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The ability of plants to grow and form organs throughout their lifetime is dependent on their sustained stem cell activity. These stem cell populations are maintained by intricate networks of intercellular signaling pathways. In Arabidopsis thaliana, the small secreted peptide CLAVATA3 (CLV3) controls shoot apical meristem (SAM) maintenance by activating a signal transduction pathway that modulates the expression of the homeodomain transcription factor WUSCHEL (WUS). Here, we demonstrate that two CLV3-related peptides, CLE16 and CLE17, restrict stem cell accumulation in the absence of CLV3. CLE16 and CLE17 contribute independently to SAM maintenance and organ production in clv3 plants at all stages of development. We show that CLE16 and CLE17 signal through a subset of CLV3 receptors, the BARELY ANY MERISTEM (BAM) receptor kinases, and act upstream of WUS. Our study reveals that CLE16 and CLE17 function in a mechanism that partially compensates for CLV3 to maintain stem cell homeostasis and plant resiliency, and expands the potential targets for enhancing yield traits in crop species.

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. 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. 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. 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. 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.

The shoot apical meristem produces all of the leaves, stems and flowers of a flowering plant from a reservoir of stem cells at its growing tip. In Arabidopsis, the small polypeptide signaling molecule CLAVATA3 (CLV3), a member of the CLV3/EMBRYO SURROUNDING REGION-RELATED (CLE) gene family, is a key component of a negative feedback loop that maintains stem cell activity in shoot and floral meristems throughout development. Because in some plant species multiple CLE genes are involved in regulating shoot apical meristem activity, we tested the hypothesis that CLE genes other than CLV3 might function in stem cell homeostasis in Arabidopsis. We identified three Arabidopsis CLE genes expressed in the post-embryonic shoot apical meristem, generated loss-of-function alleles using genome editing, and analyzed the meristem phenotypes of the resulting mutant plants. We found that null mutations in CLE16, CLE17 or CLE27 affected neither vegetative nor reproductive shoot meristem activity under normal growth conditions, although CLE27 appears to slightly prolong vegetative growth. Our results indicate that the CLE16, CLE17 and CLE27 genes have largely redundant roles in the Arabidopsis shoot apical meristem and/or regulate meristem activity only under specific environmental conditions.

Intercellular signaling mediated by small peptides is critical to coordinate organ formation in animals, but whether extracellular polypeptides play similar roles in plants is unknown. Here we describe a role in Arabidopsis leaf development for two members of the CLAVATA3/ESR‐RELATED peptide family, CLE5 and CLE6, which lie adjacent to each other on chromosome 2. Uniquely among the CLE genes, CLE5 and CLE6 are expressed specifically at the base of developing leaves and floral organs, adjacent to the boundary with the shoot apical meristem. During vegetative development CLE5 and CLE6 transcription is regulated by the leaf patterning transcription factors BLADE‐ON‐PETIOLE1 (BOP1) and ASYMMETRIC LEAVES2 (AS2), as well as by the WUSCHEL‐RELATED HOMEOBOX (WOX) transcription factors WOX1 and PRESSED FLOWER (PRS). Moreover, CLE5 and CLE6 transcript levels are differentially regulated in various genetic backgrounds by the phytohormone auxin. Analysis of loss‐of‐function mutations generated by genome engineering reveals that CLE5 and CLE6 independently and together have subtle effects on rosette leaf shape. Our study indicates that the CLE5 and CLE6 peptides function downstream of leaf patterning factors and phytohormones to modulate the final leaf morphology.