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Diversifying selection in the wheat stem rust fungus acts predominantly on pathogen-associated gene families and reveals candidate effectors.

Sperschneider J, Ying H, Dodds PN, Gardiner DM, Upadhyaya NM, Singh KB, Manners JM, Taylor JM - Front Plant Sci (2014)

Bottom Line: We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families.In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving.This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification.

View Article: PubMed Central - PubMed

Affiliation: Plant Industry, Centre for Environment and Life Sciences, Commonwealth Scientific and Industrial Research Organisation Perth, WA, Australia.

ABSTRACT
Plant pathogens cause severe losses to crop plants and threaten global food production. One striking example is the wheat stem rust fungus, Puccinia graminis f. sp. tritici, which can rapidly evolve new virulent pathotypes in response to resistant host lines. Like several other filamentous fungal and oomycete plant pathogens, its genome features expanded gene families that have been implicated in host-pathogen interactions, possibly encoding effector proteins that interact directly with target host defense proteins. Previous efforts to understand virulence largely relied on the prediction of secreted, small and cysteine-rich proteins as candidate effectors and thus delivered an overwhelming number of candidates. Here, we implement an alternative analysis strategy that uses the signal of adaptive evolution as a line of evidence for effector function, combined with comparative information and expression data. We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families. In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving. One of our top candidates has recently been shown to induce genotype-specific hypersensitive cell death in wheat. This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification. Our system can be applied to a wide range of pathogens and will give insight into host-pathogen dynamics, ultimately leading to progress in strategies for disease control.

No MeSH data available.


Related in: MedlinePlus

The distribution of pathogen-associated and fungal genes with in planta up-regulation and diversifying selection across the clusters. Diversifying selection is predominantly predicted for genes that are part of pathogen-associated gene families. At a significance threshold of p < 0.05, 81 pathogen-associated genes are rapidly evolving, compared to only 11 fungal genes. At a significance threshold of p < 0.00001, 14 rapidly evolving genes are predicted across the pathogen-associated gene families, with the majority of these being part of clusters C6, C7, C8 and C11.
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Figure 4: The distribution of pathogen-associated and fungal genes with in planta up-regulation and diversifying selection across the clusters. Diversifying selection is predominantly predicted for genes that are part of pathogen-associated gene families. At a significance threshold of p < 0.05, 81 pathogen-associated genes are rapidly evolving, compared to only 11 fungal genes. At a significance threshold of p < 0.00001, 14 rapidly evolving genes are predicted across the pathogen-associated gene families, with the majority of these being part of clusters C6, C7, C8 and C11.

Mentions: Despite the fairly similar distribution of in planta up-regulated genes across the pathogen-associated and fungal gene families, site-specific diversifying selection using PAML was almost exclusively detected across pathogen-associated gene families. In particular, 81 up-regulated genes (p < 0.05) from pathogen-associated gene families were predicted to undergo diversifying selection whereas only 11 up-regulated genes from fungal gene families are rapidly evolving. A more stringent significance threshold of p < 0.00001 returned 14 genes from pathogen-associated gene families and two genes from fungal gene families that are undergoing diversifying selection (Figure 4).


Diversifying selection in the wheat stem rust fungus acts predominantly on pathogen-associated gene families and reveals candidate effectors.

Sperschneider J, Ying H, Dodds PN, Gardiner DM, Upadhyaya NM, Singh KB, Manners JM, Taylor JM - Front Plant Sci (2014)

The distribution of pathogen-associated and fungal genes with in planta up-regulation and diversifying selection across the clusters. Diversifying selection is predominantly predicted for genes that are part of pathogen-associated gene families. At a significance threshold of p < 0.05, 81 pathogen-associated genes are rapidly evolving, compared to only 11 fungal genes. At a significance threshold of p < 0.00001, 14 rapidly evolving genes are predicted across the pathogen-associated gene families, with the majority of these being part of clusters C6, C7, C8 and C11.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4150398&req=5

Figure 4: The distribution of pathogen-associated and fungal genes with in planta up-regulation and diversifying selection across the clusters. Diversifying selection is predominantly predicted for genes that are part of pathogen-associated gene families. At a significance threshold of p < 0.05, 81 pathogen-associated genes are rapidly evolving, compared to only 11 fungal genes. At a significance threshold of p < 0.00001, 14 rapidly evolving genes are predicted across the pathogen-associated gene families, with the majority of these being part of clusters C6, C7, C8 and C11.
Mentions: Despite the fairly similar distribution of in planta up-regulated genes across the pathogen-associated and fungal gene families, site-specific diversifying selection using PAML was almost exclusively detected across pathogen-associated gene families. In particular, 81 up-regulated genes (p < 0.05) from pathogen-associated gene families were predicted to undergo diversifying selection whereas only 11 up-regulated genes from fungal gene families are rapidly evolving. A more stringent significance threshold of p < 0.00001 returned 14 genes from pathogen-associated gene families and two genes from fungal gene families that are undergoing diversifying selection (Figure 4).

Bottom Line: We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families.In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving.This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification.

View Article: PubMed Central - PubMed

Affiliation: Plant Industry, Centre for Environment and Life Sciences, Commonwealth Scientific and Industrial Research Organisation Perth, WA, Australia.

ABSTRACT
Plant pathogens cause severe losses to crop plants and threaten global food production. One striking example is the wheat stem rust fungus, Puccinia graminis f. sp. tritici, which can rapidly evolve new virulent pathotypes in response to resistant host lines. Like several other filamentous fungal and oomycete plant pathogens, its genome features expanded gene families that have been implicated in host-pathogen interactions, possibly encoding effector proteins that interact directly with target host defense proteins. Previous efforts to understand virulence largely relied on the prediction of secreted, small and cysteine-rich proteins as candidate effectors and thus delivered an overwhelming number of candidates. Here, we implement an alternative analysis strategy that uses the signal of adaptive evolution as a line of evidence for effector function, combined with comparative information and expression data. We demonstrate that in planta up-regulated genes that are rapidly evolving are found almost exclusively in pathogen-associated gene families, affirming the impact of host-pathogen co-evolution on genome structure and the adaptive diversification of specialized gene families. In particular, we predict 42 effector candidates that are conserved only across pathogens, induced during infection and rapidly evolving. One of our top candidates has recently been shown to induce genotype-specific hypersensitive cell death in wheat. This shows that comparative genomics incorporating the evolutionary signal of adaptation is powerful for predicting effector candidates for laboratory verification. Our system can be applied to a wide range of pathogens and will give insight into host-pathogen dynamics, ultimately leading to progress in strategies for disease control.

No MeSH data available.


Related in: MedlinePlus