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A "repertoire for repertoire" hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas.

Hajri A, Brin C, Hunault G, Lardeux F, Lemaire C, Manceau C, Boureau T, Poussier S - PLoS ONE (2009)

Bottom Line: In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences.Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods.Our results showed a correspondence between composition of T3E repertoires and pathovars of Xanthomonas axonopodis.

View Article: PubMed Central - PubMed

Affiliation: Département Santé des Plantes et Environnement, Institut National de la Recherche Agronomique, Beaucouzé, France.

ABSTRACT

Background: The genetic basis of host specificity for animal and plant pathogenic bacteria remains poorly understood. For plant pathogenic bacteria, host range is restricted to one or a few host plant species reflecting a tight adaptation to specific hosts.

Methodology/principal findings: Two hypotheses can be formulated to explain host specificity: either it can be explained by the phylogenetic position of the strains, or by the association of virulence genes enabling a pathological convergence of phylogenically distant strains. In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences. To challenge these two hypotheses, we selected 132 Xanthomonas axonopodis strains representative of 18 different pathovars which display different host range. First, the phylogenetic position of each strain was determined by sequencing the housekeeping gene rpoD. This study showed that many pathovars of Xanthomonas axonopodis are polyphyletic. Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods. Indeed, for pathogenic bacteria T3Es were shown to trigger and to subvert host defences. Our study revealed that T3E repertoires comprise core and variable gene suites that likely have distinct roles in pathogenicity and different evolutionary histories. Our results showed a correspondence between composition of T3E repertoires and pathovars of Xanthomonas axonopodis. For polyphyletic pathovars, this suggests that T3E genes might explain a pathological convergence of phylogenetically distant strains. We also identified several DNA rearrangements within T3E genes, some of which correlate with host specificity of strains.

Conclusions/significance: These data provide insight into the potential role played by T3E genes for pathogenic bacteria and support a "repertoire for repertoire" hypothesis that may explain host specificity. Our work provides resources for functional and evolutionary studies aiming at understanding host specificity of pathogenic bacteria, functional redundancy between T3Es and the driving forces shaping T3E repertoires.

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Among strains of pv. mangiferaeindicae, disruption of xopC by an IS element correlates with pathogenicity on Schinus terebenthifolius.Strains belonging to the pv. mangiferaeindicae are either pathogenic on Mangifera indica or on Schinus terebenthifolius. A: PCR experiments reveal the insertion of the IS1479 element in all strains pathogenic on Schinus terebenthifolius. In contrast, strains pathogenic on Mangifera indica display a xopC gene that is not inactivated by IS1479. B: However, all strains display identical repertoires in dot-blot hybridization experiments. Such result suggests that inactivation of xopC may explain a pathogenicity switch between Mangifera indica and Schinus terebenthifolius.
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pone-0006632-g005: Among strains of pv. mangiferaeindicae, disruption of xopC by an IS element correlates with pathogenicity on Schinus terebenthifolius.Strains belonging to the pv. mangiferaeindicae are either pathogenic on Mangifera indica or on Schinus terebenthifolius. A: PCR experiments reveal the insertion of the IS1479 element in all strains pathogenic on Schinus terebenthifolius. In contrast, strains pathogenic on Mangifera indica display a xopC gene that is not inactivated by IS1479. B: However, all strains display identical repertoires in dot-blot hybridization experiments. Such result suggests that inactivation of xopC may explain a pathogenicity switch between Mangifera indica and Schinus terebenthifolius.

Mentions: Most of the DNA rearrangements (21/23) corresponds to insertions of IS elements. We found that seven T3E genes (avrXv3, avrXacE2, avrRxo1, ecf, xopC, xopO, xopN) from strains belonging to 6 pathovars of X. axonopodis were disrupted by 6 different IS elements (IS1595, ISXca2, ISXac2, IS1389, IS1404 and IS1479). Interestingly, except IS1479 and IS1595, these IS elements are closely related since they are classified within the single IS3 family - IS407 group (http://www-IS.biotoul.fr/is.html). The determination of the usual 4 bp DRs generated by insertions of the IS elements belonging to the IS3 family-IS407 group revealed no consensus sequence thus reflecting no insertion site specificity (Table 2). The determination of the location of IS element insertions (Table 2) showed that a T3E gene can be disrupted at the same position by the same IS element in all strains of the same pathovar (for example avrXv3 disrupted by IS1595 at position 513 in all pathovar alfalfae strains) or at different positions by different IS elements in different strains of the same pathovar (for instance avrRxo1 disrupted by ISXca2 and IS1389 at positions 770 and 411 respectively in strains CFBP6369 and CFBP6107 of the pathovar allii). We also observed that a T3E gene can be disrupted by different IS elements at different positions in strains belonging to different pathovars. This is the case of xopC that is disrupted by IS1404 and IS1479 in strains of pathovars citrumelo and mangiferaeindicae respectively. In this latter example, it is interesting to note that xopC, carried by pathovar mangiferaeindicae strains, is altered in strains isolated from Schinus terebenthifolius but not in those isolated from Mangifera indica. Since strains from both hosts of isolation exhibited identical T3E repertoires (Figures 2 and 5), this result might suggest that the alteration of this T3E gene might have a role in host adaptation for pathovar mangiferaeindicae strains.


A "repertoire for repertoire" hypothesis: repertoires of type three effectors are candidate determinants of host specificity in Xanthomonas.

Hajri A, Brin C, Hunault G, Lardeux F, Lemaire C, Manceau C, Boureau T, Poussier S - PLoS ONE (2009)

Among strains of pv. mangiferaeindicae, disruption of xopC by an IS element correlates with pathogenicity on Schinus terebenthifolius.Strains belonging to the pv. mangiferaeindicae are either pathogenic on Mangifera indica or on Schinus terebenthifolius. A: PCR experiments reveal the insertion of the IS1479 element in all strains pathogenic on Schinus terebenthifolius. In contrast, strains pathogenic on Mangifera indica display a xopC gene that is not inactivated by IS1479. B: However, all strains display identical repertoires in dot-blot hybridization experiments. Such result suggests that inactivation of xopC may explain a pathogenicity switch between Mangifera indica and Schinus terebenthifolius.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2722093&req=5

pone-0006632-g005: Among strains of pv. mangiferaeindicae, disruption of xopC by an IS element correlates with pathogenicity on Schinus terebenthifolius.Strains belonging to the pv. mangiferaeindicae are either pathogenic on Mangifera indica or on Schinus terebenthifolius. A: PCR experiments reveal the insertion of the IS1479 element in all strains pathogenic on Schinus terebenthifolius. In contrast, strains pathogenic on Mangifera indica display a xopC gene that is not inactivated by IS1479. B: However, all strains display identical repertoires in dot-blot hybridization experiments. Such result suggests that inactivation of xopC may explain a pathogenicity switch between Mangifera indica and Schinus terebenthifolius.
Mentions: Most of the DNA rearrangements (21/23) corresponds to insertions of IS elements. We found that seven T3E genes (avrXv3, avrXacE2, avrRxo1, ecf, xopC, xopO, xopN) from strains belonging to 6 pathovars of X. axonopodis were disrupted by 6 different IS elements (IS1595, ISXca2, ISXac2, IS1389, IS1404 and IS1479). Interestingly, except IS1479 and IS1595, these IS elements are closely related since they are classified within the single IS3 family - IS407 group (http://www-IS.biotoul.fr/is.html). The determination of the usual 4 bp DRs generated by insertions of the IS elements belonging to the IS3 family-IS407 group revealed no consensus sequence thus reflecting no insertion site specificity (Table 2). The determination of the location of IS element insertions (Table 2) showed that a T3E gene can be disrupted at the same position by the same IS element in all strains of the same pathovar (for example avrXv3 disrupted by IS1595 at position 513 in all pathovar alfalfae strains) or at different positions by different IS elements in different strains of the same pathovar (for instance avrRxo1 disrupted by ISXca2 and IS1389 at positions 770 and 411 respectively in strains CFBP6369 and CFBP6107 of the pathovar allii). We also observed that a T3E gene can be disrupted by different IS elements at different positions in strains belonging to different pathovars. This is the case of xopC that is disrupted by IS1404 and IS1479 in strains of pathovars citrumelo and mangiferaeindicae respectively. In this latter example, it is interesting to note that xopC, carried by pathovar mangiferaeindicae strains, is altered in strains isolated from Schinus terebenthifolius but not in those isolated from Mangifera indica. Since strains from both hosts of isolation exhibited identical T3E repertoires (Figures 2 and 5), this result might suggest that the alteration of this T3E gene might have a role in host adaptation for pathovar mangiferaeindicae strains.

Bottom Line: In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences.Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods.Our results showed a correspondence between composition of T3E repertoires and pathovars of Xanthomonas axonopodis.

View Article: PubMed Central - PubMed

Affiliation: Département Santé des Plantes et Environnement, Institut National de la Recherche Agronomique, Beaucouzé, France.

ABSTRACT

Background: The genetic basis of host specificity for animal and plant pathogenic bacteria remains poorly understood. For plant pathogenic bacteria, host range is restricted to one or a few host plant species reflecting a tight adaptation to specific hosts.

Methodology/principal findings: Two hypotheses can be formulated to explain host specificity: either it can be explained by the phylogenetic position of the strains, or by the association of virulence genes enabling a pathological convergence of phylogenically distant strains. In this latter hypothesis, host specificity would result from the interaction between repertoires of bacterial virulence genes and repertoires of genes involved in host defences. To challenge these two hypotheses, we selected 132 Xanthomonas axonopodis strains representative of 18 different pathovars which display different host range. First, the phylogenetic position of each strain was determined by sequencing the housekeeping gene rpoD. This study showed that many pathovars of Xanthomonas axonopodis are polyphyletic. Second, we investigated the distribution of 35 type III effector genes (T3Es) in these strains by both PCR and hybridization methods. Indeed, for pathogenic bacteria T3Es were shown to trigger and to subvert host defences. Our study revealed that T3E repertoires comprise core and variable gene suites that likely have distinct roles in pathogenicity and different evolutionary histories. Our results showed a correspondence between composition of T3E repertoires and pathovars of Xanthomonas axonopodis. For polyphyletic pathovars, this suggests that T3E genes might explain a pathological convergence of phylogenetically distant strains. We also identified several DNA rearrangements within T3E genes, some of which correlate with host specificity of strains.

Conclusions/significance: These data provide insight into the potential role played by T3E genes for pathogenic bacteria and support a "repertoire for repertoire" hypothesis that may explain host specificity. Our work provides resources for functional and evolutionary studies aiming at understanding host specificity of pathogenic bacteria, functional redundancy between T3Es and the driving forces shaping T3E repertoires.

Show MeSH
Related in: MedlinePlus