Spatiotemporal patterns of gene expression are instrumental to morphogenesis. A stable pattern interface, often between reciprocal-inhibiting morphogens, must be robustly maintained after initial patterning cues diminish, organ growth, or organ geometry changes. In plants, floral and leaf primordia obtain the adaxial-abaxial pattern at the shoot apical meristem periphery. However, it is unknown how the pattern is maintained after primordia have left the shoot apex. Here, through a combination of computational simulations, time-lapse imaging, and genetic analysis, we propose a model in which auxin simultaneously promotes both adaxial and abaxial domains of expression. Furthermore, we identified multilevel feedback regulation of auxin signaling to refine the spatiotemporal patterns. Our results demonstrate that coactivation by auxin determines and stabilizes antagonistic adaxial-abaxial patterning during aerial organ formation.

How gene activities and biomechanics together direct organ shapes is poorly understood. Plant leaf and flo-ral organs develop from highly similar initial structures and share similar gene expression patterns, yet they gain drastically different shapes later-flat and bilateral leaf primordia and radially symmetric floral primordia, respectively. We analyzed cellular growth patterns and gene expression in young leaves and flowers of Ara-bidopsis thaliana and found significant differences in cell growth rates, which correlate with convergence sites of phytohormone auxin that require polar auxin transport. In leaf primordia, the PRESSED -FLOWER -ex-pressing middle domain grows faster than adjacent adaxial domain and coincides with auxin convergence. In contrast, in floral primordia, the LEAFY-expressing domain shows accelerated growth rates and pronounced auxin convergence. This distinct cell growth dynamics between leaf and flower requires changes in levels of cell-wall pectin de-methyl-esterification and mechanical properties of the cell wall. Data-driven computer model simulations at organ and cellular levels demonstrate that growth differences are central to obtaining distinct organ shape, corroborating in planta observations. Together, our study provides a mechanistic basis for the establishment of early aerial organ symmetries through local modulation of differential growth pat-terns with auxin and biomechanics.

Leaf shape is highly variable within and among plant species, ranging from slender to oval shaped. This is largely determined by the proximodistal axis of growth. However, little is known about how proximal-distal growth is controlled to determine leaf shape. Here, we show that Arabidopsis leaf and sepal proximodistal growth is tuned by two phytohormones. Two class A AUXIN RESPONSE FACTORs (ARFs), ARF6 and ARF8, activate the transcription of DWARF4, which encodes a key brassinosteroid (BR) biosynthetic enzyme. At the cellular level, the phytohormones promote more directional cell expansion along the proximodistal axis, as well as final cell sizes. BRs promote the demethyl-esterification of cell wall pectins, leading to isotropic in-plane cell wall loosening. Notably, numerical simulation showed that isotropic cell wall loosening could lead to directional cell and organ growth along the proximodistal axis. Taken together, we show that auxin acts through biosynthesis of BRs to determine cell wall mechanics and directional cell growth to generate leaves of variable roundness.

In plants and animals, self-renewing stem cell populations play fundamental roles in many developmental contexts. Plants differ from most animals in their retained ability to initiate new cycles of growth and development, which relies on the establishment and activity of branch meristems. In seed plants, branching is achieved by stem-cell-containing axillary meristems, which are initiated from a leaf axil meristematic cell population originally detached from the shoot apical meristem. It remains unclear how the meristematic cell fate is maintained. Here, we show that ARABIDOPSISTHALIANAHOMEOBOXGENE1 (ATH1) maintains the meristem marker gene SHOOT MERISTEMLESS (STM) expression in the leaf axil to enable meristematic cell fate maintenance. Furthermore, ATH1 protein interacts with STM protein to form a STM self-activation loop. Genetic and biochemical data suggest that ATH1 anchors STM to activate STM as well as other axillary meristem regulatory genes. This auto-regulation allows the STM locus to remain epigenetically active. Taken together, our findings provide a striking example of a self-activation loop that maintains the flexibility required for stem cell niche re-establishment during organogenesis.

Leaves, the primary plant organs that function in photosynthesis and respiration, have highly organized, flat structures that vary within and among species. In recent years, it has become evident that auxin plays central roles in leaf development, including leaf initiation, blade formation, and compound leaf patterning. In this review, we discuss how auxin maxima form to define leaf primordium formation. We summarize recent progress in understanding of how spatial auxin signaling promotes leaf blade formation. Finally, we discuss how spatial auxin transport and signaling regulate the patterning of compound leaves and leaf serration.

By using mechanical and optical sectioning of DII/mDII and R2D2 auxin sensors, we reconfirmed the presence of asymmetric auxin signaling in leaf primordia. We also showed that the imaging data reported by Bhatia et al. (2019) may suffer from artefacts, and that their analysis was artificially biased due to an arbitrary domain demarcation.

Stem cells must balance self-renewal and differentiation; thus, their activities are precisely controlled. In plants, the control circuits that underlie division and differentiation within meristems have been well studied, but those that underlie feedback on meristems from lateral organs remain largely unknown. Here we show that long-distance auxin transport mediates this feedback in a non-cell-autonomous manner. A low-auxin zone is associated with the shoot apical meristem (SAM) organization center, and auxin levels negatively affect SAM size. Using computational model simulations, we show that auxin transport from lateral organs can inhibit auxin transport from the SAM through an auxin transport switch and thus maintain SAM auxin homeostasis and SAM size. Genetic and microsurgical analyses confirmed the model's predictions. In addition, the model explains temporary change in SAM size of yabby mutants. Our study suggests that the canalization-based auxin flux can be widely adapted as a feedback control mechanism in plants.