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Open Access Highly Accessed Research article

Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut

Heath E O’Brien1*, Shalabh Thakur1, Yunchen Gong2, Pauline Fung2, Jianfeng Zhang2, Lijie Yuan2, Pauline W Wang12, Choseung Yong1, Marco Scortichini3 and David S Guttman12

Author Affiliations

1 Department of Cell and Systems Biology, University of Toronto, 25 Willcocks St., Toronto, ON, M5S 3B2, Canada

2 Center for the Analysis of Genome Evolution & Function, University of Toronto, 25 Willcocks St., Toronto, ON, M5S 3B2, Canada

3 C.R.A.- Fruit Crops Research Centre, Via di Fioranello, 52; I-00134, Rome, Italy

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BMC Microbiology 2012, 12:141  doi:10.1186/1471-2180-12-141

Published: 16 July 2012

Abstract

Background

Hazelnut (Corylus avellana) decline disease in Greece and Italy is caused by the convergent evolution of two distantly related lineages of Pseudomonas syringae pv. avellanae (Pav). We sequenced the genomes of three Pav isolates to determine if their convergent virulence phenotype had a common genetic basis due to either genetic exchange between lineages or parallel evolution.

Results

We found little evidence for horizontal transfer (recombination) of genes between Pav lineages, but two large genomic islands (GIs) have been recently acquired by one of the lineages. Evolutionary analyses of the genes encoding type III secreted effectors (T3SEs) that are translocated into host cells and are important for both suppressing and eliciting defense responses show that the two Pav lineages have dramatically different T3SE profiles, with only two shared putatively functional T3SEs. One Pav lineage has undergone unprecedented secretome remodeling, including the acquisition of eleven new T3SEs and the loss or pseudogenization of 15, including five of the six core T3SE families that are present in the other Pav lineage. Molecular dating indicates that divergence within both of the Pav lineages predates their observation in the field. This suggest that both Pav lineages have been cryptically infecting hazelnut trees or wild relatives for many years, and that the emergence of hazelnut decline in the 1970s may have been due to changes in agricultural practice.

Conclusions

These data show that divergent lineages of P. syringae can converge on identical disease etiology on the same host plant using different virulence mechanisms and that dramatic shifts in the arsenal of T3SEs can accompany disease emergence.

Keywords:
Effector; Host specificity; Molecular dating