Abstract
SummaryBackgroundIn all multicellular organisms, the links between patterning genes, cell growth, cell cycle, cell size homeostasis, and organ growth are poorly understood, partly due to the difficulty of dynamic, 3D analysis of cell behavior in growing organs. A crucial step in plant organogenesis is the emergence of organ primordia from the apical meristems. Here, we combined quantitative, 3D analysis of cell geometry and DNA synthesis to study the role of the transcription factor JAGGED (JAG), which functions at the interface between patterning and primordium growth in Arabidopsis flowers.ResultsThe floral meristem showed isotropic growth and tight coordination between cell volume and DNA synthesis. Sepal primordia had accelerated cell division, cell enlargement, anisotropic growth, and decoupling of DNA synthesis from cell volume, with a concomitant increase in cell size heterogeneity. All these changes in growth parameters required JAG and were genetically separable from primordium emergence. Ectopic JAG activity in the meristem promoted entry into S phase at inappropriately small cell volumes, suggesting that JAG can override a cell size checkpoint that operates in the meristem. Consistent with a role in the transition from meristem to primordium identity, JAG directly repressed the meristem regulatory genes BREVIPEDICELLUS and BELL 1 in developing flowers.ConclusionsWe define the cellular basis for the transition from meristem to organ identity and identify JAG as a key regulator of this transition. JAG promotes anisotropic growth and is required for changes in cell size homeostasis associated with accelerated growth and the onset of differentiation in organ primordia.
Highlights
A fundamental question in biology is how the activity of regulatory genes acting within cells is translated into the shape and size of macroscopic organs
Our analysis shows that cells in the meristem and early floral organ primordia have different growth regimes, and that JAG is a key regulator of the transition between these growth regimes
We focused our analysis on the growth of sepal primordia, which are the first to emerge from the floral meristem and are readily accessible for imaging
Summary
A fundamental question in biology is how the activity of regulatory genes acting within cells is translated into the shape and size of macroscopic organs. Growth is based only on increased cell number and cell size, in contrast to animals, in which cell migration and cell death play important roles. In spite of this simplifying feature, understanding the link between regulatory genes and the growth and shape of plant organs is still a considerable challenge. Shoot organs are initiated at the periphery of apical meristems, which continuously produce new cells to replenish those recruited into organ primordia [4] These primordia develop into leaves during vegetative growth and into floral buds during the reproductive phase of development. Local auxin maxima induce primordium initiation, associated with repression of regulatory genes that maintain meristem activity, such as the homeodomain proteins SHOOT MERISTEMLESS (STM) [6] and BREVIPEDICELLUS (BP) [7, 8]
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