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Nimchuk, Z. L.

Publications and source records attributed to Nimchuk, Z. L..

8 recordsLinked to original sources

CLAVATA3 peptide signaling from stem cells integrates vascular organization and stem cell maintenance in Arabidopsis shoots

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.

plant biology↗

Gene duplication dynamics and regulatory evolution shape the diversification of Asteraceae

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.

genomics↗

Floral innovation through modifications in stem cell peptide signaling.

Understanding how evolution shapes genetic networks to create new developmental forms is a central question in biology. Asteraceae (sunflower family) comprise 10% of flowering plants and have capitula, a novel flowering shoot (inflorescence) that mimics a single flower (1, 2). During capitulum development, shoot stem cells undergo prolonged proliferation relative to other species (3, 4). Here we show that capitulum evolution paralleled decreases in CLAVATA3 peptide (CLV3p) signaling, a conserved repressor of stem cell proliferation. Asteraceae CLV3p displays reduced receptor binding and downstream transcriptional outputs. Reversion of CLV3 to a more active form impairs Asteraceae stem cell regulation and capitulum development. Lastly, we trace CLV3 evolution across the Asterales allowing inferences on capitulum evolution. Our findings reveal novel evolutionary mechanisms in plant reproduction and suggest approaches for engineering crops.

plant biology↗

Canalization of flower production across thermal environments requires Florigen and CLAVATA signaling.

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 florigens 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.

plant biology↗

A network of CLAVATA receptors buffers auxin-dependent meristem maintenance

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.

plant biology↗

RGI-GOLVEN signalling promotes FLS2 abundance to regulate plant immunity

Endogenous plant signalling peptides regulate developmental and growth-related processes. Recent research indicates that some of these peptides are classified as phytocytokines as they have regulatory functions during plant immune responses. However, the mechanistic basis for phytocytokine-mediated immune modulation remains largely elusive. Here, we identify GOLVEN2 (GLV2) peptides as novel phytocytokines in Arabidopsis thaliana. By peptide application, precursor overexpression and loss-of-function studies we show that GLV2 enhances sensitivity of plants to elicitation with the bacterial flagellin epitope flg22. GLV2 is perceived by ROOT MERISTEM GROWTH FACTOR 1 INSENSITIVE (RGI) receptors and RGI3 forms an flg22-induced complex with the flg22-receptor FLAGELLIN SENSITIVE 2, suggesting that RGIs are part of activated pattern recognition receptor signalling platforms. GLV2 perception increases posttranscriptional FLS2 abundance and RGIs promote FLS2 protein accumulation. Thus, GLV-RGI signalling controls above ground plant immunity via a novel mechanism of phytocytokine activity.

plant biology↗

A conserved regulatory module regulates receptor kinase signaling in immunity and development

Ligand recognition by cell-surface receptors underlies development and immunity in both animals and plants. Modulating receptor signaling is critical for appropriate cellular responses but the mechanisms ensuring this are poorly understood. Here, we show that signaling by plant receptors for pathogen-associated molecular patterns (PAMPs) in immunity and CLAVATA3/EMBRYO SURROUNDING REGION-RELATED peptides (CLEp) in development employ a similar regulatory module. In the absence of ligand, signaling is dampened through association with specific type-2C protein phosphatases (PP2Cs). Upon activation, PAMP and CLEp receptors phosphorylate divergent cytosolic kinases, which, in turn, phosphorylate the phosphatases, thereby promoting their release from the receptor complexes. Our work reveals a regulatory circuit shared between immune and developmental receptor signaling, which may have broader important implications for plant receptor kinase-mediated signaling in general.

plant biology↗

CRISPR/Cas9-mediated resistance to cauliflower mosaic virus

Viral diseases are a leading cause of worldwide yield losses in crop production. Breeding of resistance genes (R gene) into elite crop cultivars has been the standard and most cost-effective practice. However, R gene-mediated resistance is limited by the available R genes within genetic resources and in many cases, by strain specificity. Therefore, it is important to generate new and broad-spectrum antiviral strategies. The CRISPR-Cas9 (clustered regularly interspaced palindromic repeat, CRISPR-associated) editing system has been employed to confer resistance to human viruses and several plant single-stranded DNA geminiviruses, pointing out the possible application of the CRISPR-Cas9 system for virus control. Here we demonstrate that strong viral resistance to cauliflower mosaic virus (CaMV), a pararetrovirus with a double-stranded DNA genome, can be achieved through Cas9-mediated multiplex targeting of the viral coat protein sequence. We further show that small interfering RNAs (siRNA) are produced and mostly map to the 3' end of guide RNAs (gRNA), although very low levels of siRNAs map to the spacer region as well. However, these siRNAs are not responsible for the inhibited CaMV infection because there is no resistance if Cas9 is not present. We have also observed edited viruses in systematically infected leaves in some transgenic plants, with short deletions or insertions consistent with Cas9-induced DNA breaks at the gRNA target sites in coat protein coding sequence. These edited coat proteins, in most cases, led to earlier translation stop and thus, non-functional coat proteins. We also recovered wild-type CP sequence in these infected transgenic plants, suggesting these edited viral genomes were packaged by wild-type coat proteins. Our data demonstrate that the CRISPR-Cas9 system can be used for virus control against plant pararetroviruses with further modifications.

plant biology↗