Zachary L. Nimchuk

Summary: Terrestrial plant biomass relies on the formation of vascular bundles (VBs) comprising xylem, cambial, and phloem cells that drive secondary growth and wood formation. How VB formation and organization is coordinated with stem growth remains unclear. Here, we show that the conserved CLAVATA3 peptide (CLV3p)-receptor stem cell signaling pathway represses vascular transcriptional programs in the shoot apical meristem (SAM), thereby preventing ectopic vascular differentiation in the stem center, and quantitatively regulates peripheral VB number. Mutational analysis of conserved CLV3p residues partially uncouples its roles in vascular differentiation from stem cell maintenance. However, overexpression and mutational analysis with key phloem regulators reveals that CLV3p controls vascular and stem cell programs via a DOF ( DNA-BINDING WITH ONE FINGER ) and SMXL ( SUPPRESSOR OF MAX2 1-LIKE ) transcriptional module. Our findings identify a novel role for CLV3p signaling in shoot vascular development and establish a regulatory framework integrating stem cell signaling with vascular patterning.

A plant's indeterminate growth requires constant cell proliferation and stem cell maintenance to support its developmental plasticity. The root meristem is an excellent system to study the developmental control of plant cell cycles due to the organ's accessibility and the tight link between cell cycle and developmental regulation. Studies have uncovered diverse pathways that shape root tissue patterning and cell identity, but how these mechanistically connect to cell cycle components remains unclear. Recent work and new approaches are starting to bridge this gap. In this review, we synthesize recent findings on the developmental regulation of cell cycle progression across distinct cell types and developmental zones in the Arabidopsis thaliana root apical meristem, highlighting cells and regions of the root where these processes have been thoroughly studied, and others where we know little. These discoveries reveal a nuanced relationship between cell identity and cell cycle regulation that implies an active role for cell cycle modulation in the patterning and developmental plasticity that are integral to plant growth.

The flowering plant order Asterales exhibits a striking disparity in species richness, with >30,000 species in Asteraceae compared to <50 in its sister family Calyceraceae. To investigate the genomic basis of this imbalance, we assembled three new chromosome-level genomes, including the first for Calyceraceae, and re-annotated five additional genomes. Comparative analyses revealed exceptionally high repeat content in both Asteraceae and Calyceraceae, pervasive chromosomal rearrangements, and evidence for shared and lineage-specific WGDs. In Asteraceae, tandem and dispersed duplications disproportionately drove expansions of gene families linked to secondary metabolism and stress response, while segmental duplicates bore signatures of adaptive selection for the regulation of biosynthetic and metabolic processes. Selective pressures on flowering time regulators suggest an evolved balance between regulatory flexibility and developmental constraint in floral diversification. These patterns reveal that, beyond ancient polyploidy, small-scale duplications and selective fine-tuning of regulatory networks underpinned the ecological versatility in Asteraceae, fueling its extraordinary diversification.

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 of CLV3 to a more active form impairs Asteraceae stem cell regulation and capitulum development. Additionally, we trace the evolution of CLV3 and 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.

Summary: The ability to maintain invariant developmental phenotypes across disparate environments is termed canalization, but few examples of canalization mechanisms are described. In plants, robust flower production across environmental gradients contributes to reproductive success and agricultural yields. Flowers are produced by the shoot apical meristem (SAM) in an auxin-dependent manner following the switch from vegetative growth to the reproductive phase. While the timing of this phase change, called the floral transition, is sensitized to numerous environmental and endogenous signals, flower formation itself is remarkably invariant across environmental conditions. Previously we found that CLAVATA peptide signaling promotes auxin-dependent flower primordia formation in cool environments, but that high temperatures can restore primordia formation through unknown mechanisms. Here, we show that heat promotes floral primordia patterning and formation in SAMs not by increased auxin production, but through the production of the mobile flowering signal, florigen, in leaves. Florigen, which includes FLOWERING LOCUS T ( FT ) and its paralog TWIN SISTER OF FT ( TSF ) in Arabidopsis thaliana , is necessary and sufficient to buffer flower production against the loss of CLAVATA signaling and promotes heat-mediated primordia formation through specific SAM expressed transcriptional regulators. We find that sustained florigen production is necessary for continuous flower primordia production at warmer temperatures, contrasting florigen’s switch-like control of floral transition. Lastly, we show that CLAVATA signaling and florigen synergize to canalize flower production across broad temperature ranges. This work sheds light on the mechanisms governing the canalization of plant development and provides potential targets for engineering crop plants with improved thermal tolerances.

Robust agricultural yields require consistent flower production throughout fluctuating environmental conditions. Floral primordia are produced in the inflorescence meristem, which contains a pool of continuously dividing stem cells. Daughter cells of these divisions either retain stem cell identity or are pushed to the SAM periphery, where they become competent to develop into floral primordia after receiving the appropriate signal. Thus, flower production is inherently linked to regulation of the stem cell pool. The plant hormone auxin promotes flower development throughout its early phases and has been shown to interact with the molecular pathways regulating stem cell maintenance. Here, we will summarize how auxin signaling contributes to stem cell maintenance and promotes flower development through the early phases of initiation, outgrowth, and floral fate establishment. Recent advances in this area suggest that auxin may serve as a signal that integrates stem cell maintenance and new flower production.

Plant body plans are elaborated in response to both environmental and endogenous cues. How these inputs intersect to promote growth and development remains poorly understood. During reproductive development, central zone stem cell proliferation in inflorescence meristems is negatively regulated by the CLAVATA3 (CLV3) peptide signalling pathway. In contrast, floral primordia formation on meristem flanks requires the hormone auxin. Here we show that CLV3 signalling is also necessary for auxin-dependent floral primordia generation and that this function is partially masked by both inflorescence fasciation and heat-induced auxin biosynthesis. Stem cell regulation by CLAVATA signalling is separable from primordia formation but is also sensitized to temperature and auxin levels. In addition, we uncover a novel role for the CLV3 receptor CLAVATA1 in auxin-dependent meristem maintenance in cooler environments. As such, CLV3 signalling buffers multiple auxin-dependent shoot processes across divergent thermal environments, with opposing effects on cell proliferation in different meristem regions.

Plant body plans are elaborated in response to both environmental and endogenous cues. How these inputs intersect to promote growth and development remains poorly understood. During reproductive development, central zone stem cell proliferation in inflorescence meristems is negatively regulated by the CLAVATA3 (CLV3) peptide signaling pathway. In contrast, floral primordia formation on meristem flanks requires the hormone auxin. Here we show that CLV3 signaling is also necessary for auxin-dependent floral primordia generation and that this function is partially masked by both inflorescence fasciation and heat-induced auxin biosynthesis. Stem cell regulation by CLAVATA signaling is separable from primordia formation but is also sensitized to temperature and auxin levels. Additionally, we uncover a novel role for the CLV3 receptor CLAVATA1 in auxin- dependent meristem maintenance in cooler environments. As such, CLV3 signaling buffers multiple auxin-dependent shoot processes across divergent thermal environments with opposing effects on cell proliferation in different meristem regions.