Agata Burian

Plants continuously generate new organs throughout their lifetime, a process that relies on a small population of stem cells located at the center of the shoot apical meristem (SAM). These cells self-renew and produce descendants that are displaced to the SAM periphery, where they contribute to organ formation and differentiation. Although the population is maintained over time, stochastic or biased turnover can lead to the dominance of specific lineages. Because de novo somatic mutations are inherited along cell lineages, these dynamics are expected to play a central role in shaping the accumulation and distribution of within-plant somatic genetic variation. In this Hypothesis, we discuss the mechanisms underlying stem cell behavior, and hypothesize that stem cell turnover reduces genetic diversity within the SAM over developmental timescales. We also develop a mathematical model linking stem cell turnover to somatic mutation accumulation and predict that this reduction arises because higher turnover limits the co-existence of independent stem cell lineages. Finally, we outline how lineage tracking and somatic DNA sequencing could be used to test these predictions in vivo.

Founder cells comprise the earliest state of commitment to form one organ or branch, and no other [1]. Comparative lineage analyses concur that cell fate is established later in flowering plants than in animals, and is determined by position rather than lineage, but both systems harbor large numbers of organ progenitors in lieu of a few stem cells [2]. An exciting new serial-editing strategy, applied here for the first time in plants, holds great promise for determining the cell lineage history of every structure in the plant body [3]. Unfortunately, the authors' conclusion that every shoot branch and lateral organ of the Arabidopsis plant derives from exactly three founder cells is unsupported by both the classical plant literature and more recent studies of plant cell lineage, calling for more cautious interpretation of the data and for better integration with complementary experimental strategies.

Age and longevity are key parameters for demography and life-history evolution of organisms. In clonal species, a widespread life history among animals, plants, macroalgae and fungi, the sexually produced offspring (genet) grows indeterminately by producing iterative modules, or ramets, and so obscure their age. Here we present a novel molecular clock based on the accumulation of fixed somatic genetic variation that segregates among ramets. Using a stochastic model, we demonstrate that the accumulation of fixed somatic genetic variation will approach linearity after a lag phase, and is determined by the mitotic mutation rate, without direct dependence on asexual generation time. The lag phase decreased with lower stem cell population size, number of founder cells for the formation of new modules, and the ratio of symmetric versus asymmetric cell divisions. We calibrated the somatic genetic clock on cultivated eelgrass Zostera marina genets (4 and 17 years respectively). In a global data set of 20 eelgrass populations, genet ages were up to 1,403 years. The somatic genetic clock is applicable to any multicellular clonal species where the number of founder cells is small, opening novel research avenues to study longevity and, hence, demography and population dynamics of clonal species.

Plant architecture is shaped by the production of new organs, most of which emerge postembryonically. This process includes the formation of new lateral branches along existing shoots. Current 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 cellular bottlenecks (i.e. somatic drift) that affect how de novo (epi)genetic mutations propagate through the plant body during development. Somatic drift could be particularly relevant for 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 precursor cells are randomly sampled from the SAM periphery in a way that maximizes cell lineage independence. We show that somatic drift during repeated branching gives rise to a mixture of cellular phylogenies within the SAM over time. This process is dependent on the number of branch points, the strength of drift as well as the epimutation rate. Our model predicts that cell-to-cell DNA methylation heterogeneity in the SAM converges to nonzero 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.

This article is a Commentary on Owens et al. (2024), 243: 423–439.

The formation of a flat and thin leaf presents a developmentally challenging problem, requiring intricate regulation of adaxial–abaxial (top–bottom) polarity. The patterning principles controlling the spatial arrangement of these domains during organ growth have remained unclear. Here we show that this regulation in Arabidopsis thaliana is achieved by an organ-autonomous Turing reaction‐diffusion system centred on mobile small RNAs. The data illustrate how Turing dynamics transiently instructed by prepatterned information is sufficient to self‐sustain properly oriented polarity in a dynamic, growing organ, presenting intriguing parallels to left–right patterning in the vertebrate embryo. Computational modelling demonstrates that this self-organizing system continuously adapts to coordinate the robust planar polarity of a flat leaf while affording flexibility to generate the tissue patterns of evolutionarily diverse organ shapes. Our findings identify a small-RNA-based Turing network as a dynamic regulator of organ polarity that accounts for leaf shape diversity at the level of the individual organ, plant or species.

Age and longevity are key parameters for demography and life-history evolution of organisms. In clonal species, a widespread life history among animals, plants, algae and fungi, the sexually produced offspring (the genet) grows indeterminately by producing iterative modules, or ramets. The age of large genets often remains elusive, while estimates based on their spatial extent as proxy for age are unreliable. Here, we present a method for age estimation using a molecular clock based on the accumulation of fixed somatic genetic variation (SoGV) that segregates among ramets of the same genet. Using a stochastic model of a generic clonal organism, we demonstrate that the accumulation of fixed SoGV via somatic genetic drift will approach linearity after a short lag phase, and is determined by the mitotic mutation rate, without direct dependence on asexual generation time. The lag phase decreased with lower stem cell population size ( N ), number of founder cells for the formation of new modules ( N ₀ ), and the ratio of symmetric vs. asymmetric stem cell divisions. We apply the somatic genetic clock to the clonal plant model Zostera marina (eelgrass) and show that linearity is approached within a few years. Taking advantage of two long-term cultivation experiments for Z. marina (4 and 17 years respectively) as calibration points, we find genet ages up to 1,403 years in a global data set of 20 eelgrass populations. The somatic genetic clock is applicable to any multicellular clonal species where a small number of founder cells are recruited to form new ramets, opening novel research avenues to study longevity and hence, demography and population dynamics of clonal species.

Plants are multicellular organisms of a unique structure because their tissues consist of two interwoven networks: a network of interconnected protoplasts that is embedded in a network of tightly joined cell walls