Real-time lineage analysis reveals oriented cell divisions associated with morphogenesis at the shoot apex ofArabidopsis thaliana

Abstract

Precise knowledge of spatial and temporal patterns of cell division,including number and orientation of divisions, and knowledge of cell expansion, is central to understanding morphogenesis. Our current knowledge of cell division patterns during plant and animal morphogenesis is largely deduced from analysis of clonal shapes and sizes. But such an analysis can reveal only the number, not the orientation or exact rate, of cell divisions. In this study, we have analyzed growth in real time by monitoring individual cell divisions in the shoot apical meristems (SAMs) of Arabidopsis thaliana. The live imaging technique has led to the development of a spatial and temporal map of cell division patterns. We have integrated cell behavior over time to visualize growth. Our analysis reveals temporal variation in mitotic activity and the cell division is coordinated across clonally distinct layers of cells. Temporal variation in mitotic activity is not correlated to the estimated plastochron length and diurnal rhythms. Cell division rates vary across the SAM surface. Cells in the peripheral zone (PZ)divide at a faster rate than in the central zone (CZ). Cell division rates in the CZ are relatively heterogeneous when compared with PZ cells. We have analyzed the cell behavior associated with flower primordium development starting from a stage at which the future flower comprises four cells in the L1 epidermal layer. Primordium development is a sequential process linked to distinct cellular behavior. Oriented cell divisions, in primordial progenitors and in cells located proximal to them, are associated with initial primordial outgrowth. The oriented cell divisions are followed by a rapid burst of cell expansion and cell division, which transforms a flower primordium into a three-dimensional flower bud. Distinct lack of cell expansion is seen in a narrow band of cells, which forms the boundary region between developing flower bud and the SAM. We discuss these results in the context of SAM morphogenesis.

PaCeQuant: A Tool for High-Throughput Quantification of Pavement Cell Shape Characteristics

“…To study developmental shape transitions and molecular and genetic modes of shape establishment, imaging must be combined with the quantification of PC shape characteristics. A combination of advanced imaging, automatic quantification of shape features, and computational modeling has been used to study the development of embryos (De Rybel et al, 2014;Yoshida et al, 2014), of root meristems (Campilho et al, 2006), of shoots apical meristems (Reddy et al, 2004;Kierzkowski et al, 2012;Serrano-Mislata et al, 2015), and of flower organs . In these studies, the direction of cell division and cell expansion is tracked over time from semi-and fully automatic 3D segmentations of individual cells using the MorphoGraphX software Barbier de Reuille et al, 2015).…”

Germline replications and somatic mutation accumulation are independent of vegetative life span inArabidopsis

“…According to this model, exceedingly rare divisions of cells from the center of the CZ would produce a daughter that is pushed to the border between the CZ and the PZ where it could undergo more rapid divisions to generate the transit-amplifying cells in the PZ. Real-time analysis of divisions within the SAM has identified leaf-progenitor cells abutting the CZ, but the short time frame in which real time imaging is practical has inhibited the identification of leaf progenitors in the CZ and their turnover (41). An alternative approach to testing this model is pulse labeling the nuclei of meristematic stem cells followed by an extended time-course analysis of the retention and redistribution of the DNA label.…”

ORGAN BOUNDARY1 defines a gene expressed at the junction between the shoot apical meristem and lateral organs

“…After cell division, some cells at the center remain as stem cells, whereas others shift to the periphery and differentiate into primordia, groups of specialized cells that become lateral organs, such as leaves, branches, and flowers (2). As development progresses, a shoot organ primordium is distinguished from its meristem by the creation of a groove containing narrow files of nondividing cells that define the boundaries between the meristem and organs or between adjacent organs (3)(4)(5). Establishment of such boundaries is temporally coordinated with changes in morphology and gene expression patterns in the meristem (5,6).…”