Branching architecture affects genetic diversity within an individual tree

Abstract

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, the mean genetic differences between all pairs of branches of a tree, and examine howvaries with DM and ML while keeping the total branch length constant.Key results and Conclusions(1)attains the maximum for an intermediate DM, when stem cells in the SAM are genetically homogeneous; (2)decreases monotonically with DM when stem cells are genetically heterogeneous; and (3)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.

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

“…If they are different, there is a distance between their common ancestor stem cell and fork[X, Y]. We call this portion as “before forking” segment (Tomimoto et al 2023) and denote the length of the path between two ancestral stem cells at fork[X, Y] by Bf ( X, Y ). The physical distance between the common ancestor cell and fork[X, Y] is half of Bf ( X, Y ) and was called “coalescent length” between the two ancestral cells at fork[X, Y] (Iwasa et al 2023)…”

“…1. This is referred to as “before-forking” portion (Tomimoto et al 2023). Its magnitude depends on the probability of failure in asymmetric cell division in stem cells (Iwasa et al 2023).…”

“…When a lateral branch is formed at a main branch, the stem cells of the axillary meristem of the lateral branch are sampled from the SAM of the main branch. In many trees, only a small fraction of stem cells in the main branch contribute to the axillary meristem (Tomimoto & Satake 2023; Tomimoto et al 2023). This results in an asymmetry between the two stem cell lineages sampled above the forking.…”

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

“…This is particularly important, given that the SAM, especially the ASC population, is the ultimate source for almost all above-ground plant organs. A number of mathematical models have been introduced to study the influence of different aspects on somatic mutation accumulation, such as the cellular organization and dynamics of the SAM (Burian et al, 2016; Iwasa et al, 2023; Klekowski and Kazarinova-Fukshansky, 1984a; Klekowski et al, 1985; Pineda-krch and Lehtilä, 2002), tree development (Klekowski et al, 1989; Tomimoto and Satake, 2023; Yu et al, 2023), intra-organismal selection on mutant stem cells and modules (Antolin and Strobeck, 1985; Folse and Roughgarden, 2012; Klekowski and Kazarinova-Fukshansky, 1984b; Otto and Orive, 1995; Pineda-Krch and Fagerström, 1999), and branching architecture (Tomimoto et al, 2023). Only recently has an analysis of cell lineages been considered in mathematical models studying the SAM (Iwasa et al, 2023).…”