Modelling somatic mutation accumulation and expansion in a long-lived tree with hierarchical modular architecture

Abstract Genomic sequencing revealed that somatic mutations cause a genetic differentiation of the cells in a single tree. We studied a mathematical model for stem cell proliferation in the shoot apical meristem (SAM). We evaluated the phylogenetic distance between cells sampled from different portions of a shoot, indicating their genetic difference due to mutations accumulated during shoot elongation. The plant tissue has cell walls that suppress the exchange of location between cells. This leads to the genetic differentiation of cells according to the angle around the shoot and a larger genetic variance among cells in the body. The assumptions are as follows: stem cells in the SAM normally undergo asymmetric cell division, producing successor stem cells and differentiated cells. Occasionally, a stem cell fails to leave its successor stem cell and the vacancy is filled by the duplication of one of the nearest neighbor stem cells. A mathematical analysis revealed the following: the genetic diversity of cells sampled at the same position along the shoot increases with the distance from the base of the shoot. Stem cells hold a larger variation if they are replaced only by the nearest neighbors. The coalescent length between two cells increases not only with the difference in the position along the shoot but also in the angle around the shoot axis. The dynamics of stem cells at the SAM determine the genetic pattern of the entire shoot. 

The genetic structure within a single tree is determined by the behavior of the stem cells in the meristem

Abstract Plant architecture is shaped by the continuous production of new organs, most of which emerge post-embryonically. This process includes the formation of new lateral branches along existing shoots. Shoot branching is fundamental to plant development, plant-environment interactions, and vegetative propagation. Current empirical evidence supports a “detached meristem” model as the cellular basis of lateral shoot initiation. In this model, a small number of undifferentiated cells are “sampled” from the periphery of the shoot apical meristem (SAM) to act as precursors for axillary buds, which eventually develop into new shoots. Repeated branching thus creates a series of cellular bottlenecks (i.e. somatic drift) that affect how de novo genetic and epigenetic mutations propagate through the plant body during development. Somatic drift could be particularly relevant for epigenetic changes in the form of stochastic DNA methylation gains and losses (i.e. spontaneous epimutations), as they have been shown to arise rapidly with each cell division. Here, we formalize a special case of the “detached meristem” model, where pre-cursor cells are randomly sampled from the SAM periphery in a way that maximizes cell lineage independence. By following a population of SAM cells through repeated branching processes, we show that somatic drift gives rise to a complex mixture of cellular phylogenies, which shape the evolution of cell-to-cell DNA methylation heterogeneity within the SAM over time. This process is dependent on the number of branch points, the strength of somatic drift as well as the epimutation rate. For many realistic cell biological settings, our model predicts that cell-to-cell DNA methylation heterogeneity in the SAM converges to non-zero states during development, suggesting that epigenetic variation is an inherent property of the SAM cell population. Our insights have direct implications for empirical studies of somatic (epi)genomic diversity in long-lived perennial and clonal species using bulk or single-cell sequencing approaches. 

Somatic epigenetic drift during shoot branching: a cell lineage-based model

For over a decade, the animal field has led the way in using DNA methylation measurements to construct epigenetic clocks of aging. These clocks can predict organismal age with a level of accuracy that surpasses any other molecular proxy known to date. Evidence is finally emerging that epigenetic clocks also exist in plants. However, these clocks appear to differ from those in animals in some key aspects, including in their ability to measure time beyond the life span of an individual. Clock-like epigenetic changes can be found in plant circadian rhythms (scale: 24 h), during plant aging (scale: weeks/centuries), and across plant lineage evolution (scale: decades/millennia). Here, we provide a first classification of these different types of epigenetic clocks, highlight their main features, and discuss their biological basis. 

Time's up: Epigenetic clocks in plants

ABSTRACT Old trees are remarkable for their ability to endure for centuries or even millennia, acting as recordkeepers of historical climate and custodians of genetic diversity. The secret to their longevity has long been a subject of fascination. Despite the challenges associated with studying old trees, such as massive size, slow growth rate, long lifespan and often remote habitat, accumulating studies have investigated the mechanisms underlying tree aging and longevity over the past decade. The recent publication of high‐quality genomes of long‐lived tree species, coupled with research on stem cell function and secondary metabolites in longevity, has brought us closer to unlocking the secrets of arboreal longevity. This review provides an overview of the global distribution of old trees and examines the environmental and anthropogenic factors that shape their presence. We summarize the contributions of physiological characteristics, stem cell activity, and immune system responses to their extraordinary longevity. We also explore the genetic and epigenetic ‘longevity code’, which consists of resistance and defense genes, DNA repair genes and patterns of DNA methylation modification. Further, we highlight key areas for future research that could enhance our understanding of the mechanisms underlying tree longevity. 

Tree Longevity: Multifaceted Genetic Strategies and Beyond

The rates of appearance of new mutations play a central role in evolution. However, mutational processes in natural environments and their relationship with growth rates are largely unknown, particular in tropical ecosystems with high biodiversity. Here, we examined the somatic mutation landscapes of two tropical trees, Shorea laevis (slow- growing) and S. leprosula (fast-growing), in central Borneo, Indonesia. Using newly- constructed genomes, we identified a greater number of somatic mutations in tropical trees than in temperate trees. In both species, we observed a linear increase in the number of somatic mutations with physical distance between branches. However, we found that the rate of somatic mutation accumulation per meter of growth was 3.7-fold higher in S. laevis than in S. leprosula. This difference in the somatic mutation rate was scaled with the slower growth rate of S. laevis compared to S. leprosula, resulting in a constant somatic mutation rate per year between the two species. We also found that somatic mutations are neutral within an individual, but those mutations transmitted to the next generation are subject to purifying selection. These findings suggest that somatic mutations accumulate with absolute time and older trees have a greater contribution towards generating genetic variation. Significance Statement The significance of our study lies in the discovery of an absolute time-dependent accumulation of somatic mutations in long-lived tropical trees, independent of growth rate. Through a comparative analysis of somatic mutation landscapes in slow- and fast-growing species, we observed a clock-like accumulation of somatic mutations in both species, regardless of their growth rates. Although the majority of somatic mutations were restricted to a single branch, we also identified mutations present in multiple branches, likely transmitted during growth. Our findings suggest that older trees make a greater contribution towards generating genetic variation.

The molecular clock in long-lived tropical trees is independent of growth rate

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The molecular clock in long-lived tropical trees is independent of growth rate