Main conclusion SCARECROW controls Arabidopsis root meristem size from the root endodermis tissue by regulating the DELLA protein RGA that in turn mediates the regulation of ARR1 levels at the transition zone. Coherent organ growth requires a fine balance between cell division and cell differentiation. Intriguingly, plants continuously develop organs post-embryonically thanks to the activity of meristems that allow growth and environmental plasticity. In Arabidopsis thaliana, continued root growth is assured when division of the distal stem cell and their daughters is balanced with cell differentiation at the meristematic transition zone (TZ). We have previously shown that at the TZ, the cytokinin-dependent transcription factor ARR1 controls the rate of differentiation commitment of meristematic cells and that its activities are coordinated with those of the distal stem cells by the gene SCARECROW (SCR). In the stem cell organizer (the quiescent center, QC), SCR directly suppresses ARR1 both sustaining stem cell activities and titrating non-autonomously the ARR1 transcript levels at the TZ via auxin. Here, we show that SCR also exerts a fine control on ARR1 levels at the TZ from the endodermis by sustaining gibberellin signals. From the endodermis, SCR controls the RGA REPRESSOR OF ga1-3 (RGA) DELLA protein stability throughout the root meristem, thus controlling ARR1 transcriptional activation at the TZ. This guarantees robustness and fineness to the control of ARR1 levels necessary to balance cell division to cell differentiation in sustaining coherent root growth. Therefore, this work advances the state of the art in the field of root meristem development by integrating the activity of three hormones, auxin, gibberellin, and cytokinin, under the control of different tissue-specific activities of a single root key regulator, SCR.

Symmetry establishment is a critical process in the development of multicellular organs and requires careful coordination of polarity axes while cells actively divide within tissues. Formation of the apical style in the Arabidopsis gynoecium involves a bilateral-to-radial symmetry transition, a stepwise process underpinned by the dynamic distribution of the plant morphogen auxin. Here we show that SPATULA (SPT) and the HECATE (HEC) bHLH proteins mediate the final step in the style radialisation process and synergistically control the expression of adaxial-identity genes, HOMEOBOX ARABIDOPSIS THALIANA 3 (HAT3) and ARABIDOPSIS THALIANA HOMEOBOX 4 (ATHB4). HAT3/ATHB4 module drives radialisation of the apical style by promoting basal-to-apical auxin flow and via a negative feedback mechanism that finetune auxin distribution through repression of SPT expression and cytokinin sensitivity. Thus, this work reveals the molecular basis of axes-coordination and hormonal cross-talk during the sequential steps of symmetry transition in the Arabidopsis style.

The flower is an astonishing innovation that arose during plant evolution allowing flowering plants — also known as angiosperms — to dominate life on earth in a relatively short period of geological time. Flowers are formed from secondary meristems by co-ordinated differentiation of flower organs, such as sepals, petals, stamens, and carpels. The position, number and morphology of these flower organs impose a geometrical pattern — or symmetry type — within the flower which is a trait tightly connected to successful reproduction. During evolution, flower symmetry switched from the ancestral poly-symmetric (radial symmetry) to the mono-symmetric (bilateral symmetry) type multiple times, including numerous reversals, with these events linked to co-evolution with pollinators and reproductive strategies. In this review, we introduce the diversity of flower symmetry, trace its evolution in angiosperms, and highlight the conserved genetic basis underpinning symmetry control in flowers. Finally, we discuss the importance of building upon the concept of flower symmetry by looking at the mechanisms orchestrating symmetry within individual flower organs and summarise the current scenario on symmetry patterning of the female reproductive organ, the gynoecium, the ultimate flower structure presiding over fertilisation and seed production.

O-linked β-N-acetylglucosamine (O-GlcNAc) and O-fucose are two sugar-based post-translational modifications whose mechanistic role in plant signalling and transcriptional regulation is still largely unknown. Here we investigated how two O-glycosyltransferase enzymes of Arabidopsis thaliana, SPINDLY (SPY) and SECRET AGENT (SEC), promote the activity of the basic helix–loop–helix transcription factor SPATULA (SPT) during morphogenesis of the plant female reproductive organ apex, the style. SPY and SEC modify amino-terminal residues of SPT in vivo and in vitro by attaching O-fucose and O-GlcNAc, respectively. This post-translational regulation does not impact SPT homo- and heterodimerization events, although it enhances the affinity of SPT for the kinase PINOID gene locus and its transcriptional repression. Our findings offer a mechanistic example of the effect of O-GlcNAc and O-fucose on the activity of a plant transcription factor and reveal previously unrecognized roles for SEC and SPY in orchestrating style elongation and shape.

SUMMARY: The bilateral‐to‐radial symmetry transition occurring during the development of the Arabidopsis thaliana female reproductive organ (gynoecium) is a crucial biological process linked to plant fertilization and seed production. Despite its significance, the cellular mechanisms governing the establishment and breaking of radial symmetry at the gynoecium apex (style) remain unknown. To fill this gap, we employed quantitative confocal imaging coupled with MorphoGraphX analysis, in vivo and in vitro transcriptional experiments, and genetic analysis encompassing mutants in two bHLH transcription factors necessary and sufficient to promote transition to radial symmetry, SPATULA (SPT) and INDEHISCENT (IND). Here, we show that defects in style morphogenesis correlate with defects in cell‐division orientation and rate. We showed that the SPT‐mediated accumulation of auxin in the medial‐apical cells undergoing symmetry transition is required to maintain cell‐division‐oriented perpendicular to the direction of organ growth (anticlinal, transversal cell division). In addition, SPT and IND promote the expression of specific core cell‐cycle regulators, CYCLIN‐D1;1 (CYC‐D1;1) and CYC‐D3;3, to support progression through the G1 phase of the cell cycle. This transcriptional regulation is repressed by auxin, thus forming an incoherent feed‐forward loop mechanism. We propose that this mechanism fine‐tunes cell division rate and orientation with the morphogenic signal provided by auxin, during patterning of radial symmetry at the style.

Flowers are plant structures characteristic of the phylum Angiosperms composed of organs thought to have emerged from homologous structures to leaves in order to specialize in a distinctive function: reproduction. Symmetric shapes, colours, and scents all play important functional roles in flower biology. The evolution of flower symmetry and the morphology of individual flower parts (sepals, petals, stamens, and carpels) has significantly contributed to the diversity of reproductive strategies across flowering plant species. This diversity facilitates attractiveness for pollination, protection of gametes, efficient fertilization, and seed production. Symmetry, the establishment of body axes, and fate determination are tightly linked. The complex genetic networks underlying the establishment of organ, tissue, and cellular identity, as well as the growth regulators acting across the body axes, are steadily being elucidated in the field. In this review, we summarise the wealth of research already at our fingertips to begin weaving together how separate processes involved in specifying organ identity within the flower may interact, providing a functional perspective on how identity determination and axial regulation may be coordinated to inform symmetrical floral organ structures.