Induced Local and Systemic Defense Responses in Tomato Underlying Interactions Between the Root-Knot Nematode Meloidogyne incognita and the Potato Aphid Macrosiphum euphorbiae.

Anne Mädicke,Ainhoa Martínez-Medina,Nicole M Van Dam,Crispus M Mbaluto,Katharina Grosser,Esraa M Ahmad

doi:10.3389/fpls.2021.632212

Abstract

Plants mediate interactions between different herbivores that attack simultaneously or sequentially aboveground (AG) and belowground (BG) organs. The local and systemic activation of hormonal signaling pathways and the concomitant accumulation of defense metabolites underlie such AG-BG interactions. The main plant-mediated mechanisms regulating these reciprocal interactions via local and systemic induced responses remain poorly understood. We investigated the impact of root infection by the root-knot nematode (RKN) Meloidogyne incognita at different stages of its infection cycle, on tomato leaf defense responses triggered by the potato aphid Macrosiphum euphorbiae. In addition, we analyzed the reverse impact of aphid leaf feeding on the root responses triggered by the RKN. We focused specifically on the signaling pathways regulated by the phytohormones jasmonic acid (JA), salicylic acid (SA), abscisic acid (ABA), and indole-3-acetic acid (IAA) as well as steroidal glycoalkaloids as induced defense compounds. We found that aphid feeding did not induce AG hormonal signaling, but it repressed steroidal glycoalkaloids related responses in leaves, specifically when feeding on plants in the vegetative stage. Root infection by the RKN impeded the aphid-triggered repression of the steroidal glycoalkaloids-related response AG. In roots, the RKN triggered the SA pathway during the entire infection cycle and the ABA pathway specifically during its reproduction stage. RKN infection also elicited the steroidal glycoalkaloids related gene expression, specifically when it was in the galling stage. Aphid feeding did not systemically alter the RKN-induced defense responses in roots. Our results point to an asymmetrical interaction between M. incognita and Ma. euphorbiae when co-occurring in tomato plants. Moreover, the RKN seems to determine the root defense response regardless of a later occurring attack by the potato aphid AG.

Highlights

Plants encounter several species of insect herbivores and pathogens that reduce their fitness
Because we used the M. incognita infection cycle stages [i.e., invasion (5 dpi), galling (15 dpi), and reproduction (30 dpi)] to time the experiment, the plants had different ages over the course of the experiment. This means that plants infected by M. incognita as well as their respective control plants were 33 days-old when the M. incognita were at the invasion stage, those used when M. incognita were at the galling stage were 43 days-old, and by the time the M. incognita had reached the reproduction stage, the plants were 58 days-old
We found that Ma. euphorbiae feeding did not alter the concentrations of jasmonic acid (JA)-Ile, salicylic acid (SA), and abscisic acid (ABA) compared to the control plants, regardless of plant age (Figures 1A–C,E– G,I–K; black vs. yellow boxplots; Supplementary Tables 2 and 8; JA levels were below the detection threshold)

Summary

Introduction

Plants encounter several species of insect herbivores and pathogens that reduce their fitness. While the JA and SA pathways form the backbone of the plant’s immune system, other hormones such as ethylene, abscisic acid (ABA), auxins, and cytokinins contribute to defense signaling (Bari and Jones, 2009; Erb et al, 2012; Kammerhofer et al, 2015). These hormones can antagonistically or synergistically interact with the JA-SA backbone of the plant’s immune signaling network. This so-called hormone cross-talk provides the plant with a powerful capacity to finely regulate its immune response to the specific attacker (Pieterse et al, 2009; Li et al, 2019)

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