Aphid Colonization Affects Potato Root Exudate Composition and the Hatching of a Soil Borne Pathogen

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.

Resistance and tolerance of ten carrot cultivars to the hawthorn-carrot aphid, Dysaphis crataegi Kalt., in Poland

“…However, several sugar beet genotypes showed tolerance to beet root aphid [ 86 ]. Reductions of the root mass of carrot and potato plants due to the feeding of black bean aphid and green peach aphid, respectively, were reported by Łuczak et al [ 87 ] and Hoysted et al [ 88 ], respectively. Łuczak [ 52 ] further reported that black bean aphid did not always cause a decrease in the yield of sugar beet roots, which depended largely on the size of the aphid colonies.…”

Soil microbial diversity impacts plant microbiota more than herbivory

“…The herbivory-driven effect on the bacterial community composition of the roots and rhizosphere could be driven by changes in plant physiology (e.g. defence activation, carbon metabolism) and root exudation due to aphid feeding activity (Züst and Agrawal, 2016; Hoysted et al , 2018). Herbivory has been shown to alter the types of organic compounds released at the root surface leading to changes in the composition of rhizosphere microbial communities (Lareen et al , 2016; Hu et al , 2018).…”

Aphids Influence Soil Fungal Communities in Conventional Agricultural Systems

“…Nutrient flows below-ground were not measured in the current study, but aphids can affect below-ground respiration depending on plant growth stage, potentially due to alterations in C availability to soil microbes (Vestergård et al, 2004). Aphids can also alter the profiles of compounds, released from plant roots (Hoysted et al, 2018) and can also change the profiles of sugars found in AMF hyphae sharing the same host plant (Cabral et al, 2018). Moreover, aphids excrete honeydew as a result of their C rich diet of phloem sap which can be utilized as a C source by soil microbiota, thus shaping community structure and biomass (Katayama et al, 2014; Milcu et al, 2015).…”