Abstract
Plants suffer multiple, simultaneous biotic threats from both above and below ground. These pests and/or pathogens are commonly studied on an individual basis and the effects of above-ground pests on below-ground pathogens are poorly defined. Root exudates from potato plants (Solanum tuberosum L.) were analyzed to characterize the top-down plant-mediated interactions between a phloem-sucking herbivore (Myzus persicae) and a sedentary, endoparasitic nematode (Globodera pallida). Increasing inocula of the aphid, M. persicae, reduced the root mass of potato plants. Exudates collected from these roots induced significantly lower hatching of second-stage juveniles from G. pallida eggs over a 28-day period, than those from uninfested control plants. Inhibition of hatch was significantly positively correlated with size of aphid inoculum. Diminished hatching was partially recovered after treatment with root exudate from uninfested potato plants indicating that the effect on hatching is reversible but cannot be fully recovered. Glucose and fructose content was reduced in root exudates from aphid-infested potato plants compared to controls and these sugars were found to induce hatching of G. pallida, but not to the same degree as potato root exudates (PRE). Supplementing aphid-infested PRE with sugars did not recover the hatching potential of the treatment, suggesting that additional compounds play an important role in egg hatch. The first gene upregulated in the closely related potato cyst nematode Globodera rostochiensis post-exposure to host root exudate, Neprilysin-1, was confirmed to be upregulated in G. pallida cysts after exposure to PRE and was also upregulated by the sugar treatments. Significantly reduced upregulation of Gpa-nep-1 was observed in cysts treated with root exudates from potato plants infested with greater numbers of aphids. Our data suggest that aphid infestation of potato plants affects the composition of root exudates, with consequential effects on the hatching and gene expression of G. pallida eggs. This work shows that an above-ground pest can indirectly impact the rhizosphere and reveals secondary effects for control of an economically important below-ground pathogen.
Highlights
Plants are a primary source of nutrition for a wide range of organisms and are often subject to simultaneous attack from both above and below the ground (Wondafrash et al, 2013; Van Dam et al, 2018)
We investigated the possible indirect effect that aphids may have on cyst nematodes via root exudate
Hatching of G. pallida was significantly reduced when cysts were incubated in potato root exudate (PRE) from potato plants infested with > 5 M. persicae compared to exudates from non-infested control plants (Figures 2A,B; P < 0.05)
Summary
Plants are a primary source of nutrition for a wide range of organisms and are often subject to simultaneous attack from both above and below the ground (Wondafrash et al, 2013; Van Dam et al, 2018). Plant-feeding aphids and plant-parasitic nematodes (PPN) can be linked through host-mediated interactions (Kaplan et al, 2008; Kutyniok and Müller, 2012; Hoysted et al, 2017) Aphids use their stylet-like mouthparts to feed on photoassimilates found in the host’s sap (Pollard, 1973; Blackman and Eastop, 2000). Nematodes constitute one of the most abundant phyla of the rhizosphere and many are phytophagous, feeding on the roots of plants (Jones et al, 2013; van Dam and Bouwmeester, 2016; Hewezi and Baum, 2017) Cyst nematodes, such as Globodera pallida, are a group of highly evolved sedentary endoparasites that are pathogens of temperate, subtropical, and tropical plant species (Nicol et al, 2011; Cotton et al, 2014). At maturity the female is fertilized, her body swells, and the cuticle hardens to form a protective cyst that contains hundreds of eggs (Bohlmann, 2015; Moens et al, 2018)
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