Emended classification of xanthomonad pathogens on citrus

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Emended classification of xanthomonad pathogens on citrus
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  Plant Pathology Department Papers in Plant Pathology  University of Nebraska - Lincoln  Year    Emended classification of xanthomonadpathogens on citrus Norman W. Schaad ∗ Elena Postnikova † George Lacy ‡ Aaron Sechler ∗∗ Irina V. Agarkova †† Paul E. Stromberg ‡‡ Verlyn K. Stromberg § Anne M. Vidaver ¶ ∗ ARS-USDA † ARS-USDA ‡ Virginia Polytechnic Institute and State University, Blacksburg, VA ∗∗ ARS-USDA †† University of Nebraska - Lincoln, iagarkova2@unl.edu ‡‡ ARS-USDA § Virginia Polytechnic Institute and State University, Blacksburg, VA ¶ University of Nebraska - Lincoln, avidaver1@unl.eduThis paper is posted at DigitalCommons@University of Nebraska - Lincoln.http://digitalcommons.unl.edu/plantpathpapers/96  Systematic and Applied Microbiology 29 (2006) 690–695 ERRATUM Emended classification of xanthomonad pathogens on citrus Norman W. Schaad a,  , Elena Postnikova a , George Lacy b , Aaron Sechler a ,Irina Agarkova c , Paul E. Stromberg a , Verlyn K. Stromberg b , Anne K. Vidaver c a ARS-USDA, Foreign Disease-Weed Science Research Unit, 1301 Ditto Avenue, Ft. Detrick, MD 21702, USA b Department of Plant Pathology, Physiology, and Weed Science, Virginia Polytechnic Institute and State University,Blacksburg, VA 24061, USA c Department of Plant Pathology, University of Nebraska, Lincoln, NE 68588, USA In the paper by Schaad et al. [24] on reclassification of several xanthomonads, nomenclatural errors weremade. The name  Xanthomonas smithii   subsp.  citri  proposed for the former taxon  X. campestris  pv.  citri  (  ¼  X. axonopodis  pv.  citri  ) is illegitimate. Following thereinstatement of   X. citri   ( ex  Hasse 1915) Gabriel et al.[9] as a validly published name, Young et al. [34] wrote that the reinstatement of this epithet was based on adescription that was inadequate in terms of modernpractice for the purpose of formal classification. Thisreport was subsequently summarized by the Interna-tional Committee on the Systematics of Bacteria (ICSB)Subcommittee on the Taxonomy of the Genus  Pseudo-monas  and Related Organisms [32] as implying rejectionof the epithet, which the Subcommittee itself appearedto endorse. As we now understand, in accord with theInternational Code of Nomenclature of Prokaryotes(‘the Code’—hitherto the International Code of No-menclature of Bacteria [14]) the Judicial Commission of the ICSP only may reject a name for precisely specifiedreasons (Rule 56a). We also misinterpreted the subse-quent establishment of the pathovar ‘‘ citri  ’’ within Xanthomonas axonopodis  [29] as further evidence forrejection of reinstatement of   X. citri   [9]. Finally,believing that the epithet ‘‘ citri  ’’ had been rejected, wefollowed rule 23a of the Code [14] and proposed anillegitimate specific epithet ‘‘ smithii  ’’ (which also re-quired establishing the subspecies epithet ‘‘ smithii  ’’replacing ‘‘ malvacearum ’’; see rule 13a [14]). In fact,  X.citri   Gabriel et al. 1989 was a legitimate, validlypublished name that was allowed to fall into abeyancebecause of the inadequacies perceived in its description.Schaad et al. [24] indicated their support for theconclusions of Gabriel et al. [9] but included DNA–D-NA reassociation data indicated as necessary by formodern classification [26,31]. One purpose of this note isto recognize by effective publication the species relatedto pathogenic xanthomonads of citrus. The secondpurpose is to avoid confusion in plant pathologicalliterature by replacing the illegitimate subspecies name X. smithii   subsp. ‘‘smithii’’ with  X. citri   subsp. ‘‘mal-vacearum’’. For that purpose, corrected protologues forthose species and subspecies are reported here:  X. citri  subsp.  citri   and  X. citri   subsp.  malvacearum ;  X. fuscans subsp.  fuscans  and  X. fuscans  subsp.  aurantifolii  ; and  X.alfalfae  subsp.  alfalfae  and  X. alfalfae  subsp.  citrumelonis .We also present (Table 1) GenBank accessionnumbers for the intergeneric spacer (ITS) sequencesfor the type strains proposed in this note [24]. Protologues Abbreviations for culture collections in which typestrains are on deposit: ATCC  ¼  American Type CultureCollection, Manassas, VA, USA; CFBP  ¼  CollectionFrancaise de Bacteries Phytopathogenes, Angers,France; ICMP  ¼  International Collection of Micro-organisms from Plants, Auckland, New Zealand;ICPB  ¼  International Collection of Phytopathogenic ARTICLE IN PRESS www.elsevier.de/syapm0723-2020/$-see front matter r 2006 Elsevier GmbH. All rights reserved.doi:10.1016/j.syapm.2006.08.001DOI of srcinal article: 10.1016/j.syapm.2005.03.017  Corresponding author. E-mail address:  norman.schaad@ars.usda.gov (N.W. Schaad).  Bacteria, USDA, Ft. Detrick, MD, USA; LMG  ¼  La-boratorium Microbiologie Gent, Gent, Belgium;NCPPB  ¼  National Collection of Plant PathogenicBacteria, York, England. Xanthomonas citri   ( ex  Hasse 1915) Gabriel et al. [9]emend. Etymology : ci’tri. N.L. gen. n.  citri   of citrus. Description : The description of the species  X. citri   isencompassed within the description of the genus Xanthomonas  Dowson, 1939 [25] emend. Vauterinet al. [29] and within the description provided byGabriel et al. [9].  X. citri   subsp.  citri   causes bacterialcanker on  Citrus  spp. and  X. citri   subsp.  malvacearum causes angular leaf spot and black arm of cotton( Gossypium  spp.) whereas  X. campestris  and  X. axono- podis  do not affect either host [24].  X. citri   does notproduce a brown water soluble pigment on commonmedia as does  X. fuscans  and  X. campestris  pv.  vignicola [24].  X. citri   is differentiated from all other xanthomo-nads, except  X. campestris  pv.  melonis  and  X. campestris pv.  viticola,  by fatty acid profiles [33]. Additionally,  X.citri   differs from  X. campestris  and most otherpathovars, subspecies, and species of   Xanthomonas  byserology [1,28], SDS-PAGE analysis of membraneproteins [28,30], isozyme analysis [13], DNA-DNA reassociation assays [8,24,29], ITS sequencing [24], RFLP [9,15], and rep-PCR profiles [20]. Type strain : ICPB 10518  ¼  ATCC 49118  ¼  LMG9322. Xanthomonas citri   subsp.  citri   ( ex  Hasse 1915) Gabrielet al. 1989, subsp. nov. Etymology : ci’tri. N.L. gen. n.  citri   of citrus. Description :  X. citri   subsp.  citri   causes bacterialcanker of citrus whereas  X. citri   subsp.  malvacearum does not [24].  X. citri   subsp.  citri   may be distinguishedfrom  X. campestris  and most other  Xanthomonas pathovars, subspecies, and species by DNA-DNAreassociation assays [8,24,29], ITS sequencing [24], rep- PCR profiles [20], and phenotypic traits [24]. Strains of  X. citri   subsp.  citri   produce single colonies on YDC andFS agars [23] after 40–44 and 56–60h, respectively at28–30 1 C [24]. In contrast,  X. fuscans  subsp.  fuscans  and X. fuscans  subsp.  aurantifolii   produce single colonies in56–60 and 70–76h, respectively, and  X. alfalfae  subsp. alfalfa e and  X. alfalfae  subsp.  citrumelonis  grow in30–34 and 40–44h, respectively [24].  X. citri   subsp.  citri  utilizes arabinose and lactose and hydrolyzes pectatewhereas  X. citri   subsp.  malvacearum  does not [24].  X.citri   subsp.  citri   reduces aspartic acid whereas  X.campestris  pv.  campestris  does not [24]. The latterutilizes raffinose and reduces saccharic acid whereasthe former does not [24]. Both bacteria are differentiatedby host pathogenicity assays and by serology [1–3,5,28]and membrane protein analysis [16,28,30]. Serologydifferentiates  X. citri   subsp.  citri   from  X. fuscans  subsp. aurantifolii   [10,11,19]. Strains of   X. citri   subsp.  citri   aresusceptible to bacteriophage CP1 and CP2 whereasthose of   X. fuscans  subsp.  aurantifolii   are not [18].  X.citri   subsp.  citri   is differentiated from  X. alfalfae  subsp. citrumelonis  by isozyme analysis [13].  X. citri   subsp.  citri  grows on FS and mSX agars, utilizes arabinose,maltose, lactose, mannitol, cellobiose, and asparaticacid; hydrolyzes pectate, liquifies gelatin, and results inan alkaline hydrolysis of litmus milk [24]. Type strain : ICPB 10518  ¼  ATCC 49118  ¼  LMG9322. Xanthomonas citri   subsp.  malvacearum  ( ex  Smith1901) subsp. nov., nom. rev. Etymology : mal.va.ce.a’rum. N.L. pl. gen. n. mal-vacearum, of   Malvaceae  (of malvaceous plants of thefamily  Malvaceae ). Description :  X. citri   subsp.  malvacearum  causesangular leaf spot and black arm of cotton ( Gossypiumhirsutum ) whereas  X. citri   subsp.  citri   does not [24].  X.citri   subsp.  malvacearum  is differentiated from  X.campestris  pv.  campestris  and most other  Xanthomonas pathovars, subspecies, and species by DNA-DNAreassociation assays [8,24,29], rep-PCR profiles [20], by serology [3], and SDS-PAGE patterns of membraneproteins [30], ITS sequencing [24], and phenotypic characters [24]. Strains of   X. citri   subsp.  malvacearum produce single colonies on YDC and FS agars [23] after40–44 and 56–60h, respectively, at 28–30 1 C [24]. Incontrast,  X. fuscans  subsp.  fuscans  and  X. fuscans  subsp. ARTICLE IN PRESS Table 1.  16S-23S Ribosomal intergeneric spacer sequences for type strains [24]Proposed name Strain designation GenBank accession Xanthomonas citri X. citri   subsp.  citri   ATCC 49118 DQ660898 X. citri   subsp.  malvacearum  ATCC 9924 DQ660901 Xanthomonas fuscansX. fuscans  subsp . fuscans  ATCC 19315 DQ660900 X. fuscans  subsp.  aurantifolii   NCPPB 3236 DQ660897 Xanthomonas alfalfaeX. alfalfae  subsp.  alfalfae  ATCC 11765 DQ660896 X. alfalfae  subsp.  citrumelonis  ATCC 49120 DQ660899 N.W. Schaad et al. / Systematic and Applied Microbiology 29 (2006) 690–695 691  aurantifolii   produce single colonies in 56–60 and70–76h, respectively, and  X. alfalfae  subsp.  alfalfa eand  X. alfalfae  subsp.  citrumelonis  grow in 30–34 and40–44h, respectively [24]. Further, RFLP profilesdifferentiate  X. citri   subsp.  malvacearum  from  X. fuscans subsp.  fuscans , and  X. alfalfae  subsp.  alfalfae  [15].  X.campestris  pv.  campestris  utilizes melizitose and hydro-lyzes pectate whereas  X. citri   subsp.  malvacearum  doesnot [24].  X. citri   subsp.  malvacearum  produces analkaline reaction without hydrolysis in litmus milkwhereas  X. citri   subsp.  citri   causes an alkaline reactionwith hydrolysis [24].  X. citri   subsp.  malvacearum  growson FS and mSX agars [23], liquifies gelatin, and moststrains (60%) utilize maltose [24]. Type strain : ICPB 10528  ¼  ATCC 9924  ¼  ICMP217  ¼  LMG 785.The type strain designated here, although identical inpathogenicity [24], is different from strain ICMP5739  ¼  LMG 761  ¼  NCPPB 633, indicated as the typestrain for  X. campestris  pv.  malvacearum  ( X. axonopodis pv.  malvacearum ) [7,29]. Xanthomonas fuscans  sp. nov. Etymology : fus’cans. L. part. adj.  fuscans  browning/darkening. Description : The description of the species  X. fuscans is encompassed within the description of the genus Xanthomonas  Dowson 1939 (Approved Lists 1980 [25])emend. Vauterin et al., 1995 [29].  X. fuscans  subsp.  fuscans , causes blight of beans ( Phaseolus vulgaris ) and X. fuscans  subsp.  aurantifolii   causes cankers on  Citrus spp. whereas  X. campestris  and  X. axonopodis  do notaffect either host [24].  X. fuscans  is differentiated fromall other xanthomonads, except  X. campestris  pv. vignicola,  by production of a water soluble brownpigment on several common agar media includingYDC [4,17,22–24]. Additionally , X. fuscans  is differ-entiated from most other  Xanthomonas  pathovars andspecies by DNA–DNA reassociation assays [8,24,29],ITS sequencing [24], and rep-PCR profiles [20]. Type strain : ICPB 10520  ¼  ATCC 19315  ¼  ICMP239  ¼  LMG 826  ¼  NCPPB 381. Xanthomonas fuscans  subsp . fuscans  subsp. nov. Etymology : fus 0 cans. L. part. adj.  fuscans  browning/darkening. Description :  X. fuscans  subsp.  fuscans , originallydescribed as  Phytomonas phaseoli   var. fuscans byBurkholder [4], causes fuscous blight of beans ( Phaseo-lus vulgaris ) whereas  X. fuscans  subsp.  aurantifolii   doesnot [24]. Fuscous blight may resemble common blight,caused by  X. campestri   pv.  phaseoli. X. fuscans  subsp.  fuscans  is differentiated from  X. campestris  pv.  campes-tris  by serology [27] and membrane protein analysis[16,28].  X. fuscans  subsp.  fuscans  is differentiated frommost other  Xanthomonas  pathovars, subspecies, andspecies by DNA–DNA reassociation assays [24,29], ITSsequences [24], rep-PCR profiles [20], RFLP profiles [15], and phenotypic traits [24]. Strains of   X. fuscans subsp.  fuscans  produce single colonies on YDC and FSagar after 56–60 and 70–76h, respectively, at 28–30 1 C[24]. In contrast,  X. citri   subsp.  citri   and  X. citri   subsp. malvcearum  produce single colonies in 40–44 and56–60h, respectively, and  X. alfalfae  subsp.  alfalfa eand  X. alfalfae  subsp.  citrumelonis  grow in 30–34 and40–44h, respectively [24]. Strains of   X. fuscans  subsp.  fuscans  grow on FS and mSX agars [23], utilize maltose,hydrolyze pectin, and produce an alkaline hydrolysis of litmus milk [24].  X. fuscans  subsp.  fuscans  produces awater soluble brown pigment on several common agarmedia including YDC [4,17,22–24]. Except for  X. fuscans  subsp.  aurantifolii   and  X. campestris  pv. vignicola , no other xanthomonad produces this brownpigment [24]. Type strain : ICPB 10520  ¼  ATCC 19315  ¼  ICMP239  ¼  LMG 826  ¼  NCPPB 381. Xanthomonas fuscans  subsp . aurantifolii   subsp. nov. Etymology : au.ran.ti.fol 0 i.i. N.L. n.  Aurantium , agenus of citrus plants; N.L. gen. n.  folii   of/from a leaf;N.L. gen. n.  aurantifolli   of/from a citrus leaf. Description :  X. fuscans  subsp.  aurantifolii  , srcinallydescribed as a pathovar of   X. campestris  [9], causescankers on Mexican lime ( Citrus aurantifolia ) [18] andoccasionally on lemon ( C. limon ), orange ( C. sinensis ),and grapefruit ( C. paradisi  ) whereas  X. fuscans  subsp.  fuscans  does not affect citrus [24].  X. fuscans  subsp. aurantifolii   is differentiated from most other  Xanthomo-nas  pathovars, subspecies, and species by DNA–DNAreassociation assays [8,24,29], rep-PCR profiles [20], ITS sequences [24], and phenotypic traits [24]. Strains of   X. fuscans  subsp.  aurantifolii   produce single colonies onYDC and FS agars [23] after 56–60 and 70–76h,respectively, at 28–30 1 C [24]. In contrast,  X. citri   subsp. citri   and  X. citri   subsp.  malvacearum  produce singlecolonies in 40–44 and 56–60h, respectively, and  X.alfalfae  subsp.  alfalfa e and  X. alfalfae  subsp.  citrumello-nis  grow in 30–34 and 40–44h, respectively [24].  X. fuscans  subsp.  aurantifolii   is distinguished from  X. citri  subsp.  citri   and  X. alfalfae  subsp.  citrumelonis  as itprecipitates litmus milk and hydrolyses gelatin.  X. fuscans  subsp.  aurantifolii   does not utilize maltose orhydrolyze pectate whereas  X. citri   subsp.  citri   and  X. fuscans  subsp.  fuscans  do [24].  X. fuscans  subsp. aurantifolii   precipitates litmus milk, whereas  X. fuscans subsp.  fuscans  does not [24].  X. fuscans  subsp.  fuscans  isdistinguished from  X. citri   subsp.  citri   and  X. campestris pv.  campestris  by failing to utilize arabinose and lactose[24]. Serology differentiates  X. citri   subsp.  citri   from  X. fuscans  subsp.  aurantifolii   [10,11,19]. Strains of   X. citri  subsp.  citri   are susceptible to bacteriophage CP1 andCP2 whereas those of   X. fuscans  subsp.  aurantifolii   arenot [18]. Strains of   X. fuscans  subsp.  aurantifolii   utilizelactose, mannitol, and cellobiose and precipitate litmusmilk [24]. Strains of   X. fuscans  subsp.  aurantifolii  ARTICLE IN PRESS N.W. Schaad et al. / Systematic and Applied Microbiology 29 (2006) 690–695692  produce a water-soluble brown pigment on severalcommon agar media including YDC [6,22,24]. Exceptfor  X. fuscans  subsp.  fuscans  and  X. campestris  pv. vignicola , no other xanthomonad produces this brownpigment [24]. Type strain : ICPB 10470  ¼  NCPPB 3236  ¼  CFBP2901. Xanthomonas alfalfae  ( ex  Riker et al. 1935) sp. nov.,nom. rev. Etymology : al.fal’fae. N.L. gen. n.  alfalfae  fromalfalfa ( Medicago sativa ). Description : The description of the species  X. alfalfae is encompassed within the description of the genus Xanthomonas  Dowson 1939 (Approved Lists 1980 [25])emend. Vauterin et al. 1995 [29]. Strains of   X. alfalfae subsp.  alfalfae  cause leaf spots on alfalfa ( Medicagosativa ) and strains of   X. alfalfae  subsp.  citrumelonis cause leaf spots on seedlings of   Citrus  spp. whereasother strains of   X. campestris ,  X. axonopodis , and anyother xanthomonads do not [24].  X. alfalfae  is differ-entiated from other  Xanthomonas  pathovars, subspecies,and species by DNA–DNA reassociation assays[8,24,29], rep-PCR profiles [20], RFLP profiles [15], ITS sequences [24] and phenotypic traits [24].  X. alfalfae does not produce a brown water soluble pigment oncommon media as does  X. fuscans  and  X. campestris  pv. vignicola  [24]. Strains of   X. alfalfae  grow much fasterthan other xanthomonads on SX and FS agars [23] andutilize a broader range of carbon sources [24].  X.alfalfae , and its subspecies, utilize arabinose, maltose,lactose, mannitol, and cellobiose; liquify gelatin; andproduce an alkaline hydrolysis of litmus milk whereas  X.axonopodis  does not [24]. Type strain : ICPB 10701  ¼  ATCC 11765  ¼  LMG495. Xanthomonas alfalfae  subsp.  alfalfae  ( ex  Riker et al.,1935) subsp. nov. Etymology : al.fal’fae. N.L. gen. n.  alfalfae  fromalfalfa ( Medicago sativa ). Description :  X. alfalfae  subsp.  alfalfae  causes leaf spotof alfalfa [21] whereas  X. alfalfae  subsp.  citrumelonis does not [24].  X. alfalfae  subsp.  alfalfae  is distinguishedfrom  X. campestris  pv.  campestris  and most other Xanthomonas  pathovars, subspecies, and species byDNA–DNA reassociation assays [8,24,29], RFLP pro-files [15], rep-PCR profiles [20], and ITS sequences [24]. Strains of   X. alfalfae  subsp.  alfalfae  produce singlecolonies on YDC and FS agarss [23] after 30–34 and40–44h, respectively, at 28–30 1 C [24]. In contrast,  X.citri   subsp.  citri   and  X. citri   subsp.  malvcearum  producesingle colonies in 40–44 and 56–60h, respectively, and X. fuscans  subsp.  fuscans  and  X. fuscans  subsp aurantifolii   grow in 56–60 and 70–76h, respectively[24].  X. alfalfae  subsp.  alfalfae  produces acid from mostcarbon sources whereas  X. campestris  pv.  campestris does not [24].  X. campestris  pv.  campestris  utilizesraffinose whereas  X. alfalfae  subsp.  alfalfae  does not[24].  X. alfalfae  subsp.  alfalfae  grows faster on YDCagar than do most other xanthomonads [24]. Strains of  X. alfalfae  subsp.  alfalfae  produce an alkaline reactionon saccharic acid whereas strains of   X. alfalfae  subsp. citrumelonis  do not [24].  X. alfalfae  subsp.  alfalfae utilizes arabinose, maltose, lactose, mannitol, melizitose,and cellobiose, liquifies gelatin, and produces an alka-line hydrolysis of litmus milk [24]. Type strain : ICPB 10701  ¼  ATCC 11765  ¼  LMG495. Xanthomonas alfalfae  subsp . citrumelonis  subsp. nov. Etymology : ci.tru.me’lo.nis. N.L. gen. n.  citrumelonis of citrumelo ( Citroncirus  sp.; hybrid of   Citrus paradisi   x Poncirus trifoliata ). Description :  X. alfalfae  subsp.  citrumelonis , srcinallydescribed as pathovar ‘‘ citrumelo ’’ of   X. campestris  [9],causes citrus bacterial spot [12];  X. alfalfae  subsp alfalfae  does not [24].  X. alfalfae  subsp  citrumelonis  isdistinguished from  X. campestris  pv.  campestris  andother  Xanthomonas  pathovars, subspecies, and speciesby DNA-DNA reassociation assays [8,24,29], rep-PCRprofiles [20], ITS sequences [24], and phenotypic traits [24]. Strains of   X. alfalfae  subsp.  citrumelonis  producesingle colonies on YDC and FS agars [23] after 30–34and 40–44h, respectively, at 28–30 1 C [24]. In contrast, X. citri   subsp.  citri   and  X. citri   subsp.  malvacearum produce single colonies in 40–44 and 56–60h, respec-tively, and  X. fuscans  subsp.  fuscans  and  X. fuscans subsp.  aurantifolii   grow in 56–60 and 70–76h, respec-tively [24].  X. alfalfae  subsp.  citrumelonis  strains aredifferentiated from  X. citri   subsp.  citri   and  X. citri  subsp.  malvacearum  and  X. fuscans  subsp.  aurantifolii   byserological assays [2,12,19].  X. alfalfae  subsp.  citrume-lonis  utilizes raffinose whereas  X. alfalfae  subsp.  alfalfae , X. citri   subsp.  citri  , and  X. citri   subsp.  malvacearum strains do not [24].  X. alfalfae  subsp.  alfalfae  and  X.alfalfae  subsp.  citrumelonis  can be differentiated from  X. fuscans  subsp.  aurantifolii   on their more rapid growth onagar media, liquefaction of gelatin, and utilization of maltose [24].  X. alfalfae  subsp.  citrumelonis  is distin-guished from  X. citri   subsp.  citri   by utilizing raffinose,producing acid from cellobiose and mannitol, andgrowing faster on YDC and FS agars [24]. All strainsof   X. alfalfae  subsp.  citrumelonis  utilize mannitol andraffinose whereas strains of   X. citri   subsp.  malvacearum do not [24]. Type strain : ICPB 10483  ¼  ATCC 49120  ¼  LMG9325. Acknowledgements We thank Dr. J.P. Euzeby for proof reading ourprotologues and Dr. B.J. Tindall and Dr. J.M. Youngfor reviewing our nomenclature. ARTICLE IN PRESS N.W. Schaad et al. / Systematic and Applied Microbiology 29 (2006) 690–695 693
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