Horizontal Transfer of the Plant Virulence Gene, nec1 , and Flanking Sequences among Genetically Distinct Streptomyces Strains in the Diastatochromogenes Cluster

Abstract

Evidence for the horizontal transfer of a pathogenicity island (PAI) carrying the virulence gene nec1 and flanking sequences among Streptomyces strains in the Diastatochromogenes cluster is presented. Plant-pathogenic, thaxtomin-producing Streptomyces strains, previously classified as S. scabiei based on the conventionally used phenotypic characteristics, were found to be genetically distinct from the type strain of S. scabiei based on DNA relatedness and 16S rDNA sequence analysis. Pairwise DNA-DNA hybridizations between some of these strains and the S. scabiei type strain were as low as 36%, a value much below what is conventionally accepted for species identity (70%). The sequence of the nec1 gene, however, was identical in all the S. scabiei and S. scabiei-like strains tested, irrespective of their DNA relatedness to the type strain of S. scabiei, their geographic origin, or the isolation host. Furthermore, a 26-kb DNA fragment including and flanking nec1 was also conserved among these strains based on restriction and Southern analyses. These data indicate that the etiology of potato scab is more complex than previously recognized; this result has important implications for potato scab management strategies. Previous research has suggested that horizontal transfer of a PAI was the mechanism for evolution of pathogenicity in S. acidiscabies and S. turgidiscabies, species that lie outside of the Diastatochromogenes cluster. Data presented here support this model and indicate that PAI transfer also has occurred frequently in species closely related to S. scabiei.Hundreds of soil-dwelling, saprophytic streptomycetes have been described, while relatively few species are known pathogens of plants (see reference 20 for a review); hence, pathogenicity is considered a rare phenotype in the genus Streptomyces. Streptomycetes are filamentous, gram-positive prokaryotes that produce an array of agriculturally and clinically important secondary metabolites. Members of this genus have a complex morphology: spores germinate to produce substrate mycelium from which aerial hyphae arise, which, in turn, fragment into spore chains.Three well-characterized, genetically diverse species, S. scabiei, S. acidiscabies, and S. turgidiscabies, cause scab symptoms on potato and tap root crops (20). S. scabiei (18) was the first species to be described and occurs worldwide. S. acidiscabies (17) and S. turgidiscabies (22) were first reported as a cause of potato scab in 1977 and 1996, respectively. In contrast to S. scabiei, S. acidiscabies and S. turgidiscabies have very limited geographic distributions, the northeastern United States and the island of Hokkaido in Japan, respectively. The similarity in symptoms and host range of the three pathogenic species suggests a common mechanism of pathogenicity. Members of S. scabiei, S. acidiscabies, and S. turgidiscabies are known to produce a family of dipeptide phytotoxins, thaxtomins (3,14,19), which have recently been shown to be required for disease development (10). Although these three sp...

A Patchwork of Streptomyces Species Isolated from Potato Common Scab Lesions in North America

“…4). This finding substantiates an earlier report that S. bottropensis may include pathogenic strains (Bukhalid et al 2002). The 16S rDNA gene from an isolate of a third ribotype was sequenced; it is most closely related to two nonpathogenic isolates also derived from potato CS lesions, ME02-6987.2a (GenBank accession EU080949.1) and AK03-4B (EU080939.1), and to S. achromogenes subspecies tomaymyceticus.…”

“…With the advent of molecular genetic characterization of CS-causing species, it became apparent that Streptomyces scabies was a complex of species (BouchekMechiche et al 2000;Bukhalid et al 2002;Doering-Saad et al 1992;Healy and Lambert 1991;Takeuchi et al 1996). Morphological, physiological and molecular evidence currently supports the designation of about ten CS-causing species known from one or more geographic locations around the world.…”

“…Thaxtomin is the only known pathogenicity determinant in Streptomyces, and the presence or absence of txtAB is 100% correlated with pathogenicity in more than 100 isolates for which pathogenicity assays have been carried out ( (Wanner 2006(Wanner , 2007a; see also 16S-1R 5′-AGAAAGGAGGTGATCCAGCC-3′ (Bukhalid et al 2002) species S. scabies, S. europaeiscabiei, S. stelliscabiei, a recently identified strain from Idaho, S. acidiscabies and S. turgidiscabies have been described (Wanner 2006). The decision matrix used to assign species for North American plant pathogenic Streptomyces isolates based on characteristic sequence types at the +, !…”

Molecular Evolution of Pathogenicity-Island Genes in Pseudomonas viridiflava

“…While there is sound evidence that the evolution of pathogenesis involves the acquisition of virulence-related genes (including entire PAIs) via HGT (Reid et al 2000;Bukhalid et al 2002), some studies reported that PAIs have been retained within pathogen species over evolutionary time (e.g., Escobar-Paramo et al 2003;Gressmann et al 2005;Rohmer et al 2004;Nallapareddy et al 2005). We do not know why some PAIs are evolutionary stable whereas others are not, but our results provide one possible explanation: Unlike a PAI acquired via recent HGT, an evolutionary stable PAI can work as a large reservoir of preexisting genetic variation in this highly polymorphic species.…”

An Arabidopsis Mutant Resistant to Thaxtomin A, a Cellulose Synthesis Inhibitor fromStreptomycesSpecies[W]

“…Potato scab is a disease of major economic importance in most potato-producing areas of the world (Lambert and Loria, 1989). The genes that encode the thaxtomin biosynthetic pathway appear to lie on a pathogenicity island that was transmitted to Streptomyces species, resulting in the emergence of new pathogenic species in agricultural production systems (Healy et al, 1999(Healy et al, , 2000Bukhalid et al, 2002). The pathogenicity of various S. scabies isolates is correlated with their ability to produce thaxtomin A (King et al, 1991;Loria et al, 1995;Goyer et al, 1998;Kinkel et al, 1998).…”