Accelerated growth increases the somatic epimutation rate in trees.

Abstract

Trees are integral to ecosystems and hold considerable economic importance. Their exceptional longevity and modular structure also make them valuable models for studying the long-term accumulation of somatic mutations and epimutations in plants. Empirical evidence indicates that the annual rate of these stochastic events correlates negatively with generation time, suggesting that species with long lifespans have evolved mechanisms to mitigate the build-up of deleterious somatic variants. It has been hypothesized that this reduction is achieved by slowing growth and minimizing the number of cell divisions per unit time, thereby reducing errors associated with DNA replication. However, a direct test of this "mitotic-rate hypothesis" remains technically challenging. Here we take advantage of a 150 year-old experiment in European beech to show that a thinning-induced growth acceleration increases the annual rate of somatic epimutations in main stems and lateral branches of trees. We demonstrate that this effect is accompanied by a proportional increase in the rate of cell divisions per unit time. These findings support the notion that life-history constraints on growth rates in trees are not merely a trade-off between resource allocation and structural stability but also a strategy to preserve genetic and epigenetic fidelity over extended lifespans.