Abstract

In natural and agricultural conditions, plants are attacked by a community of herbivores, including aphids and mites. The green peach aphid and the two-spotted spider mite, both economically important pests, may share the same plant. Therefore, an important question arises as to how plants integrate signals induced by dual herbivore attack into the optimal defensive response. We showed that regardless of which attacker was first, 24 h of infestation allowed for efficient priming of the Arabidopsis defense, which decreased the reproductive performance of one of the subsequent herbivores. The expression analysis of several defense-related genes demonstrated that the individual impact of mite and aphid feeding spread systematically, engaging the salicylic acid (SA) and jasmonic acid (JA) signaling pathways. Interestingly, aphids feeding on the systemic leaf of the plant simultaneously attacked by mites, efficiently reduced the magnitude of the SA and JA activation, whereas mites feeding remotely increased the aphid-induced SA marker gene expression, while the JA-dependent response was completely abolished. We also indicated that the weaker performance of mites and aphids in double infestation essays might be attributed to aliphatic glucosinolates. Our report is the first to provide molecular data on signaling cross-talk when representatives of two distinct taxonomical classes within the phylum Arthropoda co-infest the same plant.

Highlights

  • In natural and agricultural conditions, plants are often attacked by multiple herbivores

  • Induced responses are triggered by elicitors such as herbivore-associated molecular patterns (HAMPs) and damage-associated molecular patterns (DAMPs) [9,10]

  • Sci. 2019, 20, 806 when TSSM was transferred onto Arabidopsis rosette leaves with only a few min delay after GPA had been caged on one of the leaves of the rosette, the presence of GPA had no impact on the oviposition of TSSM (Figure 1A)

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Summary

Introduction

In natural and agricultural conditions, plants are often attacked by multiple herbivores. Induced responses are triggered by elicitors such as herbivore-associated molecular patterns (HAMPs) and damage-associated molecular patterns (DAMPs) [9,10]. HAMPs are herbivore-derived molecules coming from the invaders’ oral or ovipositor secretions, while DAMPs are released by the host plant undergoing necrosis and are related to the mode of herbivore feeding and the range of tissue damage at the feeding site [11]. For a given host plant, herbivores representing similar feeding strategies, salivary composition, type and range of wounding, etc., trigger a systemic acquired resistance (SAR), which by phytohormonal signaling [jasmonic acid (JA)/ethylene (ET), salicylic acid (SA), abscisic acid (ABA)] spreads to non-infested, distal organs of the plant [12]. Systemic changes in defense signaling in the non-infested leaves of the mite-infested host-plants can prepare the plant for the attack of the invader. The growing knowledge of systemic effects of the mentioned herbivores opens another, mostly unexplored field—the defense signaling crosstalk and integration with various biotic and abiotic stresses

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