High-quality genome and methylomes illustrate features underlying evolutionary success of oaks

Abstract

The genus Quercus, which emerged ~55 million years ago during globally warm temperatures, diversified into ~450 species. We present a high-quality de novo genome assembly of a California endemic oak, Quercus lobata, revealing features consistent with oak evolutionary success. Effective population size remained large throughout history despite declining since the early Miocene. Analysis of 39,373 mapped protein-coding genes outlined copious duplications consistent with genetic and phenotypic diversity, both by retention of genes created during the ancient γ whole genome hexaploid duplication event and by tandem duplication within families, including the numerous resistance genes and also unexpected candidate genes for an incompatibility system involving multiple non-self-recognition genes. An additional surprising finding is that subcontext-specific patterns of DNA methylation associated with transposable elements reveal broadly-distributed heterochromatin in intergenic regions, similar to grasses (another highly successful taxon). Collectively, these features promote genetic and phenotypic variation that would facilitate adaptability to changing environments.

A chromosome‐scale genome assembly of the Mongolian oak (Quercus mongolica)

“…Investigation of the syntenic relationship between Q. mongolica , Q. robur , and Q. lobata revealed a higher degree of syntenic conservation between Q. mongolica and Q. lobata genomes than that between Q. mongolica and Q. robur genomes, showing a contradictory phylogenetic relationship based on the phylogenetic tree and Ks analysis, which demonstrated a closer evolutionary relationship between Q. mongolica and Q. robur than that between Q. mongolica and Q. lobata . The reasonable explanation for this contradictory phylogenetic relationship is that the quality of the Q. robur genome assembly differs significantly from that of Q. mongolica and Q. lobata (Sork et al, 2021). This difference may be due to the use of PacBio long reads in the genome assembly of Q. mongolica and Q. lobata (Jiao & Schneeberger, 2017).…”

“…We filtered alternative splicing for each gene and retained only the longest transcript of each gene to represent the coding region. Then the protein‐coding genes with an ostensibly complete CDS were retained (Sork et al, 2021). The ostensibly complete means the CDS, as derived exclusively from the assembly, starts on a codon boundary with a start codon, ends on a codon boundary with a stop codon, and has no internal stop codons (Sork et al, 2021).…”

“…Then the protein-coding genes with an ostensibly complete CDS were retained (Sork et al, 2021). The ostensibly complete means the CDS, as derived exclusively from the assembly, starts on a codon boundary with a start codon, ends on a codon boundary with a stop codon, and has no internal stop codons (Sork et al, 2021). Protein sequences from these six species were used to perform gene family construction using orthofinder v2.2.7 (https://github.com/david emms/ Ortho Finder) (Emms & Kelly, 2019).…”

“…The non-coding RNAs were identified, including 129 miRNAs, 768 tRNAs, 4896 rRNAs, and 371 snRNAs (Table S13). Note: Information on the genome assembly and gene annotation of Q. robur and Q. lobata was referenced from the previous reports (Plomion et al, 2018;Sork et al, 2021). The Q. suber genome assembly information was referenced from the previous report (Ramos et al, 2018).…”

“…Therefore, the availability of whole-genome sequencing data for white oaks from disparate geographic backgrounds is essential to aid the phylogenetic inference of section Quercus (Crowl et al, 2020). However, only two white oak species from Western Europe (Q. robur, belonging to the Roburoid lineage; Plomion et al, 2016Plomion et al, , 2018 and North America (Q. lobata, belonging to the Dumosae lineage; Sork et al, 2016Sork et al, , 2021 have available genome-wide data and East Asia, one of the six main distribution areas of white oaks (Denk et al, 2017), does not have any available genome-wide data for native white oak.…”