Abstract

Plants suffer multiple, simultaneous assaults from above and below ground. In the laboratory, pests and/or pathogen attack are commonly studied on an individual basis. The molecular response of the plant to attack from multiple organisms and the interaction of different defense pathways is unclear. The inducible systemic responses of the potato (Solanum tuberosum L.) host plant were analyzed to characterize the plant-mediated indirect interactions between a sedentary, endoparasitic nematode (Globodera pallida), and a phloem-sucking herbivore (Myzus persicae). The reproductive success of M. persicae was greater on potato plants pre-infected with G. pallida compared to control plants. Salicylic acid (SA) increased systemically in the leaves of potato plants following nematode and aphid infection singly with a corresponding increase in expression of SA-mediated marker genes. An increase in jasmonic acid associated with aphid infection was suppressed when plants were co-infected with nematodes. Our data suggests a positive, asymmetric interaction between a sedentary endoparasitic nematode and a sap-sucking insect. The systemic response of the potato plant following infection with G. pallida indirectly influences the performance of M. persicae. This work reveals additional secondary benefits of controlling individual crop pests.

Highlights

  • Plants are simultaneously attacked by a number of invading organisms, both above and below ground

  • There was a significant increase in endogenous Salicylic acid (SA) in the leaves of potato plants 14 days after infection with G. pallida

  • The presence of nematodes significantly increased total levels of SA in leaves of potato plants, (4541.42 ± 268.2 ng/g FW for nematode-infected plants and 2132.77 ± 758.57 ng/g FW for control plants, P ≤ 0.01) (Figure 1A). These results suggest an activation of the systemic acquired resistance (SAR) pathway in the leaves of potato plants, which is mediated by SA (Gaffney et al, 1993)

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Summary

Introduction

Plants are simultaneously attacked by a number of invading organisms, both above and below ground. Infection of a host plant that carries a pre-existing pest or pathogen burden will influence the success of the secondary or primary infection, depending on a range of factors including the species under investigation, the sequence of pest arrival, the severity of the infestation (Erb et al, 2011; Johnson et al, 2012; Huang et al, 2016; Papadopoulou and van Dam, 2017), and the changes in primary and secondary metabolites in the shared plant tissues (Bezemer et al, 2003; Wardle et al, 2004; Schoonhoven et al, 2005; van Geem et al, 2016) Given this context dependency, it is unsurprising that both positive and negative effects of below-ground organisms on those above-ground have been reported. Salicylic acid (SA)-dependent signaling seems to be crucial for resistance against biotrophic pathogens (Glazebrook, 2005; Loake and Grant, 2007) and cyst nematodes have been reported to activate a strong SA-mediated defense response in shoots of Arabidopsis thaliana from 5 days post inoculation (Wubben et al, 2008)

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