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

Authors: FLETCHER, KYLE - University Of California; SHIN, OON-HA - University Of California; Clark, Kelley; FENG, CHUNDA - University Of Arkansas; PUTMAN, ALEXANDER - University Of California; CORRELL, JAMES - University Of Arkansas; Klosterman, Steven; VAN DEYNZE, ALLEN - University Of California; MICHELMORE, RICHARD - University Of California

Submitted to: Molecular Plant-Microbe Interactions
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/24/2022
Publication Date: 5/2/2022
Citation: Fletcher, K., Shin, O.H., Clark, K.J., Feng, C., Putman, A.I., Correll, J.C., Klosterman, S.J., Van Deynze, A., Michelmore, R.W. 2022. Ancestral chromosomes for family Peronosporaceae inferred from a telomere-to-telomere genome assembly of Peronospora effusa. Molecular Plant-Microbe Interactions. 35(6):450-463. https://doi.org/10.1094/MPMI-09-21-0227-R.
DOI: https://doi.org/10.1094/MPMI-09-21-0227-R

Interpretive Summary: Downy mildew, caused by P. effusa, threatens spinach production as infection results in leaves unsuitable for sale and consumption. To date, there are 19 named races of P. effusa, however isolates with variations in resistance are continuously identified and the biology behind the emergence of new races is not clearly understood. Previous genomic investigations have yielded fragmented and repeat-sparse genome assemblies. Genome assemblies are important resources for determining the molecular basis for changes in virulence resulting in the emergence of new pathotypes and to provide informative loci for population studies. In the current study, a 17-chromosome assembly is described for P. effusa that was generated using PacBio High Fidelity reads. Sixteen telomere-to-telomere gapless contigs and one telomere-to-telomere scaffold were assembled. There was a high degree of synteny between P. effusa, P. sojae, and Bremia lactucae. This is a landmark genome assembly for oomycete genomics.

Technical Abstract: Downy mildew disease of spinach, caused by the oomycete Peronospora effusa, causes major losses to spinach production. In this study, the 17 chromosomes of P. effusa were assembled telomere-to-telomere, using Pacific Biosciences high-fidelity reads. Of these, 16 chromosomes are complete and gapless; chromosome 15 contains one gap bridging the nucleolus organizer region. This is the first telomere-to-telomere genome assembly for an oomycete. Putative centromeric regions were identified on all chromosomes. This new assembly enables a reevaluation 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 species. Genome fragments consistently underrepresented 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. Putative effectors were annotated on 16 of the 17 chromosomes. The intergenic distances between annotated genes were consistent with compartmentalization of the genome into gene-dense and gene-sparse regions. Genes encoding putative effectors were enriched 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. Extensive synteny between phylogenetically distant species suggests that many other oomycete species may have similar chromosome organization. Therefore, this assembly provides the foundation for genomic analyses of diverse oomycetes.