An Indirect Defence Trait Mediated through Egg-Induced Maize Volatiles from Neighbouring Plants

Abstract

Attack of plants by herbivorous arthropods may result in considerable changes to the plant’s chemical phenotype with respect to emission of herbivore-induced plant volatiles (HIPVs). These HIPVs have been shown to act as repellents to the attacking insects as well as attractants for the insects antagonistic to these herbivores. Plants can also respond to HIPV signals from other plants that warn them of impending attack. Recent investigations have shown that certain maize varieties are able to emit volatiles following stemborer egg deposition. These volatiles attract the herbivore’s parasitoids and directly deter further oviposition. However, it was not known whether these oviposition-induced maize (Zea mays, L.) volatiles can mediate chemical phenotypic changes in neighbouring unattacked maize plants. Therefore, this study sought to investigate the effect of oviposition-induced maize volatiles on intact neighbouring maize plants in ‘Nyamula’, a landrace known to respond to oviposition, and a standard commercial hybrid, HB515, that did not. Headspace volatile samples were collected from maize plants exposed to Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) egg deposition and unoviposited neighbouring plants as well as from control plants kept away from the volatile emitting ones. Behavioural bioassays were carried out in a four-arm olfactometer using egg (Trichogramma bournieri Pintureau & Babault (Hymenoptera: Trichogrammatidae)) and larval (Cotesia sesamiae Cameron (Hymenoptera: Braconidae)) parasitoids. Coupled Gas Chromatography-Mass Spectrometry (GC-MS) was used for volatile analysis. For the ‘Nyamula’ landrace, GC-MS analysis revealed HIPV production not only in the oviposited plants but also in neighbouring plants not exposed to insect eggs. Higher amounts of EAG-active biogenic volatiles such as (E)-4,8-dimethyl-1,3,7-nonatriene were emitted from these plants compared to control plants. Subsequent behavioural assays with female T. bournieri and C. sesamiae parasitic wasps indicated that these parasitoids preferred volatiles from oviposited and neighbouring landrace plants compared to those from the control plants. This effect was absent in the standard commercial hybrid we tested. There was no HIPV induction and no difference in parasitoid attraction in neighbouring and control hybrid maize plants. These results show plant-plant signalling: ‘Nyamula’ maize plants emitting oviposition-induced volatiles attractive to the herbivore’s natural enemies can induce this indirect defence trait in conspecific neighbouring undamaged maize plants. Maize plants growing in a field may thus benefit from this indirect defence through airborne signalling which may enhance the fitness of the volatile-emitting plant by increasing predation pressure on herbivores.

Chemical, Physiological and Molecular Responses of Host Plants to Lepidopteran Egg-Laying

“…Egg deposition or treatment with elicitors did not show particular effects in commercial standard maize hybrids, indicating a possible loss of defense traits in plants subjected to artificial selection and breeding (Mutyambai et al, 2016;Tamiru et al, 2017) and, as in the case of HR-like necrosis in B. nigra (Griese et al, 2017), highlighting the role of plant genotype in defense mechanisms.…”

“…Lepidopteran egg elicitors can also induce the production of oviposition-induced plant volatiles (OIPVs) enabling the plants 7) to attract egg or larval parasitoids, that upon locating their hosts, inject their own eggs and kill the lepidopteran instars to feed their off-spring (Tamiru et al, 2011;Fatouros et al, 2012;Cusumano et al, 2015;Ponzio et al, 2016) or 8) insectivorous birds (Mrazova et al, 2019). In addition, OIPVs can also prime 9) neighboring plants (Mutyambai et al, 2016;Guo et al, 2019).…”

Responses of stemborer Chilo partellus to volatiles emitted by maize landraces exposed to signal grass (Brachiaria brizantha)

“…Plant to plant communication is known to be a mechanism of pest control through herbivore-induced plant volatiles (HIPVs) (Khan et al 2001;Cook et al 2007;Heil 2008;Tamiru et al 2012;Magara et al 2015;Mutyambai et al 2016). Studies have shown that B. brizantha is preferred to maize for oviposition by gravid C. partellus (Midega et al 2011;Cheruiyot et al 2018).…”

Plant volatiles induced by herbivore eggs prime defences and mediate shifts in the reproductive strategy of receiving plants

“…The current results suggest that oviposition‐induced volatiles can also prime plant defences; this finding complements other recent work showing that oviposition‐induced volatiles also play a communicative function in indirect plant defence by serving as foraging cues for natural enemies of herbivores, as well as herbivores themselves. For example, both egg and larval parasitoids showed a stronger preference for maize plants exposed to volatiles of plants infested by eggs of the herbivore Chillo partellus than control plants (Mutyambai et al 2016). Ovipositing herbivores were also seen to avoid poplar plants exposed to volatiles from egg‐infested neighbours (Guo et al 2019).…”

“…Plants infested with P. brassicae eggs were also found to flower earlier and produce significantly more seeds than control plants (Lucas‐Barbosa et al 2013; Pashalidou et al 2015b) and to emit volatiles that recruit larval parasitoids (Pashalidou et al 2013; Pashalidou et al 2015b). Recent studies in other systems have also reported effects of volatiles induced by herbivore oviposition, including enhanced parasitoid attraction in teosinte (Mutyambai et al 2016) and decreased herbivore recruitment in poplar (Guo et al 2019). In the light of these findings, we hypothesised that it might be adaptive for B. nigra plants themselves to detect and respond to volatile cues associated with the presence of P. brassicae eggs.…”