Cell identity specification in plants: lessons from flower development

Abstract

Multicellular organisms display a fascinating complexity of cellular identities and patterns of diversification. The concept of ‘‘cell type’’ aims to describe and categorize this complexity. In this review, we discuss the traditional concept of cell types and highlight the impact of single-cell technologies and spatial omics on the understanding of cellular differentiation in plants. We summarize and compare position-based and lineage-based mechanisms of cell identity specification using flower development as a model system. More than understanding ontogenetic origins of differentiated cells, an important question in plant science is to understand their position- and developmental stage-specific heterogeneity. Combinatorial action and crosstalk of external and internal signals is the key to cellular heterogeneity, often converging on transcription factors that orchestrate gene expression programs.

Petal Cellular Identities

“…How these signals are integrated at the molecular level and result in a specific gene expression profile and cellular function is mostly unknown. Today, the petal should not be viewed as an organ with a single identity, but rather as a population of cells in a petal specification context, each with a slightly different combination of lineage and positional signals ( Xu et al, 2021 ). Single-cell technologies (transcriptome, proteome, interactome, chromatin accessibility, metabolome…) will surely lead to breakthroughs in the understanding of cell type specification in the petal and the molecular basis for its variation between species.…”

A 3D gene expression atlas of the floral meristem based on spatial reconstruction of single nucleus RNA sequencing data

“…The identity and function of plant cells is strongly influenced by their precise location within the plant body (Xu et al 2021). Therefore, to understand plant development at the molecular level, it is important not only to characterize the molecular status and dynamics of each individual cell but also to know their physical location in the plant.…”

“…However, the physical location of these cells is lost during the experimental process. In plants and other multicellular organisms, cell fate strongly depends on its precise position within the developing organism (Xu et al 2021). Therefore, it is essential to characterize gene expression patterns of each cell in their native physical context to fully understand the link between gene activity and organ development.…”

Cell types as species: Exploring a metaphor

“…Cell type classification systems prior to the availability of single cell transcriptomes were based largely on morphology, and identified a relatively small number of basic types. For plants, Xu et al (2021) cited textbooks that list fewer than 20 cell types, most or all of which are found in more than one tissue and organ (e.g., parenchyma), though often with distinctive morphologies in different regions. For example, Arabidopsis leaf epidermal cells have a jigsaw puzzle shape, in contrast to the smoother borders of sepal epidermal cells ( Xu et al, 2021 ).…”

“…Notably, at the dawn of the molecular biology revolution several cell biologists wrote detailed papers that drew explicitly on the philosophy and practice of systematics, applying principles from the species debate to identify and classify cell types based on the available morphological and physiological characters then available ( Tyner, 1975 ; Rowe and Stone, 1977 ; Rodieck and Brening, 1983 ). Their conclusions, particularly concerning the amazing diversity of neurons, are now being revisited in light of new data, and their successors are again looking to the long debate on defining species with either hope or despair in the search for a single unifying definition of “cell type” ( Clevers et al, 2017 ; Zeng and Sanes, 2017 ; Tasic, 2018 ; Northcutt et al, 2019 ; Xia and Yanai, 2019 ; Weinreb and Klein, 2020 ; Osumi-Sutherland et al, 2021 ; Xu et al, 2021 ). For example, the section of the paper by Zeng and Sanes (2017) on “Neuronal Cell Types as Species” begins:…”