Phytoplasma PMU1 exists as linear chromosomal and circular extrachromosomal elements and has enhanced expression in insect vectors compared with plant hosts

Abstract

SummaryPhytoplasmas replicate intracellularly in plants and insects and are dependent on both hosts for dissemination in nature. Phytoplasmas have small genomes lacking genes for major metabolic pathways. Nevertheless, their genomes harbour multicopy gene clusters that were named potential mobile units (PMUs). PMU1 is the largest most complete repeat among the PMUs in the genome of Aster Yellows phytoplasma strain Witches' Broom (AY-WB). PMU1 is c. 20 kb in size and contains 21 genes encoding DNA replication and predicted membrane-targeted proteins. Here we show that AY-WB has a chromosomal linear PMU1 (L-PMU1) and an extrachromosomal circular PMU1 (C-PMU1). The C-PMU1 copy number was consistently higher by in average approximately fivefold in insects compared with plants and PMU1 gene expression levels were also considerably higher in insects indicating that C-PMU1 synthesis and expression are regulated. We found that the majority of AY-WB virulence genes lie on chromosomal PMU regions that have similar gene content and organization as PMU1 providing evidence that PMUs contribute to phytoplasma host adaptation and have integrated into the AY-WB chromosome.

Effector Biology of Plant-Associated Organisms: Concepts and Perspectives

“…T3SS effectors released early in the epiphytic growth of P. syringae PsyB728a are important for pathogen survival during this phase and T3SS effectors such as HopAA1 and HopZ3 may play specific roles during epiphytic growth of this pathogen on specific hosts (Lee et al 2012b). Phytoplasmas, which require insect vectors for transmission to plants, differentially regulate effector genes for insect and plant colonization (Toruno et al 2010;MacLean et al 2011). Fungal pathogens Colletotrichum higginsianum and Colletotrichum graminicola, infecting Arabidopsis thaliana and maize, respectively, use transcriptional regulation to synthesize and secrete different sets of effectors and enzymes important for different phases of infection: The biotrophic phase is augmented by effectors and secondary metabolism enzymes whereas the necrotrophic phase brings in hydrolases and transporters (O'Connell et al 2012).…”

“…When the environment changes, for instance, through the emergence of disease resistance in the host plant, preexisting isolates harboring a set of effectors advantageous for the new conditions could be positively selected. This evolutionary "bet-hedging" strategy, in which the pathogen population benefits from extensive heterogeneity in the effector complement, could be one of the tactics that enable pathogens to avoid extinction in the arms race (Toruno et al 2010;Simons 2011). For example, a functionally redundant heterogeneous effector repertoire would enable the pathogen population to include strains that can disable key ETPs while evading perception by plant immunoreceptors (Boller and Felix 2009).…”

Phytoplasma Effector SAP54 Induces Indeterminate Leaf-Like Flower Development in Arabidopsis Plants

“…2). One of these effectors, SAP36, is encoded within a potential mobile unit (referred to as PMU1) whose expression we have previously shown to be up-regulated in insects, where PMU1 exists as an extrachromosomal circular element (Toruñ o et al, 2010).…”

“…We have hypothesized that phytoplasmas such as AY-WB produce a range of proteinaceous effectors that are released into the cytoplasm of host cells to modulate developmental processes in a host-specific (i.e. regulated) manner (Hogenhout and Loria, 2008;Bai et al, 2009;Toruñ o et al, 2010;Sugio et al, 2011). Having established that Arabidopsis is susceptible to AY-WB infection and exhibits symptoms that are characteristic of this phytoplasma strain, we set out to identify AY-WB effector(s) that induce the formation of the leaf-like flowers that are a hallmark of phytoplasma infection through the expression of candidate effectors in transgenic Arabidopsis.…”

Exploring the phytoplasmas, plant pathogenic bacteria

“…P. asteris Macrosteles striifrons Shiomi and Sugiura (1983) from their hosts . Phytoplasma genomes contain the sodA gene, which encodes superoxide dismutase that can inactivate reactive oxygen species (ROS) (Miura et al 2012 (Toruño et al 2010), suggesting the ability to transpose within the genome.…”