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Evidence for suppression of immunity as a driver for genomic introgressions and host range expansion in races of Albugo candida, a generalist parasite.

McMullan M, Gardiner A, Bailey K, Kemen E, Ward BJ, Cevik V, Robert-Seilaniantz A, Schultz-Larsen T, Balmuth A, Holub E, van Oosterhout C, Jones JD - Elife (2015)

Bottom Line: Despite this divergence, their genomes are mosaic-like, with ∼25% being introgressed from other races.This facilitates introgression and the exchange of effector repertoires, and may enable the evolution of novel races that can undergo clonal population expansion on new hosts.We discuss recent studies on hybridization in other eukaryotes such as yeast, Heliconius butterflies, Darwin's finches, sunflowers and cichlid fishes, and the implications of introgression for pathogen evolution in an agro-ecological environment.

View Article: PubMed Central - PubMed

Affiliation: The Sainsbury Laboratory, Norwich, United Kingdom.

ABSTRACT
How generalist parasites with wide host ranges can evolve is a central question in parasite evolution. Albugo candida is an obligate biotrophic parasite that consists of many physiological races that each specialize on distinct Brassicaceae host species. By analyzing genome sequence assemblies of five isolates, we show they represent three races that are genetically diverged by ∼1%. Despite this divergence, their genomes are mosaic-like, with ∼25% being introgressed from other races. Sequential infection experiments show that infection by adapted races enables subsequent infection of hosts by normally non-infecting races. This facilitates introgression and the exchange of effector repertoires, and may enable the evolution of novel races that can undergo clonal population expansion on new hosts. We discuss recent studies on hybridization in other eukaryotes such as yeast, Heliconius butterflies, Darwin's finches, sunflowers and cichlid fishes, and the implications of introgression for pathogen evolution in an agro-ecological environment.

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PCR with race-specific markers on DNA prepared from plant tissue generated from co-infection assays.(A) Co-infection assay of AcNc2 followed by Ac2V onto Ws-eds1 and Ws-2. (B) Co-infection of AcBoT followed by Ac2V onto Ws-eds1 and B. oleracea (B.o). (C) Co-infection of Ac2V followed by AcNc2 onto Ws-eds1 and B. juncea (B.j). Bands highlighted in orange indicate amplification of secondary inoculum on usually non-host plants upon primary inoculation with virulent A. candida. These experiments were repeated multiple times with similar results (see Supplementary file 6).DOI:http://dx.doi.org/10.7554/eLife.04550.011
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fig6: PCR with race-specific markers on DNA prepared from plant tissue generated from co-infection assays.(A) Co-infection assay of AcNc2 followed by Ac2V onto Ws-eds1 and Ws-2. (B) Co-infection of AcBoT followed by Ac2V onto Ws-eds1 and B. oleracea (B.o). (C) Co-infection of Ac2V followed by AcNc2 onto Ws-eds1 and B. juncea (B.j). Bands highlighted in orange indicate amplification of secondary inoculum on usually non-host plants upon primary inoculation with virulent A. candida. These experiments were repeated multiple times with similar results (see Supplementary file 6).DOI:http://dx.doi.org/10.7554/eLife.04550.011

Mentions: A. candida infection compromises host resistance against otherwise avirulent pathogen species (Cooper et al., 2008). Conceivably, A. candida could suppress host defenses to otherwise avirulent races of A. candida, enabling co-infection and sexual exchange. To test this we performed sequential inoculation experiments, identifying races using the genome sequences to create race-specific DNA markers. Race-specific PCR of pre-inoculated plants (Supplementary files 5, 6) shows preinfection by AcNc2 suppresses resistance in A. thaliana accession Ws-2 leaves towards the B. juncea-infecting race, Ac2V (Figure 6A). Also, preinfection by AcBoT suppresses B. oleracea resistance towards Ac2V (Figure 6B). Furthermore, defense suppression was so effective that Ac2V was able to complete its life cycle on both A. thaliana Ws-2 and B. oleracea as observed by successful subsequent infection on B. juncea from the sequentially inoculated plants. In a reciprocal experiment, preinfection of B. juncea with Ac2V enabled AcNc2 growth on B. juncea (Figure 6C). Therefore, AcNc2 not only can suppress Ac2V recognition on A. thaliana, but Ac2V is also capable of suppressing B. juncea resistance towards AcNc2. TIR-NB-LRR resistance genes likely confer Ac2V resistance in Arabidopsis (McHale et al., 2006), as Ac2V grows on an eds1-1 mutant of A. thaliana Ws-2 (Supplementary file 6; [Parker et al., 1996]). It has long been noted that Albugo sp. have a remarkable capacity to suppress immunity in their hosts (Cooper et al., 2008). We hypothesise that suppression of host innate immunity enables co-infection of hosts by races with otherwise non-overlapping host ranges, thus providing a remarkable mechanism to enable sexual genetic exchange between specialised A. candida races.10.7554/eLife.04550.011Figure 6.PCR with race-specific markers on DNA prepared from plant tissue generated from co-infection assays.


Evidence for suppression of immunity as a driver for genomic introgressions and host range expansion in races of Albugo candida, a generalist parasite.

McMullan M, Gardiner A, Bailey K, Kemen E, Ward BJ, Cevik V, Robert-Seilaniantz A, Schultz-Larsen T, Balmuth A, Holub E, van Oosterhout C, Jones JD - Elife (2015)

PCR with race-specific markers on DNA prepared from plant tissue generated from co-infection assays.(A) Co-infection assay of AcNc2 followed by Ac2V onto Ws-eds1 and Ws-2. (B) Co-infection of AcBoT followed by Ac2V onto Ws-eds1 and B. oleracea (B.o). (C) Co-infection of Ac2V followed by AcNc2 onto Ws-eds1 and B. juncea (B.j). Bands highlighted in orange indicate amplification of secondary inoculum on usually non-host plants upon primary inoculation with virulent A. candida. These experiments were repeated multiple times with similar results (see Supplementary file 6).DOI:http://dx.doi.org/10.7554/eLife.04550.011
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4384639&req=5

fig6: PCR with race-specific markers on DNA prepared from plant tissue generated from co-infection assays.(A) Co-infection assay of AcNc2 followed by Ac2V onto Ws-eds1 and Ws-2. (B) Co-infection of AcBoT followed by Ac2V onto Ws-eds1 and B. oleracea (B.o). (C) Co-infection of Ac2V followed by AcNc2 onto Ws-eds1 and B. juncea (B.j). Bands highlighted in orange indicate amplification of secondary inoculum on usually non-host plants upon primary inoculation with virulent A. candida. These experiments were repeated multiple times with similar results (see Supplementary file 6).DOI:http://dx.doi.org/10.7554/eLife.04550.011
Mentions: A. candida infection compromises host resistance against otherwise avirulent pathogen species (Cooper et al., 2008). Conceivably, A. candida could suppress host defenses to otherwise avirulent races of A. candida, enabling co-infection and sexual exchange. To test this we performed sequential inoculation experiments, identifying races using the genome sequences to create race-specific DNA markers. Race-specific PCR of pre-inoculated plants (Supplementary files 5, 6) shows preinfection by AcNc2 suppresses resistance in A. thaliana accession Ws-2 leaves towards the B. juncea-infecting race, Ac2V (Figure 6A). Also, preinfection by AcBoT suppresses B. oleracea resistance towards Ac2V (Figure 6B). Furthermore, defense suppression was so effective that Ac2V was able to complete its life cycle on both A. thaliana Ws-2 and B. oleracea as observed by successful subsequent infection on B. juncea from the sequentially inoculated plants. In a reciprocal experiment, preinfection of B. juncea with Ac2V enabled AcNc2 growth on B. juncea (Figure 6C). Therefore, AcNc2 not only can suppress Ac2V recognition on A. thaliana, but Ac2V is also capable of suppressing B. juncea resistance towards AcNc2. TIR-NB-LRR resistance genes likely confer Ac2V resistance in Arabidopsis (McHale et al., 2006), as Ac2V grows on an eds1-1 mutant of A. thaliana Ws-2 (Supplementary file 6; [Parker et al., 1996]). It has long been noted that Albugo sp. have a remarkable capacity to suppress immunity in their hosts (Cooper et al., 2008). We hypothesise that suppression of host innate immunity enables co-infection of hosts by races with otherwise non-overlapping host ranges, thus providing a remarkable mechanism to enable sexual genetic exchange between specialised A. candida races.10.7554/eLife.04550.011Figure 6.PCR with race-specific markers on DNA prepared from plant tissue generated from co-infection assays.

Bottom Line: Despite this divergence, their genomes are mosaic-like, with ∼25% being introgressed from other races.This facilitates introgression and the exchange of effector repertoires, and may enable the evolution of novel races that can undergo clonal population expansion on new hosts.We discuss recent studies on hybridization in other eukaryotes such as yeast, Heliconius butterflies, Darwin's finches, sunflowers and cichlid fishes, and the implications of introgression for pathogen evolution in an agro-ecological environment.

View Article: PubMed Central - PubMed

Affiliation: The Sainsbury Laboratory, Norwich, United Kingdom.

ABSTRACT
How generalist parasites with wide host ranges can evolve is a central question in parasite evolution. Albugo candida is an obligate biotrophic parasite that consists of many physiological races that each specialize on distinct Brassicaceae host species. By analyzing genome sequence assemblies of five isolates, we show they represent three races that are genetically diverged by ∼1%. Despite this divergence, their genomes are mosaic-like, with ∼25% being introgressed from other races. Sequential infection experiments show that infection by adapted races enables subsequent infection of hosts by normally non-infecting races. This facilitates introgression and the exchange of effector repertoires, and may enable the evolution of novel races that can undergo clonal population expansion on new hosts. We discuss recent studies on hybridization in other eukaryotes such as yeast, Heliconius butterflies, Darwin's finches, sunflowers and cichlid fishes, and the implications of introgression for pathogen evolution in an agro-ecological environment.

Show MeSH
Related in: MedlinePlus