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Abstract Understanding how evolution shapes genetic networks to create new developmental forms is a central question in biology. Flowering shoot (inflorescence) architecture varies significantly across plant families and is a key target of genetic engineering efforts in many crops^1–4. Asteraceae (sunflower family), comprising 10% of flowering plants, all have capitula, a novel inflorescence that mimics a single flower^5,6. Asteraceae capitula are highly diverse but are thought to have evolved once via unknown mechanisms^7,8. During capitulum development, shoot stem cells undergo prolonged proliferation to accommodate the formation of intersecting spirals of flowers (florets) along the disk-shaped head^9,10. Here we show that capitulum evolution paralleled decreases in CLAVATA3 (CLV3) peptide signaling, a conserved repressor of stem cell proliferation. We trace this to novel amino acid changes in the mature CLV3 peptide which decrease receptor binding and downstream transcriptional outputs. Using genetically tractable Asteraceae models, we show that reversion ofCLV3to a more active form impairs Asteraceae stem cell regulation and capitulum development. Additionally, we trace the evolution ofCLV3and its receptors across the Asterales allowing inferences on capitulum evolution within this lineage. Our findings reveal novel mechanisms driving evolutionary innovation in plant reproduction and suggest new approaches for genetic engineering in crop species. 

Abstract Fusion of petals to form a corolla tube is considered a key innovation contributing to the diversification of many flowering plant lineages. Corolla tube length often varies dramatically among species and is a major determinant of pollinator preference. However, our understanding of the developmental dynamics underlying corolla tube length variation is very limited. Here we examined corolla tube growth in theMimulus lewisiispecies complex, an emerging model system for studying the developmental genetics and evo‐devo of pollinator‐associated floral traits. We compared developmental and cellular processes associated with corolla tube length variation among the bee‐pollinatedM. lewisii, the hummingbird‐pollinatedMimulus verbenaceus, and the self‐pollinatedMimulus parishii. We found that in all three species, cell size is non‐uniformly distributed along the mature tube, with the longest cells just distal to the stamen insertion site. Differences in corolla tube length among the three species are not associated with processes of organogenesis or early development but are associated with variation in multiple processes occurring later in development, including the location and duration of cell division and cell elongation. The tube growth curves of the small‐floweredM. parishiiand large‐floweredM. lewisiiare essentially indistinguishable, except thatM. parishiitubes stop growing earlier at a smaller size, suggesting a critical role of heterochrony in the shift from outcrossing to selfing. These results not only highlight the developmental process associated with corolla tube variation among species but also provide a baseline reference for future developmental genetic analyses of mutants or transgenic plants with altered corolla tube morphology in this emerging model system. 

Summary Style length is a major determinant of breeding strategies in flowering plants and can vary dramatically between and within species. However, little is known about the genetic and developmental control of style elongation.We characterized the role of two classes of leaf adaxial–abaxial polarity factors, SUPPRESSOR OF GENE SILENCING3 (SGS3) and the YABBY family transcription factors, in the regulation of style elongation inMimulus lewisii. We also examined the spatiotemporal patterns of auxin response during style development.Loss ofSGS3function led to reduced style length via limiting cell division, and downregulation ofYABBYgenes by RNA interference resulted in shorter styles by decreasing both cell division and cell elongation. We discovered an auxin response minimum between the stigma and ovary during the early stages of pistil development that marks style differentiation. Subsequent redistribution of auxin response to this region was correlated with style elongation. Auxin response was substantially altered when bothSGS3andYABBYfunctions were disrupted.We suggest that auxin signaling plays a central role in style elongation and that the way in which auxin signaling controls the different cell division and elongation patterns underpinning natural style length variation is a major question for future research.