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 (abbrev. SAM). We evaluated phylogenetic distance between cells sampled from different portion 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 rates and patterns of somatic mutations in wild plants, as well as how they relate to longevity, are largely unknown. Here, we examined the somatic mutation landscapes of slow- and fast-growing tropical species in central Borneo, Indonesia. Using newly-constructed genomes, we identified an average of 480 mutations in the slow-growing species (265-year-old, 44.1 m in height), which was five times greater than that observed in the fast-growing species (66-year-old, 43.9 m). The number of somatic mutations increased linearly with branch length. The somatic mutation rate per meter was higher in the slow-growing species, yet the rate per year remained constant across both species. The mutational spectra exhibited a dominance of spontaneous mutations, specifically cytosine-to-thymine substitutions at CpG sites. An analysis of nucleotide substitutions at both the intra- and inter-individual level revealed that somatic mutations are neutral within an individual, but those mutations transmitted to the next generation are subject to purifying selection. We developed a model to evaluate the relative contribution of cell division on mutational processes, and postulate that cell-division independent mutagenesis predominates. These findings deepen our understanding of mutational processes underlying the generation of genetic diversity in a tropical ecosystem.
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 sequenced 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 decreased the intra-meristem mosaicism, resulting in mutation distribution strictly reflecting tree topology. Our modelling framework can help interpret and replenish the new empirical findings of genetic mosaicism in long-lived trees.
The rates and patterns of somatic mutations in wild plants, as well as how they relate to longevity, are largely unknown 1–3 . Here, we examined the somatic mutation landscapes of slow- and fast-growing tropical species in central Borneo, Indonesia. Using newly-constructed genomes, we identified an average of 480 mutations in the slow-growing species (265-year-old, 44.1 m in height), which was five times greater than that observed in the fast-growing species (66-year-old, 43.9 m). The number of somatic mutations increased linearly with branch length. The somatic mutation rate per meter was higher in the slow-growing species, yet the rate per year remained constant across both species. The mutational spectra exhibited a dominance of spontaneous mutations, specifically cytosine-to-thymine substitutions at CpG sites. An analysis of nucleotide substitutions at both the intra- and inter-individual level revealed that somatic mutations are neutral within an individual, but those mutations transmitted to the next generation are subject to purifying selection. We developed a model to evaluate the relative contribution of cell division on mutational processes, and postulate that cell-division independent mutagenesis predominates. These findings deepen our understanding of mutational processes underlying the generation of genetic diversity in a tropical ecosystem.
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