Prerpints.org logo
Preprint
Review

Research Progress of CLE and Its Prospects in Woody Plants

This version is not peer-reviewed.

Submitted:

21 March 2025

Posted:

21 March 2025

You are already at the latest version

Abstract
The peptide ligands of the CLAVATA3/EMBRYO SURROUNDING REGION-RELATED (CLE) family have been previously identified as essential signals for both short- and long-distance communication in plants, particularly during stem cell homeostasis, cell fate determination, and overall growth and development. To date, most studies on the CLE family have focused on model plants and especially those involving stem and apical meristems. Relatively little is known about the role of CLE peptides in tall trees and other plant meristems. In this review, we summarize the role of CLE genes in regulating plant Root Apical Meristem (RAM), Shoot Apical Meristem (SAM), Procambium, Leaf and Floral Meristems (FM), as well as their involvement in multiple signaling pathways. We also highlight the evolutionary conservation of the CLE gene family and provides a comprehensive summary of its distribution across various plant developmental tissues. This paper aims to provide insights into novel regulatory networks of CLE in plant meristems, offering guidance for understanding intercellular signaling pathways in forest trees and the development of new plant organs.
Keywords: 
CLE family
;  
meristem
;  
regulatory networks
;  
compensation mechanism
;  
plant development
Subject: 
Biology and Life Sciences  -   Plant Sciences

1. Introduction

The growth of trees originates from the development of embryonic stem cells within the seed. When plants have fully matured and sensed the appropriate external conditions, the differentiation and division of embryonic stem cells are precisely and stably regulated that is the basis for the formation and maintenance of meristem tissues for sustaining development of plants after embryo [1,2]. The radicle firstly divides into RAM, and with the elongation of the plumular axis, the germ differentiated SAM to form stems and leaves, and then the procambium cells continued to increase differentiation. Eventually, the plant transitions from vegetative growth to reproductive development, marked by the formation of the FM [3,4,5]. In recent years, many genes have been concerned in the regulation of plant meristem, such as FAS1/2; STM; CLV3/ESR. Among them, the CLE gene family have been extensively studied as key genes [6,7,8,9,10].
The CLE family of plant-specific genes is named after its founding CLV3/ESR that is specifically expressed in the maize (Zea mays) [11,12,13]. Furthermore, regarding the structure of genes, Cock and McCormick discovered that they obtained 39 related protein sequences which were named CLV3/ESR associated CLE family which was characterized by 12-residue conserved domains that were the most basic and necessary to ensure the function of signal peptides at the C-terminal and hydrophobic signaling peptides at the N-terminal [11]. The similarity of the remaining sequences is very low except for the conserved motif and secreted signal peptide [14]. Subsequently, CLE is explicitly described as a signal peptide that is cleaved from a longer pre-peptide with a similar structure: small proteins (usually fewer than 150 amino acids) consisting of an N-terminal signal peptide, followed by a variable domain with significant sequence diversity, and a conserved C-terminal CLE motif. These pre-peptides are translated and modified one or more times [11,15,16,17]. As for CLE family gene function studies, as early as the mid-1990s, most CLV1/3 mutants were found to affect the meristem activity of plant stems, roots, and flowers [18,19]. Subsequently, the WUS-CLV3 regulatory network was discovered, which controls the activity of the apical meristem at the stem tip [20]. In 2002, CLV3-CLV1/2 was found as a receptor ligand in plants to signal from the stem cell population [21]. This marked further study of the CLE family. However, this is only applicable to the CLV1/2/3 genes. In 2006, CLV3/ESR1-LIKE 41 (CLE41) was shown to repress xylem differentiation in cell culture [22]. In a later study, similar to WUS and CLV3, CLE40 and WOX5 were found to play a role in regulating the root meristem [23,24,25]. As the research on various genes of the CLE family has been continuously deepened, it has been discovered that CLE family genes have different functions to control the development of plants.
Based on domain structure and functional analyses, Whitford classified the peptide types of the CLE family into two categories: A (CLAVATA3 (CLV3)-like) and B (TRACHEARY ELEMENT DIFFERENTIATION INHIBITORY FACTOR (TDIF)-like) [26]. A-type CLE peptides promote cell differentiation in root and shoot apical meristems, whereas the B-type peptides CLE41– CLE44 do not promote. B-type CLE genes and peptides suppress differentiation into tracheary elements. B-Type CLE peptides are mainly Tracheary Element Differentiation Inhibitory Factor TDIF-like [27,28]. The synergistic interaction of these two peptides inhibits differentiation and promotes auxin-mediated cell proliferation in the secondary meristem (vascular cambium), suggesting that specific CLE genes have dual functions and cell type-specific responses [29].
While recent advances have established the CLE gene family as a systemic regulatory hub governing stem cell dynamics across Arabidopsis thaliana tissues—particularly during organogenesis from embryogenesis to post-meristematic differentiation—the functional characterization of CLE networks in woody perennials remains critically understudied.
The earliest research on CLE genes in forest trees was reported in Populus trichocarpa in 2016 [30]. Since then, while several studies have been conducted, progress in understanding the CLE gene family in both Populus trichocarpa and other forest trees have been limited. Forest trees play a crucial role in water resource conservation, maintaining ecological balance, and providing medicinal compounds from their roots and leaves along with edible fruits, making them indispensable for both environmental sustainability and human well-being. For tall trees to grow healthily and vigorously, it is essential to maintain and properly differentiate the stem cells in the meristematic tissues. Therefore, this study, to offer guidance for the growth and development of forest trees, we investigate the regulatory pathway of the CLE family in Arabidopsis thaliana by tracing the developmental sequence of plant organ formation.

2. Development and Maintenance of CLEs in Root Apical Meristem

Root developmental plasticity is a critical determinant of plant fitness, enabling efficient acquisition of soil resources (water and nutrients) and systemic coordination of whole-plant growth. The establishment of RAM architecture begins with a stereotypical radial pattern at the root tip, where a small cohort of progenitor cells undergoes precisely oriented divisions to generate distinct tissue lineages [31]. Central to this process is the stem cell niche (SCN), a dynamic microdomain organized around the mitotically inactive quiescent center (QC)(Figure1A). This niche contains the QC that is thought to be the initial cell that maintains the first surrounding cell in an undifferentiated state and gives rise to other stem cells, stem cells on the proximal (toward the shoot) site of the QC which generate vasculature and pericycle, lateral stem cells of the QC give rise to endodermis, cortex, epidermis, lateral root cap and distal columella stem cells (CSC) of the QC generate the protective cap of columella cells (CC) [32,33,34,35,36].
Unlike stems, root ecological niche restriction is mediated not by individual stem cells but by entire meristematic stem cell populations enveloped by the root cap [37,38]. CLE40 expression is localized to the basal region of the embryo during the globular embryo stage, where it initiates root meristem and vasculature formation. Post-germination, CLE40 is expressed in the CCs and triggers a signaling cascade involving the WUS-related gene WOX5 through receptor-like kinase CLV1 and ARABIDOPSIS CRINKLY4 (ACR4) located at the distal end of QC, limiting WOX5 movement outside QC for promoting distal root meristem differentiation [37,39]. In Solanum tuberosum, the homologous gene of CLV3 is StCLE4 regulates stem cell activity and modulates both stem and root growth [40]. In lateral root apex meristem activity, CLV3 plays a central role in lateral root apical meristem activity. Under normal conditions, CLV3 is expressed in the mesothelial sheath of roots and lateral root length is inversely correlated with CLV3 expression levels. However, CLV3 overexpression disrupts root tip meristem activity, leading to a short-root phenotype that is positively influenced by sucrose levels in the root [41]. Additionally, the CLV3-CLV2/SOL pathway regulates root meristem signaling, with SOL2/CRN deficiency resulting in markedly reduced root length [42,43] (Figure1A). CLE19 restricts root meristem cell size without directly affecting the QC or adjacent stem cells, instead acting on central sheath initiation cells via the CLV2 complex [44] [45].

3. Development and Maintenance of CLEs in Shoot Apical Meristem

In forest trees, almost all above-ground tissues originate from the conserved dome-like SAM, which is actually a highly heterogeneous and highly organized structure controlled by stem cells [46,47]. According to cell Structurally, in monocotyledons like Oryza sativa L., SAM is organized into distinct layers: the L1 layer covering the L2 layer [48,49]. In dicotyledons, SAM forms between the two cotyledon and comprises three stem cell layers): the L1 layer which generates the epidermis via anticlinal divisions; The L2 layer where cells undergo periclinal divisions in the meristem and produce mesophyll cells through vertical/peripheral divisions in leaf primordia; and The L3 layer, which differentiates into stem cell centers and vascular tissues via both anticlinal and periclinal divisions, as seen in Arabidopsis thaliana [46,50]. Functionally, Stem cells organize the SAM into three domains: the organizing center (OC) , a central domain with slow division rates that maintains meristem integrity and supplies cells to the peripheral zone (PZ); PZ, surrounding the OC, where rapid cell divisions generate organ primordia；The rib meristem (RM), located below the OC, which specifies central stem cell identity [50,51] (Figure 1B). Cells continuously proliferate, progressing through three cellular functional regions that is aimed to control different cells and thus regulate the differentiation, division, and formation of organ primordia and internal tissues [52].
CLV3 is localized to the overlying cell layers of the stem cell niche, where it regulates cell division and organogenesis, while WUSCHEL (WUS), which specifies stem cell identity and controls meristem activity, resides at the base of the stem tip [24,53,54]. SHOOT MERISTEMLESS (STM), which maintains stem cell pluripotency, works synergistically with WUS and CLV3 to form a WUS-CLV3-STM regulatory loop that governs SAM homeostasis [55,56]. During the proliferation and differentiation of SAM stem cells, a Homebox（HB） family transcription factor WUS and a Class I KNOX transcription factor STM can up-regulate CLV3 expression by binding to the CLV3 promoter cis-acting elements (TAAT and TGACA), respectively [37,57]. Furthermore, STM assists WUS in forming WUS-STM heterodimers, which enhance WUS binding affinity to the CLV3 promoter via protein-protein interactions. This promotes CLV3 expression in the central zone (CZ), ensuring stem cell population stability [57,58,59]. The CLV3 gene encodes a 96-amino acid precursor protein that is post-translationally modified to yield a mature arabinosylated glycopeptide. This peptide contains a conserved 12- to 13-amino acid motif, with Leu and Arg identified as critical residues for restricting SAM size [11,53,60,61,62]. Spatiotemporally, CLV3 expression is confined to the epidermal and subepidermal layers of the CZ in shoot and floral meristems but is absent in the RM [53,55,63] (Figure 1C).
When CLV3 promotes cell proliferation, elevated WUS levels recruit HAM1 and HAM2 (members of the GRAS transcription factor-encoding HAM family). These WUS-HAM heterodimers suppress CLV3 expression, thereby establishing apical polarity of the CLV3 expression domain along the SAM axis to regulate stem cell homeostasis [64,65,66,67,68,69]. In embryonic development, CLV3 expression is regulated exclusively by WUS, independent of STM [70]. However, during later developmental stages, STM and WUS jointly modulate CLV3 levels, with CLV3 responsiveness to WUS confined to the apical meristem. Sustained overexpression of WUS triggers exocytosis-dependent CLV3 signaling, which coordinates three distinct cellular pathways to repress WUS in the RM, forming a negative feedback loop [21,71]. Mechanistically, CLV3 inhibits WUS primarily via LEUCINE-RICH REPEAT RECEPTOR-LIKE KINASES (LRR-RLKs) and CLAVATA3 INSENSITIVE RECEPTOR KINASES (CIKs). These receptors act synergistically, where CIKs enhance LRR-RLK activity to amplify downstream signaling cascades that suppress WUS expression [62,72,73].

3.1. CLV3-CLV1

As a ligand-receptor pair, CLV3 undergoes proteolytic cleavage and directly binds to CLV1, an LRR-RLK, with a dissociation constant (Kd) of 17.5 nM. This interaction triggers CLV1 endocytosis to regulate its membrane trafficking [74,75,76]. The binding ability between CLV3 and CLV1 is mainly affected by the arabinosylation of CLV3 and the affinity of different amino acids in the extracellular domain of CLV1 [74,76,77,78] (Figure1C).

3.2. CLV3-CLV2 CRN/SOL2

Both CLV2 ,a LEUCINE-RICH REPEAT（LRR）,protein lacking a kinase domain) and SUPPRESSOR OF LLP1 2 (SOL2)/CORYNE (CRN) (a transmembrane pseudokinase devoid of LRRs) are synthesized on the endoplasmic reticulum (ER). The transmembrane (TM) domain of CRN binds specifically to CLV2, enabling the CRN-CLV2 complex to localize to the plasma membrane (PM). This interaction neutralizes an acidic inhibitory motif in the extracellular region of CLV2, which is essential for PM trafficking. Notably, CRN does not enhance CLV2 accumulation at the PM but facilitates its targeting. The mature CRN-CLV2 complex subsequently binds CLV3 to mediate signaling [74,79,80,81]. CLV2-CRN is parallel to CLV1 and co-responds to CLV3 signal transduction [82,83] (Figure1C).

3.3. CLV3-RPK2

As a member of the RLKS family of receptor-like kinases, (RECEPTOR-LIKE PROTEIN KINASE2 (RPK2)) /TOAD2 regulates the development of anther microspores and tapetum and mutations in RPK 2 cause anther breakage [84,85]. In CLV3-null backgrounds, RPK2 mutants exhibit reduced SAM size and increased carpel number, indicating that RPK2 participates in CLV3-dependent signaling within the SAM to repress WUS expression. While RPK2 does not directly bind CLV3 via its leucine-rich repeat (LRR) domain, the mechanism of interaction remains unclear [86]. We hypothesize that RPK2 participates in the CLV3 pathway not solely as a ligand, but may act through alternative mechanisms in plant signaling (Figure1C).

3.4. CLV1-BAMs

BARELY ANY MERISTEM(BAM) is one of the leucine-rich repeat receptor-like kinases (LRR-RLK). Constitutive expression of BAM1/ BAM2 partially rescues the CLV1 mutant phenotype, confirming their functional homology with CLV1. Unlike CLV1, BAM1/BAM2 exhibit broader expression patterns [87]. Photoaffinity labeling assays demonstrate direct binding between the BAM1 ectodomain and CLV3 peptide. While single mutants (BAM1, BAM2, or BAM3) show no obvious developmental defects, double (BAM1/BAM2) and triple (BAM1/BAM2/BAM3) mutants exhibit reduced SAM size due to stem cell depletion [86,88] (Figure 1C). Thus, the CLV3-BAMs regulatory pathway was identified.
Current understanding of CLV3 downstream signaling—particularly phosphorylation cascades involving kinases and phosphatases—remains limited. CLV3 activates a phosphorylation cascade mediated by MPK3/MPK6, which partially rescues the CLV1 mutant phenotype, implicating these kinases in dependent signaling CLV1 [89]. The kinase-associated protein phosphatase KAPP directly interacts with CLV1, dephosphorylating it to attenuate CLV1 activity. Additionally, the PP2C-type phosphatases POLTERGEIST (POL) and POL-LIKE1 (PLL1) act as negative regulators downstream of CLV1/BAM receptors, modulating WUS expression to control apical stem cell dynamics [73,90] (Figure 1C). Genetic evidence shows that CLV3-CLV1, CLV3-CLV2/SOR and function independent of each other. However, studies on pathway crosstalk show that the first two pathways may be connected these pathways may converge, potentially compensating for each other to form a regulatory network that maintains stem cell homeostasis when one pathway is dysregulated [72].

4. Development and Maintenance of CLEs in Stem and Root Cambium

When stem and root apical meristem cells continue to divide and differentiate to form the procambium that have a tissue with permanent meristematic activity. Procambium serves as the primary source of xylem and phloem cells, while also contributing to the structural framework of plant stems and roots [91].
In the stem, shoot apical localized procambium (PC) initials are described as the primary meristem that differentiates basally to produce primary vascular bundles that daughter cells of PC differentiate into protophloem (PPh) toward the outside of the stem and protoxylem (PXy) toward the inside of the stem. Moving basally toward developmentally older tissues, actively dividing meristematic cells within vascular bundles were described as metacambium (MC) that subsequently divide into the secondary vascular cambium meristematic cells that produce secondary phloem and secondary xylem [92,93,94]. In this review, we classify stem tissues into procambium, xylem, and phloem to elucidate CLE family-mediated regulatory mechanisms. Within the procambium, the TDIF predominantly regulates cambial activity [26]. In Populus trichocarpa, MYB31 located in the cambium layer regulates the PtCLE41p/PtCLE42p/PtCLE44 peptides produced by the phloem to translocate the cambium and through the TDIF RECEPTOR (TDR)/ PHLOEM INTERCALATED WITH XYLEM (PXY) membrane protein kinase signaling pathway, the PtCLE41p/PtCLE42p/PtCLE44p combine with WOX4/WOX14 to promote procambial cell proliferation while suppressing xylem cell differentiation [95,96]. As a downstream transcription factor of TDIF-PXY, glycogen synthase kinase 3 proteins (GSK3s) inhibit BRI1-EMS SUPPRESSOR 1 (BES1), thereby inhibiting cambium-to-xylem cell differentiation [97]. MYB31 could either promote cell proliferation through the MYB31-MYB72-WOX4 module or inhibit cambial activity through the MYB31-MYB72-VASCULAR CAMBIUM-RELATED MADS2 (VCM2)/PIN-FORMED5 (PIN5) modules (VCM2/PIN5) [98,99]. In gymnosperms, CLE41/44 play a role not only in the phloem but also in the tracheary elements (TEs) [96,100]. PtCLE47 and PtCLE20, two poplar CLE polypeptides, respectively promote and inhibit procambial cell proliferation [101,102] (Figure 1D).
In the root, the procambium originating from the stem cells on the proximal (toward the shoot) can generate the pericycle which generates lateral roots and initiates vascular cambium (responsible for secondary phloem and xylem production); primary xylem, primary phloem which includes sieve elements (SEs) , companion cells (CCs)and related cell types [103,104]. In xylem precursor cells, the receptor-like kinases CLV1, BAM2, and BAM3 collectively function as major receptors for CLE9/10 peptides, regulating periclinal cell division to control xylem file numbers [22,105] (Figure 1E). During protophloem development, CLV3 critically modulates BAM1/2/3 and CLV2/CRN complexes to regulate SE differentiation [106]. In the protophloem, CLE25/CLE26 are expressed early in the SE cells lineage and regulate the initiation and development of phloem through the complex interaction with CLE-RESISTANT RECEPTOR KINASE -CLV2 (CLERK -CLV2) receptor to control the SE precursor cell (SPC) receptor-like protein [32,107,108]. A suppressor screen of BREVIS RADIX (BRX) mutants identified the CLE45-BAM3 axis as a compensatory pathway for SE differentiation [109]. MEMBRANE-ASSOCIATED KINASE REGULATOR 5 (MAKR5) acts as a post-transcriptionally regulated amplifier of the CLE45p signal that acts downstream of BAM3 [110,111]. BAM3-mediated CLE45 signaling antagonizes BAM1/2-mediated CLE11/12/13 signaling in the phloem initials [111]. Additionally, phloem-Dofs not only enforce SE and CC formation, but also activate the production of CLE25, CLE26 and CLE45 that they reduce the level of phloem-Dofs by interacting with BAMs/CIKs, thereby inhibiting the excessive production of SEs and CCs [112]. Furthermore, CLE peptides (CLE1/3/4/7) modulate lateral root growth and branching through the CLE-CLV1 signaling module in response to nitrogen availability, without affecting primary root development [113]. Collectively, these pathways fine-tune root architecture and elongation (Figure 2D).

5. Development and Maintenance of CLEs in Leaf

Leaf initiation and proper spatial orientation are essential for efficient photosynthesis, thereby ensuring plant survival. Within the SAM, the CZ harbors stem cells, while organogenesis initiates in the PZ [114]. During vegetative SAM development, CZ-derived stem cells undergo continuous division, with daughter cells migrating laterally into the PZ to form leaf primordia structures that is small and regularly spaced [115]. Cells in the PZ region divide rapidly and continuously, forming leaf protodermal cells, which can either directly divide into pavement cells (general epidermal cells) or become meristemoid mother cells (MMCs) ——stomatal lineage stem cells [116,117]. Following primordium initiation, leaves develop along three distinct polarity axes: axial-dorsal, proximal-distal, and central-lateral [118,119] (Figure1E).
Auxin determines the fate of organ primordia in the peripheral region of PZ, and the formation of leaf primordia is dependent on the auxin maximum formed by the polar auxin transport mediated by the PIN-FORMED (PIN1) gene [120,121]. Belonging to AUXIN RESPONSE FACTORs (ARFs), ARF5(Mp) also showed threshold expression in PZ to CZ and inhibits the expression of DORNROSCHEN /ENHANCER OF SHOOT REGENERATION1 (DRN/ESR1) to reduce the expression of CLV3 in CZ that can prevent the axillary meristem (AM) disturbance caused by high expression of CLV3 [71,122,123,124,125]. This suggests that CLV3 affects the development of leaf initials, CLE5/CLE6 induced by BOP1/2 are expressed at the petiole base that their loss of function makes the petiole slightly wider and AS2 inhibits the transcription of CLE5/CLE6 at the distant position of petiole and leaf. But CLE5/CLE6 have little effect on the leaf. Referring to the CLE-WOX pathway in SAM, it was found that the expression of CLE5/6 in leaves is also regulated by the WOX transcription factors, PRS and WOX1, which promote leaf growth and leaf margin cell-files [126]. In MCCs, CLE9/10 bind to HAESA-LIKE1 receptor kinase (HSL1) to phosphorylate SPCH through a MAPK cascade to control epidermal division [105]. By controlling ACS (endogenous ethylene), CLE42 accumulates EIN3 (ETHYLENE-INSENSITIVE3)-binding F-box1/2 (EBF1/EBF2) protein, which degrades EIN3 (a master transcription factor in the ethylene pathway), a key component of the ethylene signaling pathway, through the ubiquitin-proteasome pathway, thereby delaying leaf senescence [127]. Additionally, CLE14 regulates age-dependent and stress-induced leaf senescence through JUB1- ROS scavenging gene (CAT3, APX1, APX3) to mediate ROS scavenging [127,128,129] (Figure 1E).

6. Development and Mai[71,122–125ntenance of CLEs in Floral Meristem

When the plant's internal organs mature under a favorable external environment, SAM receives the flowering signal and transforms into the inflorescence meristem (IM), which marks the transition from vegetative growth to reproductive growth and the formation of young flower primordia [130]. The young floral primordia retain apical stem cells that undergo lateral divisions within the IM, generating FMs. Each FM orchestrates the sequential development of floral organ whorls (sepals, petals, stamens, and carpels) to form a complete flower [131,132]. Floral organogenesis proceeds through a temporally and spatially regulated sequence, with partially overlapping phases ensuring precise whorl patterning [133]. Therefore, FMs are continuously produced by multiple developing organs, and unlike the SAM, which maintains expansive growth zones, FMs activity occurs within spatially confined regions separated by narrow developmental boundaries [134].
CLV2 is expressed in IM and CRN is expressed in the early flower primordium that even expresses in the whole flower primordia. The CLV2/CRN receptor complex promotes the growth and development of flower primordium [135]. Mutations in the CLV2 site leads to enlargement of stem and flower meristem, and developmental defects in pistil, petals, and stamens [136]. CLV1 and CLV3 are expressed in the center and apex of FMs. Compared with STM, CLV1/CLV3 has the same expression pattern but opposite function in that STM mutants fail to form undifferentiated cells in stem meristem during meristem development while CLV1 and CLV3 accumulates excessive undifferentiated cells in flower meristems to causes over proliferation of central floral tissues [18,53,56]. STM and KNAT-6 mutations have additive effects in regulating CLV3 inflorescence size [137,138]. This suggests that CLV1/2/3 genes affect both flowers. Notably, WUS is not involved in the floral meristems and in the CLV3-CLV1 regulatory pathway. If the external environment temperature changes, CLE family genes, combined with auxin, play an irreplaceable role in responding to flower primordium [73]. At normal temperatures, the CLV3 pathway, like the thermal sensing ELF3 factor containing the Poly-Q structure, is functionally degraded by being covered by the YUCCA (YUC) complex [139,140,141]. Under lower temperatures, receptor complexes CLV1 and CLV2/CRN transduce the CLV3/CLE25 signal to coordinate the effect of promote normal flowering in plants by regulating YUC -dependent auxin biosynthesis [142]. Although CLE25 is inhibited by CLV3, in the case of CLV3 mutation, CLV3 promoter can bind to CLE25 to compensate for the flower phenotype [143]. High temperatures bypass CLV signaling, ELF3 upregulates auxin to control development of flower development [144]. Therefore, the significance of temperature to the regulation of CLE channels should also be paid attention to [145]. CLV3 promoter pathway is shown to be important in regulating the transition state of flower primordia during vegetative-to-reproductive growth, though the intermediate pathways and associated genes remain uncharacterized (Figure 1F).

7. Compensation Mechanism of CLEs in Plant

The compensation mechanism provides fault tolerance for plant development, enabling maximization of growth along normal developmental trajectories [146,147,148]. Due to lineage-specific factors, the number, functional relationships, homologous retention, and diversity variation (including redundancy) of inbred family members differ significantly among distantly related species. However, the CLE protein family demonstrates remarkable structural conservation—particularly in the C-terminal CLE motif, which is critical for receptor binding [149]. In Arabidopsis thaliana, following CLV3 deletion, the CLE16 and CLE17 signaling pathways actively regulate WUS, limiting stem and floral stem cell accumulation and buffering infinite apical enlargement caused by CLV3 loss. These pathways are not sensed by CLV1 or CLV2 but exclusively by the BAM1/BAM2 receptor kinases, indicating their role as compensatory mechanisms for CLV3 deficiency [87,150]. In CLV1 mutants, ectopic BAM expression in the RM partially compensates for CLV1 loss [86,151,152]. Additionally, other CLE peptides may exhibit functional redundancy during SAM maintenance. This is evidenced by complete or partial CLV3 complementation when CLE1, CLE6, CLE9, CLE11, CLE12, CLE13, CLE19, CLE21, or CLE22 are expressed under the CLV3 promoter [153,154]. Notably, single and double mutants of CLE16, CLE17, and CLE27 show no detectable phenotypes in the SAM or IM.
In Solanum lycopersicum, SlCLE compensation is functionally active, with SlCLE9 partially restoring SlCLV3 stem cell homeostasis primarily via CLV1 [143]. However, in Arabidopsis thaliana，the CLE9-CLV1 regulatory pathway remains poorly characterized. CLE40, encoding a putatively secreted protein with functional similarity to CLV3, can fully substitute for CLV3 in the SAM. The CLV3 promoter drives CLE40 expression to compensate for CLV3 deficiency [39]. In Zea mays L., ZmFCP1 and ZmCLE1E5 partially rescue the enlarged inflorescence meristem phenotype caused by ZmCLE7 mutations [155].

8. Conclusions

When we review the research process of the CLE gene family, it is not difficult to find that although the CLE family has continuously evolved over millions of years and in addition to parasitic nematodes, the CLE family is found in plants and is one of the largest families of plant polypeptides expansions [16,156]. However, reports of CLE in non-pattern woody plants are very limited. Here we extensively study on mosses (such as P. patens [149]), ferns (such as S. moellendorffii), gymnosperms (such as P. abies) and angiosperms (such as O. sativa [157], Arabidopsis [11], P. trichocarpa [30] S. purpurea, P. deltoides, P. persica, A. trichopoda [158](Figure 2). We found the CLE family between lower plants and higher plants has changed significantly, and more complex and precise gene branches have been differentiated. However, the amino acid structure of CLE was still conservative. Therefore, we can use the research methods in Arabidopsis thaliana, such as molecular probes and gene editing, to locate the CLE gene family in forest trees (Figure 2).
Secondly, modern molecular exploration experiments have shown that the CLE family plays a role in plant meristems. Although the architectural simplicity of Arabidopsis thaliana—particularly its absence of secondary growth machinery—confers limited translational applicability for arboreal species, developmental genetic analyses of meristem regulatory networks have established that a phloem-specific CLE41-PXY/TDR-WOX4 regulatory circuit in Populus trichocarpa is discovered based on the WUS- CLV3 ligand-receptor module that is an evolutionarily conserved regulatory module governing stem cell homeostasis in the procambium (Figure 1).This necessitates synergistic integration of pan-omics analyses (spatiotemporal proteomics, phospho-signaling mapping) with CRISPR-Cas9-mediated tissue-specific CLE knockout systems to resolve the mechanistic coupling between peptide ligand gradients and xylary differentiation trajectories in woody perennials. This suggests that the reference Arabidopsis regulatory network is crucial for elucidating the CLE foundation in forest trees. Furthermore, it is imperative to integrate additional biological experiments to advance this research and address existing challenges for ultimately enhancing wood yield. For floral and foliar organs in forest plants, auxin regulation could serve as a key entry point to elucidate the CLE signal transduction network in forest trees. To systematically interrogate CLE family, we generated an expression atlas of CLE family genes across angiosperm lineages, with focused comparative analysis in Arabidopsis thaliana and Populus trichocarpa (Figure 3). Our analysis revealed overlapping expression profiles of CLE family genes in diverse meristematic tissues, such as CLV1 being expressed in roots, stems, and cambium. This suggests that CLE peptides can function both as individual initiation signals and as signaling molecules that coordinate with other genes to regulate plant development (Figure 3).
Finally, the investigation into the compensation mechanism of the CLE gene family has revealed functional complementarity among its members. This signaling compensation fundamentally underpins meristem homeostasis, wherein developmental robustness is achieved via multilayered feedback control rather than isolated genetic components. Given this systems-level complexity, reductionist approaches focusing on single-gene characterization fail to capture the gene function. Therefore, it is imperative to explore diverse methodologies for a more scientific and comprehensive understanding of genes involved in forest tree development. Such as protein interactome mapping, genome sequencing and so on. The mechanistic insights derived from such multidimensional analyses hold significant potential for optimizing genome-informed silvicultural practices aimed at enhancing carbon sequestration efficiency and ecosystem service provisioning in managed forest stands.
In summary, as members of the polypeptide family, the CLE family genes act as signal regulators in meristems, maintaining the balance and transformation of stem cell homeostasis and thereby exerting regulatory effects on plant growth and development. Although extensive research has been conducted on model plants such as Arabidopsis thaliana and herbaceous plants, research on large, long-lived trees that play a key role in climate regulation and ecological balance is still limited. Therefore, it is more important to expand the research on how the CLE family regulates the meristems of forest trees.

Author Contributions

Writing—original draft, Z.S.; Data curation, W.Z.; Software—Image processing, Z.S., W.Z. and H.J.; Review—editing, Z.S. and D.Y. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD).

Data Availability Statement

Data is contained within the NCBI.

Acknowledgments

The authors gratefully acknowledge all contributors for their intellectual inputs in this work. Appreciation is extended to the editorial team and anonymous reviewers whose constructive comments significantly strengthened the manuscript. Special acknowledgment is given to Plants for serving as a premier platform for botanical research dissemination.

Conflicts of Interest

The authors declare no conflicts of interest.

Abbreviations

The following abbreviations are used in this manuscript: Because there are many Arabidopsis species gene names involved in this paper, we default to not adding prefixes, and other species CLE gene families add abbreviations before the species.

References

  1. Khavinson, V.; Linkova, N.; Diatlova, A.; Dudkov; Aleksandr. Peptide regulation of plant cells differentiation and growth. BIO Web of Conferences 2024. [Google Scholar] [CrossRef]
  2. Baskin, C.C.; Baskin, J.M. The rudimentary embryo: An early angiosperm invention that contributed to their dominance over gymnosperms. Seed Science Research 2023. [Google Scholar] [CrossRef]
  3. Kathryn Barton, M. Cell type specification and self renewal in the vegetative shoot apical meristem. Current Opinion in Plant Biology 1998, 1, 37–42. [Google Scholar] [CrossRef] [PubMed]
  4. Ali, S.; Khan, N.; Xie, L. Molecular and hormonal regulation of leaf morphogenesis in Arabidopsis. International Journal of Molecular Sciences 2020. [Google Scholar] [CrossRef]
  5. Dinneny, J.R.; Benfey, P.N. Plant stem cell niches: standing the test of time. Cell 2008. [Google Scholar] [CrossRef]
  6. Scofield, S.; Murray, J.A.H. KNOX gene function in plant stem cell niches. Plant Molecular Biology 2006. [Google Scholar] [CrossRef]
  7. Scofield, S.; Dewitte, W.; Murray, J.A. STM sustains stem cell function in the Arabidopsis shoot apical meristem and controls KNOX gene expression independently of the transcriptional repressor AS1. Plant Signaling & Behavior, 2014. [Google Scholar]
  8. Kwon, C.S.; Chen, C.; Wagner, D. WUSCHEL is a primary target for transcriptional regulation by SPLAYED in dynamic control of stem cell fate in Arabidopsis. Genes & Development, 2005. [Google Scholar] [CrossRef]
  9. Singh, S.; Singh, A.; Singh, A.; Yadav, S.; Bajaj, I.; Kumar, S.; Jain, A.; Sarkar, A.K. Role of chromatin modification and remodeling in stem cell regulation and meristem maintenance in Arabidopsis. Journal of Experimental Botany 2020. [Google Scholar] [CrossRef]
  10. Kaya, H.; Shibahara, K.I.; Taoka, K.I.; Iwabuchi, M.; Stillman, B.; Araki, T. FASCIATA genes for chromatin assembly factor-1 in Arabidopsis maintain the cellular organization of apical meristems. Cell 2001. [Google Scholar] [CrossRef]
  11. Cock, J.M.; McCormick, S. A large family of genes that share homology with CLAVATA3. Plant Physiology 2001. [Google Scholar] [CrossRef]
  12. Li, J.; Huang, Y.; Yu, X.; Wu, Q.; Man, X.; Diao, Z.; You, H.; Shen, J.; Cai, Y. Identification and application of CLE peptides for drought resistance in Solanaceae Crops. Journal of Agricultural and Food Chemistry 2024. [Google Scholar] [CrossRef]
  13. Chu, Y.; Gao, X.; Wen, L.; Deng, Z.; Liu, T.; Guo, Y. Characterization of the CLE Family in three nicotiana species and potential roles of CLE peptides in osmotic and salt stress responses. Agronomy 2023. [Google Scholar] [CrossRef]
  14. Gao Xiaoming; Yongfeng, G. CLE Peptides in Plants: Proteolytic processing structure-activity relationship, and ligand-receptor interaction. Journal of Integrative Plant Biology, 2012, 54 (10): 738–745. [CrossRef]
  15. Murphy, E.; Smith, S.; De Smet, I. Small signaling peptides in Arabidopsis development: how cells communicate over a short distance. The Plant Cell 2012. [Google Scholar] [CrossRef] [PubMed]
  16. Olsen, A. Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3. Trends in Plant Science 2003. [Google Scholar] [CrossRef] [PubMed]
  17. Gao, X.; Guo, Y. CLE peptides in plants: proteolytic processing, structure-activity relationship, and ligand-receptor interaction. Journal of Integrative Plant Biology 2012. [Google Scholar] [CrossRef]
  18. Clark, S.E.; Running, M.P.; Meyerowitz, E.M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development 1993. [Google Scholar] [CrossRef]
  19. Clark, S.E.; Running, M.P.; Meyerowitz, E.M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 1995, 121, 2057–2067. [Google Scholar] [CrossRef]
  20. Schoof; Lenhard; Haecker; Mayer; K, F.; Jurgens; Laux. The stem cell population of Arabidopsis shoot meristems in maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell, 2000.
  21. Rojo, E.; Sharma, V.K.; Kovaleva, V.; Raikhel, N.V.; Fletcher, J.C. CLV3 is localized to the extracellular space, where it activates the Arabidopsis CLAVATA stem cell signaling pathway. The Plant Cell 2002. [Google Scholar] [CrossRef]
  22. Ito, Y.; Nakanomyo, I.; Motose, H.; Iwamoto, K.; Sawa, S.; Dohmae, N.; Fukuda, H. Dodeca-CLE Peptides as suppressors of plant stem cell differentiation. Science 2006. [Google Scholar] [CrossRef]
  23. Somssich, M.; Je, B.I.; Simon, R.; Jackson, D. CLAVATA-WUSCHEL signaling in the shoot meristem. Development 2016, 143, 3238–3248. [Google Scholar] [CrossRef]
  24. Lopes, F.L.; Galvan-Ampudia, C.; Landrein, B. WUSCHEL in the shoot apical meristem: old player, new tricks. Journal of Experimental Botany 2021, 72, 1527–1535. [Google Scholar] [CrossRef]
  25. Stahl, Y.; Wink, R.H.; Ingram, G.C.; Simon, R. A Signaling module controlling the stem cell niche in Arabidopsis root meristems. Current Biology 2009. [Google Scholar] [CrossRef] [PubMed]
  26. Whitford, R.; Fernandez, A.; De Groodt, R.; Ortega, E.; Hilson, P. Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proceedings of the National Academy of Sciences of the United States of America 2008. [Google Scholar] [CrossRef] [PubMed]
  27. Fukuda, H.; Hirakawa, Y.; Sawa, S. Peptide signaling in vascular development. Current Opinion in Plant Biology 2007. [Google Scholar] [CrossRef] [PubMed]
  28. Gancheva, M.S.; Losev, M.R.; Dodueva, I.E.; Lutova, L.A. Phloem-expressed CLAVATA3/ESR-like genes in Potato. Horticulturae 2023. [Google Scholar] [CrossRef]
  29. Skripnikov, A. Bioassays for Identifying and Characterizing Plant Regulatory Peptides. Biomolecules 2023. [Google Scholar] [CrossRef]
  30. Han, H.; Zhang, G.; Wu, M.; Wang, G. Identification and characterization of the Populus trichocarpa CLE family. BMC Genomics 2016. [CrossRef]
  31. Brumfield, R.T.J.A.J.o.B. cell-lineage studies in root meristems by means of chromosome rearrangements induced by x-rays. Am. J. Bot. 1943, 30, 101–110. [Google Scholar]
  32. Zhang, H.; Mu, Y.; Zhang, H.; Yu, C. Maintenance of stem cell activity in plant development and stress responses. Frontiers in Plant Science 2023. [Google Scholar] [CrossRef]
  33. Lee, Y.; Lee, W.S.; Kim, S.-H. Hormonal regulation of stem cell maintenance in roots. Journal of Experimental Botany 2013, 64, 1153–1165. [Google Scholar] [CrossRef]
  34. Kumpf, R.P.; Nowack, M.K. The root cap: a short story of life and death. Journal of Experimental Botany 2015, 66, 5651–5662. [Google Scholar] [CrossRef]
  35. Dolan, L.; Janmaat, K.; Willemsen, V.; Linstead, P.; Poethig, S.; Roberts, K.; Scheres, B. Cellular organisation of the Arabidopsis thaliana root. Development 1993, 119, 71–84. [Google Scholar] [CrossRef] [PubMed]
  36. Fisher, A.P.; Sozzani, R. Uncovering the networks involved in stem cell maintenance and asymmetric cell division in the Arabidopsis root. Current Opinion in Plant Biology 2015. [Google Scholar] [CrossRef] [PubMed]
  37. Stahl, Y.; Wink, R.H.; Ingram, G.C.; Simon, R. A signaling module controlling the stem cell niche in Arabidopsis root meristems. Current Biology 2009, 19, 909–914. [Google Scholar] [CrossRef] [PubMed]
  38. Olt, P.; Ding, W.; Schulze, W.X.; Ludewig, U. The LaCLE35 peptide modifies rootlet density and length in cluster roots of white lupin. Plant, Cell & Environment. [CrossRef]
  39. Hobe, M.; Müller, R.; Grünewald, M.; Brand, U.; Simon, R. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Development Genes and Evolution 2003. [Google Scholar] [CrossRef]
  40. Gancheva, M.S.; Lutova, L.A. Nitrogen-activated CLV3/ESR-Related 4 (CLE4) regulates shoot, root, and stolon growth in Potato. Plants 2023, 12. [Google Scholar] [CrossRef]
  41. Nakagami, S.; Aoyama, T.; Sato, Y.; Kajiwara, T.; Ishida, T.; Sawa, S. CLE3 and its homologs share overlapping functions in the modulation of lateral root formation through CLV1 and BAM1 in Arabidopsis thaliana. The Plant Journal 2023. [Google Scholar] [CrossRef]
  42. Miwa, H.; Betsuyaku, S.; Iwamoto, K.; Kinoshita, A.; Fukuda, H.; Sawa, S. The receptor-like kinase SOL2 mediates CLE Signaling in Arabidopsis. Plant and Cell Physiology 2008, 49, 1752–1757. [Google Scholar] [CrossRef]
  43. Fiers, M.; Golemiec, E.; Xu, J.; van der Geest, L.; Heidstra, R.; Stiekema, W.; Liu, C.-M. The 14–amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through aCLAVATA2-Dependent Pathway. The Plant Cell 2005, 17, 2542–2553. [Google Scholar] [CrossRef]
  44. Casamitjana-Martínez, E.; Hofhuis, H.F.; Xu, J.; Liu, C.-M.; Heidstra, R.; Scheres, B. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance. Current Biology 2003. [Google Scholar] [CrossRef]
  45. Fiers, M.; Hause, G.; Boutilier, K.; Casamitjana-Martinez, E.; Weijers, D.; Offringa, R.; van der Geest, L.; van Lookeren Campagne, M.; Liu, C.-M. Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. Gene 2004. [Google Scholar] [CrossRef]
  46. Barton, M.K. Twenty years on: The inner workings of the shoot apical meristem, a developmental dynamo. Developmental Biology 2010, 341, 95–113. [Google Scholar] [CrossRef] [PubMed]
  47. Hirakawa, Y. Evolution of meristem zonation by CLE gene duplication in land plants. Nature Plants 2022. [Google Scholar] [CrossRef] [PubMed]
  48. Steffensen, D.M. A reconstruction of cell development in the shoot apex of maize. American Journal of Botany 1968. [Google Scholar] [CrossRef]
  49. Itoh, J.I.; Kitano, H.; Matsuoka, M.; Nagato, Y. Shoot organization genes regulate shoot apical meristem organization and the pattern of leaf primordium initiation in rice. Plant Cell 2000, 12, 2161–2174. [Google Scholar] [CrossRef]
  50. Meyerowitz, E.M. Genetic control of cell division patterns in developing plants. Cell 1997. [Google Scholar] [CrossRef]
  51. Gallois, J.-L.; Woodward, C.; Reddy, G.V.; Sablowski, R. Combined shoot meristemless and WUSCHEL trigger ectopic organogenesis in Arabidopsis. Development 2002. [Google Scholar] [CrossRef]
  52. Vernoux, T.; Autran, D.; Traas, J. Developmental control of cell division patterns in the shoot apex. Plant Molecular Biology 2000. [Google Scholar] [CrossRef]
  53. Fletcher, J.C.; Brand, U.; Running, M.P.; Simon, R.; Meyerowitz, E.M. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristems. Science 1999. [Google Scholar] [CrossRef]
  54. Meyerowitz, E.M. Genetic control of cell division patterns in developing plants. Cell 1997. [CrossRef]
  55. Klaus F., X. Mayer, H.S., Achim Haecker,; Michael Lenhard, G.J.r., and Thomas Laux*. Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell, 1998, Vol. 95, 805–815.
  56. Clark, S.E.; Jacobsen, S.E.; Levin, J.Z.; Meyerowitz, E.M. The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 1996. [Google Scholar] [CrossRef]
  57. Yadav, R.K.; Perales, M.; Gruel, J.; Girke, T.; Jönsson, H.; Reddy, G.V. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex. Genes & Development 2011, 25, 2025–2030. [Google Scholar] [CrossRef]
  58. Su, Y.H.; Zhou, C.; Li, Y.J.; Yu, Y.; Tang, L.P.; Zhang, W.J.; Yao, W.J.; Huang, R.; Laux, T.; Zhang, X.S. Integration of pluripotency pathways regulates stem cell maintenance in the Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences of the United States of America 2020. [Google Scholar] [CrossRef] [PubMed]
  59. Li, R.; Wei, Z.; Li, Y.; Shang, X.; Cao, Y.; Duan, L.; Ma, L. Ski-interacting protein interacts with shoot meristemless to regulate shoot apical meristem formation. Plant Physiology 2022. [Google Scholar] [CrossRef] [PubMed]
  60. Jun, J.; Fiume, E.; Roeder, A.H.K.; Meng, L.; Sharma, V.K.; Osmont, K.S.; Baker, C.; Ha, C.M.; Meyerowitz, E.M.; Feldman, L.J.; et al. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis. Plant Physiology 2010. [Google Scholar] [CrossRef]
  61. Xu, T.-T.; Song, X.-F.; Ren, S.-C.; Liu, C.-M. The sequence flanking the N-terminus of the CLV3 peptide is critical for its cleavage and activity in stem cell regulation in Arabidopsis. BMC Plant Biology 2013. [Google Scholar] [CrossRef]
  62. Hirakawa, Y. CLAVATA3, a plant peptide controlling stem cell fate in the meristem. Peptides 2021. [Google Scholar] [CrossRef]
  63. Su, Y.H.; Zhou, C.; Li, Y.J.; Yu, Y.; Tang, L.P.; Zhang, W.J.; Yao, W.J.; Huang, R.; Laux, T.; Zhang, X.S. Integration of pluripotency pathways regulates stem cell maintenance in the Arabidopsis shoot meristem. Proceedings of the National Academy of Sciences of the United States of America 2020, 117, 22561–22571. [Google Scholar] [CrossRef]
  64. Stuurman, J.; Jäggi, F.; Kuhlemeier, C. Shoot meristem maintenance is controlled by a GRAS-gene mediated signal from differentiating cells. Genes & Development 2002, 16, 2213–2218. [Google Scholar] [CrossRef]
  65. Zhou, Y.; Yan, A.; Han, H.; Li, T.; Geng, Y.; Liu, X.; Meyerowitz, E.M. HAIRY MERISTEM with WUSCHEL confines CLAVATA3 expression to the outer apical meristem layers. Science 2018. [Google Scholar] [CrossRef]
  66. Zhou, Y.; Liu, X.; Engstrom, E.M.; Nimchuk, Z.L.; Pruneda-Paz, J.L.; Tarr, P.T.; Yan, A.; Kay, S.A.; Meyerowitz, E.M. Control of plant stem cell function by conserved interacting transcriptional regulators. Nature 2014. [Google Scholar] [CrossRef]
  67. Han, H.; Liu, X.; Zhou, Y. Transcriptional circuits in control of shoot stem cell homeostasis. Current Opinion in Plant Biology 2019. [Google Scholar] [CrossRef] [PubMed]
  68. Perales, M.; Rodriguez, K.; Snipes, S.; Yadav, R.K.; Diaz-Mendoza, M.; Reddy, G.V. Threshold-dependent transcriptional discrimination underlies stem cell homeostasis Proceedings of the National Academy of Sciences of the United States of America 2016. [CrossRef]
  69. Engstrom, E.M.; Andersen, C.M.; Gumulak-Smith, J.; Hu, J.; Orlova, E.; Sozzani, R.; Bowman, J.L. Arabidopsis homologs of the petunia hairy meristem gene are required for maintenance of shoot and root indeterminacy. Plant Physiology 2010. [Google Scholar] [CrossRef]
  70. Brand, U.; Grünewald, M.; Hobe, M.; Simon, R. Regulation of CLV3 expression by two homeobox genes in Arabidopsis. Plant Physiology 2002. [Google Scholar] [CrossRef] [PubMed]
  71. Brand, *!!! REPLACE !!!*; Fletcher, *!!! REPLACE !!!*; J, C.; Hobe, *!!! REPLACE !!!*; Meyerowitz, *!!! REPLACE !!!*; E, M. Brand; Fletcher; J, C.; Hobe; Meyerowitz; E, M.; Simon. Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science, 2000. [CrossRef]
  72. Hu, C.; Zhu, Y.; Cui, Y.; Cheng, K.; Liang, W.; Wei, Z.; Zhu, M.; Yin, H.; Zeng, L.; Xiao, Y.; et al. A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis. Nature Plants 2018, 4, 205–211. [Google Scholar] [CrossRef]
  73. Wang, Y.; Jiao, Y. Cell signaling in the shoot apical meristem. Plant Physiology 2023. [Google Scholar] [CrossRef]
  74. Clark; S, E. ; Williams; R, W.; Meyerowitz; E, M. The CLAVATA1 gene encodes a putative receptor kinase that controls shoot and floral meristem size in Arabidopsis. Cell 1997. [Google Scholar] [CrossRef]
  75. Nimchuk, Z.L.; Tarr, P.T.; Ohno, C.; Qu, X.; Meyerowitz, E.M. Plant stem cell signaling involves ligand-dependent trafficking of the CLAVATA1 receptor kinase. Current Biology 2011. [Google Scholar] [CrossRef]
  76. Ogawa, M.; Shinohara, H.; Sakagami, Y.; Matsubayashi, Y. Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 2008. [Google Scholar] [CrossRef]
  77. Ni, J.U.N.; Clark, S.E. CHAPTER 3 - CLAVATA3: A putative peptide ligand controlling Arabidopsis stem cell specification. In Handbook of Biologically Active Peptides, Kastin, A.J., Ed.; Academic Press: Burlington, 2006; pp. 9–15. [Google Scholar]
  78. Julie, M. Stone2, Amy E. Trotochaud2, John C. Walker, and Steven E. Clark. Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions. Plant Physiology, 1998, 1217±1225.
  79. Nimchuk, Z.L.; Tarr, P.T.; Meyerowitz, E.M. An evolutionarily conserved pseudokinase mediates stem cell production in plants. The Plant Cell 2011. [Google Scholar] [CrossRef]
  80. Bleckmann, A.; Weidtkamp-Peters, S.; Seidel, C.A.M.; Simon, R. Stem Cell Signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiology 2010, 152, 166–176. [Google Scholar] [CrossRef]
  81. Sangho Jeong, A.E.T. , and Steven E. Clark1. The Arabidopsis CLAVATA2 gene encodes a receptor-like protein required for the stability of the CLAVATA1 receptor-like kinase. Cell, 1999, 1925–1933.
  82. Müller, R.; Bleckmann, A.; Simon, R.d. The receptor kinase CORYNE of Arabidopsis transmits the stem cell–limiting signal CLAVATA3 independently of CLAVATA1. The Plant Cell 2008, 20, 934–946. [Google Scholar] [CrossRef] [PubMed]
  83. Diévart, A.; Dalal, M.; Tax, F.E.; Lacey, A.D.; Huttly, A.; Li, J.; Clark, S.E. CLAVATA1 dominant-negative alleles reveal functional overlap between multiple receptor kinases that regulate meristem and organ development. The Plant Cell 2003, 15, 1198–1211. [Google Scholar] [CrossRef]
  84. Mizuno, S.; Osakabe, Y.; Maruyama, K.; Ito, T.; Osakabe, K.; Sato, T.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Receptor-like protein kinase 2 (RPK 2) is a novel factor controlling anther development in Arabidopsis thaliana. The Plant Journal 2007, 50, 751–766. [Google Scholar] [CrossRef] [PubMed]
  85. Betsuyaku, S.; Takahashi, F.; Kinoshita, A.; Miwa, H.; Shinozaki, K.; Fukuda, H.; Sawa, S. Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis. Plant and Cell Physiology 2011, 52, 14–29. [Google Scholar] [CrossRef] [PubMed]
  86. Shinohara, H.; Matsubayashi, Y. 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. The Plant Journal 2015, 82, 328–336. [Google Scholar] [CrossRef]
  87. DeYoung, B.J.; Bickle, K.L.; Schrage, K.J.; Muskett, P.; Patel, K.; Clark, S.E. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. The Plant Journal 2006. [Google Scholar] [CrossRef]
  88. Guo, Y.; Han, L.; Hymes, M.; Denver, R.; Clark, S.E. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. The Plant Journal 2010. [Google Scholar] [CrossRef]
  89. Lee, H.; Jun, Y.S.; Cha, O.-K.; Sheen, J. Mitogen-activated protein kinases MPK3 and MPK6 are required for stem cell maintenance in the Arabidopsis shoot apical meristem. Plant Cell Reports 2018, 38, 311–319. [Google Scholar] [CrossRef]
  90. Yu LP, M.A. , Clark SE. Poltergeist encodes a PROTEIN PHOSPHATASE 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems. Current Biology, 2003, 13(13):179-188.
  91. Chaffey, N. Esau's Plant anatomy, meristems, cells, and tissues of the plant body: their structure, function, and development. 3rd edn. Annals of Botany 2006. [Google Scholar] [CrossRef]
  92. Du, J.; Wang, Y.; Chen, W.; Xu, M.; Zhou, R.; Shou, H.; Chen, J. High-resolution anatomical and spatial transcriptome analyses reveal two types of meristematic cell pools within the secondary vascular tissue of poplar stem. Molecular Plant 2023. [Google Scholar] [CrossRef]
  93. Larson, P.R. Procambium vs. Cambium and Protoxylem vs. Metaxylem in Populus deltoides seedlings. American Journal of Botany 1976, 63, 1332–1348. [Google Scholar] [CrossRef]
  94. Lucas, W.J.; Groover, A.; Lichtenberger, R.; Furuta, K.; Yadav, S.-R.; Helariutta, Y.; He, X.-Q.; Fukuda, H.; Kang, J.; Brady, S.M.; et al. The plant vascular system: evolution, development and functions. Journal of Integrative Plant Biology 2013. [Google Scholar] [CrossRef] [PubMed]
  95. Etchells, J.P.; Turner, S.R. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 2010. [Google Scholar] [CrossRef] [PubMed]
  96. Hirakawa, Y.; Shinohara, H.; Kondo, Y.; Inoue, A.; Nakanomyo, I.; Ogawa, M.; Sawa, S.; Ohashi-Ito, K.; Matsubayashi, Y.; Fukuda, H. Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proceedings of the National Academy of Sciences of the United States of America 2008. [Google Scholar] [CrossRef]
  97. Kondo, Y.; Ito, T.; Nakagami, H.; Hirakawa, Y.; Saito, M.; Tamaki, T.; Shirasu, K.; Fukuda, H. Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling. Nature Communications 2014. [Google Scholar] [CrossRef]
  98. Zhang, Y.; Chen, S.; Xu, L.; Chu, S.; Yan, X.; Lin, L.; Wen, J.; Zheng, B.; Chen, S.; Li, Q. Transcription factor PagMYB31 positively regulates cambium activity and negatively regulates xylem development in poplar. The Plant Cell 2024. [Google Scholar] [CrossRef]
  99. Han, S.; Cho, H.; Noh, J.; Qi, J.; Jung, H.-J.; Nam, H.; Lee, S.; Hwang, D.; Greb, T.; Hwang, I. BIL1-mediated MP phosphorylation integrates PXY and cytokinin signalling in secondary growth. Nature Plants 2018. [Google Scholar] [CrossRef]
  100. Etchells, J.P.; Turner, S.R. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 2010, 137, 767–774. [Google Scholar] [CrossRef]
  101. Zhu, Y.; Song, D.; Zhang, R.; Luo, L.; Cao, S.; Huang, C.; Sun, J.; Gui, J.; Li, L. A xylem-produced peptide PtrCLE20 inhibits vascular cambium activity in Populus. Plant Biotechnology Journal 2019. [Google Scholar] [CrossRef]
  102. Kucukoglu, M.; Chaabouni, S.; Zheng, B.; Mähönen, A.P.; Helariutta, Y.; Nilsson, O. Peptide encoding Populus CLV3/ESR-RELATED 47 (PtCLE47) promotes cambial development and secondary xylem formation in hybrid aspen. New Phytologist 2019. [Google Scholar] [CrossRef]
  103. Song, X.-F.; Hou, X.-L.; Liu, C.-M. CLE peptides: critical regulators for stem cell maintenance in plants. Planta 2021. [Google Scholar] [CrossRef] [PubMed]
  104. Bauby, H.; Divol, F.; Truernit, E.; Grandjean, O.; Palauqui, J.-C. Protophloem differentiation in early Arabidopsis thaliana development. Plant & Cell Physiology, 2007. [CrossRef]
  105. Qian, P.; Song, W.; Yokoo, T.; Minobe, A.; Wang, G.; Ishida, T.; Sawa, S.; Chai, J.; Kakimoto, T. The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors. Nature Plants 2018, 4, 1071–1081. [Google Scholar] [CrossRef] [PubMed]
  106. Carbonnel, S.; Cornelis, S.; Hazak, O. The CLE33 peptide represses phloem differentiation via autocrine and paracrine signaling in Arabidopsis. Communications Biology 2023. [Google Scholar] [CrossRef] [PubMed]
  107. Ren, S.-C.; Song, X.-F.; Chen, W.-Q.; Lu, R.; Lucas, W.J.; Liu, C.-M. CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex. Journal of Integrative Plant Biology 2019. [Google Scholar] [CrossRef]
  108. Anne, P.; Amiguet-Vercher, A.; Brandt, B.; Kalmbach, L.; Geldner, N.; Hothorn, M.; Hardtke, C.S. CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis. Development 2018. [Google Scholar] [CrossRef]
  109. Depuydt, S.; Rodriguez-Villalon, A.; Santuari, L.; Wyser-Rmili, C.; Ragni, L.; Hardtke, C.S. Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3. Proceedings of the National Academy of Sciences of the United States of America 2013, 110, 7074–7079. [Google Scholar] [CrossRef]
  110. Kang, Y.H.; Hardtke, C.S. Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling. EMBO reports. 2016, 17, 1145-1154-1154. [CrossRef]
  111. Hang, Z.; Qian, W.; Noel, B.-T.; Christian, S.H. Antagonistic CLE peptide pathways shape root meristem tissue patterning. Nature Plants 2024. [Google Scholar] [CrossRef]
  112. Qian, P.; Song, W.; Zaizen-Iida, M.; Kume, S.; Wang, G.; Zhang, Y.; Kinoshita-Tsujimura, K.; Chai, J.; Kakimoto, T. A Dof-CLE circuit controls phloem organization. Nature Plants 2022. [Google Scholar] [CrossRef]
  113. Araya, T.; Miyamoto, M.; Wibowo, J.; Suzuki, A.; Kojima, S.; Tsuchiya, Y.N.; Sawa, S.; Fukuda, H.; von Wirén, N.; Takahashi, H. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proceedings of the National Academy of Sciences 2014, 111, 2029–2034. [Google Scholar] [CrossRef]
  114. Pazourek, J. T.A. Steeves & I.M. Sussex patterns in plant development. Folia Geobotanica et Phytotaxonomica 1992, 27, 136–136. [Google Scholar] [CrossRef]
  115. Berná, G.; Robles, P.; Micol, J.L. A mutational analysis of leaf morphogenesis in Arabidopsis thaliana. GENETICS 1999. [Google Scholar] [CrossRef] [PubMed]
  116. Pillitteri, L.J.; Torii, K.U. Mechanisms of stomatal development. Annual Review of Plant Biology 2012. [Google Scholar] [CrossRef]
  117. Geisler, M.; Nadeau, J.; Sack, F.D. Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. The Plant Cell 2000. [Google Scholar] [CrossRef] [PubMed]
  118. Cho, K.H.; Jun, S.E.; Jeong, S.J.; Lee, Y.K.; Kim, G.T. Developmental processes of leaf morphogenesis in Arabidopsis. Journal of Plant Biology 2007, 50, 282–290. [Google Scholar] [CrossRef]
  119. Kalve, S.; De Vos, D.; Beemster, G.T.S. Leaf development: a cellular perspective. Frontiers in Plant Science 2014. [Google Scholar] [CrossRef]
  120. Bennett, T.; Hines, G.; van Rongen, M.; Waldie, T.; Sawchuk, M.G.; Scarpella, E.; Ljung, K.; Leyser, O. Connective auxin transport in the shoot facilitates communication between shoot apices. PLOS Biology 2016. [Google Scholar] [CrossRef]
  121. de Reuille, P.B.; Bohn-Courseau, I.; Ljung, K.; Morin, H.; Carraro, N.; Godin, C.; Traas, J. Computer simulations reveal properties of the cell-cell signaling network at the shoot apex in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 2006. [Google Scholar] [CrossRef]
  122. Vidaurre, D.P.; Ploense, S.; Krogan, N.T.; Berleth, T. AMP1 and MP antagonistically regulate embryo and meristem development in Arabidopsis. Development 2007. [Google Scholar] [CrossRef]
  123. Zhao, Z.; Andersen, S.U.; Ljung, K.; Dolezal, K.; Miotk, A.; Schultheiss, S.J.; Lohmann, J.U. Hormonal control of the shoot stem-cell niche. Nature 2010. [Google Scholar] [CrossRef]
  124. Rademacher, E.H.; Möller, B.; Lokerse, A.S.; Llavata-Peris, C.I.; van den Berg, W.; Weijers, D. A cellular expression map of the Arabidopsis AUXIN RESPONSE FACTOR gene family. The Plant Journal 2011. [Google Scholar] [CrossRef] [PubMed]
  125. Lv, Z.; Zhao, W.; Kong, S.; Li, L.; Lin, S. Overview of molecular mechanisms of plant leaf development: a systematic review. Frontiers in Plant Science 2023. [Google Scholar] [CrossRef] [PubMed]
  126. DiGennaro, P.; Grienenberger, E.; Dao, T.Q.; Jun, J.H.; Fletcher, J.C. Peptide signaling molecules CLE5 and CLE6 affect Arabidopsis leaf shape downstream of leaf patterning transcription factors and auxin. Plant Direct 2018. [Google Scholar] [CrossRef] [PubMed]
  127. Zhang, Y.; Tan, S.; Gao, Y.; Kan, C.; Wang, H.-L.; Yang, Q.; Xia, X.; Ishida, T.; Sawa, S.; Guo, H.; et al. CLE42 delays leaf senescence by antagonizing ethylene pathway in Arabidopsis. New Phytologist 2022. [Google Scholar] [CrossRef]
  128. Han, H.; Zhuang, K.; Qiu, Z. CLE peptides join the plant longevity club. Trends in Plant Science 2022. [Google Scholar] [CrossRef]
  129. Zhang, Z.; Liu, C.; Li, K.; Li, X.; Xu, M.; Guo, Y. CLE14 functions as a “brake signal” to suppress age-dependent and stress-induced leaf senescence by promoting JUB1-mediated ROS scavenging in Arabidopsis. Molecular Plant 2021. [Google Scholar] [CrossRef]
  130. Dennis, L.; Peacock, J. Genes directing flower development in Arabidopsis. The Plant Cell 2019. [Google Scholar] [CrossRef]
  131. Zheng, Y.; Zhang, K.; Guo, L.; Liu, X.; Zhang, Z. AUXIN RESPONSE FACTOR3 plays distinct role during early flower development. Plant Signaling & Behavior, 2018. [CrossRef]
  132. Nakajima, K.; Benfey, P.N. Signaling in and out: control of cell division and differentiation in the shoot and root. The Plant Cell 2002. [Google Scholar] [CrossRef]
  133. Takeda, S.; Iwasaki, A.; Matsumoto, N.; Uemura, T.; Tatematsu, K.; Okada, K. Physical interaction of floral organs controls petal morphogenesis in Arabidopsis. Plant Physiology 2013, 161, 1242–1250. [Google Scholar] [CrossRef]
  134. Liu, H.; Yang, L.; Tu, Z.; Zhu, S.; Zhang, C.; Li, H. Genome-wide identification of MIKC-type genes related to stamen and gynoecium development in Liriodendron. Scientific Reports 2021. [Google Scholar] [CrossRef]
  135. Jones, D.S.; John, A.; VanDerMolen, K.R.; Nimchuk, Z.L. CLAVATA signaling ensures reproductive development in plants across thermal environments. Current Biology 2021, 31, 220–227.e225. [Google Scholar] [CrossRef] [PubMed]
  136. Kayes JM, C.S. CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development, 1998, 125(119):3843-3851. [CrossRef]
  137. Steven, E. Clark, M.P. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development, 1995, 121 (127): 2057–2067. [CrossRef]
  138. Nidhi, S.; Preciado, J.; Tie, L. Knox homologs shoot meristemless (STM) and KNAT6 are epistatic to CLAVATA3 (CLV3) during shoot meristem development in Arabidopsis thaliana. Molecular Biology Reports 2021, 48, 6291–6302. [Google Scholar] [CrossRef] [PubMed]
  139. Box, M.S.; Huang, B.E.; Domijan, M.; Jaeger, K.E.; Khattak, A.K.; Yoo, S.J.; Sedivy, E.L.; Jones, D.M.; Hearn, T.J.; Webb, A.A.R.; et al. ELF3 Controls thermoresponsive growth in Arabidopsis. Current Biology 2014. [Google Scholar] [CrossRef] [PubMed]
  140. Jung, J.-H.; Barbosa, A.D.; Hutin, S.; Kumita, J.R.; Gao, M.; Derwort, D.; Silva, C.S.; Lai, X.; Pierre, E.; Geng, F.; et al. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 2020. [Google Scholar] [CrossRef]
  141. Lindsay, R.J.; Stelzl, L.S.; Pietrek, L.; Hummer, G.; Wigge, P.A.; Hanson, S.M. Helical region near poly-Q tract in prion-like domain of Arabidopsis ELF3 plays role in temperature-sensing mechanism. Biophysical Journal 2022. [Google Scholar] [CrossRef]
  142. Cheng, Y.; Dai, X.; Zhao, Y. Auxin biosynthesis by the YUCCA flavin monooxygenases controls the formation of floral organs and vascular tissues in Arabidopsis. Genes & development 2006, 20, 1790–1799. [Google Scholar] [CrossRef]
  143. Rodriguez-Leal, D.; Xu, C.; Kwon, C.-T.; Soyars, C.; Demesa-Arevalo, E.; Man, J.; Liu, L.; Lemmon, Z.H.; Jones, D.S.; Van Eck, J.; et al. Evolution of buffering in a genetic circuit controlling plant stem cell proliferation. Nature Genetics 2019, 51, 786–792. [Google Scholar] [CrossRef]
  144. John, A.; Smith, E.S.; Jones, D.S.; Soyars, C.L.; Nimchuk, Z.L. A network of CLAVATA receptors buffers auxin-dependent meristem maintenance. Nature Plants 2023, 9, 1306–1317. [Google Scholar] [CrossRef]
  145. Bashyal, S.; Gautam, C.K.; Müller, L.M. CLAVATA signaling in plant–environment interactions. Plant Physiology 2023. [Google Scholar] [CrossRef]
  146. Diss, G.; Ascencio, D.; DeLuna, A.; Landry, C.R. Molecular mechanisms of paralogous compensation and the robustness of cellular networks. Journal of Experimental Zoology Part B: Molecular and Developmental Evolution 2013, 322, 488–499. [Google Scholar] [CrossRef]
  147. Hanada, K.; Sawada, Y.; Kuromori, T.; Klausnitzer, R.; Saito, K.; Toyoda, T.; Shinozaki, K.; Li, W.H.; Hirai, M.Y. Functional compensation of primary and secondary metabolites by duplicate genes in Arabidopsis thaliana. Molecular Biology and Evolution 2010, 28, 377–382. [Google Scholar] [CrossRef] [PubMed]
  148. Moens, C.; El-Brolosy, M.A.; Stainier, D.Y.R. Genetic compensation: A phenomenon in search of mechanisms. PLOS Genetics 2017, 13. [Google Scholar] [CrossRef]
  149. Goad, D.M.; Zhu, C.; Kellogg, E.A. Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function. New Phytologist 2016. [Google Scholar] [CrossRef] [PubMed]
  150. Dao, T.Q.; Weksler, N.; Liu, H.M.H.; Leiboff, S.; Fletcher, J.C. Interactive CLV3, CLE16, and CLE17 signaling mediates stem cell homeostasis in the Arabidopsis shoot apical meristem. Development 2022. [Google Scholar] [CrossRef]
  151. Nimchuk, Z.L.; Zhou, Y.; Tarr, P.T.; Peterson, B.A.; Meyerowitz, E.M. Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases. Development 2015, 142, 1043–1049. [Google Scholar] [CrossRef]
  152. Shimizu, N.; Ishida, T.; Yamada, M.; Shigenobu, S.; Tabata, R.; Kinoshita, A.; Yamaguchi, K.; Hasebe, M.; Mitsumasu, K.; Sawa, S. BAM 1 and RECEPTOR-LIKE PROTEIN KINASE 2 constitute a signaling pathway and modulate CLE peptide-triggered growth inhibition in Arabidopsis root. New Phytologist 2015. [Google Scholar] [CrossRef]
  153. Ni, J.; Clark, S.E. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiology 2006. [Google Scholar] [CrossRef]
  154. Wulf, K.; Sun, J.; Wang, C.; Ho-Plagaro, T.; Kwon, C.-T.; Velandia, K.; Correa-Lozano, A.; Tamayo-Navarrete, M.I.; Reid, J.B.; García Garrido, J.M.; et al. The role of CLE peptides in suppression of mycorrhizal colonisation of tomato. Plant & Cell Physiology, 2023. [CrossRef]
  155. Liu, L.; Gallagher, J.; Arevalo, E.D.; Chen, R.; Skopelitis, T.; Wu, Q.; Bartlett, M.; Jackson, D. Enhancing grain-yield-related traits by CRISPR–Cas9 promoter editing of maize CLE genes. Nature Plants 2021, 7, 287–294. [Google Scholar] [CrossRef]
  156. Selby, R.; Jones, D.S. Complex peptide hormone signaling in plant stem cells. Current Opinion in Plant Biology 2023. [Google Scholar] [CrossRef]
  157. Strabala, T.J.; Phillips, L.; West, M.; Stanbra, L. Bioinformatic and phylogenetic analysis of the CLAVATA3/EMBRYO-SURROUNDING REGION (CLE) and the CLE-LIKE signal peptide genes in the Pinophyta. BMC Plant Biology 2014. [Google Scholar] [CrossRef]
  158. Zhang, Z.; Liu, L.; Kucukoglu, M.; Tian, D.; Larkin, R.M.; Shi, X.; Zheng, B. Predicting and clustering plant CLE genes with a new method developed specifically for short amino acid sequences. BMC Genomics 2020, 21(1), 709. [Google Scholar] [CrossRef]
Preprints 153103 g001
Figure 1. The regulatory network map of the CLE family in plant meristems. Fig A. Summarize the mechanism model of root cell maintenance and differentiation in the root of CLE family. Thick line segment: SCN; Arrow: Ligand reception/receptor activation; Blunt arrow: depressed. Fig. B. The Arabidopsis SAM are divided L1/epidermis, L2/sub-epidermis and Corpus/L3. The same Arabidopsis SAM is divided into distinct zones, including CZ, PZ, OC and RM (Refer to: Han et al.,2020). Fig. C.WUS-CLV3-STM regulatory circuits involved in peptide hormones and receptor kinases in SAM. In the rectangular box of the picture, the following is drawn the CLV3-WUS regulatory pathway（Refer to: Hirakawa et al.,2010）Arrow: Ligand reception/receptor activation; Blunt arrow. Fig D. CLE genes transcription control and receptor-ligand signaling are involved in the balance between procambium, phloem and xylem maintenance in stem and root. Arrow: Ligand reception/receptor activation; Blunt arrow: depressed. Fig. E. The regulatory pathway of CLE family genes between petiole and stomata in leaf epidermis. Arrow: Ligand reception/receptor activation; Blunt arrow: depressed. Fig. F. The pathway and ambient temperature of CLV3-CLV1 act on auxin synthesis and control the growth of flower primordium at different temperatures. Arrow: Ligand reception/receptor activation; Blunt arrow: depressed (Refer to: Yufang Wen et al.,2023).
Figure 1. The regulatory network map of the CLE family in plant meristems. Fig A. Summarize the mechanism model of root cell maintenance and differentiation in the root of CLE family. Thick line segment: SCN; Arrow: Ligand reception/receptor activation; Blunt arrow: depressed. Fig. B. The Arabidopsis SAM are divided L1/epidermis, L2/sub-epidermis and Corpus/L3. The same Arabidopsis SAM is divided into distinct zones, including CZ, PZ, OC and RM (Refer to: Han et al.,2020). Fig. C.WUS-CLV3-STM regulatory circuits involved in peptide hormones and receptor kinases in SAM. In the rectangular box of the picture, the following is drawn the CLV3-WUS regulatory pathway（Refer to: Hirakawa et al.,2010）Arrow: Ligand reception/receptor activation; Blunt arrow. Fig D. CLE genes transcription control and receptor-ligand signaling are involved in the balance between procambium, phloem and xylem maintenance in stem and root. Arrow: Ligand reception/receptor activation; Blunt arrow: depressed. Fig. E. The regulatory pathway of CLE family genes between petiole and stomata in leaf epidermis. Arrow: Ligand reception/receptor activation; Blunt arrow: depressed. Fig. F. The pathway and ambient temperature of CLV3-CLV1 act on auxin synthesis and control the growth of flower primordium at different temperatures. Arrow: Ligand reception/receptor activation; Blunt arrow: depressed (Refer to: Yufang Wen et al.,2023).
Preprints 153103 g001
Preprints 153103 g002
Figure 2. Evolutionary analysis of the CLE gene family in multiple species. Fig A. Select 10 representative species spanning from lower to higher organisms, and construct a CLE motif map based on the conserved regions of 12 amino acids. (The protein sequences were obtained from NCBI (supplement table) and draw the CLE motif map by using the online software webLogo (http://weblogo.berkeley.eduMogo.cgi)). Fig B. Phylogenetic tree analysis of CLE protein families. Relationship of CLE proteins with homologs from other important plant species was constructed using the MEGA 11 program, after aligning the protein sequences with MUSCLE. The phylogenetic tree analysis revealed distinct clusters, denoted as Cluster I, Cluster II, Cluster III, Cluster Ⅳ, Cluster Ⅴ, Cluster Ⅵ, Cluster Ⅶ and Cluster Ⅷ.
Figure 2. Evolutionary analysis of the CLE gene family in multiple species. Fig A. Select 10 representative species spanning from lower to higher organisms, and construct a CLE motif map based on the conserved regions of 12 amino acids. (The protein sequences were obtained from NCBI (supplement table) and draw the CLE motif map by using the online software webLogo (http://weblogo.berkeley.eduMogo.cgi)). Fig B. Phylogenetic tree analysis of CLE protein families. Relationship of CLE proteins with homologs from other important plant species was constructed using the MEGA 11 program, after aligning the protein sequences with MUSCLE. The phylogenetic tree analysis revealed distinct clusters, denoted as Cluster I, Cluster II, Cluster III, Cluster Ⅳ, Cluster Ⅴ, Cluster Ⅵ, Cluster Ⅶ and Cluster Ⅷ.
Preprints 153103 g002
Preprints 153103 g003
Figure 3. The position where the CLE family performs its own functions throughout the development of Meristem in plants. Different colors represent different genes.
Figure 3. The position where the CLE family performs its own functions throughout the development of Meristem in plants. Different colors represent different genes.
Preprints 153103 g003
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.
Copyright: This open access article is published under a Creative Commons CC BY 4.0 license, which permit the free download, distribution, and reuse, provided that the author and preprint are cited in any reuse.

Downloads

48

Views

24

Comments

0

Subscription

Notify me about updates to this article or when a peer-reviewed version is published.

Email

Prerpints.org logo

Preprints.org is a free preprint server supported by MDPI in Basel, Switzerland.

facebook logotwitter logolinkedin logo
MDPI Initiatives
Important Links
Subscribe

Disclaimer

Terms of Use

Privacy Policy

© 2025 MDPI (Basel, Switzerland) unless otherwise stated