title: Analysis of genome sequences from plant pathogenic Rhodococcus reveals genetic novelties in virulence loci.
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.
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America; Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Allison L
authors.initials: AL
authors.lastname: Creason
authors.affiliation: Laboratoire de Biotechnologie Vegetale, Universite Libre de Bruxelles, Gosselies, Belgium.
authors.forename: Olivier M
authors.initials: OM
authors.lastname: Vandeputte
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Elizabeth A
authors.initials: EA
authors.lastname: Savory
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America; Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Edward W
authors.initials: EW
authors.lastname: Davis
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Melodie L
authors.initials: ML
authors.lastname: Putnam
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Erdong
authors.initials: E
authors.lastname: Hu
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: David
authors.initials: D
authors.lastname: Swader-Hines
authors.affiliation: Laboratoire de Biotechnologie Vegetale, Universite Libre de Bruxelles, Gosselies, Belgium.
authors.forename: Adeline
authors.initials: A
authors.lastname: Mol
authors.affiliation: Laboratoire de Biotechnologie Vegetale, Universite Libre de Bruxelles, Gosselies, Belgium.
authors.forename: Marie
authors.initials: M
authors.lastname: Baucher
authors.affiliation: University of Antwerp, Department of Biology, Laboratory of Plant Growth and Development, Antwerp, Belgium.
authors.forename: Els
authors.initials: E
authors.lastname: Prinsen
authors.affiliation: University of Antwerp, Department of Biology, Laboratory of Plant Growth and Development, Antwerp, Belgium.
authors.forename: Magdalena
authors.initials: M
authors.lastname: Zdanowska
authors.affiliation: Informatics Research Core Facility, University of Missouri, Columbia, Missouri, United States of America.
authors.forename: Scott A
authors.initials: SA
authors.lastname: Givan
authors.affiliation: Laboratoire de Biotechnologie Vegetale, Universite Libre de Bruxelles, Gosselies, Belgium.
authors.forename: Mondher
authors.initials: M
authors.lastname: El Jaziri
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America; Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America; United States Department of Agriculture, Agricultural Research Service, Horticultural Crops Research Laboratory, Corvallis, Oregon, United States of America.
authors.forename: Joyce E
authors.initials: JE
authors.lastname: Loper
authors.affiliation: Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America; Department of Pharmaceutical Sciences, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Taifo
authors.initials: T
authors.lastname: Mahmud
authors.affiliation: Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon, United States of America; Molecular and Cellular Biology Program, Oregon State University, Corvallis, Oregon, United States of America; Center for Genome Research and Biocomputing, Oregon State University, Corvallis, Oregon, United States of America.
authors.forename: Jeff H
authors.initials: JH
authors.lastname: Chang
mesh_terms: D000595:Amino Acid Sequence; D001426:Bacterial Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D017124:Conserved Sequence; D019143:Evolution, Molecular; D050939:Gene Fusion; D022761:Gene Transfer, Horizontal / Q000235:genetics; D056426:Genetic Loci / Q000235:genetics*; D016680:Genome, Bacterial / Q000235:genetics; D023281:Genomics; D007541:Isopentenyladenosine / Q000378:metabolism; D008969:Molecular Sequence Data; D009876:Operon / Q000235:genetics; D010944:Plants / Q000382:microbiology*; D010957:Plasmids / Q000235:genetics; D011110:Polymorphism, Genetic; D012240:Rhodococcus / Q000235:genetics* / Q000378:metabolism / Q000472:pathogenicity* / Q000502:physiology; D017421:Sequence Analysis
chemical_list: D001426:Bacterial Proteins; C001478:N(6)-(delta(2)-isopentenyl)adenine; D007541:Isopentenyladenosine