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Biology subjects

Tomimoto, S.

Publications and source records attributed to Tomimoto, S..

6 recordsLinked to original sources

Inferring somatic mutation dynamics from genomic variation across branches within long-lived tropical trees

Trees accumulate somatic mutations throughout their long lifespan, resulting in genetic mosaicism among branches. While recent genomic studies quantified these mutations, they were largely limited to describing static patterns of variation. In this study, we developed a mathematical model to infer the dynamic processes of somatic mutation accumulation from snapshot genomic data obtained from four tropical trees (Dipterocarpaceae), which dominate tropical rain forests in Southeast Asia. Our model focus on genetic differences between shoot apical meristems (SAMs) at branch tips and explicitly incorporate stem cell dynamics within SAMs during shoot elongation and branching, enabling us to quantify somatic genetic drift arising from stem cell lineage replacement. By comparing model predictions with empirical data from Dipterocarpaceae trees, we estimated key parameters governing stem cell dynamics and somatic mutation rates. Our results indicate that both shoot elongation and branching involve replacement of stem cell lineages, leading to a moderate degree of somatic genetic drift. Accounting for stem cell dynamics resulted in slightly lower mutation rate estimates than previous approaches that ignored these processes. Using the estimated parameters, we further performed stochastic simulations to predict patterns of somatic mutations, including features not directly observed in the sampled trees, such as occasional deviations of somatic mutation phylogenies from physical architecture. Together, our modeling framework provides insights into how genetic mosaicism is shaped within tropical trees and reveals the stem cell dynamics underlying their long-term growth and accumulation of somatic mutations. (236 words) Highlights- We built mathematical models to predict the genetic differences between branch tips by somatic mutations. - The model considers the varying dynamics of stem cells in shoot meristem during shoot elongation and branching. - We compared the model prediction with empirical data from tropical trees, Dipterocarpaceae, and estimated the dynamics of stem cells and mutation rate. - Somatic mutation dynamics were shaped by somatic genetic drift arising from stem cell lineage replacement during shoot elongation and branching. - Accounting for stem cell dynamics led to slightly smaller estimates of mutation rates compared with previous estimates that ignored the dynamics. - Our models offer insights into how genetic variability is shaped in the tropical trees and the stem cell dynamics underlying their long-term growth.

evolutionary biology↗

Genetic diversity within a tree and alternative indexes for different evolutionary effects

Trees, living for centuries, accumulate somatic mutations in their growing trunks and branches, causing genetic divergence within a single tree. Stem cell lineages in a shoot apical meristem accumulate mutations independently and diverge from each other. In plants, somatic mutations can alter the genetic composition of reproductive organs and gametes, impacting future generations. To evaluate the genetic variation among a trees reproductive organs, we consider three indexes: mean pairwise phylogenetic distance [Formula], phylogenetic diversity (PD; sum of branch lengths in molecular phylogeny), and parent-offspring phylogenetic distance (DPO). The tissue architecture of trees facilitated the accumulation of somatic mutations, which have various evolutionary effects, including enhancing fitness under strong sib competition and intense host-pathogen interactions, efficiently eliminating deleterious mutations through epistasis, and increasing genetic variance in the population. Choosing appropriate indexes for the genetic diversity of somatic mutations depends on the specific aspect of evolutionary influence being assessed.

genetics↗

Branching architecture affects genetic diversity within an individual tree

PremiseWhile a tree grows over many years, somatic mutations accumulate and generate a genetically diverse individual. Trees can transmit such mutations to subsequent generations, potentially enhancing the genetic diversity of the population. We study a mathematical model to understand the relationship between within-individual genetic variation and branching architecture. MethodsWe generate branching architecture by repeatedly adding two new branches (main and lateral daughter branches) to each terminal branch (mother branch). Tree shape is determined by two key parameters: daughter-mother ratio (DM) and main-lateral ratio (ML). During branch elongation, somatic mutations accumulate in the stem cells of a shoot apical meristem (SAM) at the tip of each branch. In branching, all the stem cells are passed on from the mother to the main daughter branch, but only one stem cell is chosen for the lateral daughter branch. We evaluate genetic variation by [Formula], the mean genetic differences between all pairs of branches of a tree, and examine how [Formula] varies with DM and ML while keeping the total branch length constant. Key results and Conclusions(1) [Formula] attains the maximum for an intermediate DM, when stem cells in the SAM are genetically homogeneous; (2) [Formula] decreases monotonically with DM when stem cells are genetically heterogeneous; and (3) [Formula] increases monotonically with ML. Even though the total branch length remains constant, the within-individual genetic variation differs substantially. The results demonstrate the importance of branching architecture in storing genetic diversity.

evolutionary biology↗

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

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 StatementThe 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.

evolutionary biology↗

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

Genomic sequencing revealed that somatic mutations cause a genetic differentiation of the cells in a single tree. In this study, we consider a mathematical model for stem cell proliferation in the shoot apical meristem (abbrev. SAM), which results in genetic diversification between the cells differing in the distance along the shoot and the angle around a shoot axis. The assumptions are as follows. Stem cells in the SAM normally undergo asymmetric cell division and produce successor stem cells and differentiated cells. The differentiated cells proliferate and contribute to shoot elongation. Occasionally, a stem cell is replaced by a copy of an adjacent stem cell. We discuss the "coalescent length" between cells indicating their genetic difference with respect to neutral mutations. 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 bottom of the shoot. Stem cells hold a larger variation if they are replaced only by the nearest neighbors than if they are replaced by any cells. 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.

evolutionary biology↗

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

In a long-lived organism with a modular architecture, such as trees, somatic mutations accumulate throughout the long lifespan and result in genetic mosaicism in each module within the same individual. In recent years, next-generation sequencing technology has provided a snapshot of such intra-organismal genetic variability. However, the dynamic processes underlying the accumulation and expansion of somatic mutations during the growth remain poorly understood. In this study, we constructed a model to describe these processes in a form that can be applied to a real tree. Given that the proliferation dynamics of meristematic cells vary across plant species, multiple possible processes for elongation and branching were comprehensively expressed in our model. Using published data from a poplar tree, we compared the prediction of the models with the observation and explained the cell lineage dynamics underlying somatic mutations accumulation that were not evident from the snapshot of the sequenced data. We showed that the somatic genetic drift during growth increases inter-meristem mosaicism, resulting in genetically distinct branches and less integrity within an individual tree. We also showed that the somatic genetic drift during branching leads to the mutation accumulation pattern that does not reflect the tree topology. Our modelling framework can help interpret and provide further insights into the empirical findings of genetic mosaicism in long-lived trees.

plant biology↗