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Abstract
Members of Gram-positive Actinobacteria cause economically important diseases to plants. Within the Rhodococcus genus, some members can cause growth deformities and persist as pathogens on a wide range of host plants. The current model predicts that phytopathogenic isolates require a cluster of three loci present on a linear plasmid, with the fas operon central to virulence. The Fas proteins synthesize, modify, and activate a mixture of growth regulating cytokinins, which cause a hormonal imbalance in plants, resulting in abnormal growth. We sequenced and compared the genomes of 20 isolates of Rhodococcus to gain insights into the mechanisms and evolution of virulence in these bacteria. Horizontal gene transfer was identified as critical but limited in the scale of virulence evolution, as few loci are conserved and exclusive to phytopathogenic isolates. Although the fas operon is present in most phytopathogenic isolates, it is absent from phytopathogenic isolate A21d2. Instead, this isolate has a horizontally acquired gene chimera that encodes a novel fusion protein with isopentyltransferase and phosphoribohydrolase domains, predicted to be capable of catalyzing and activating cytokinins, respectively. Cytokinin profiling of the archetypal D188 isolate revealed only one activate cytokinin type that was specifically synthesized in a fas-dependent manner. These results suggest that only the isopentenyladenine cytokinin type is synthesized and necessary for Rhodococcus phytopathogenicity, which is not consistent with the extant model stating that a mixture of cytokinins is necessary for Rhodococcus to cause leafy gall symptoms. In all, data indicate that only four horizontally acquired functions are sufficient to confer the trait of phytopathogenicity to members of the genetically diverse clade of Rhodococcus.
Highlights
Plant pathogenic bacteria employ an array of molecules to dampen immunity, alter plant physiological responses, and mimic plant hormones to modulate host-signaling pathways [1,2]
Our data indicate that Horizontal gene transfer (HGT) is important in virulence evolution but only four functions need to be acquired by members of Rhodococcus to gain the trait of phytopathogenicity
Isolates A44a and D188 were selected as references and were more deeply sequenced using hybrid approaches
Summary
Plant pathogenic bacteria employ an array of molecules to dampen immunity, alter plant physiological responses, and mimic plant hormones to modulate host-signaling pathways [1,2]. And often coordinately, the virulence molecules manipulate host cells to give pathogens access to host tissues and resources as well as facilitate egress and spread. Because of the intimate interactions of these pathogen-synthesized molecules with host cells, virulence genes are subject to strong selective pressures and are often dynamic, exhibiting patterns of high genetic diversity [3]. Horizontal gene transfer (HGT) is one mechanism that contributes to evolutionary dynamism, as virulence genes are often found on plasmids, associated with mobile genetic elements, and/ or located within large stretches of genomic islands that have signatures indicative of HGT [4]. A very small number of genera within Actinobacteria have members that are pathogenic to plants. Rhodococcus is a persistent pathogen and can remain associated with the plant throughout its life [13]. Its host range is exceedingly large and includes more than 120 species representing both monocots and dicots, herbaceous and woody plants [12]
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