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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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Rearrangements in gene order in the P. ultimum genome relative to Phytophthora genomes. Vertical brown bars indicate orthologs shared among P. ultimum, Ph. infestans and Ph. ramorum. Gold bars indicate orthologs shared only between Ph. infestans and Ph. ramorum. Turquoise bars indicate genes with orthologs in other regions of the compared genomes (that is, non-syntenic orthologs). Grey bars indicate genes without orthologs. Gray and red shaded connections indicate blocks of syntenic orthologs with the same or opposite relative transcriptional orientations, respectively. Non-coding regions of the genome are not depicted.
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Figure 3: Rearrangements in gene order in the P. ultimum genome relative to Phytophthora genomes. Vertical brown bars indicate orthologs shared among P. ultimum, Ph. infestans and Ph. ramorum. Gold bars indicate orthologs shared only between Ph. infestans and Ph. ramorum. Turquoise bars indicate genes with orthologs in other regions of the compared genomes (that is, non-syntenic orthologs). Grey bars indicate genes without orthologs. Gray and red shaded connections indicate blocks of syntenic orthologs with the same or opposite relative transcriptional orientations, respectively. Non-coding regions of the genome are not depicted.

Mentions: A phylogenetic approach (PHRINGE [103]) was used to identify P. ultimum proteins orthologous to proteins encoded in the genomes of Ph. infestans, Ph. sojae, and Ph. ramorum. Of the 15,322 proteins predicted from the P. ultimum genome sequence, 12,230 were identified as orthologous to a protein in at least one Phytophthora genome sequence. A total of 11,331 proteins were identified as orthologs common to all three Phytophthora spp., and of these, 8,504 had identifiable orthologs in P. ultimum. PHRINGE was also used to examine the conservation of gene order (synteny) between the Phytophthora and P. ultimum genomes. As previously described [27], the gene order of orthologs is very highly conserved among Phytophthora spp. In P. ultimum the ortholog content was very similar between broad regions of the P. ultimum and Phytophthora genomes, but the local gene order was greatly rearranged, primarily as a result of inversions. Only short runs of up to 10 orthologs were found to be collinear, whereas runs of more than 100 could be identified between the Phytophthora spp. Figure 3 shows an example spanning a well-assembled region of the Ph. infestans, Ph. ramorum and P. ultimum genome sequences. In Ph. ramorum, the region spans 1.18 Mb and 383 predicted genes and in P. ultimum the region spans 1.15 Mb and 435 predicted genes. Of these genes, 286 are identified as orthologs. In the Ph. ramorum sequence there are an additional 38 genes with orthologs in Ph. infestans but not in P. ultimum. Due to a much larger number of repeat sequences, and expanded gene numbers, the corresponding region in Ph. infestans spans 2.38 Mb and 499 predicted genes, but the order of the orthologous genes is highly conserved with that of Ph. ramorum. The Ph. sojae genome shows similar conservation of gene order in this region but for simplicity is not shown.


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)

Rearrangements in gene order in the P. ultimum genome relative to Phytophthora genomes. Vertical brown bars indicate orthologs shared among P. ultimum, Ph. infestans and Ph. ramorum. Gold bars indicate orthologs shared only between Ph. infestans and Ph. ramorum. Turquoise bars indicate genes with orthologs in other regions of the compared genomes (that is, non-syntenic orthologs). Grey bars indicate genes without orthologs. Gray and red shaded connections indicate blocks of syntenic orthologs with the same or opposite relative transcriptional orientations, respectively. Non-coding regions of the genome are not depicted.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Rearrangements in gene order in the P. ultimum genome relative to Phytophthora genomes. Vertical brown bars indicate orthologs shared among P. ultimum, Ph. infestans and Ph. ramorum. Gold bars indicate orthologs shared only between Ph. infestans and Ph. ramorum. Turquoise bars indicate genes with orthologs in other regions of the compared genomes (that is, non-syntenic orthologs). Grey bars indicate genes without orthologs. Gray and red shaded connections indicate blocks of syntenic orthologs with the same or opposite relative transcriptional orientations, respectively. Non-coding regions of the genome are not depicted.
Mentions: A phylogenetic approach (PHRINGE [103]) was used to identify P. ultimum proteins orthologous to proteins encoded in the genomes of Ph. infestans, Ph. sojae, and Ph. ramorum. Of the 15,322 proteins predicted from the P. ultimum genome sequence, 12,230 were identified as orthologous to a protein in at least one Phytophthora genome sequence. A total of 11,331 proteins were identified as orthologs common to all three Phytophthora spp., and of these, 8,504 had identifiable orthologs in P. ultimum. PHRINGE was also used to examine the conservation of gene order (synteny) between the Phytophthora and P. ultimum genomes. As previously described [27], the gene order of orthologs is very highly conserved among Phytophthora spp. In P. ultimum the ortholog content was very similar between broad regions of the P. ultimum and Phytophthora genomes, but the local gene order was greatly rearranged, primarily as a result of inversions. Only short runs of up to 10 orthologs were found to be collinear, whereas runs of more than 100 could be identified between the Phytophthora spp. Figure 3 shows an example spanning a well-assembled region of the Ph. infestans, Ph. ramorum and P. ultimum genome sequences. In Ph. ramorum, the region spans 1.18 Mb and 383 predicted genes and in P. ultimum the region spans 1.15 Mb and 435 predicted genes. Of these genes, 286 are identified as orthologs. In the Ph. ramorum sequence there are an additional 38 genes with orthologs in Ph. infestans but not in P. ultimum. Due to a much larger number of repeat sequences, and expanded gene numbers, the corresponding region in Ph. infestans spans 2.38 Mb and 499 predicted genes, but the order of the orthologous genes is highly conserved with that of Ph. ramorum. The Ph. sojae genome shows similar conservation of gene order in this region but for simplicity is not shown.

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