechanisms involved remain ambiguous. We hypothesized that the impact of root infection by the root-knot nematode Meloidogyne incognita on the performance of the aboveground caterpillar Spodoptera exigua is modulated by the nematode's infection cycle. We challenged root-knot nematode infected tomato plants with caterpillars when the nematode's infection cycle was either at the invasion, galling, or reproduction stage. We found that M. incognita root infection enhanced S. exigua performance during the galling stage, while it did not affect the caterpilar's performance at the invasion and reproduction stages. Molecular and chemical analyses performed at the different stages of the nematode infection cycle revealed that M. incognita root infection systemically affected the jasmonic acid-, salicylic acid- and abscisic acid-related responses, as well as changes in the leaf metabolome during S. exigua feeding. The M. incognita induced leaf responses significantly varied over the nematode's root infection cycle. These findings suggest that specific leaf responses triggered systemically by the nematode at its different life-cycle stages underlie the differential impact of M. incognita on plant resistance against the caterpillar S. exigua.