Beneficial Insects Deliver Plant Growth-Promoting Bacterial Endophytes between Tomato Plants.

Nikoletta Galambos,Gianfranco Anfora,Valerio Mazzoni,Angela Sessitsch,Michele Perazzolli,Stéphane Compant,Felix Wäckers,Ilaria Pertot

doi:10.3390/microorganisms9061294

Abstract

Beneficial insects and mites, including generalist predators of the family Miridae, are widely used in biocontrol programs against many crop pests, such as whiteflies, aphids, lepidopterans and mites. Mirid predators frequently complement their carnivore diet by feeding plant sap with their piercing–sucking mouthparts. This implies that mirids may act as vectors of phytopathogenic and beneficial microorganisms, such as plant growth-promoting bacterial endophytes. This work aimed at understanding the role of two beneficial mirids (Macrolophus pygmaeus and Nesidiocoris tenuis) in the acquisition and transmission of two plant growth-promoting bacteria, Paraburkholderia phytofirmans strain PsJN (PsJN) and Enterobacter sp. strain 32A (32A). Both bacterial strains were detected on the epicuticle and internal body of both mirids at the end of the mirid-mediated transmission. Moreover, both mirids were able to transmit PsJN and 32A between tomato plants and these bacterial strains could be re-isolated from tomato shoots after mirid-mediated transmission. In particular, PsJN and 32A endophytically colonised tomato plants and moved from the shoots to roots after mirid-mediated transmission. In conclusion, this study provided novel evidence for the acquisition and transmission of plant growth-promoting bacterial endophytes by beneficial mirids.

Highlights

Beneficial insects provide vital services in agricultural ecosystems, such as pollination and natural pest control [1,2]
The NONEUB probe was used as a negative probe not targeting bacterial sequences and only a few green/blue-cyan fluorescent microbes could be detected on mirids fed on mock, PsJN- and 32A-inoculated plants, as an indicator of the rare presence of indigenous microorganisms (Figure S1)
Our results demonstrated that both mirids tested (M. pygmaeus and N. tenuis) are able to acquire the two beneficial bacterial strains (PsJN and 32A), both as bacteria adhering to the mirid epicuticle and in the mirid internal body through tissue contact and feeding on seed-inoculated tomato plants

Summary

Introduction

Beneficial insects (e.g., hymenopteran parasitoids, bumblebees, hoverflies, lacewings, ladybugs and mirids) provide vital services in agricultural ecosystems, such as pollination and natural pest control [1,2]. The mirids Macrolophus pygmaeus (Rambur) and Nesidiocoris tenuis (Reuter) (Hemiptera: Miridae) are widely used for the biocontrol of whiteflies, aphids and moths, among others [3,4,5,6]. Tomato can be damaged by phytophagous arthropods worldwide [7], both under field and greenhouse conditions [8]. Aphids (e.g., Myzus persicae, Aphis sp.), thrips (e.g., Frankliniella occidentalis and Thrips tabaci) and whitefly species (e.g., Bemisia tabaci and Trialeurodes vaporariorum) cause direct and indirect damage due to virus transmission [9]. To counteract these pests, the generalist mirids

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