Invasive mutualisms between a plant pathogen and insect vectors in the Middle East and Brazil

Abstract

Complex multi-trophic interactions in vectorborne diseases limit our understanding and ability to predict outbreaks. Arthropod-vectored pathogens are especially problematic, with the potential for novel interspecific interactions during invasions. Variations and novelties in plant–arthropod–pathogen triumvirates present significant threats to global food security. We examined aspects of a phytoplasma pathogen of citrus across two continents. ‘Candidatus Phytoplasma aurantifolia’ causes Witches' Broom Disease of Lime (WBDL) and has devastated citrus production in the Middle East. A variant of this phytoplasma currently displays asymptomatic or ‘silent’ infections in Brazil. We first studied vector capacity and fitness impacts of the pathogen on its vectors. The potential for co-occurring weed species to act as pathogen reservoirs was analysed and key transmission periods in the year were also studied. We demonstrate that two invasive hemipteran insects—Diaphorina citri and Hishimonus phycitis—can vector the phytoplasma. Feeding on phytoplasma-infected hosts greatly increased reproduction of its invasive vector D. citri both in Oman and Brazil; suggesting that increased fitness of invasive insect vectors thereby further increases the pathogen's capacity to spread. Based on our findings, this is a robust system for studying the effects of invasions on vectorborne diseases and highlights concerns about its spread to warmer, drier regions of Brazil.

Asymptomatic Phytoplasma Reveal a Novel and Troublesome Infection

“…The site was chosen as plant material there had previously been found to be infected with "Ca. P. aurantifolia," but showing no visible symptoms [17].…”

“…Detailed research into this system has been limited, some suggest that the silent infection may be due to ultra-low pathogen titre levels within the host plant [12,14] or due to different interactions with plant defences [15] or insect vectors [16,17]. Silent infections are difficult to monitor and pose a significant risk to global food security, given that the limited knowledge we have suggests they may be as destructive as symptomatic [18], but we do not yet know the full extent of their range.…”

“…Our study examined DEGs in symptomatic and asymptomatic infections of the Phytoplasma in acid lime trees. Although asymptomatic infections have been linked to fitness benefits in the vectors of this pathogen [17], our knowledge of understanding of gene expression differences in an asymptomatic infection are extremely limited. One way to understand the effects and biology of asymptomatic infections is by developing our knowledge of these differentially expressed genes.…”

The influence of bacteria on multitrophic interactions among plants, psyllids, and pathogen

“…Surprisingly, D. citri can transmit 'Ca. Phytoplasma aurantifolia' to acid lime (Citrus aurantifolia), albeit at a lower frequency than the leafhopper vector Hishimonus phycitis (Queiroz et al, 2016). So far, transovarial transmission was detected only in H. phycitis.…”

“…Liberibacter europaeus' causing symptoms in Scotch broom might have been introduced with the psyllid A. spartiophila (Nelson, 2015). A similar risk results by the introduction of invasive vectors into an ecosystem in which novel pathogen-vector interactions can occur (Queiroz et al, 2016). In light of those events, identifying bacteria associated with psyllids and their influence on multitrophic interactions among plants, psyllids, and pathogen is a main priority.…”