CLE peptide-mediated signaling in shoot and vascular meristem development

doi:10.1007/s11515-017-1468-9

Front. Biol.

2017, Vol. 12

Issue (6) : 406-420 https://doi.org/10.1007/s11515-017-1468-9

REVIEW

CLE peptide-mediated signaling in shoot and vascular meristem development

Thai Q. Dao^1,², Jennifer C. Fletcher^1,²(

)

¹. Plant Gene Expression Center, United States Department of Agriculture-Agricultural Research Service, Albany, CA 94710, USA
². Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA 94720, USA

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Abstract

BACKGROUND: Multicellular organisms rely on the transmission of information between cells to coordinate various biological processes during growth and development. Plants, like animals, utilize small peptide ligands as signaling molecules to transmit information between cells. These polypeptides typically act as extracellular messengers that are perceived by membrane-bound receptors, which then transduce the signal into the recipient cell to modify downstream gene transcription. The CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) proteins represent one of the largest and best understood families of small polypeptides in plants. Members of the CLE family play critical roles in mediating cell fate decisions during plant development, particularly within the unique meristem structures that contain stem cell reservoirs acting as sources of cells for continuous organ formation.

OBJECTIVE: Here we review the roles of CLE family members in regulating the activity of the shoot apical meristems that generate the aerial parts of the plants, and of the vascular meristems that produce the sugar- and water-conducting tissues.

METHODS: A systematic literature search was performed using the Google Scholar and PubMed search engines. The keywords “CLE”, “CLV3”, “TDIF”, “meristem”, and “plant stem cells” were used as search terms. The 95 retrieved articles, dating from 1992, were organized by topic and their key findings incorporated into the text.

RESULTS: We summarize our current understanding of how the CLE peptide CLV3 orchestrates the activity of shoot apical meristems, describing its expression, processing and movement, as well as its intracellular signal transduction pathways, key target genes and downstream gene regulatory networks. We also discuss the roles of CLE peptide signaling in the vascular meristems to promote procambial cell proliferation and suppress xylem differentiation.

CONCLUSIONS: Signaling pathways mediated by CLE peptides are critical for stem cell maintenance and differentiation in shoot apical and vascular meristems in plants, exposing CLE genes as potential targets for increasing yield and biomass production. While large numbers of CLE genes are being discovered in plants, only a few have been functionally characterized. We anticipate that future research will continue to elucidate the roles of the CLE family in plant development, and their potential impacts on agriculture and commerce.

Keywords CLE CLV3 TDIF WUS stem cells procambium

Corresponding Author(s): Jennifer C. Fletcher

Just Accepted Date: 03 November 2017 Online First Date: 07 December 2017 Issue Date: 10 January 2018

Cite this article:

Thai Q. Dao,Jennifer C. Fletcher. CLE peptide-mediated signaling in shoot and vascular meristem development[J]. Front. Biol., 2017, 12(6): 406-420.

URL:

https://academic.hep.com.cn/fib/EN/10.1007/s11515-017-1468-9
https://academic.hep.com.cn/fib/EN/Y2017/V12/I6/406

Fig.1 Functional domains of keySAM regulatory proteins. (A) The CLV3 pre-propeptide contains a signalsequence that directs it into the extracellular space, a variableregion, and a CLE domain. The pre-propeptide is cleaved at the N terminusof the CLE domain (red arrowhead), and the released 12-13 amino-acidpeptide is modified to generate a functional ligand. (B) The CLV1protein is a receptor-like kinase (RLK) that consists of a signalsequence that directs it to the plasma membrane, 21 extracellularleucine-rich repeat domains, a transmembrane domain, and a cytosolicserine/threonine kinase domain. (C) The WUS protein is a transcriptionfactor that contains an N-terminal DNA binding homeodomain consistingof three helices, as well as three conserved sequence motifs at thecarboxyl-terminus: an acidic domain (AD), a WUS box (W), and an EARdomain (E). Molecules are not drawn to scale.

Fig.2 Organization of the Arabidopsis thaliana shoot apical meristem(SAM). The SAM is located at the growing shoot tip of the plant (bluecircle and black arrowhead mark the location of the SAM in plantsat three successive developmental stages). L1, L2, and L3 denote layersof distinct cell lineages. The central zone (CZ) is located at theapex and consists of stem cells that divide slowly into the surroundingperipheral zone (PZ) and the underlying rib zone (RZ). Cells in thePZ divide more rapidly and are recruited to form organ primordia (P₀, P₁, and P₂) or stem tissue. The organizing center (OC) at the top of the RZfunctions as a niche that maintains stem cell identity in the CZ.Also shown is the vasculature (V) forming underneath the SAM and towardthe developing organs.

Fig.3 CLV3 signaling pathways.The mature CLV3 peptide forms a horseshoe-shaped kink around the Gly⁶ and Hyp⁷ residues thatis likely recognized by its receptors. The Hyp⁷ residue is post-translationally modified with three L-arabinoseresidues (red). The Pro⁹ and His¹¹ residues (gold) are most critical for the abilityof CLV3 to restrict SAM size in vitro. CLV3 signaling is mediatedby a suite of receptors. The LRR-RLK CLV1 forms homodimers that bindto CLV3 peptide, and the protein phosphatases POL and PLL1 act downstreamof CLV1 to promote WUS transcription.The LRR protein CLV2 and the pseudokinase CRN form a heterodimericcomplex that is involved in CLV3 signal transduction, but whetherit directly binds CLV3 is unclear. The LRR-RLK RPK2 forms homodimersthat associate with the G protein subunit AGB1, but also does notbind directly to CLV3. RPK2 physically interacts with the CLV3-bindingLRR-RLK BAM1 in the peripheral zone of the SAM, but not with CLV1or CLV2. Molecules are not drawn to scale.

Fig.4 The CLV3-WUS stem cell homeostasisnetwork. CLV3 ligand produced in the CZ diffuses into the underlyingOC cells to associate with CLV1 and other receptors. CLV1 bindingtriggers signaling pathways that repress BAM1 expression and limit the WUS expressiondomain to the OC. The WUS expressiondomain overlaps with that of the GRAS domain transcriptional regulatorygene HAM1, which is repressed byCLV3 signaling, and the WUS and HAM proteins act together as cofactorsthat share common target genes. WUS activity in the OC represses theexpression of differentiation-promoting transcription factors (TFs)and the bHLH TF gene HEC1. WUSprotein also moves into the adjacent CZ to promote stem cell fateand regulate CLV3 transcription.WUS protein recognizes cis-elements both upstream and downstream ofthe CLV3 coding region (inserts).In the CZ, where WUS protein concentration is low, WUS binds the cis elements as a monomer to activate CLV3 transcription. In the OC, where WUSprotein concentration is high, WUS binds the cis elements as a dimer to repress CLV3 transcription. HEC1 activity in the PZ represses CLV3 and WUS expression, and acts oppositely to WUS in the regulation of cytokininsignaling. Together this complex signaling network coordinates stemcell maintenance in the SAM.

Fig.5 CLE regulation of vascularcambium activity. A wedge-shaped vascular bundle in the Arabidopsis stem containing meristematicprocambial cells that divide to generate phloem and xylem cells isshown. CLE41 and CLE44, both encoding the same peptide, areexpressed in the phloem. The resulting ligand, called TDIF, is perceivedby PXY, an LRR-RLK in the procambium. TDIF-PXY signaling induces WOX4 and WOX14 expression to promote procambial cell division. In addition, PXYphysically interacts with BIN2 to inhibit the transcription factorBES1, thus preventing procambial cell differentiation into xylem.

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