Oak genome reveals facets of long lifespan

Abstract

Oaks are an important part of our natural and cultural heritage. Not only are they ubiquitous in our most common landscapes¹ but they have also supplied human societies with invaluable services, including food and shelter, since prehistoric times². With 450 species spread throughout Asia, Europe and America³, oaks constitute a critical global renewable resource. The longevity of oaks (several hundred years) probably underlies their emblematic cultural and historical importance. Such long-lived sessile organisms must persist in the face of a wide range of abiotic and biotic threats over their lifespans. We investigated the genomic features associated with such a long lifespan by sequencing, assembling and annotating the oak genome. We then used the growing number of whole-genome sequences for plants (including tree and herbaceous species) to investigate the parallel evolution of genomic characteristics potentially underpinning tree longevity. A further consequence of the long lifespan of trees is their accumulation of somatic mutations during mitotic divisions of stem cells present in the shoot apical meristems. Empirical⁴ and modelling⁵ approaches have shown that intra-organismal genetic heterogeneity can be selected for⁶ and provides direct fitness benefits in the arms race with short-lived pests and pathogens through a patchwork of intra-organismal phenotypes⁷. However, there is no clear proof that large-statured trees consist of a genetic mosaic of clonally distinct cell lineages within and between branches. Through this case study of oak, we demonstrate the accumulation and transmission of somatic mutations and the expansion of disease-resistance gene families in trees.

Fig. 1. Genomic landscape of the 12 assembled oak chromosomes.

Gene (A) and TE (B) density, percentage heterozygosity (purple in C) and genetic diversity (green in C). These four metrics are calculated in 1-Mb sliding windows, moved in 250-kb steps. A ruler is drawn on each chromosome, with tick marks every 10 Mb.

Fig. 2. Genetic diversity and somatic mutations.

a, Distribution of π₀/π₄ plotted against π₄ among plants (modified from a previous publication), including oak (red square). Species names are according to. b, Genomic location of somatic mutations along the 12 chromosomes of a 100-year-old oak tree. Mutations are represented as coloured arrows according to where they took place during tree growth (see inset). Location and age (left of the trunk) of the three levels (L1, L2 and L3) sampled for somatic mutation detection in the reference pedunculate oak genotype 3P. L1, L2 and L3 represent the end of selected branches; X_L1 and X_L2 represent L1-branch and L2-branch initiation sites, respectively. For each branch, the recovery or non-recovery of mutations in acorns is indicated by filled and open squares, respectively. The numbers of copies of the alternative (coloured) and reference (grey) alleles are shown below each square.

Fig. 3. Evolutionary history of the oak genome.

a, Evolutionary scenario of oak from the AEK of 21 (post-γ) and 7 (pre-γ) protochromosomes reconstructed from a comparison of the Vitales (grape), Rosales (peach) and Malvales (cocoa) major subfamilies. The modern genomes (bottom) are illustrated with different colours reflecting the seven ancestral chromosomes of AEK origin (top). WGT (red star) refers to the whole-genome triplication (γ) shared among the eudicots. b, K_s distribution of gene pairs for oak–peach orthologues as well as the shared γ triplication in grape, peach, cocoa and oak. K_s distribution of all gene pairs in oak illuminate gene pairs from the γ triplication as well as recent duplicates. c, Dot plot representation of the oak genome against itself for the complete set of paralogous pairs (left) and without TDGs (right) representing the disappearance of the diagonal (TDGs) when low K_s values are removed. d, Expansion (524 orthogroups) and contraction (72 orthogroups) in oak relative to 15 other eudicot species. The pie charts reflect the contribution of TDGs, LDGs and singleton genes (SGs) to the significantly expanded and contracted orthogroups and to outstanding outliers (labelled 1–9). Numbers in square brackets associated with circle sizes stand for -log(P-value), computed from the oak branch-specific P-value provided by CAFE.

Fig. 4. Expanded gene families in trees.

a, Phylogeny of orthogroup 1 from Figs. 3d and 4b, established from the nucleotide-binding domains of 1,641 NB–LRR genes. Branches for trees and herbaceous species are shown in brown and green, respectively. Branches expanded in oak are shaded. For a higher resolution image see Supplementary Fig. 6. b, Scatter plot showing orthogroups expanded in trees and herbaceous plants (images from http://openclipart.org). Numbers in square brackets associated with circle sizes stand for -log(P-adjust), where P-adjust is the P-value of the binomial test adjusted for multiple testing.