The lifespan of plants ranges from a few weeks in annuals to thousands of years in trees. It is hard to explain such extreme longevity considering that DNA replication errors inevitably cause mutations. Without purging through meiotic recombination, the accumulation of somatic mutations will eventually result in mutational meltdown, a phenomenon known as Muller’s ratchet. Nevertheless, the lifespan of trees is limited more often by incidental disease or structural damage than by genetic aging. The key determinants of tree architecture are the axillary meristems, which form in the axils of leaves and grow out to form branches. The number of branches is low in annual plants, but in perennial plants iterative branching can result in thousands of terminal branches. Here, we use stem cell ablation and quantitative cell-lineage analysis to show that axillary meristems are set aside early, analogous to the metazoan germline. While neighboring cells divide vigorously, axillary meristem precursors maintain a quiescent state, with only 7–9 cell divisions occurring between the apical and axillary meristem. During iterative branching, the number of branches increases exponentially, while the number of cell divisions increases linearly. Moreover, computational modeling shows that stem cell arrangement and positioning of axillary meristems distribute somatic mutations around the main shoot, preventing their fixation and maximizing genetic heterogeneity. These features slow down Muller’s ratchet and thereby extend lifespan.

Introduction

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Schultz S.T. Mitosis, stature and evolution of plant mating systems: low-Phi and high-Phi plants. Figure 1 Three Models of Axillary Meristem Formation Show full caption Model 1: late specification of axillary meristems. Left: the cells in the boundary region acquire leaf or internode fate and divide continuously. Middle: a subset of these cells is re-specified shortly before forming the axillary meristem. Right: cell-lineage graph: the number of cell divisions between the cells at the shoot apical meristem and axillary meristem (arrowhead) increases with internode length/leaf size. Model 2: early specification of axillary meristems; position dependence. Left: the specified cell (magenta) attains its identity as progenitor of the axillary meristem. Middle: this cell resumes division based on its position at the base of either the leaf primordium or the internode until the formation of the axillary meristem. Right: cell-lineage graph: the number of cell divisions between the cells at the shoot apical meristem and axillary meristem increases with internode length/leaf size. Model 3: early specification of axillary meristems; lineage dependence. Left: the specified cell (magenta) attains its identity as progenitor of the axillary meristem. Middle: the specified cell (magenta) does not divide until it forms the axillary meristem, whereas the surrounding cells divide continuously to form the leaf and the internode. Right: the number of cell divisions between the cells at the shoot apical meristem and axillary meristem is independent of internode length/leaf size. Asterisk indicates center of the shoot apical meristem; arrowhead indicates axillary meristem. The number of cell divisions between apical and axillary meristems is not known. Clonal analyses have shown that somatic sectors can extend through multiple nodes and encompass leaves, axillary meristems, and internodes []. This proves that a single cell can contribute to multiple organs, but it is hard to extrapolate back from the sector to its founder cell. We consider three possible models ( Figure 1 ). In model 1, axillary meristems derive from differentiated shoot cells, either of the internode or the leaf (late specification of axillary meristem) []. These differentiated cells undergo multiple cell divisions during elongation of the internode or outgrowth of the leaf. In this model, the number of cell divisions between the apical meristem and the terminal organs correlates with plant stature and will become very high in big-statured plants, as favored by population geneticists [].

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Theres K. Molecular analysis of the LATERAL SUPPRESSOR gene in Arabidopsis reveals a conserved control mechanism for axillary meristem formation. 27 Keller T.

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Barton M.K. Initiation of axillary and floral meristems in Arabidopsis. Models 2 and 3 take into account that cell division ceases during the formation of the boundary between the leaf primordium and the apical meristem (the position of the future leaf axil) [] and that gene expression studies indicate the separate identity of the boundary []. Note, however, that the formation of an axillary meristem is delayed relative to the formation of the subtending leaf. In Arabidopsis, this delay can be as much as 11 plastochrons, that is, the first anatomical indication of axillary meristem formation occurs in the axil of a leaf that has already ten younger leaves above it on the stem []. The patterns of cell division during those ten plastochrons are not known. In model 2, we assume that cells in the leaf axil engage in cell division until a few of them develop into an axillary meristem, and that axillary meristem specification is position dependent. If this is correct, the number of cell divisions between the apical meristem and the terminal organs correlates with plant stature, as in model 1. Model 3 assumes that cells in the leaf axil retain their quiescent state until axillary meristems are formed, and that axillary meristem specification is lineage dependent. In this model, the number of cell divisions between apical and axillary meristems will be low and not related to plant stature. Therefore, key questions to be answered are whether axillary meristems are specified at the same time as the subtending leaf, and whether progenitor cells of axillary meristems maintain a quiescent state.

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Kazarinova-Fukshansky N. Shoot apical meristems and mutation - fixation of selectively neutral genotypes. Unless a mutation arises in the zygote, the resulting individual will consist of sectors with different genotypes. Indeed, chimerism appears to be common in plants [] and especially long-lived trees should be considered not as single organisms but as colonies of competing branches []. For the case of selectively neutral mutations, the extent of mutant sectors depends on the number and pattern of cell divisions. The largest sectors derive from mutations occurring in stem cells. How does a mutation that arises in a stem cell of the shoot apical meristem propagate through the plant and what is the chance of fixation? The width of the widest clonal sectors suggests that one to three stem cells contribute to the circumference of the stem. Their length suggests that stem cells are not permanent, with interpretations ranging from essentially non-permanent (“temporary inhabitants of a permanent office” []) to surprisingly stable []. Existing mathematical models, which are based on the assumption that stem cells in the shoot apical meristem are non-permanent, conclude that the chance of fixation of somatic mutations is high [].