The CLAVATA receptor FASCIATED EAR2 responds to distinct CLE peptides by signaling through two downstream effectors

Meristems contain groups of indeterminate stem cells, which are maintained by a feedback loop between CLAVATA (CLV) and WUSCHEL (WUS) signaling. CLV signaling involves the secretion of the CLV3 peptide and its perception by a number of Leucine-Rich-Repeat (LRR) receptors, including the receptor-like kinase CLV1 and the receptor-like protein CLV2 coupled with the CORYNE (CRN) pseudokinase. CLV2, and its maize ortholog FASCIATED EAR2 (FEA2) appear to function in signaling by CLV3 and several related CLV3/EMBRYO-SURROUNDING REGION (CLE) peptide ligands. Nevertheless, how signaling specificity is achieved remains unknown. Here we show that FEA2 transmits signaling from two distinct CLE peptides, the maize CLV3 ortholog ZmCLE7 and ZmFON2-LIKE CLE PROTEIN1 (ZmFCP1) through two different candidate downstream effectors, the alpha subunit of the maize heterotrimeric G protein COMPACT PLANT2 (CT2), and ZmCRN. Our data provide a novel framework to understand how diverse signaling peptides can activate different downstream pathways through common receptor proteins.

• Publication year

  2018

• Venue

  eLife

• Publication date

  2018-03-15

• Fields of study

  Biology, Medicine

• Identifiers
  DOI 10.7554/eLife.35673PMID 29543153PMCID 5854466
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• Perception of root‐active CLE peptides requires CORYNE function in the phloem vasculature

  2017influential reference
• CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop

  2017cited by this paper
• Arabinosylation Modulates the Growth-Regulating Activity of the Peptide Hormone CLE40a from Soybean.

  2017cited by this paper
• Improved maize reference genome with single-molecule technologies

  2017cited by this paper
• CLAVATA-WUSCHEL signaling in the shoot meristem

  2016cited by this paper
• Ready, aim, shoot: stem cell regulation of the shoot apical meristem.

  2016cited by this paper
• Co-expression of hepatitis C virus polytope–HBsAg and p19-silencing suppressor protein in tobacco leaves

  2016cited by this paper
• The Multifunction of CLAVATA2 in Plant Development and Immunity

  2016cited by this paper
• Arabidopsis CLAVATA1 and CLAVATA2 receptors contribute to Ralstonia solanacearum pathogenicity through a miR169-dependent pathway.

  2016cited by this paper
• Signaling from maize organ primordia via FASCIATED EAR3 regulates stem cell proliferation and yield traits

  2016influential reference
• PartitionFinder 2: New Methods for Selecting Partitioned Models of Evolution for Molecular and Morphological Phylogenetic Analyses.

  2016cited by this paper
• Regulation of pattern recognition receptor signalling in plants

  2016cited by this paper
• Axillary Meristem Formation in Rice Requires the WUSCHEL Ortholog TILLERS ABSENT1[OPEN]

  2015influential reference
• Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases

  2015influential reference
• Genetic architecture of maize kernel row number and whole genome prediction

  2015influential reference
• A cascade of arabinosyltransferases controls shoot meristem size in tomato

  2015influential reference
• Reevaluation of the CLV3-receptor interaction in the shoot apical meristem: dissection of the CLV3 signaling pathway from a direct ligand-binding point of view.

  2015influential reference
• MONOCULM 3, an ortholog of WUSCHEL in rice, is required for tiller bud formation.

  2015influential reference
• The Pfam protein families database: towards a more sustainable future

  2015cited by this paper
• Real-time dynamics of peptide ligand–dependent receptor complex formation in planta

  2015cited by this paper
• A novel single-nucleotide mutation in a CLAVATA3 gene homolog controls a multilocular silique trait in Brassica rapa L.

  2014cited by this paper
• RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies

  2014cited by this paper
• Significant reduction of BiFC non-specific assembly facilitates in planta assessment of heterotrimeric G-protein interactors

  2014cited by this paper
• A mechanistic framework for noncell autonomous stem cell induction in Arabidopsis

  2014cited by this paper
• WUSCHEL-RELATED HOMEOBOX4 Is Involved in Meristem Maintenance and Is Negatively Regulated by the CLE Gene FCP1 in Rice[W]

  2013cited by this paper
• Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex

  2013cited by this paper
• Quantitative variation in maize kernel row number is controlled by the FASCIATED EAR2 locus

  2013influential reference
• Fluorescent protein marker lines in maize: generation and applications.

  2013cited by this paper
• MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability

  2013cited by this paper
• The Amborella Genome and the Evolution of Flowering Plants

  2013cited by this paper
• Structural Basis for flg22-Induced Activation of the Arabidopsis FLS2-BAK1 Immune Complex

  2013cited by this paper
• The maize Gα gene COMPACT PLANT2 functions in CLAVATA signalling to control shoot meristem size

  2013influential reference
• Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels

  2012influential reference
• The tomato genome sequence provides insights into fleshy fruit evolution

  2012cited by this paper
• WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex.

  2011cited by this paper
• Brassinosteroids modulate plant immunity at multiple levels

  2011cited by this paper
• The Arabidopsis Information Resource (TAIR): improved gene annotation and new tools

  2011cited by this paper
• Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase.

  2011influential reference
• Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE.

  2011cited by this paper
• An Evolutionarily Conserved Pseudokinase Mediates Stem Cell Production in Plants

  2011influential reference
• Mixed linear model approach adapted for genome-wide association studies

  2010influential reference
• Post-Translational Modifications in Secreted Peptide Hormones in Plants

  2010cited by this paper
• CLE14/CLE20 peptides may interact with CLAVATA2/CORYNE receptor-like kinases to irreversibly inhibit cell division in the root meristem of Arabidopsis

  2010cited by this paper
• CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification.

  2010influential reference
• RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis

  2010influential reference
• RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis

  2010influential reference
• A glycopeptide regulating stem cell fate in Arabidopsis thaliana.

  2009influential reference
• FON2 SPARE1 Redundantly Regulates Floral Meristem Maintenance with FLORAL ORGAN NUMBER2 in Rice

  2009cited by this paper
• A receptor-like cytoplasmic kinase, BIK1, associates with a flagellin receptor complex to initiate plant innate immunity

  2009influential reference
• Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane1[W][OA]

  2009influential reference
• Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis.

  2009influential reference
• Transposon Resources for Forward and Reverse Genetics in Maize

  2009cited by this paper
• Arabidopsis CLV3 Peptide Directly Binds CLV1 Ectodomain

  2008cited by this paper
• The Receptor-Like Kinase SOL2 Mediates CLE Signaling in Arabidopsis

  2008influential reference
• The Receptor Kinase CORYNE of Arabidopsis Transmits the Stem Cell–Limiting Signal CLAVATA3 Independently of CLAVATA1[W]

  2008influential reference
• Functional Diversification of CLAVATA3-Related CLE Proteins in Meristem Maintenance in Rice[W][OA]

  2008influential reference
• BAM Receptors Regulate Stem Cell Specification and Organ Development Through Complex Interactions With CLAVATA Signaling

  2008cited by this paper
• Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana.

  2007influential reference
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  2007influential reference
• A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence

  2007cited by this paper
• Emerging roles of pseudokinases.

  2006cited by this paper
• A Plant Peptide Encoded by CLV3 Identified by in Situ MALDI-TOF MS Analysis

  2006influential reference
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  2006cited by this paper
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  2006cited by this paper
• The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis.

  2006cited by this paper
• The shoot stem cell niche in angiosperms: expression patterns of WUS orthologues in rice and maize imply major modifications in the course of mono- and dicot evolution.

  2006influential reference
• Dodeca-CLE Peptides as Suppressors of Plant Stem Cell Differentiation

  2006cited by this paper
• The FLORAL ORGAN NUMBER4 Gene Encoding a Putative Ortholog of Arabidopsis CLAVATA3 Regulates Apical Meristem Size in Rice1[W]

  2006cited by this paper
• The TIGR Rice Genome Annotation Resource: improvements and new features

  2006cited by this paper
• MAFFT version 5: improvement in accuracy of multiple sequence alignment

  2005cited by this paper
• thick tassel dwarf1 encodes a putative maize ortholog of the Arabidopsis CLAVATA1 leucine-rich repeat receptor-like kinase

  2005influential reference
• The 14–Amino Acid CLV3, CLE19, and CLE40 Peptides Trigger Consumption of the Root Meristem in Arabidopsis through a CLAVATA2-Dependent Pathwayw⃞

  2005influential reference
• The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine-rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1

  2004cited by this paper
• CLANS: a Java application for visualizing protein families based on pairwise similarity

  2004influential reference
• A combined transmembrane topology and signal peptide prediction method.

  2004cited by this paper
• MUSCLE: multiple sequence alignment with high accuracy and high throughput.

  2004cited by this paper
• CLAVATA1 Dominant-Negative Alleles Reveal Functional Overlap between Multiple Receptor Kinases That Regulate Meristem and Organ Development Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010504.

  2003influential reference
• CLV3 Is Localized to the Extracellular Space, Where It Activates the Arabidopsis CLAVATA Stem Cell Signaling Pathway Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.002196.

  2002cited by this paper
• BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling.

  2002cited by this paper
• Faculty Opinions recommendation of BRI1/BAK1, a receptor kinase pair mediating brassinosteroid signaling.

  2002cited by this paper
• The fasciated ear2 gene encodes a leucine-rich repeat receptor-like protein that regulates shoot meristem proliferation in maize.

  2001influential reference
• The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes.

  2000cited by this paper
• Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity.

  2000influential reference
• The Arabidopsis CLAVATA2 Gene Encodes a Receptor-like Protein Required for the Stability of the CLAVATA1 Receptor-like Kinase

  1999cited by this paper
• Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems.

  1999cited by this paper
• CLAVATA2, a regulator of meristem and organ development in Arabidopsis.

  1998cited by this paper
• Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signaling pathways in Arabidopsis.

  1998cited by this paper
• Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem.

  1998cited by this paper
• The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis.

  1997cited by this paper
• Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot

  1994cited by this paper
• CLAVATA1, a regulator of meristem and flower development in Arabidopsis.

  1993cited by this paper
• Wuschel Protein Movement Mediates Stem Cell Homeostasis in Material Supplemental

  year unknowncited by this paper

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• CT2 is involved in yield-related traits and cell proliferation of maize

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• How meristems shape plant architecture in cereals—Cereal Stem Cell Systems (CSCS) Consortium

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  2024cites this paper
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  2024cites this paper
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  2021influential citation
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• the ear1 locus controls the fate of inflorescence meristem cells in maize.

  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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• Next Generation Cereal Crop Yield Enhancement: From Knowledge of Inflorescence Development to Practical Engineering by Genome Editing

  2021cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
• Plant receptor-like kinase signaling through heterotrimeric G-proteins

  2020cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
• The analysis of functional genes in maize molecular breeding

  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2018cites this paper
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  2018cites this paper
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