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Taxonomy of Pseudomonas Syringae

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Taxonomy of Pseudomonas Syringae 002_Young_S5 9-09-2010 12:02 Pagina 5 Journal of Plant Pathology (2010), 92 (1, Supplement), S1.5-S1.14 Edizioni ETS Pisa, 2010 S1.5 MINIREVIEW TAXONOMY OF PSEUDOMONAS SYRINGAE J.M. Young Landcare Research, Private Bag 92170, Auckland, New Zealand SUMMARY ported but, without giving practical means of identifica- tion of taxa, they are impractical because they cannot be The evolution of the processes of classification, iden- applied. tification and nomenclature of Pseudomonas syringae are An underlying theme of the history of bacteriology is described. Originally referring to a pathogenic species of of the uncertainty that has arisen when the taxonomic lilac, in the revision of bacterial names in 1980, P. sy- elements, classification, identification and nomencla- ringae came to represent more than 40 host specific ture, have not been in synchrony. The taxonomy of pathogenic populations, as pathovars. DNA-DNA hy- plant pathogenic bacteria was subject to the same con- bridization studies and recent multilocus sequence fusion as in other fields, and within the genus analyses (MLSA) indicate a ‘P. syringae complex’ that Pseudomonas, a pathogenic population identified for now encompasses up to ten Pseudomonas species and 60 part of its history as the ‘P. syringae complex’, has given pathovars of P. syringae. A re-evaluation of the complex expression to many of the issues. This discussion briefly using poly-phasic approaches could see the revision of describes the history of the P. syringae complex to show these species and the distribution of pathovars in a num- how the problems were resolved, and to outline the ber of species or genomospecies. Alternative classifica- principles that may guide taxonomy in future. tions and nomenclature of these taxa is discussed. EARLY HISTORY OF THE GENUS INTRODUCTION PSEUDOMONAS AND P. SYRINGAE Biological discussion is dependent on reliable sys- When it was first proposed by Migula (1894), the tems of names (nomenclature) provided by taxonomic genus Pseudomonas was understood to comprise all bac- studies. Bacterial taxonomy comprises two interdepend- teria that were Gram-negative rods, aerobic with ent activities; classification and identification. These chemorganotrophic metabolisms and motile by one or taxonomic activities cannot be conducted in isolation more polar flagella. Only recently was this definition re- from one another. Classifications are based on compara- fined largely using comparative analyses of 16S rDNA. tive studies of authenticated strains and aim to give ex- The ‘fluorescent, poly-β-hydroxybutyrate negative pression to relationships as natural hierarchies (Young pseudomonads’ associated with the type species, P. aerug- et al., 1992). The outcome of classification is the provi- inosa, and including P. syringae and related species, are sion of names (nomenclature) to be applied to identified now included in the γ-Proteobacteria. Most ‘non-fluores- taxa. One expectation of modern systematics has been cent, poly-β-hydroxybutyrate positive pseudomonads’, that genera and species will be precisely circumscribed Acidovorax, Burkholderia and Ralstonia, are now includ- and that methods would be available for the allocation ed in the β-Proteobacteria. of isolates to those groups (Murray et al., 1990; Van- With the proposal of the genus, populations of plant damme et al., 1996; Stackebrandt et al., 2002; Tindall et pathogenic bacteria were reported as Pseudomonas al., 2010). If taxonomists do not provide means of iden- species, beginning with P. mori (Boyer and Lambert, tification then there is no way to differentiate known 1893) Stevens 1913, followed by P. syringae van Hall from unknown taxa and to expand repositories of au- 1902. Many plant pathogenic Pseudomonas spp. fol- thentic strains for further study. Informative classifica- lowed thereafter. Early on it was established that, with tions that indicate bacterial relationships have been re- important exceptions, most pathogenic pseudomonads were specific to limited numbers of host taxa. P. mori was then, and still is, considered to be specific to Morus Corresponding author: J.M. Young spp. By contrast, a small number of pathogens affected Fax: +64.95744101 E-mail: [email protected] more than one unrelated host, most notably P. syringae, 002_Young_S5 9-09-2010 12:02 Pagina 6 S1.6 Taxonomy of Pseudomonas syringae Journal of Plant Pathology (2010), 92 (1, Supplement), S1.5-S1.14 first isolated from lilac (see ‘The pathogenic structure of without the designation or deposition of type or other P. syringae’ below). reference strains, making reinvestigation and revision Until the 1960s, it was believed that a significant impossible. It was only when adequate culture collec- component of the physiology of pathogenic bacteria tions of authentic strains were made, allowing the sys- must be devoted to pathogenic activity (Burkholder and tematic comparison of comprehensive numbers of Starr, 1948) and it was further assumed that simple nu- strains of plant pathogenic bacteria under standardized tritional and cultural differences reflected deep-seated conditions, that it became clear that many species, in- metabolic and genetic differences associated with path- cluding many Pseudomonas spp. (Stanier et al., 1966), ogenicity. Early proposals of pathogenic species were were not differentiated using any of the biochemical based on small numbers of morphological, biochemical and nutritional tests or other methods then available. A and nutritional tests, and colony appearance on differ- survey (Buchanan et al., 1966) found that most bacterial ent media, many of which are now known to be highly names, of which there were 20,000-30,000, were illegiti- variable or unstable. This assumption, that specific eco- mate, were synonyms, or for which there was no record logical responses involved large components of cell me- of authentic reference strains, making reinvestigation of tabolism was generally assumed by bacteriologists and taxa impossible. Recognition of the enormity of nomen- resulted in a proliferation of species names as synonyms clatural confusion and the lack of regulation of nomen- for the same pathogen. It was common for synonyms to clature led the International Committee on the System- be used in different parts of the world without under- atics of Bacteria (now the International Committee on standing that these referred to the same pathogen and the Systematics of Prokaryotes) to propose a complete disease. revision of bacterial nomenclature, embodied in the 1976 Revision of the International Code of Nomencla- Origins of the ‘P. syringae complex’. In a study of 15 ture of Bacteria (the Code; Lapage et al., 1975, now su- determinative tests considered to differentiate fluores- perseded by Lapage et al., 1992 and amendments). This cent plant pathogenic Pseudomonas spp., Lelliott et al. first edition legislated a new start to bacterial nomencla- (1966) showed that only five tests: production of levan, ture based upon an inventory of those bacteria pub- oxidase activity, capacity to rot potato, production of lished previously that met the criteria of the revised arginine dihydrolase, and hypersensitivity reaction in to- Code, and specified the requirements for the legitimate bacco (LOPAT) differentiated five distinct pathogenic publication of correct names, discussed in Young species groups. Species that gave negative reactions in (2008). Central to the revision was the development of the tests for oxidase activity, capacity to rot potato and the Approved Lists of Bacterial Names (Skerman et al., production of arginine dihydrolase, and positive hyper- 1980), which were to include only names that con- sensitivity reactions in tobacco were identified as formed fully to the revised Code. When published, LOPAT Group I pathogens. Subsequently, the more ex- 1791 species in 290 genera were recorded (Euzeby, tensive study of Sands et al. (1970) showed that many 1997-2010). As a consequence of this revision, names of named species in LOPAT Group I could not be distin- most important bacterial plant pathogenic species did guished phenotypically and that the distinct pathogenic not conform to the criteria for listing and would not be populations could not be differentiated using the bio- included as valid names in the Approved Lists, leaving chemical and nutritional tests then available. Prelimi- them without standing in nomenclature. This lacuna led nary DNA-DNA hybridization studies (Palleroni et al., directly to the proposal (Young et al., 1978) that specific 1972; Pecknold and Grogan, 1973) indicated a genomic pathogens be named at infrasubspecific level as patho- diversity within LOPAT Group 1, but were inadequate vars (a level not covered by the Code), to be regulated as the basis for significant taxonomic conclusions. The under the auspices of the International Society for Plant idea evolved that there existed a ‘P. syringae complex’ Pathology. This recommendation was accepted and In- represented as a single species comprising distinct pop- ternational Standards for Naming Pathovars (the Stan- ulations capable of infecting limited ranges of hosts dards; Dye et al., 1980) were introduced. The origins of (Stolp et al., 1965; Doudoroff and Palleroni, 1974). pathovar nomenclature and a critique of it are detailed in Young (2008). THE GENERAL REVISION OF BACTERIAL P. syringae pathovars. Because most fluorescent NOMENCLATURE plant pathogenic Pseudomonas spp. did not satisfy the criteria for recognition as distinct species, all LOPAT The
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