Table 1.
Summary of CLE-RLK signaling.
| CLE peptide | RLK and/or other receptors involved | Origin of the peptide | Destination of the peptide/location of RLK | Short-term (molecular, cellular) and long-term (tissue, organ, organism) effects |
|---|---|---|---|---|
| Signaling range | ||||
| In the apical meristem of Marchantia | ||||
| MpCLE2 | Signals through MpCLV1 | The apical notch but outside the central region that hosts central subapical cells | The meristem with the apical and subapical cells where MpCLV1 is expressed | Short-term: Inhibits differentiation of the subapical cells Long-term: Mediates accumulation of subapical cells and enables their subsequent differentiation and dichotomous branching |
| Paracrine signaling | ||||
| MpCLE1 | Signals through MpTDR | The ventral part around the apical cell | Dorsal part where MpTDR is expressed | Short-term: Inhibits proliferation of the apical meristem Long-term: Regulates expansion of the thallus and proper formation of gametangiophores and gemma cups |
| Both auto- and paracrine signaling | ||||
| During Physcomitrium gametophore formation | ||||
| PpCLEs 1, -2, and -7 | (PpCLE1 to -7) Signal through PpRPK2 and PpCLV1a and -b | Different regions in the gametophores | Gametophore | Short-term: Initiation of formative division, maintenance of CD orientation and specification of cell fate Long-term: 1. Mediates formation of properly sized mature gametophores 2. Inhibits proliferative divisions in gametophore, thus maintaining gametophore and leaf size |
| PpCLE6 | Protonemal filament | Likely gametophore | ||
| PpCLE 3, -4, and -5 | Not characterized | Likely gametophore | ||
| In the SAM of Arabidopsis | ||||
| CLE40 | Signals through (and likely binds) BAM1 | PZ of IFM and SAM | PZ where BAM1 is expressed | Short-term: 1. Induces WUS in the OC 2. Promotes proliferation and suppresses differentiation of stem cells Long-term: 1. Promotes SAM growth 2. Proper formation of floral organs |
| Likely autocrine signaling | ||||
| CLV3 | Binds and signals through CLV1; signals through RPK2, CLV2/CRN | CZ of IFM and SAM | OC where it binds and signals through CLV1 | Short-term: 1. Represses WUS and its expansion into CZ 2. Suppresses proliferation of stem cells and enables their differentiation Long-term: 1. Inhibits SAM growth 2. Regulates proper formation of floral organs |
| Paracrine signaling | ||||
| In the root apical meristem of Arabidopsis | ||||
| CLE45 | Binds BAM3; signals through CLV2/CRN, RPK2 | PSE and SPC | 1. PSE and SPC where it binds and signals through BAM3 | Short-term: 1. Inhibits periclinal, formative division of SPC into proto- and metaphloem cells 2. Inhibits the acquisition of morphological changes during PSE differentiation Long-term: 1. Regulates PSE cell file formation 2. Regulates PRM development |
| Autocrine signaling | ||||
| 2. Likely CC and PPP where RPK2 is expressed | Short-term: Inhibits CC and PPP differentiation into PSE Long-term: Maintains a reservoir of phloem cells with plastic identity for future needs | |||
| Likely paracrine signaling | ||||
| CLE25 | Signals through CIK and CLV2 | In root: SPCs and its lineage; In stem: sieve elements | Not characterized | Short-term: Regulates periclinal, formative division of SPC into proto- and metaphloem cells Long-term: Regulates PRM development, phloem transport and starch immobilization |
| In the vascular meristem | ||||
| CLE41 | Signals through PXY | Phloem | Cambium where PXY is expressed | Short-term: 1. Triggers proliferation of procambium/cambium by upregulating WOX4 2. Inhibits its differentiation into xylem 3. Controls orientation of procambial cell division Long-term: 1. Organized vascular patterning 2. Maintenance of stele size and radial growth of the vascular system |
| Paracrine signaling | ||||
| PttCLE41 | Likely signals through PttPXY | Phloem | Likely vascular cambium where PttPXY is expressed | Short-term: Likely induces proliferation of cambial cells, which then differentiate into xylem cells Long-term: 1. Maintains overall secondary vascular growth and stem diameter 2. Regulates the internodal length and height of the plant |
| Likely paracrine signaling | ||||
| PtrCLE20 | Likely signals through PtrCLV2 | Xylem | Vascular cambium | Short-term: Likely suppresses cambial cell proliferation leading to a decreased rate of xylem differentiation Long-term: Maintains overall secondary vascular growth and stem diameter 2. Regulates the internodal length and height of the plant |
| Paracrine signaling | ||||
| CLE9 | Binds BAM1; signals through BAM2 and -3 | Xylem precursors, particularly of protoxylem cell file positions | Likely xylem precursors of protoxylem cell file positions, where it binds and signals through BAM1, although BAM1 is broadly expressed in vascular and pericycle cells | Short-term: Prevents peri- and anticlinal divisions of xylem precursors that increases xylem and procambial cell number Long-term: 1. Regulates the number of xylem and procambium cell files 2. Regulates the overall plant growth |
| Likely autocrine signaling | ||||
| In stomatal lineage development | ||||
| CLE9 | Binds HSL1-SERK1, the RLK-coreceptor complex | MMC, meristemoids and GCs | MMC and meristemoids, where it binds and signals through HSL1 | Short-term: 1. Destabilizes SPCH to prevent MMC from acquiring its identity 2. Prevents its further asymmetric divisions Long-term: Regulates the density of GCs and PCs in leaves |
| Likely autocrine signaling | ||||
| In root nodulation | ||||
| MtCLE12 and -13 | Signals through MtSUNN, MtCRN | Nodule primordium in root | Likely shoot where MtSUNN is expressed | Short-term: MtCLE13 suppresses the proliferative divisions likely right after the initial cell divisions of the cortex and pericycle Long-term: 1. Both peptides inhibit nodule primordium development 2. Decrease the nodule numbers, thus establishing N homeostasis |
| Likely endocrine signaling | ||||
| LjCLE-RS1 and -2 | Binds LjHAR1; signals through LjKLV and LjCLV2 | Nodule primordium in root | Shoot, likely in leaf phloem, where LjHAR1 is expressed | Short-term: LjCLE-RS1 and −2 peptides negatively regulate continuous cortical cell divisions after a few rounds of initial divisions Long-term: 1. Both peptides inhibit nodule primordium development 2. Decrease the nodule numbers, thus establishing N homeostasis |
| Endocrine signaling | ||||
| In nematode infection | ||||
| HsCLEB | Signals through TDR, CLV1, RPK2, CLV2/CRN | Nematode esophageal gland | Likely procambial cells in the root and/or the syncytial cells expressing TDR | Short-term: Induces procambial proliferative divisions Long-term: Induces syncytia formation and increases rate of infection |
| In organ primordium and organ development | ||||
| CLE26 | Can bind and possibly signals through BAM1 and -2 | Phloem pole of the stele in basal meristem | Not characterized | Short-term: Affects the PIN1 protein level in the root Long-term: 1. Alters the auxin distribution in roots 2. Regulates PR length and LR density |
| CLE3 | Signals through CLV1 | Pericycle cells in PR and LR | Likely companion cells where CLV1 is expressed | Short-term: Not characterized Long-term: 1. Inhibits LR emergence 2. Prevents root expansion in low N conditions |
| Likely paracrine signaling | ||||
| CLE5 | Not characterized | Bases of young rosette leaves, of cauline leaves and of cotyledons of mature embryo; at both the adaxial and abaxial domains of vegetative shoot apex in developing rosette leaves | Not characterized | Short-term: Not characterized Long-term: Regulates leaf width and symmetry |
| CLE6 | Not characterized | Bases of young rosette leaves and floral organs; only at the adaxial domain of vegetative shoot apex in developing rosette leaves | Not characterized | Short-term: Not characterized Long-term: Regulates leaf width, symmetry and curvature |
| Not characterized | CLV2/CRN | Not characterized | Not characterized | Short-term: 1. Upregulates auxin synthesis genes in the IFM cells 2. Maintains PIN1 protein levels in the IFM cells Long-term: 1. Maintains overall auxin signaling in the IFM 2. Mediates flower primordia outgrowth and complete flower formation |
| CLV3 and other CLEs | Signal through BAM1, -2, and -3 | Not characterized | Not characterized | Short-term: Not characterized Long-term: 1. Mediate flower primordia outgrowth and complete flower formation |
| In regulation of non-developmental responses | ||||
| CLE25 | Signals through BAM1 and -3 | Vascular procambium of, possibly, the root | Leaf where BAM1 and -2 are expressed | Short-term: 1. Promotes ABA synthesis 2. Enables stomatal closure Long-term: Reduces water loss and ensures overall survival of the plant during water deficiency |
| Endocrine signaling | ||||
| CLE9 | Not characterized | Stomatal GCs | Likely the stomatal GCs | Short-term: 1. Activates MPK3,−6 2. Enables stomatal closure by signaling through effectors, such as, ABA, NO, H2O2 Long-term: Prevents excessive water loss, thus conferring resistance to drought stress |
| Likely autocrine signaling | ||||
| MtCLE53 | Signals through MtSUNN | Vascular tissue with increased expression near colonization sites | Not characterized | (MtCLE53/-33) Short-term: 1. Upregulates MtSUNN 2. Suppresses the expression of strigolactone biosynthetic genes (MtCLE53/-33) Long-term: Suppresses excessive AM fungal colonization thus attaining Pi homeostasis |
| MtCLE33 | Signals through MtSUNN | Vascular tissue with strong expression in pericycle and xylem parenchyma (no change due to colonization) | Not characterized | |
| RiCLE1 | Not characterized | Fungi colonizing the root | Likely the epidermal and cortical cells | Short-term: Not characterized Long-term: 1. Modulates root architecture by promoting PR and LR branching 2. Promotes the entry and spread of the fungi |
| CLE45 | Binds SKM1 and signals through SKM1 and -2 | Stigma of the pistil at 22°C and expanded to the transmitting tract where pollen elongates at 30°C | Pollen where it binds SKM1 | Short-term: Retains mitochondrial dehydrogenase activity at high temperature, thus prolonging pollen viability 2. Sustains pollen performance and increases the chances of pollen tubes reaching the ovules Long-term: Ensures stable seed production |
| Paracrine signaling | ||||
The list of CLE peptides and RLKs and other receptors they bind and/or signal through, their signaling range, the origin of the peptide and its destination where it exerts its effect, the short- and long-term effects covering the molecular, cellular, tissue, organ, and organism levels. ABA, abscisic acid; AM, arbuscular mycorrhiza; BAM, BARELY ANY MERISTEM; CC, companion cells; CD, cell division; CIK, CLAVATA3 INSENSITIVE RECEPTOR KINASES; CLE, CLAVATA3/EMBRYO SURROUNDING REGION-RELATED; CRN, CORYNE; CLV, CLAVATA; CZ, central zone; GC, guard cell; HSL, HAESA-LIKE 1; IFM, inflorescence meristem; LR, lateral root; MMC, meristemoid mother cell; MPK, MITOGEN-ACTIVATED PROTEIN KINASE; OC, organizing center; PC, pavement cell; PIN, PIN-FORMED; PPP, phloem pole pericycle; PRM, proximal root meristem; PSE, protophloem sieve element; PXY, PHLOEM INTERCALATED WITH XYLEM; PZ, peripheral zone; RLK, receptor-like kinase; RPK2, RECEPTOR-LIKE PROTEIN KINASE 2; SAM, shoot apical meristem; SKM, STERILITY-REGULATING KINASE MEMBER; SPC, sieve element precursor cell; SPCH, SPEECHLESS; SERK, SOMATIC EMBRYOGENESIS RECEPTOR KINASE; SUNN, SUPER NUMERIC NODULES; TDR, TDIF RECEPTOR; WOX, WUSCHEL-related HOMEOBOX 4; WUS, WUSCHEL. The name of the CLE peptide, its signaling range and the long term effects it mediates are described in bold letters.