Bone morphogenetic proteins (BMPs), members of the transforming growth factor-ß (TGF-ß) family, have been shown to contribute to embryogenesis and organogenesis during animal development. Relevant studies provide support for the following concepts: (a) BMP signals are evolutionarily highly conserved as a genetic toolkit; (b) spatiotemporal distributions of BMP signals are precisely controlled at the post-translational level; and (c) the BMP signaling network has been co-opted to adapt to diversified animal development. These concepts originated from the historical findings of the Spemann-Mangold orga-nizer and the subsequent studies about how this organizer functions at the molecular level. In this Commentary, we focus on two topics. First, we review how the BMP morphogen gradient is formed to sustain larval wing imaginal disc and early embryo growth and patterning in Drosophila. Second, we discuss how BMP signal is tightly controlled in a context-dependent manner, and how the signal and tissue dynamics are coupled to facilitate complex tissue structure formation. Finally, we argue how these concepts might be developed in the future for further understanding the significance of BMP signaling in animal development.

Stomatal pores and the leaf cuticle regulate evaporation from the plant body and balance the tradeoff between photosynthesis and water loss. MYB16, encoding a transcription factor involved in cutin biosynthesis, is expressed in stomatal lineage ground cells, suggesting a link between cutin biosynthesis and stomatal development. Here, we show that the downregulation of MYB16 in meristemoids is directly mediated by the stomatal master transcription factor SPEECHLESS (SPCH) in Arabidopsis thaliana. The suppression of MYB16 before an asymmetric division is crucial for stomatal patterning, as its overexpression or ectopic expression in meristemoids increased stomatal density and resulted in the formation of stomatal clusters, as well as affecting the outer cell wall structure. Expressing a cutinase gene in plants ectopically expressing MYB16 reduced stomatal clustering, suggesting that cutin affects stomatal signaling or the polarity setup in asymmetrically dividing cells. The clustered stomatal phenotype was rescued by overexpressing EPIDERMAL PATTERNING FACTOR2, suggesting that stomatal signaling was still functional in these plants. Growing seedlings ectopically expressing MYB16 on high-percentage agar plates to modulate tensile strength rescued the polarity and stomatal cluster defects of these seedlings. Therefore, the inhibition of MYB16 expression by SPCH in the early stomatal lineage is required to correctly place the polarity protein needed for stomatal patterning during leaf morphogenesis.

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Stomata and leaf cuticle regulate water evaporation from the plant body and balance the trade-off between photosynthesis and water loss. We identified MYB16, a key transcription factor controlling cutin biosynthesis, from previous stomatal lineage ground cell (SLGC)-enriched transcriptome study. The preferential localization of MYB16 in SLGCs but not meristemoids suggests a link between cutin synthesis and stomatal development. Here, we showed that downregulation of MYB16 in meristemoids was directly mediated by the stomatal master transcription factor, SPEECHLESS (SPCH). The suppression of MYB16 before asymmetric division was crucial for stomatal patterning because overexpression or ectopic expression of MYB16 in meristemoids increased impermeability and elevated stomatal density and clusters. The aberrant pattern of stomata was due to reduced and disrupted establishment of polarity during asymmetric cell division. Manipulating polarity by growing seedlings on hard agar rescued stomatal clusters and polarity defects in MYB16 ectopic lines. By expressing a cutinase in MYB16 ectopic lines, stomatal clustering was reduced, which suggests that the ectopic accumulation of cuticle affects the polarity in asymmetrically dividing cells and causes clustered stomata. Taken together, inhibiting MYB16 expression by SPCH in early stomatal lineage is required to correctly place the polarity complex for proper stomatal patterning during leaf morphogenesis.

Developmental patterning is thought to be regulated by conserved signalling pathways. Initial patterns are often broad before refining to only those cells that commit to a particular fate1,2. However, the mechanisms by which pattern refinement takes place remain to be addressed. Using the posterior crossvein (PCV) of the Drosophila pupal wing as a model, into which bone morphogenetic protein (BMP) ligand is extracellularly transported to instruct vein patterning3,4, we investigate how pattern refinement is regulated. We found that BMP signalling induces apical enrichment of Myosin II in developing crossvein cells to regulate apical constriction. Live imaging of cellular behaviour indicates that changes in cell shape are dynamic and transient, only being maintained in those cells that retain vein fate after refinement. Disrupting cell shape changes throughout the PCV inhibits pattern refinement. In contrast, disrupting cell shape in only a subset of vein cells can result in a loss of BMP signalling. We propose that cell shape changes of future PCV cells allow them to compete more efficiently for basally localised BMP signal by forming a mechano-chemical feedback loop. This study highlights a new form of cell competition: competing for a signal that induces cell fate rather than promotes cell survival.