Abstract

BackgroundPlant fungal pathogens can rapidly evolve and adapt to new environmental conditions in response to sudden changes of host populations in agro-ecosystems. However, the genomic basis of their host adaptation, especially at the forma specialis level, remains unclear.ResultsWe sequenced two isolates each representing Puccinia striiformis f. sp. tritici (Pst) and P. striiformis f. sp. hordei (Psh), different formae speciales of the stripe rust fungus P. striiformis highly adapted to wheat and barley, respectively. The divergence of Pst and Psh, estimated to start 8.12 million years ago, has been driven by high nucleotide mutation rates. The high genomic variation within dikaryotic urediniospores of P. striiformis has provided raw genetic materials for genome evolution. No specific gene families have enriched in either isolate, but extensive gene loss events have occurred in both Pst and Psh after the divergence from their most recent common ancestor. A large number of isolate-specific genes were identified, with unique genomic features compared to the conserved genes, including 1) significantly shorter in length; 2) significantly less expressed; 3) significantly closer to transposable elements; and 4) redundant in pathways. The presence of specific genes in one isolate (or forma specialis) was resulted from the loss of the homologues in the other isolate (or forma specialis) by the replacements of transposable elements or losses of genomic fragments. In addition, different patterns and numbers of telomeric repeats were observed between the isolates.ConclusionsHost adaptation of P. striiformis at the forma specialis level is a complex pathogenic trait, involving not only virulence-related genes but also other genes. Gene loss, which might be adaptive and driven by transposable element activities, provides genomic basis for host adaptation of different formae speciales of P. striiformis.

Highlights

  • Plant fungal pathogens can rapidly evolve and adapt to new environmental conditions in response to sudden changes of host populations in agro-ecosystems

  • Our genomic analyses showed that the host adaptation of formae speciales is a complex trait in P. striiformis, supported by the following two factors: i) no specific gene loss or gain could explain their adaptation, even though the two formae speciales were slightly different in specific protein family compositions (Table 2); and ii) a large number of both non-Secreted Protein (SP) and SP genes were under diversifying selections, in contrast to B. graminis f. sp. tritici and B. graminis f. sp. hordei in which SP genes have much higher dN/dS ratios compared to non-SP

  • We found the following genomic features associated with the host adaptations of Puccinia striiformis f. sp. tritici (Pst) and P. striiformis f. sp. hordei (Psh): i) the high genetic variations between two nuclei in a urediniospore provide raw genetic materials for genome evolution; ii) the rapidly evolving isolate-specific genes are dispensable and subject to functional loss; iii) gene loss may be adaptive during the host adaptation; and iv) transposable elements accelerate the evolution of host adaptation by involving in gene loss

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Summary

Introduction

Plant fungal pathogens can rapidly evolve and adapt to new environmental conditions in response to sudden changes of host populations in agro-ecosystems. Tremendous genomic studies of filamentous plant pathogens have shown that the pathogenicity-related genes reside in such rapidly evolving genomic compartments including gene clusters [6], gene-sparse and repeat-rich regions [7], AT-rich isochores [8] and supernumerary (conditionally dispensable) chromosomes [9, 10]. While most of these studies were on pathogenicity-related genes, details of genomic basis of host adaptation in filamentous plant pathogens remain to be elucidated even though some of the pathogenicity genes were host specificity determinants [10]

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