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.
Highlights
We sequenced the highly heterozygous genome of pedunculate oak (Quercus robur L.; Supplementary Notes 1 and 2) using a combination of long and short sequence reads (Supplementary Table 1)
52% of the genome was found to consist of diverse transposable elements (TEs), which were dominated by class I retrotransposons (70%) (Supplementary Table 4, Supplementary Fig. 3, Supplementary Notes 3.1 and 3.4)
We sampled buds at the extremities of branches initiated at the ages 15, 47 and 85 years on the reference tree sequenced in this study (Fig. 2b, Supplementary Fig. 5)
Summary
Animal species[9] indicated that oak was remarkable in terms of both its high nucleotide diversity (π4) and the high rate at which it accumulates deleterious mutations Ten of the 15 gene families displaying striking expansion in tree genomes (Fig. 4b) corresponded to NB–LRRs (orthogroups 1, 4, 8, 11 and 12), LRR–RLKs (orthogroups 3 (subgroup XIIb), 5 (subgroup XIIa) and 9) or LRR–RLPs (orthogroups 6 and 13). We observed a parallel expansion of R generelated gene families across multiple tree species, suggesting that the immune system makes an essential contribution to the survival of long-lived plants over several centuries. The remarkable relaxation of purifying selection observed in oaks may facilitate the evolution of a richer and more diverse set of R genes, thereby conferring an advantage on these trees in their continuous arms race with pathogens[32] This dynamic is likely to apply to oaks, with their remarkably long lifespan. The maintenance of such a diversity of R genes may be costly, and future studies should look at how trees control the expression of these immune receptors, through microRNA control, for example[22]
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