Genome-wide increased copy number is associated with emergence of super-fit clones of the Irish potato famine pathogen Phytophthora infestans

Abstract

The plant pathogen that caused the Irish potato famine, Phytophthora infestans, continues to reemerge globally. These modern epidemics are caused by clonally reproducing lineages. In contrast, a sexual mode of reproduction is observed at its center of origin in Mexico. We conducted a comparative genomic analysis of 47 high coverage genomes to infer changes in genic copy number. We included samples from sexual populations at the center of origin as well as several dominant clonal lineages sampled worldwide. We conclude that sexual populations at the center of origin are diploid as was the lineage that caused the famine, while modern clonal lineages showed increased copy number (3x). Copy number variation (CNV) was found genome-wide and did not to adhere to the two-speed genome hypothesis. Although previously reported, tetraploidy was not found in any of the genomes evaluated. We propose a model of super-fit clone emergence supported by the epidemiological record (e.g., EU_13_A2, US-11, US-23) whereby higher copy number provides fitness leading to replacement of prior clonal lineages.

Analysis of the lineage of Phytophthora infestans isolates using mating type assay, traditional markers, and next generation sequencing technologies

“…Some genomic variations may alter the host specificity and geographical location of isolates [17,25]. According to a recent report [26], CNVs are associated with the emergence of superfit clones of P. infestans. However, effector genes do not diverge among the Egyptian isolates, possibly because most of the tomato and potato cultivars in Egypt are susceptible to late blight, leading to minimal selection pressure and low mutation rates.…”

Analysis of the lineage ofPhytophthora infestansisolates using mating type assay, traditional markers, and next generation sequencing technologies

“…Some genomic variations may alter the host specificity and geographical location of isolates [17, 25]. According to a recent report [26], CNVs are associated with the emergence of super-fit clones of P. infestans . However, effector genes do not diverge among the Egyptian isolates, possibly because most of the tomato and potato cultivars in Egypt are susceptible to late blight, leading to minimal selection pressure and low mutation rates.…”

Variance of allele balance calculated from low coverage sequencing data infers departure from a diploid state

“…Increased cell size in plants is a consequence of polyploidy, possibly resulting in thicker, broader leaves and larger flowers, fruits, pollen, and stomata (Dar and Rehman, 2017; Otto and Whitton, 2000). Oomycetes (Stramenopiles), while somatically diploid, exhibit ploidy variation and/or heterokaryosis, which has consequences to fitness and virulence (Fletcher, et al, 2019; Knaus, et al, 2019). Many fungal species are somatically haploid, but like oomycetes, exhibit ploidy variation and/or heterokaryosis (Stajich, et al, 2009; Strom and Bushley, 2016; Zhu, et al, 2016).…”

“…High-throughput, whole-genome sequencing has enabled the detection of polyploidy and heterokaryosis in multiple species (Ament-Velásquez, et al, 2021; Bensasson, et al, 2019; Bertier, et al, 2013; Fletcher, et al, 2019; Fletcher, et al, 2018; Knaus, et al, 2019; Li, et al, 2016; Marburger, et al, 2018; Melo, et al, 2017; Strom and Bushley, 2016; Todd, et al, 2017; Tripp, et al, 2017; Weiß, et al, 2018; Yoshida, et al, 2013; Zhu, et al, 2016; Zhuang and Tripp, 2017). Several in silico approaches have been developed to summarize nucleotide frequencies at polymorphic sites and determine if two or more haplotypes exist in a sample (Knaus, et al, 2019; Weiß, et al, 2018). These approaches resolve the number of haplotypes present in a DNA sample by inferring the allele balance at bi-allelic single nucleotide polymorphisms (SNPs).…”

“…This approach was reported to work well at lower coverage for S. cerevisiae (∼20x), but still required a higher read depth for analysis of P. infestans (Weiß, et al, 2018). Another approach that summarizes allele balance across multiple windows of a genome assembly was recently deployed in vcfR and was deployed on low coverage data (12x) to infer copy number variation of Phytophthora infestans isolates (Knaus and Grünwald, 2018; Knaus, et al, 2019). The latter method aims to determine if parts of the genome are present in higher quantities than expected and reports the proportions of inferred diploidy and polyploidy in each sample.…”