Ancestral chromosomes for the Peronosporaceae inferred from a telomere-to-telomere genome assembly of Peronospora effusa

Abstract

We report the first telomere-to-telomere genome assembly for an oomycete. This assembly has extensive synteny with less complete genome assemblies of other oomycetes and will therefore serve as a reference genome for this taxon. Downy mildew disease of spinach, caused by the oomycete Peronospora effusa, causes major losses to spinach production. The 17 chromosomes of P. effusa were assembled telomere-to-telomere using Pacific Biosciences High Fidelity reads. Sixteen chromosomes are complete and gapless; Chromosome 15 contains one gap bridging the nucleolus organizer region. Putative centromeres were identified on all chromosomes. This new assembly enables a re-evaluation of the genomic composition of Peronospora spp.; the assembly was almost double the size and contained more repeat sequences than previously reported for any Peronospora spp. Genome fragments consistently under-represented in six previously reported assemblies of P. effusa typically encoded repeats. Some genes annotated as encoding effectors were organized into multigene clusters on several chromosomes. At least two effector-encoding genes were annotated on every chromosome. The intergenic distances between annotated genes were consistent with the two-speed genome hypothesis, with some effectors located in gene-sparse regions. The near-gapless assembly revealed apparent horizontal gene transfer from Ascomycete fungi. Gene order was highly conserved between P. effusa and the genetically oriented assembly of the oomycete Bremia lactucae. High levels of synteny were also detected with Phytophthora sojae. Many oomycete species may have similar chromosome organization; therefore, this genome assembly provides the foundation for genomic analyses of diverse oomycetes.

Sexual reproduction contributes to the evolution of resistance‐breaking isolates of the spinach pathogen Peronospora effusa

“…High quality, complete genome assemblies of multiple P. effusa isolates are thus invaluable to fully uncover the molecular underpinning of race emergence in P. effusa (Thomma et al ., 2016 ). The newly generated high‐quality genome assembly of P. effusa is much longer and more repetitive compared with previous genome assemblies (Fletcher et al ., 2021 ), providing a valuable resource to start comparative research between races. To link genotypic variation to differences in resistance breaking on spinach cultivars, emphasis should be given to the systematic mining of effector genes and their variation between genetically and phenotypically distinct P. effusa isolates.…”

“…Like many oomycetes, P. effusa is a heterozygous diploid organism. Its genome sequence is relatively small compared with other oomycetes (58.6 Mb compared with, for instance, Phytophthora infestans which is 240 Mb; Haas et al ., 2009 ), and it is organized in 17 chromosomes with 53.7% repeat content (Fletcher et al ., 2021 ). P. effusa can reproduce both asexually and sexually.…”

“…Nevertheless, genotypic diversity in historical isolates is likely influenced by sexual recombination (Lyon et al ., 2016 ). The complete genome assembly of the P. effusa isolate UA202013 has been compared with closely related isolates from races 12, 13, and 14 with limited variation being observed (Fletcher et al ., 2021 ). Consequently, we still know surprisingly little about genome‐wide diversity between most of P. effusa isolates and races, as well as evolutionary processes that contribute to the emergence of new P. effusa races.…”

The genome of the oomycete Peronosclerospora sorghi, a cosmopolitan pathogen of maize and sorghum, is inflated with dispersed pseudogenes

“…Genomic resources are foundational for accurately defining the variation present in populations of a pathogen, conducting bio-surveillance, and identifying vulnerabilities and opportunities that can be utilized for disease management. Recently, two 17-chromosome-scale genome assemblies have been reported for the oomycetes Bremia lactucae and Peronospora effusa, which cause lettuce and spinach downy mildew, respectively [15, 16]. Despite being taxonomically distant, these oomycetes share a high degree of synteny.…”

Sexual reproduction contributes to the evolution of resistance breaking isolates of the spinach pathogen Peronospora effusa

“…Like many oomycetes, P. effusa is a heterozygous diploid organism. Its genome sequence is relatively small compared with other oomycetes (58.6 Mb compared with for instance Phytophthora infestans which is 240 Mb (Haas et al ., 2009)), and it is organised in 17 chromosomes with 53.7% repeat content (Fletcher et al ., 2021). P. effusa can reproduce both asexually and sexually.…”