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 crops1–4. Asteraceae (sunflower family), comprising 10% of flowering plants, all have capitula, a novel inflorescence that mimics a single flower5,6. Asteraceae capitula are highly diverse but are thought to have evolved once via unknown mechanisms7,8. During capitulum development, shoot stem cells undergo prolonged proliferation to accommodate the formation of intersecting spirals of flowers (florets) along the disk-shaped head9,10. 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.
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Evolutionary conservation of receptor compensation for stem cell homeostasis in Solanaceae plants
Abstract Stem cell homeostasis is pivotal for continuous and programmed formation of organs in plants. The precise control of meristem proliferation is mediated by the evolutionarily conserved signaling that encompasses complex interactions among multiple peptide ligands and their receptor-like kinases. Here, we identified compensation mechanisms involving the CLAVATA1 (CLV1) receptor and its paralogs, BARELY ANY MERISTEMs (BAMs), for stem cell proliferation in two Solanaceae species, tomato and groundcherry. Genetic analyses of higher-order mutants deficient in multiple receptor genes, generated via CRISPR-Cas9 genome editing, reveal that tomato SlBAM1 and SlBAM2 compensate for slclv1 mutations. Unlike the compensatory responses between orthologous receptors observed in Arabidopsis, tomato slclv1 mutations do not trigger transcriptional upregulation of four SlBAM genes. The compensation mechanisms within receptors are also conserved in groundcherry, and critical amino acid residues of the receptors associated with the physical interaction with peptide ligands are highly conserved in Solanaceae plants. Our findings demonstrate that the evolutionary conservation of both compensation mechanisms and critical coding sequences between receptor-like kinases provides a strong buffering capacity during stem cell homeostasis in tomato and groundcherry.
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- Award ID(s):
- 2216612
- PAR ID:
- 10526916
- Publisher / Repository:
- bioRxiv
- Date Published:
- Journal Name:
- Horticulture Research
- Volume:
- 11
- Issue:
- 6
- ISSN:
- 2052-7276
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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