Constitutive and induced subterranean plant volatiles attract both entomopathogenic and plant parasitic nematodes

Abstract

Summary1. Indirect plant defences are well documented for the above-ground constituents of plants. Although less investigated to date, below-ground defences that mediate multitrophic interactions are equally important. Entomopathogenic nematodes (Steinernema diaprepesi) are attracted to herbivore-induced volatiles from Swingle var. (Citrus paradisi · Poncirus trifoliata) when fed upon by root weevil, Diaprepes abbreviatus. 2. We examined the extent to which below-ground volatiles modify behaviour of nematode species representing various foraging strategies (cruisers versus ambushers) and trophic levels (plant parasites versus entomopathogens). We compared attraction to volatiles of weevil-infested and non-infested roots from Swingle citrus rootstock and a parent line of the Swingle hybrid, Poncirus trifoliata (Pt). 3. Swingle weevil-infested roots attracted more nematodes than non-infested roots irrespective of nematode foraging strategy and trophic status. The parental line, Pt, attracted all nematode species irrespective of insect herbivory. 4. Dynamic in situ collection and GC-MS analysis of volatiles from soil revealed that Pt roots release attracting cues constitutively. A different non-hybrid citrus species (sour orange, Citrus aurantium) released nematode attracting cues only in response to larval feeding, similar to responses found in Swingle. Volatile collections from above-and below-ground portions of citrus plants revealed that above-ground feeding by weevils does not induce production of nematode attracting cues analogous to that induced by root damage, nor does damage by larvae below-ground induce a similar volatile above ground. 5. Synthesis. Our results suggest that release of nematode attractants by citrus roots occurs broadly and can be constant or herbivore-induced. The major constituent of this indirect defence is produced by roots and not shoots and in response to below-ground, but not above-ground herbivory. Our findings suggest that this cue acts on nematode species broadly, attracting entomopathogenic nematodes that exhibit various foraging strategies. Unexpectedly, we also found that this cue attracts a plant parasitic nematode species. It appears, thus, that release of nematode attracting cues by citrus plants can cause ecological costs. The plants, however, appear to counteract against these costs, because constitutive release was found only in a cultivar that is resistant to phytopathogenic nematodes, while herbivore-induced release occurred in lines susceptible to pathogenic nematode species.

The Role of Root-Produced Volatile Secondary Metabolites in Mediating Soil Interactions

“…Tylenchulus semipenetrans nematodes were more attracted to Citrus roots infested by weevil larvae compared to uninfested plants (Ali, Alborn, and Stelinski 2011). A series of terpene compounds were identified a possible attractants for the plant parasitic nematode, including -pinene, -pinene, limonene, geijerene, and pregeijerene (Ali, Alborn, and Stelinski 2011). Interestingly the same compounds were also responsible for the attraction of entomopathogenic nematodes, which function as bodyguards against insect root feeders Stelinski 2010, 2011).…”

“…Only very recently, it was shown that phytopathogenic nematodes can also follow gradients of herbivore induced terpene volatile organic compounds. Tylenchulus semipenetrans nematodes were more attracted to Citrus roots infested by weevil larvae compared to uninfested plants (Ali, Alborn, and Stelinski 2011). A series of terpene compounds were identified a possible attractants for the plant parasitic nematode, including -pinene, -pinene, limonene, geijerene, and pregeijerene (Ali, Alborn, and Stelinski 2011).…”

Characterization of Volatile Organic Compounds Emitted by Barley (Hordeum vulgare L.) Roots and Their Attractiveness to Wireworms

“…aboveground plant insect interactions (Effmert et al 2012;Johnson et al 2009;Soler et al 2012;Wenke et al 2010); however, the belowground VOCs potentially responsible for such interactions have to date been partially neglected, due to technical limitations. The release of root VOCs can mediate various interactions: direct or indirect defense of roots against herbivores (Ali et al 2011;Rasmann et al 2005Rasmann et al , 2012a, plant -plant competition (Ens et al 2009;Jassbi et al 2010;Viles and Reese 1996), resistance of roots against pathogens (Cobb et al 1968;Kalemba et al 2002;Vilela et al 2009), and symbiotic interactions (Asensio et al 2012;Paavolainen et al 1998). Root derived compounds can also attract herbivores (Wenke et al 2010), and their emission tends to decrease in unattacked conditions (Piesik et al 2011b), thus limiting the energy costs incurred by their synthesis (Herms and Mattson 1992;Rasmann et al 2012a, b).…”

Behaviour and Population Dynamics of Entomopathogenic Nematodes Following Application

“…Other plant species also release volatiles from their roots in response to insect feeding, that attract EPN, though not all EPN respond similarly (Ali, Alborn, & Stelinski, 2011;Hiltpold, Baroni, Toepfer, Kuhlmann, & Turlings, 2010;. Species with all categories of foraging strategy respond (Ali et al, 2011). Indeed, the same signal also attracted freeliving bacterial feeding nematodes that might compete with EPN for the cadaver as a resource (Ali, Campos-Herrera, Alborn, Duncan, & Stelinski, 2013).…”

“…Rasmann et al (2005) reported that maize plants released (E)-"-caryophyllene in response to feeding by larvae of corn rootworm Diabrotica virgifera virgifera Le Conte (Coleoptera: Chrysomelidae), and that this volatile was highly attractive to H. megidis. Other plant species also release volatiles from their roots in response to insect feeding, that attract EPN, though not all EPN respond similarly (Ali, Alborn, & Stelinski, 2011;Hiltpold, Baroni, Toepfer, Kuhlmann, & Turlings, 2010;. Species with all categories of foraging strategy respond (Ali et al, 2011).…”