Karyotype variation, spontaneous genome rearrangements affecting chemical insensitivity, and expression level polymorphisms in the plant pathogen Phytophthora infestans revealed using its first chromosome-scale assembly

Abstract

Natural isolates of the potato and tomato pathogen Phytophthora infestans exhibit substantial variation in virulence, chemical sensitivity, ploidy, and other traits. A chromosome-scale assembly was developed to expand genomic resources for this oomyceteous microbe, and used to explore the basis of variation. Using PacBio and Illumina data, a long-range linking library, and an optical map, an assembly was created and coalesced into 15 pseudochromosomes spanning 219 Mb using SNP-based genetic linkage data. De novo gene prediction combined with transcript evidence identified 19,981 protein-coding genes, plus about eight thousand tRNA genes. The chromosomes were comprised of a mosaic of gene-rich and gene-sparse regions plus very long centromeres. Genes exhibited a biased distribution across chromosomes, especially members of families encoding RXLR and CRN effectors which clustered on certain chromosomes. Strikingly, half of F1 progeny of diploid parents were polyploid or aneuploid. Substantial expression level polymorphisms between strains were identified, much of which could be attributed to differences in chromosome dosage, transposable element insertions, and adjacency to repetitive DNA. QTL analysis identified a locus on the right arm of chromosome 3 governing sensitivity to the crop protection chemical metalaxyl. Strains heterozygous for resistance often experienced megabase-sized deletions of that part of the chromosome when cultured on metalaxyl, increasing resistance due to loss of the sensitive allele. This study sheds light on diverse phenomena affecting variation in P. infestans and relatives, helps explain the prevalence of polyploidy in natural populations, and provides a new foundation for biologic and genetic investigations.

Population Dynamics of Phytophthora infestans in Egypt Reveals Clonal Dominance of 23_A1 and Displacement of 13_A2 Clonal Lineage

“…Phenylamide fungicides (metalaxyl, oxadixyl, benalaxyl) act through inhibition of ribosomal RNA synthesis in the pathogen cells [ 44 ]. Although the exact genetics of metalaxyl resistance is unknown, it is believed to be associated with multiple mutations in the RPA190 gene [ 45 ] or the spontaneous deletion of chromosome regions containing the sensitive alleles of this gene [ 45 , 46 ]. However, studies on the inheritance in genetic crosses of P. infestans also suggest other genes are involved [ 46 ].…”

“…Although the exact genetics of metalaxyl resistance is unknown, it is believed to be associated with multiple mutations in the RPA190 gene [ 45 ] or the spontaneous deletion of chromosome regions containing the sensitive alleles of this gene [ 45 , 46 ]. However, studies on the inheritance in genetic crosses of P. infestans also suggest other genes are involved [ 46 ]. Unlike 13_A2, the 23_A1 genotype is considered as sensitive to intermediate in response to metalaxyl [ 47 ].…”

Quantitative plant resistance enhances pathogen adaptation to ecological stresses

“…Comparison of SNPs and Indels between pathogen genomes of potato cultivars with LQPR and HQPR identified 11335 mutated genes, accounting for 56.73% of 19981 protein-coding genes predicted from the P. infestans genome 56 . Among them, 3154, 2064 and 1503 genes were mutated only in the CDS, upstream or downstream regions respectively while 4614 genes were mutated in two or three of the three regions at the same time, suggesting that genetic adaptation through changes in gene structure and epigenetic adaptation through changes in gene expression play a similar role in the pathogen adaptation to host resistance.…”

Comparative genomics ofCryptococcusandKwoniellareveals pathogenesis evolution and contrasting karyotype dynamics via intercentromeric recombination or chromosome fusion

“…Chromosomal rearrangements, including inversions, translocations, fusions, and fissions, underlie the extensive karyotypic variability seen across eukaryotes [26][27][28]. These sources of structural variation aid organisms in adapting to diverse environments [29,30], influence changes in mating systems [23,[31][32][33], drive the evolution of pathogenic traits [34][35][36], and play roles in speciation [37][38][39][40][41].…”