Constant versus herbivore induced chemical signaling for recruitment of beneficial and parasitic nematodes by plant roots: Effects of nematode life history and plant breeding

Indirect defenses are well documented for the aboveground constituents of plants. Belowground signals that mediate multitrophic interactions are equally important. Entomopathogenic nematodes (S.diaprepesi) are attracted to herbivore-induced volatiles released from Swingle var. (P.trifoliate x C.paradise) citrus when fed upon by the root weevil, D.abbreviatus. Herein, we examined the extent to which belowground recruitment signals modify behavior of nematode species representing various foraging strategies, and trophic levels. We compared attraction to extracts of infested roots and non-infested roots from Swingle citrus rootstock and a parent line of the hybrid, P.trifoliate (Pt). Swingle roots infested by weevils attracted more nematodes than non-infested roots irrespective of nematode foraging strategy and trophic status. The parental line of the swingle rootstock, Pt, attracted all nematode species irrespective of insect herbivory. Dynamic in situ collection and GC-MS analysis of soil volatiles revealed that Pt roots released recruitment signals constitutively, regardless of weevil feeding. A different non-hybrid citrus species (Sour orange, C.aurantium) released nematode recruitment signals only in response to larval feeding. Volatile collections from above/belowground portions of citrus plants revealed that aboveground feeding does not induce production of nematode recruitment signals analogous to that induced by root damage nor does damage by larvae belowground induce a similar signal aboveground. Results suggest that constitutive release of nematode attractants by citrus roots occurs broadly and can be constant or herbivore-induced. The major constituent of this indirect signal is produced by roots, not shoots, in response to belowground, not aboveground herbivory. Our findings suggest that this recruitment signal acts on nematode species broadly, attracting both entomopathogenic and plant parasitic.