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Presence͞absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis Hitoshi Araki†‡, Dacheng Tian§, Erica M. Goss†, Katrin Jakob†, Solveig S. Halldorsdottir†, Martin Kreitman†, and Joy Bergelson†¶ †Department of Ecology and Evolution, University of Chicago, Chicago, IL 60637; and §Department of Biology, Nanjing University, Nanjing 210093, Republic of China Communicated by Tomoko Ohta, National Institute of Genetics, Mishima, Japan, March 1, 2006 (received for review January 25, 2006) The contribution of arms race dynamics to plant–pathogen coevo- pathogens are defined and differentiated from close relatives by lution has been called into question by the presence of balanced horizontally acquired virulence factors (12). However, a survey polymorphisms in resistance genes of Arabidopsis thaliana, but of effectors in Pseudomonas syringae finds effectors that have less is known about the pathogen side of the interaction. Here we been acquired recently and others that have been transmitted investigate structural polymorphism in pathogenicity islands (PAIs) predominantly by descent, indicating that pathogenicity may in Pseudomonas viridiflava, a prevalent bacterial pathogen of A. evolve in both genomic contexts (13). thaliana. PAIs encode the type III secretion system along with its In this study, we investigated PAIs in P. viridiflava, which is a effectors and are essential for pathogen recognition in plants. P. prevalent bacterial pathogen of wild A. thaliana populations viridiflava harbors two structurally distinct and highly diverged PAI (14). P. viridiflava is in the P. syringae group (15). Although P. paralogs (T- and S-PAI) that are integrated in different chromo- syringae is intensively studied as a bacterial plant pathogen (13, some locations in the P. viridiflava genome. Both PAIs are segre- 16–18), little is known about the genetic basis of pathogenicity gating as presence͞absence polymorphisms such that only one PAI in P. viridiflava. Here we report a previously undescribed ar- GENETICS ١ ١ ([T-PAI, S-PAI] and [ T-PAI, S-PAI]) is present in any individual cell. rangement of PAIs and a long-term presence of an unusual dual A worldwide population survey identified no isolate with neither PAI polymorphism in this bacterial pathogen. This polymor- or both PAI. T-PAI and S-PAI genotypes exhibit virulence differ- phism is not caused by recent HGT but rather is analogous to ences and a host-specificity tradeoff. Orthologs of each PAI can be polymorphism in host defense genes: evolutionarily long-lived found in conserved syntenic locations in other Pseudomonas spe- polymorphism for two paralogous PAIs in a single pathogen cies, indicating vertical phylogenetic transmission in this genus. species. Molecular evolutionary analysis of PAI sequences also argues against ‘‘recent’’ horizontal transfer. Spikes in nucleotide diver- Results ١ gence in flanking regions of PAI and -PAI alleles suggest that the We first examined the structure and DNA sequence of PAIs in dual PAI polymorphism has been maintained in this species under five P. viridiflava strains (LP23.1a, PNA3.3a, ME3.1b, some form of balancing selection. Virulence differences and host RMX23.1a, and RMX3.1b) that were collected from naturally specificities are hypothesized to be responsible for the mainte- occurring A. thaliana plants in populations in the Midwest nance of the dual PAI system in this bacterial pathogen. United States, and their entire PAIs and flanking sequences were isolated. LP23.1a and PNA3.3a possess a PAI similar in bacteria ͉ balancing selection ͉ plant–pathogen interaction ͉ arms structure to that found in the congener P. syringae (16). It has a race ͉ horizontal gene transfer tripartite mosaic structure composed of a gene cluster encoding the Type III protein-secretion apparatus (hrp͞hrc gene cluster), rms race dynamics were once thought to dominate plant– the 5Ј effector loci (exchangeable effector loci or EEL), and the Apathogen coevolution through the process of rapid substi- 3Ј effector loci (conserved effector loci or CEL). We designate tutions of adaptive mutation in both sides of the interaction (1). this structural form as the T- (tripartite) PAI (Fig. 1A; see also However, the presence of balanced polymorphisms in some Table 1, which is published as supporting information on the resistance (R) genes in the plant host Arabidopsis thaliana PNAS web site). The other three isolates (ME3.1b, RMX23.1a, suggests a different type of coevolutionary dynamic (2–5). For and RMX3.1b) possess a PAI with a single component hrp͞hrc example, diversifying selection, rather than directional selection, cluster (Fig. 1B; see also Table 2, which is published as support- A. thaliana R is observed in the extremely polymorphic -gene ing information on the PNAS web site), a structure previously RPP13 and the downey mildew avirulence gene, ATR13, which not reported in any pathogenic bacteria. We designate this type triggers RPP13-mediated resistance (6). In bacteria, effector as the S- (single) PAI. proteins such as ATR13 are transported into host cells via the The T-PAIs of LP23.1a and PNA3.3a are 47 kb and 43 kb, Type III secretion system (TTSS), which is found in both animal respectively, differing primarily by an insertion͞deletion (indel) and plant pathogens (7). Effectors delivered by the TTSS are essential for causing disease in susceptible hosts and for eliciting defense responses in resistant hosts. In a variety of Gram- Conflict of interest statement: No conflicts declared. negative bacterial pathogens, the genes encoding the TTSS and Abbreviations: HGT, horizontal gene transfer; HR, hypersensitive response; PAI, pathoge- its effectors comprise a physical gene cluster called a pathoge- nicity island; TTSS, Type III secretion system. nicity island (PAI) (8). Data deposition: The sequences reported in this paper have been deposited in the GenBank Pathogenicity-related genes, including entire PAIs, are often database (accession nos. AY597274–AY597283, AY859111, AY859112, AY859115, introduced into bacterial species by horizontal (or lateral) gene AY859128, AY859131, AY859183, AY859184, AY859351, AY859355, AY859358, transfer (HGT) (8–10), which is believed to be important DQ158500–158855, DQ168848, and DQ220702). because it allows the recipient pathogen to immediately use ‡Present address: Department of Zoology, Oregon State University, Corvallis, OR 97331. already-evolved pathogenicity strategies and, thereby, accelerate ¶To whom correspondence should be addressed. E-mail: [email protected]. the pace of pathogen evolution (11). In fact, several human © 2006 by The National Academy of Sciences of the USA www.pnas.org͞cgi͞doi͞10.1073͞pnas.0601431103 PNAS ͉ April 11, 2006 ͉ vol. 103 ͉ no. 15 ͉ 5887–5892 Downloaded by guest on September 23, 2021 Fig. 1. Two PAIs in P. viridiflava. Gene compositions of Region 1 (A) and Region 2 (B), locations of the T- and S-PAIs, respectively, in P. viridiflava. Boxes represent ORFs, and numbers above or below boxes are ORF numbers corresponding to Tables 1 and 2. The clade (19) of each isolate and which PAI it contains is indicated. difference in the EEL region (Fig. 1A). Gene compositions in isolates containing an S-PAI in Region 2 have a 3-kb-long .([the hrp͞hrc gene cluster and in the CEL region are otherwise sequence in Region 1 instead of a T-PAI ([ٌT-PAI, S-PAI identical to one another and are nearly identical to the T-PAI of This sequence is similar to part of the EEL sequence in the P. syringae pv. tomato (Pto) DC3000 (16). The gene compositions T-PAI but lacks any known effector gene homologs. Note that in the EEL region are nearly identical in the two P. viridiflava we defined the 5Ј end of the T-PAI as being immediately isolates but different from that of Pto DC3000. This region is downstream of tgt, queA, and tRNALeu following a definition of known to be hypervariable among P. syringae pathovars (16–17). PAIs in P. syringae (16). This genomic region does not necessarily The T-PAI contains three known avirulence (avr) gene ho- represent a unit that shares the same evolutionary history in mologs, hopPsyA, avrE, and avrF (18, 20, 21) and two effector P. viridiflava. gene candidates (hopPtoA1 and hopPtoM). We have reported previously the presence of two diverged The S-PAIs in ME3.1b, RMX23.1a, and RMX3.1b are Ϸ30 kb (and nonrecombining) clades in P. viridiflava, which likely in length and contain a 10-kb-long insertion in the middle of the represent two distinct subspecies (19). However, these clades do hrp͞hrc cluster relative to the T-PAI (Fig. 1B). The S-PAI not correspond to the PAI haplotypes: in a survey of 96 isolates, contains only two avr gene homologs (avrE and avrF), and these the two PAI haplotypes coexist within clade A (10 AT and 57 .(homologs are located in the 10-kb insertion. The T- and S-PAIs AS), whereas clade B is fixed for [ٌT-PAI, S-PAI] (29 BS share 25 gene homologs and many operon structures (Tables 1 Recombination between AT and AS isolates is clearly evident at and 2), and yet are distinct in gene composition and order, other loci spread around the genome (19), so divergent clades especially for effector gene loci. The sequences of these gene cannot explain this disassociation between the S- and T-PAIs. homologs are also highly diverged between the two PAIs. Other possible explanations for the absence of recombinant Nucleotide divergence (22, 23) between the 25 shared genes PAI genotypes include tight physical linkage and͞or natural averages 0.701 across all sites and 1.44 for synonymous sites. selection. According to the similarities of the flanking regions In a previous study (23) we investigated nucleotide polymor- (Tables 1 and 2), Region 1 and Region 2 are 2.1–2.4 Mb apart phism at five genomic regions in a worldwide collection of P. in three divergent genomes of P. syringae (6.1–6.3 Mb circular viridiflava isolates.
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