Multiple guests in a single host: interactions across symbiotic and phytopathogenic bacteria in phloem‐feeding vectors – a review

Abstract

Some pathogenic phloem‐limited bacteria are a major threat for worldwide agriculture due to the heavy economic losses caused to many high‐value crops. These disease agents – phytoplasmas, spiroplasmas, liberibacters, and Arsenophonus‐like bacteria – are transmitted from plant to plant by phloem‐feeding Hemiptera vectors. The associations established among pathogens and vectors result in a complex network of interactions involving also the whole microbial community harboured by the insect host. Interactions among bacteria may be beneficial, competitive, or detrimental for the involved microorganisms, and can dramatically affect the insect vector competence and consequently the spread of diseases. Interference is observed among pathogen strains competing to invade the same vector specimen, causing selective acquisition or transmission. Insect bacterial endosymbionts are another pivotal element of interactions between vectors and phytopathogens, because of their central role in insect life cycles. Some symbionts, either obligate or facultative, were shown to have antagonistic effects on the colonization by plant pathogens, by producing antimicrobial substances, by stimulating the production of antimicrobial substances by insects, or by competing for host infection. In other cases, the mutual exclusion between symbiont and pathogen suggests a possible detrimental influence on phytopathogens displayed by symbiotic bacteria; conversely, examples of microbes enhancing pathogen load are available as well. Whether and how bacterial exchanges occurring in vectors affect the relationship between insects, plants, and phytopathogens is still unresolved, leaving room for many open questions concerning the significance of particular traits of these multitrophic interactions. Such complex interplays may have a serious impact on pathogen spread and control, potentially driving new strategies for the containment of important diseases.

Functional variation in phyllogen, a phyllody‐inducing phytoplasma effector family, attributable to a single amino acid polymorphism

“…These findings suggest that horizontal gene transfer of phyllogens by PMUs has contributed to the acquisition and sharing of phyllody‐inducing activity among phytoplasmas. Phytoplasmas have a wide plant host range and can naturally co‐infect the same host plants (Wei et al ., 2016), whereas insect transmission is specific between different phytoplasmas and distinct insect vector taxa (Gonella et al ., 2019). These results suggest that the co‐infection of phylogenetically diverse phytoplasma strains/species in their common plant hosts can facilitate horizontal gene transfer among phytoplasma genomes.…”

Activation of Immune Genes in Leafhoppers by Phytoplasmas and Symbiotic Bacteria

“…Besides carrying phytoplasmas, E. variegatus harbors bacterial symbionts, like many other Auchenorrhyncha (Baumann, 2005); among these, the acetic acid bacterium Asaia has been experimentally documented to limit the acquisition of FDp, after oral administration (Gonella et al, 2018). Symbiont-mediated control mechanisms against phytopathogens include competitive nutrient uptake by symbiotic bacteria, erection of a physical barrier preventing gut establishment and crossing by pathogens, symbiont-mediated immune response of the insect, and the release of antagonistic compounds (Gonella et al, 2019). In E. variegatus , the involvement of either Asaia -mediated mechanisms stimulating the host immune response or physical exclusion were suggested (Gonella et al, 2018); however, little experimental evidence has been provided on the effects of symbiotic bacteria on E. variegatus immunity (Tedeschi et al, 2017) and no data are available on the influence of phytoplasma-symbiont multiple infection on the insect response.…”

Symbionts in insect biology and pest control – an introduction

“…This is nicely illustrated by Gonella et al. () who review the interactions between symbionts of phloem‐feeding phytophagous insects. These insects may act as vectors of bacterial phytopathogens when they move from infected to uninfected (or infected) host plants.…”