Limits...
The role of horizontal transfer in the evolution of a highly variable lipopolysaccharide biosynthesis locus in xanthomonads that infect rice, citrus and crucifers.

Patil PB, Bogdanove AJ, Sonti RV - BMC Evol. Biol. (2007)

Bottom Line: In Xoc, the remainder of the LPS gene cluster, consisting of seven genes, is novel and unrelated to LPS gene clusters of any of the sequenced xanthomonads.We also report substantial interstrain variation suggestive of very recent horizontal gene transfer (HGT) at the LPS biosynthetic locus of Xanthomonas campestris pv. campestris (Xcc), the black rot pathogen of crucifers.Our analyses indicate that HGT has altered the LPS locus during the evolution of Xanthomonas oryzae pathovars and suggest that the ancestor of all Xanthomonas oryzae pathovars had an Xac type of LPS gene cluster.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre for Cellular and Molecular Biology, Hyderabad-500007, India. patilpb@ccmb.res.in

ABSTRACT

Background: Lipopolysaccharide (LPS) is a pathogen associated molecular pattern (PAMP) of animal and plant pathogenic bacteria. Variation at the interstrain level is common in LPS biosynthetic gene clusters of animal pathogenic bacteria. This variation has been proposed to play a role in evading the host immune system. Even though LPS is a modulator of plant defense responses, reports of interstrain variation in LPS gene clusters of plant pathogenic bacteria are rare.

Results: In this study we report the complete sequence of a variant 19.9 kb LPS locus present in the BXO8 strain of Xanthomonas oryzae pv. oryzae (Xoo), the bacterial blight pathogen of rice. This region is completely different in size, number and organization of genes from the LPS locus present in most other strains of Xoo from India and Asia. Surprisingly, except for one ORF, all the other ORFs at the BXO8 LPS locus are orthologous to the genes present at this locus in a sequenced strain of X. axonopodis pv. citri (Xac; a pathogen of citrus plants). One end of the BXO8 LPS gene cluster, comprised of ten genes, is also present in the related rice pathogen, X. oryzae pv. oryzicola (Xoc). In Xoc, the remainder of the LPS gene cluster, consisting of seven genes, is novel and unrelated to LPS gene clusters of any of the sequenced xanthomonads. We also report substantial interstrain variation suggestive of very recent horizontal gene transfer (HGT) at the LPS biosynthetic locus of Xanthomonas campestris pv. campestris (Xcc), the black rot pathogen of crucifers.

Conclusion: Our analyses indicate that HGT has altered the LPS locus during the evolution of Xanthomonas oryzae pathovars and suggest that the ancestor of all Xanthomonas oryzae pathovars had an Xac type of LPS gene cluster. Our finding of interstrain variation in two major xanthomonad pathogens infecting different hosts suggests that the LPS locus in plant pathogenic bacteria, as in animal pathogens, is under intense diversifying selection.

Show MeSH

Related in: MedlinePlus

A schematic comparison of LPS gene clusters described in the present study. Genes conserved in different strains are given identical colour. Genes specific to individual strains are given unique colour. ORFs marked by red colour represent IS elements. Hpo pro indicates a hypothetical protein encoding ORF.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC2238763&req=5

Figure 6: A schematic comparison of LPS gene clusters described in the present study. Genes conserved in different strains are given identical colour. Genes specific to individual strains are given unique colour. ORFs marked by red colour represent IS elements. Hpo pro indicates a hypothetical protein encoding ORF.

Mentions: In the genomes of all sequenced xanthomonads, there is an LPS locus between the metB and etfA genes. However, what is present at this locus is variable. A schematic diagram of the different xanthomonad LPS gene clusters compared in this study is shown in Fig. 6. It appears that multiple horizontal gene transfer events in the Xanthomonas lineage have contributed to this diversity. The genome of the pepper and tomato pathogen Xav strain 85-10 is more related to that of Xac strain 306 than either is to Xcc [29]. Even though both the Xanthomonas axonopodis pathovars are closely related, Xac strain 306 and Xav strain 85-10 have entirely different LPS gene clusters, the LPS locus of Xav strain 85-10 being similar, in overall gene organization and content, to that of Xcc strain B100 and Xca 756C. This suggests that at least one HGT has occurred in the ancestor of Xac and Xav. A 2.1 kb ORF (XCC0613/XC_3621O) in Xcc strains ATCC33913 and 8004 encodes a hypothetical protein that has no orthologs in the sequenced xanthomonads. We propose that a HGT event might have introduced this unique ORF into the genome of the ancestor of Xcc strains ATCC33913 and 8004. Overall, the results of this study indicate that multiple HGT events have occurred at this locus in the xanthomonads and that the variation introduced by HGT can involve either the entire LPS locus or part of the locus. A hypothetical evolutionary tree illustrating a pattern of HGT events that could explain the relationships observed among the LPS gene clusters of the Xanthomonas strains examined here is presented in Figure 7.


The role of horizontal transfer in the evolution of a highly variable lipopolysaccharide biosynthesis locus in xanthomonads that infect rice, citrus and crucifers.

Patil PB, Bogdanove AJ, Sonti RV - BMC Evol. Biol. (2007)

A schematic comparison of LPS gene clusters described in the present study. Genes conserved in different strains are given identical colour. Genes specific to individual strains are given unique colour. ORFs marked by red colour represent IS elements. Hpo pro indicates a hypothetical protein encoding ORF.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2238763&req=5

Figure 6: A schematic comparison of LPS gene clusters described in the present study. Genes conserved in different strains are given identical colour. Genes specific to individual strains are given unique colour. ORFs marked by red colour represent IS elements. Hpo pro indicates a hypothetical protein encoding ORF.
Mentions: In the genomes of all sequenced xanthomonads, there is an LPS locus between the metB and etfA genes. However, what is present at this locus is variable. A schematic diagram of the different xanthomonad LPS gene clusters compared in this study is shown in Fig. 6. It appears that multiple horizontal gene transfer events in the Xanthomonas lineage have contributed to this diversity. The genome of the pepper and tomato pathogen Xav strain 85-10 is more related to that of Xac strain 306 than either is to Xcc [29]. Even though both the Xanthomonas axonopodis pathovars are closely related, Xac strain 306 and Xav strain 85-10 have entirely different LPS gene clusters, the LPS locus of Xav strain 85-10 being similar, in overall gene organization and content, to that of Xcc strain B100 and Xca 756C. This suggests that at least one HGT has occurred in the ancestor of Xac and Xav. A 2.1 kb ORF (XCC0613/XC_3621O) in Xcc strains ATCC33913 and 8004 encodes a hypothetical protein that has no orthologs in the sequenced xanthomonads. We propose that a HGT event might have introduced this unique ORF into the genome of the ancestor of Xcc strains ATCC33913 and 8004. Overall, the results of this study indicate that multiple HGT events have occurred at this locus in the xanthomonads and that the variation introduced by HGT can involve either the entire LPS locus or part of the locus. A hypothetical evolutionary tree illustrating a pattern of HGT events that could explain the relationships observed among the LPS gene clusters of the Xanthomonas strains examined here is presented in Figure 7.

Bottom Line: In Xoc, the remainder of the LPS gene cluster, consisting of seven genes, is novel and unrelated to LPS gene clusters of any of the sequenced xanthomonads.We also report substantial interstrain variation suggestive of very recent horizontal gene transfer (HGT) at the LPS biosynthetic locus of Xanthomonas campestris pv. campestris (Xcc), the black rot pathogen of crucifers.Our analyses indicate that HGT has altered the LPS locus during the evolution of Xanthomonas oryzae pathovars and suggest that the ancestor of all Xanthomonas oryzae pathovars had an Xac type of LPS gene cluster.

View Article: PubMed Central - HTML - PubMed

Affiliation: Centre for Cellular and Molecular Biology, Hyderabad-500007, India. patilpb@ccmb.res.in

ABSTRACT

Background: Lipopolysaccharide (LPS) is a pathogen associated molecular pattern (PAMP) of animal and plant pathogenic bacteria. Variation at the interstrain level is common in LPS biosynthetic gene clusters of animal pathogenic bacteria. This variation has been proposed to play a role in evading the host immune system. Even though LPS is a modulator of plant defense responses, reports of interstrain variation in LPS gene clusters of plant pathogenic bacteria are rare.

Results: In this study we report the complete sequence of a variant 19.9 kb LPS locus present in the BXO8 strain of Xanthomonas oryzae pv. oryzae (Xoo), the bacterial blight pathogen of rice. This region is completely different in size, number and organization of genes from the LPS locus present in most other strains of Xoo from India and Asia. Surprisingly, except for one ORF, all the other ORFs at the BXO8 LPS locus are orthologous to the genes present at this locus in a sequenced strain of X. axonopodis pv. citri (Xac; a pathogen of citrus plants). One end of the BXO8 LPS gene cluster, comprised of ten genes, is also present in the related rice pathogen, X. oryzae pv. oryzicola (Xoc). In Xoc, the remainder of the LPS gene cluster, consisting of seven genes, is novel and unrelated to LPS gene clusters of any of the sequenced xanthomonads. We also report substantial interstrain variation suggestive of very recent horizontal gene transfer (HGT) at the LPS biosynthetic locus of Xanthomonas campestris pv. campestris (Xcc), the black rot pathogen of crucifers.

Conclusion: Our analyses indicate that HGT has altered the LPS locus during the evolution of Xanthomonas oryzae pathovars and suggest that the ancestor of all Xanthomonas oryzae pathovars had an Xac type of LPS gene cluster. Our finding of interstrain variation in two major xanthomonad pathogens infecting different hosts suggests that the LPS locus in plant pathogenic bacteria, as in animal pathogens, is under intense diversifying selection.

Show MeSH
Related in: MedlinePlus