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Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire.

Lévesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J, Zerillo MM, Beakes GW, Boore JL, Busam D, Dumas B, Ferriera S, Fuerstenberg SI, Gachon CM, Gaulin E, Govers F, Grenville-Briggs L, Horner N, Hostetler J, Jiang RH, Johnson J, Krajaejun T, Lin H, Meijer HJ, Moore B, Morris P, Phuntmart V, Puiu D, Shetty J, Stajich JE, Tripathy S, Wawra S, van West P, Whitty BR, Coutinho PM, Henrissat B, Martin F, Thomas PD, Tyler BM, De Vries RP, Kamoun S, Yandell M, Tisserat N, Buell CR - Genome Biol. (2010)

Bottom Line: The predicted proteome includes a large repertoire of proteins involved in plant pathogen interactions, although, surprisingly, the P. ultimum genome does not encode any classical RXLR effectors and relatively few Crinkler genes in comparison to related phytopathogenic oomycetes.A lower number of enzymes involved in carbohydrate metabolism were present compared to Phytophthora species, with the notable absence of cutinases, suggesting a significant difference in virulence mechanisms between P. ultimum and more host-specific oomycete species.Access to the P. ultimum genome has revealed not only core pathogenic mechanisms within the oomycetes but also lineage-specific genes associated with the alternative virulence and lifestyles found within the pythiaceous lineages compared to the Peronosporaceae.

View Article: PubMed Central - HTML - PubMed

Affiliation: Agriculture and Agri-Food Canada, 960 Carling Ave, Ottawa, ON, K1A 0C6, Canada.

ABSTRACT

Background: Pythium ultimum is a ubiquitous oomycete plant pathogen responsible for a variety of diseases on a broad range of crop and ornamental species.

Results: The P. ultimum genome (42.8 Mb) encodes 15,290 genes and has extensive sequence similarity and synteny with related Phytophthora species, including the potato blight pathogen Phytophthora infestans. Whole transcriptome sequencing revealed expression of 86% of genes, with detectable differential expression of suites of genes under abiotic stress and in the presence of a host. The predicted proteome includes a large repertoire of proteins involved in plant pathogen interactions, although, surprisingly, the P. ultimum genome does not encode any classical RXLR effectors and relatively few Crinkler genes in comparison to related phytopathogenic oomycetes. A lower number of enzymes involved in carbohydrate metabolism were present compared to Phytophthora species, with the notable absence of cutinases, suggesting a significant difference in virulence mechanisms between P. ultimum and more host-specific oomycete species. Although we observed a high degree of orthology with Phytophthora genomes, there were novel features of the P. ultimum proteome, including an expansion of genes involved in proteolysis and genes unique to Pythium. We identified a small gene family of cadherins, proteins involved in cell adhesion, the first report of these in a genome outside the metazoans.

Conclusions: Access to the P. ultimum genome has revealed not only core pathogenic mechanisms within the oomycetes but also lineage-specific genes associated with the alternative virulence and lifestyles found within the pythiaceous lineages compared to the Peronosporaceae.

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Related in: MedlinePlus

Phylogenetic tree of the cadherin family, showing all members of the novel oomycete subfamily (green) and their relationships to representative metazoan and choanoflagellate cadherins. The major clades of cadherins [96] are colored: C-1 (blue), Cr-1a and Cr-1b (red), C-2 (purple), and Cr-3 (orange). Most of the oomycete cadherins fall within a fairly distinct subfamily (green), though this subfamily has many long branches and also includes some cadherins from the choanoflagellate M. brevicollis (labeled starting with 'MB') that are also highly diverged from other cadherins. Reliable branches (bootstrap > 50%) are labeled with a circle. All full-length oomycete cadherin domains are shown, from P. ultimum (labeled starting with 'Pu' and ending with the number of the repeat relative to the amino terminus), Ph. infestans (labeled starting with 'Pi'), Ph. sojae (Ps) and Ph. ramorum (Pr). Other cadherins are from the human genome ('Hs') unless labeled starting with 'Dm' (Drosophila melanogaster) or 'Ce' (Caenorhabditis elegans). The figure was drawn using the iTOL tool [143].
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Figure 2: Phylogenetic tree of the cadherin family, showing all members of the novel oomycete subfamily (green) and their relationships to representative metazoan and choanoflagellate cadherins. The major clades of cadherins [96] are colored: C-1 (blue), Cr-1a and Cr-1b (red), C-2 (purple), and Cr-3 (orange). Most of the oomycete cadherins fall within a fairly distinct subfamily (green), though this subfamily has many long branches and also includes some cadherins from the choanoflagellate M. brevicollis (labeled starting with 'MB') that are also highly diverged from other cadherins. Reliable branches (bootstrap > 50%) are labeled with a circle. All full-length oomycete cadherin domains are shown, from P. ultimum (labeled starting with 'Pu' and ending with the number of the repeat relative to the amino terminus), Ph. infestans (labeled starting with 'Pi'), Ph. sojae (Ps) and Ph. ramorum (Pr). Other cadherins are from the human genome ('Hs') unless labeled starting with 'Dm' (Drosophila melanogaster) or 'Ce' (Caenorhabditis elegans). The figure was drawn using the iTOL tool [143].

Mentions: In order to explore the evolution of these domains in the oomycetes, we performed a phylogenetic analysis. The first (amino-terminal) cadherin EC domain has been used to explore gene phylogeny among the cadherins [96,99], and to facilitate comparison we used both neighbor joining [100] and maximum likelihood (using the PhyML program [101,102]) to estimate a phylogenetic tree for these same sequences together with all of the intact cadherin domains from the P. ultimum and Ph. infestans genomes (Figure 2). To generate a high-quality protein sequence alignment for phylogeny estimation, we used the manual alignment of Nollet et al. [99] as a 'seed' for alignment of other sequences using MAFFT [102]. We found that all of the oomycete domains fall within a single clade. However, this clade is broad and also contains several cadherins from the choanoflagellate M. brevicollis, as well as some of the more divergent metazoan cadherins (Cr-2 and Cr-3 subfamilies). In general, the branches in this clade are very long, making phylogenetic reconstruction somewhat unreliable (all branches with bootstrap values > 50% are marked with a circle in Figure 2). Nevertheless, most of the cadherin domains found in P. ultimum are reliably orthologous to domains in one or more Phytophthora species, suggesting descent from a common ancestor by speciation. The most notable example is for the genes PITG_09983 and PYU1_T011030, in which a region spanning three consecutive EC repeats appears to have been inherited by both species from that common ancestor (apparently followed by substantial duplication and rearrangement of individual cadherin domains). These repeats are also apparently orthologous to repeats in both Ph. sojae and Ph. ramorum. The oomycete cadherins may have been initially obtained either vertically (by descent from the common ancestor with metazoans) or horizontally (by transfer of metazoan DNA long after divergence). No cadherins have been found in genomes sequenced from other clades more closely related to either oomycetes (for example, diatoms and alveolates) or the metazoan/choanoflagellates (for example, Fungi and amoebozoa). This means that, if cadherins were present in the most recent common ancestor of oomycetes and metazoans, these genes must have been lost independently in all of these other diverging lineages. Given the data currently available, it is more probable that at least one horizontal cadherin gene transfer event occurred from a choanoflagellate or metazoan to an oomycete ancestor, prior to the divergence of Pythium from Phytophthora. The source of the metazoan DNA may have been a host of the ancestral oomycete, or possibly introduced by a virus. Nevertheless, the subsequent preservation of cadherin domains in at least two lineages of oomycetes over a substantial period of time suggests that the genes are likely to perform an important function, which remains to be explored.


Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire.

Lévesque CA, Brouwer H, Cano L, Hamilton JP, Holt C, Huitema E, Raffaele S, Robideau GP, Thines M, Win J, Zerillo MM, Beakes GW, Boore JL, Busam D, Dumas B, Ferriera S, Fuerstenberg SI, Gachon CM, Gaulin E, Govers F, Grenville-Briggs L, Horner N, Hostetler J, Jiang RH, Johnson J, Krajaejun T, Lin H, Meijer HJ, Moore B, Morris P, Phuntmart V, Puiu D, Shetty J, Stajich JE, Tripathy S, Wawra S, van West P, Whitty BR, Coutinho PM, Henrissat B, Martin F, Thomas PD, Tyler BM, De Vries RP, Kamoun S, Yandell M, Tisserat N, Buell CR - Genome Biol. (2010)

Phylogenetic tree of the cadherin family, showing all members of the novel oomycete subfamily (green) and their relationships to representative metazoan and choanoflagellate cadherins. The major clades of cadherins [96] are colored: C-1 (blue), Cr-1a and Cr-1b (red), C-2 (purple), and Cr-3 (orange). Most of the oomycete cadherins fall within a fairly distinct subfamily (green), though this subfamily has many long branches and also includes some cadherins from the choanoflagellate M. brevicollis (labeled starting with 'MB') that are also highly diverged from other cadherins. Reliable branches (bootstrap > 50%) are labeled with a circle. All full-length oomycete cadherin domains are shown, from P. ultimum (labeled starting with 'Pu' and ending with the number of the repeat relative to the amino terminus), Ph. infestans (labeled starting with 'Pi'), Ph. sojae (Ps) and Ph. ramorum (Pr). Other cadherins are from the human genome ('Hs') unless labeled starting with 'Dm' (Drosophila melanogaster) or 'Ce' (Caenorhabditis elegans). The figure was drawn using the iTOL tool [143].
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2926784&req=5

Figure 2: Phylogenetic tree of the cadherin family, showing all members of the novel oomycete subfamily (green) and their relationships to representative metazoan and choanoflagellate cadherins. The major clades of cadherins [96] are colored: C-1 (blue), Cr-1a and Cr-1b (red), C-2 (purple), and Cr-3 (orange). Most of the oomycete cadherins fall within a fairly distinct subfamily (green), though this subfamily has many long branches and also includes some cadherins from the choanoflagellate M. brevicollis (labeled starting with 'MB') that are also highly diverged from other cadherins. Reliable branches (bootstrap > 50%) are labeled with a circle. All full-length oomycete cadherin domains are shown, from P. ultimum (labeled starting with 'Pu' and ending with the number of the repeat relative to the amino terminus), Ph. infestans (labeled starting with 'Pi'), Ph. sojae (Ps) and Ph. ramorum (Pr). Other cadherins are from the human genome ('Hs') unless labeled starting with 'Dm' (Drosophila melanogaster) or 'Ce' (Caenorhabditis elegans). The figure was drawn using the iTOL tool [143].
Mentions: In order to explore the evolution of these domains in the oomycetes, we performed a phylogenetic analysis. The first (amino-terminal) cadherin EC domain has been used to explore gene phylogeny among the cadherins [96,99], and to facilitate comparison we used both neighbor joining [100] and maximum likelihood (using the PhyML program [101,102]) to estimate a phylogenetic tree for these same sequences together with all of the intact cadherin domains from the P. ultimum and Ph. infestans genomes (Figure 2). To generate a high-quality protein sequence alignment for phylogeny estimation, we used the manual alignment of Nollet et al. [99] as a 'seed' for alignment of other sequences using MAFFT [102]. We found that all of the oomycete domains fall within a single clade. However, this clade is broad and also contains several cadherins from the choanoflagellate M. brevicollis, as well as some of the more divergent metazoan cadherins (Cr-2 and Cr-3 subfamilies). In general, the branches in this clade are very long, making phylogenetic reconstruction somewhat unreliable (all branches with bootstrap values > 50% are marked with a circle in Figure 2). Nevertheless, most of the cadherin domains found in P. ultimum are reliably orthologous to domains in one or more Phytophthora species, suggesting descent from a common ancestor by speciation. The most notable example is for the genes PITG_09983 and PYU1_T011030, in which a region spanning three consecutive EC repeats appears to have been inherited by both species from that common ancestor (apparently followed by substantial duplication and rearrangement of individual cadherin domains). These repeats are also apparently orthologous to repeats in both Ph. sojae and Ph. ramorum. The oomycete cadherins may have been initially obtained either vertically (by descent from the common ancestor with metazoans) or horizontally (by transfer of metazoan DNA long after divergence). No cadherins have been found in genomes sequenced from other clades more closely related to either oomycetes (for example, diatoms and alveolates) or the metazoan/choanoflagellates (for example, Fungi and amoebozoa). This means that, if cadherins were present in the most recent common ancestor of oomycetes and metazoans, these genes must have been lost independently in all of these other diverging lineages. Given the data currently available, it is more probable that at least one horizontal cadherin gene transfer event occurred from a choanoflagellate or metazoan to an oomycete ancestor, prior to the divergence of Pythium from Phytophthora. The source of the metazoan DNA may have been a host of the ancestral oomycete, or possibly introduced by a virus. Nevertheless, the subsequent preservation of cadherin domains in at least two lineages of oomycetes over a substantial period of time suggests that the genes are likely to perform an important function, which remains to be explored.

Bottom Line: The predicted proteome includes a large repertoire of proteins involved in plant pathogen interactions, although, surprisingly, the P. ultimum genome does not encode any classical RXLR effectors and relatively few Crinkler genes in comparison to related phytopathogenic oomycetes.A lower number of enzymes involved in carbohydrate metabolism were present compared to Phytophthora species, with the notable absence of cutinases, suggesting a significant difference in virulence mechanisms between P. ultimum and more host-specific oomycete species.Access to the P. ultimum genome has revealed not only core pathogenic mechanisms within the oomycetes but also lineage-specific genes associated with the alternative virulence and lifestyles found within the pythiaceous lineages compared to the Peronosporaceae.

View Article: PubMed Central - HTML - PubMed

Affiliation: Agriculture and Agri-Food Canada, 960 Carling Ave, Ottawa, ON, K1A 0C6, Canada.

ABSTRACT

Background: Pythium ultimum is a ubiquitous oomycete plant pathogen responsible for a variety of diseases on a broad range of crop and ornamental species.

Results: The P. ultimum genome (42.8 Mb) encodes 15,290 genes and has extensive sequence similarity and synteny with related Phytophthora species, including the potato blight pathogen Phytophthora infestans. Whole transcriptome sequencing revealed expression of 86% of genes, with detectable differential expression of suites of genes under abiotic stress and in the presence of a host. The predicted proteome includes a large repertoire of proteins involved in plant pathogen interactions, although, surprisingly, the P. ultimum genome does not encode any classical RXLR effectors and relatively few Crinkler genes in comparison to related phytopathogenic oomycetes. A lower number of enzymes involved in carbohydrate metabolism were present compared to Phytophthora species, with the notable absence of cutinases, suggesting a significant difference in virulence mechanisms between P. ultimum and more host-specific oomycete species. Although we observed a high degree of orthology with Phytophthora genomes, there were novel features of the P. ultimum proteome, including an expansion of genes involved in proteolysis and genes unique to Pythium. We identified a small gene family of cadherins, proteins involved in cell adhesion, the first report of these in a genome outside the metazoans.

Conclusions: Access to the P. ultimum genome has revealed not only core pathogenic mechanisms within the oomycetes but also lineage-specific genes associated with the alternative virulence and lifestyles found within the pythiaceous lineages compared to the Peronosporaceae.

Show MeSH
Related in: MedlinePlus