Abstract
The fungus Mycosphaerella graminicola has been a pathogen of wheat since host domestication 10,000–12,000 years ago in the Fertile Crescent. The wheat-infecting lineage emerged from closely related Mycosphaerella pathogens infecting wild grasses. We use a comparative genomics approach to assess how the process of host specialization affected the genome structure of M. graminicola since divergence from the closest known progenitor species named M. graminicola S1. The genome of S1 was obtained by Illumina sequencing resulting in a 35 Mb draft genome sequence of 32X. Assembled contigs were aligned to the previously sequenced M. graminicola genome. The alignment covered >90% of the non-repetitive portion of the M. graminicola genome with an average divergence of 7%. The sequenced M. graminicola strain is known to harbor thirteen essential chromosomes plus eight dispensable chromosomes. We found evidence that structural rearrangements significantly affected the dispensable chromosomes while the essential chromosomes were syntenic. At the nucleotide level, the essential and dispensable chromosomes have evolved differently. The average synonymous substitution rate in dispensable chromosomes is considerably lower than in essential chromosomes, whereas the average non-synonymous substitution rate is three times higher. Differences in molecular evolution can be related to different transmission and recombination patterns, as well as to differences in effective population sizes of essential and dispensable chromosomes. In order to identify genes potentially involved in host specialization or speciation, we calculated ratios of synonymous and non-synonymous substitution rates in the >9,500 aligned protein coding genes. The genes are generally under strong purifying selection. We identified 43 candidate genes showing evidence of positive selection, one encoding a potential pathogen effector protein. We conclude that divergence of these pathogens was accompanied by structural rearrangements in the small dispensable chromosomes, while footprints of positive selection were present in only a small number of protein coding genes.
Highlights
We know little about the evolutionary processes leading to the origin and emergence of new fungal plant pathogens despite their significant impact on our food supply
We used paired end Illumina sequencing at 32X coverage to derive a high-quality assembly of the wild S1 species and aligned it to the Mycosphaerella graminicola genome to address the following questions: 1) Which structural genome changes have occurred since divergence and how can these be related to host specialization? 2) Have essential and dispensable chromosomes diverged to the same extent over the time course of 11,000 years?
The fungal wheat pathogen Mycosphaerella graminicola emerged in the Middle East 11,000 years ago, coinciding with host domestication
Summary
We know little about the evolutionary processes leading to the origin and emergence of new fungal plant pathogens despite their significant impact on our food supply. Mass sequencing technologies that enable the acquisition of complete pathogen genome sequences provide a new approach to address questions related to the roles played by host specialization and speciation. By comparing the genomes of pathogens that have recently diverged and specialized onto different hosts we can quantify how much of the genome was affected by the process of divergence and identify genomic regions or particular genes that were involved in host specialization. We confirm a recent and rapid development of reproductive isolation, report a strikingly different pattern of genome evolution for essential and dispensable chromosomes and identify genes and gene categories that appear associated with host specialization or reproductive isolation
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