The somatic genetic and epigenetic mutation rate in a wild long-lived perennialPopulus trichocarpa

Abstract

perennial Populus trichocarpa 2 3 AUTHORS 4 5 Brigitte T. ABSTRACT 38 39 Background: Plants can transmit somatic mutations and epimutations to offspring, 40 which in turn can affect fitness. Knowledge of the rate at which these variations arise is 41 necessary to understand how plant development contributes to local adaption in an eco-42 evolutionary context, particularly in long-lived perennials.43Results: Here, we generated a new high-quality reference genome from the oldest 44 branch of a wild Populus trichocarpa tree with two dominant stems which have been 45 evolving independently for 330 years. By sampling multiple, age-estimated branches of 46 3 this tree, we used a multi-omics approach to quantify age-related somatic changes at 47 the genetic, epigenetic and transcriptional level. We show that the per-year somatic 48 mutation and epimutation rates are lower than in annuals and that transcriptional 49 variation is mainly independent of age divergence and cytosine methylation. 50Furthermore, a detailed analysis of the somatic epimutation spectrum indicates that 51 transgenerationally heritable epimutations originate mainly from DNA methylation 52 maintenance errors during mitotic rather than during meiotic cell divisions. 53 Conclusion: Taken together, our study provides unprecedented insights into the origin 54 of nucleotide and functional variation in a long-lived perennial plant. 55 56 BACKGROUND 57 58The significance of somatic mutations, i.e., variations in DNA sequence that occur after 59 fertilization, in long-lived plant and animal species have been a point of debate and 60 investigation for the past 30 years [1][2][3][4]. It has been hypothesized that the evolutionary 61 consequences of such mutations are likely even more profound in woody perennial 62 plants, where undifferentiated meristematic cells produce all above-ground and below-63 ground structures. As meristems undergo constant cell division throughout the lifetime 64 of a plant, somatic mutations arising in meristems may result in genetic differences 65 being passed onto progeny cells [5][6][7][8]. The accumulation of somatic mutations can thus 66 lead to genetic and occasionally also phenotypic divergence among vegetative lineages 67 within the same individual. In trees, for instance, different branches have been shown to 68 differ in their responses to pest and pathogen attack, alternate reactions to drought 69 4 and/or nutrient availability, or dissimilar demands for photosynthate material, even 70 within the same individual [9]. Beyond the impact of point mutations and small 71 insertions/deletions on gene function, alterations in chromatin structure and DNA 72 methylation might also impact gene expression variation. 73 74 Phenotypic variation has been attributed to somatic mutations in several perennial 75 plants, including the derivation of Nectarines in peach [10] and the origin of modern 76 grape cultivars (Vitis vinifera L.) [11]. In Populus tremuloides, somatic mutations have 77 been hypothesized as the cause for variation in DN...

Population-level consequences of inheritable somatic mutations and the evolution of mutation rates in plants

“…Hence, results indicate that while we should expect more efficient mechanisms reducing the accumulation of deleterious mutations during growth to evolve in more long-lived species, so that their per unit of growth and per year mutation rate should be lower, their per generation mutation rates should still be higher. These predictions are in line with empirical evidence, which suggest that mutation rates per generation tend to be higher in more long-lived species although the mutation rates per unit of growth tend to be lower [18][19][20]. I modelled the evolution of the mutation rate following the work of Kimura [15], by assuming there is a direct fitness cost to DNA replication fidelity opposing the indirect selection generated by deleterious mutations linked to the modifier, so that the mutation rate was maintained greater than zero in response to a trade-off.…”

“…Consistent with this view, it was shown at the cellular level that axillary meristems cells are set aside early during the growth of a shoot [1], resulting in the number of cell divisions increasing linearly with the number of branching events in trees although the number of terminal branches increases exponentially. Furthermore, multiple studies showed that somatic mutation rates tend to be considerably lower in taller, more long-lived species [18][19][20][21][22][23]. For instance, Orr et al [20] found the somatic mutation rate per generation to be only 10 times higher in Eucalyptus melliodora than in Arabidopsis, despite being greater than 100 times larger in size.…”

Sequencing and Analysis of the Sex Determination Region of Populus trichocarpa

“…Hood, Oregon. The tree was originally collected as part of a study to determine the rates of somatic mutation and variation in methylation status [ 24 ]. The genome was sequenced to ~120× depth using PacBio technology, with an average read length of 10,477 bp.…”

“…The genome assembly also contained ~232.2 Mb of alternative haplotypes. Full details of the assembly and annotation can be found in [ 24 ].…”

Region-level Epimutation Rates inArabidopsis thaliana

“…We have shown that the rates of region-level mCG changes, while only marginally dependent on region size and cytosine density, strongly depended on genome annotation and are consistently highest in genes and lowest in TEs. This hierarchy of epimutation rates per annotation is not only preserved from single CG estimates in A. thaliana (van der Graaf et al, 2015), but is also conserved in mitotic studies of epimutation rates in Populus trichocarpa (Hofmeister et al, 2019). This suggests that the hierarchy of epimutations is not a product of methylation reinforcement events during seed development but is conserved by DNA methylation maintenance pathways during mitotic cell division upon somatic development in plants (Hofmeister et al, 2019;Johannes and Schmitz, 2019).…”