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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

For the gene family of protein PGTG_08638, diversifying selection is only detected for the orthologs. A phylogenetic tree for the gene family of PGTG_08638 was predicted using PhyML and branch support values are shown. PAML detects site-specific diversifying selection only for the branch with the three orthologs (stem rust PGTG 08638, stripe rust PSTG_14557, leaf rust PTTG 06270), but not for the other variants PGTG_08639 and PGTG_08644 and their orthologs.
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Figure 5: For the gene family of protein PGTG_08638, diversifying selection is only detected for the orthologs. A phylogenetic tree for the gene family of PGTG_08638 was predicted using PhyML and branch support values are shown. PAML detects site-specific diversifying selection only for the branch with the three orthologs (stem rust PGTG 08638, stripe rust PSTG_14557, leaf rust PTTG 06270), but not for the other variants PGTG_08639 and PGTG_08644 and their orthologs.

Mentions: In particular, PGTG_08638, PGTG_16225, PGTG_04972, PGTG_14091, PGTG_09276, and PGTG_05592 are highly induced in haustoria (fold change > 100, Table 4). Indeed, one variant of protein PGTG_08638 was identified in a functional screen of candidate effectors from the stem rust fungus P. graminis f. sp. tritici as an inducer of host genotype-specific hypersensitive cell death in wheat (Upadhyaya et al., 2013). This is in agreement with our PAML analysis, which detects diversifying selection only for the three orthologs (stem rust PGTG_08638, stripe rust PSTG_14557, leaf rust PTTG 06270), but not for the other variants (Figure 5). From this data, one could speculate that a gene duplication event with successive diversification has led to a gain of function in the stem rust variant PGTG_08638. This protein is recognized inside wheat cells (Upadhyaya et al., 2013) and would therefore belong to a class of effectors that are delivered into host cells from haustoria. The other haustorially expressed gene candidates described here are likely also to be in this class.


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)

For the gene family of protein PGTG_08638, diversifying selection is only detected for the orthologs. A phylogenetic tree for the gene family of PGTG_08638 was predicted using PhyML and branch support values are shown. PAML detects site-specific diversifying selection only for the branch with the three orthologs (stem rust PGTG 08638, stripe rust PSTG_14557, leaf rust PTTG 06270), but not for the other variants PGTG_08639 and PGTG_08644 and their orthologs.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: For the gene family of protein PGTG_08638, diversifying selection is only detected for the orthologs. A phylogenetic tree for the gene family of PGTG_08638 was predicted using PhyML and branch support values are shown. PAML detects site-specific diversifying selection only for the branch with the three orthologs (stem rust PGTG 08638, stripe rust PSTG_14557, leaf rust PTTG 06270), but not for the other variants PGTG_08639 and PGTG_08644 and their orthologs.
Mentions: In particular, PGTG_08638, PGTG_16225, PGTG_04972, PGTG_14091, PGTG_09276, and PGTG_05592 are highly induced in haustoria (fold change > 100, Table 4). Indeed, one variant of protein PGTG_08638 was identified in a functional screen of candidate effectors from the stem rust fungus P. graminis f. sp. tritici as an inducer of host genotype-specific hypersensitive cell death in wheat (Upadhyaya et al., 2013). This is in agreement with our PAML analysis, which detects diversifying selection only for the three orthologs (stem rust PGTG_08638, stripe rust PSTG_14557, leaf rust PTTG 06270), but not for the other variants (Figure 5). From this data, one could speculate that a gene duplication event with successive diversification has led to a gain of function in the stem rust variant PGTG_08638. This protein is recognized inside wheat cells (Upadhyaya et al., 2013) and would therefore belong to a class of effectors that are delivered into host cells from haustoria. The other haustorially expressed gene candidates described here are likely also to be in this class.

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