4.7 Review

CLE peptides: critical regulators for stem cell maintenance in plants

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Review Cell Biology

Evolution of CLE peptide signalling

C. D. Whitewoods

Summary: CLEs are small non-cell autonomous signalling peptides that regulate cell division rate and orientation in various developmental contexts in plants. They play important roles across the whole plant, controlling stem cell division, developmental investment, leaf development, stomatal patterning, and axillary branching. Additionally, they have been utilized by parasitic nematodes to mediate infection.

SEMINARS IN CELL & DEVELOPMENTAL BIOLOGY (2021)

Review Plant Sciences

WOX going on: CLE peptides in plant development

Andrew C. Willoughby et al.

Summary: This review discusses recent advances in CLE signaling, showing that CLE pathways are conserved in plants, regulate stem cell identity and cell division in root tissues, and have connections to auxin biosynthesis in regulating flower and leaf development.

CURRENT OPINION IN PLANT BIOLOGY (2021)

Article Developmental Biology

ERECTA family signaling constrains CLAVATA3 and WUSCHEL to the center of the shoot apical meristem

Liang Zhang et al.

Summary: The shoot apical meristem is a crucial reservoir of stem cells in plants, with its size regulated by a balance of stem cell replenishment and cell incorporation into organ primordia. The WUS/CLV negative feedback loop plays a central role in SAM size regulation, depending on accurate spatial expression of WUS and CLV3. A signaling pathway involving ERf receptors and EPFL ligands restricts SAM width and promotes leaf initiation by inhibiting the expression of WUS and CLV3 in the periphery and confining them to the center of the SAM.

DEVELOPMENT (2021)

Article Multidisciplinary Sciences

Functional analysis of the cotton CLE polypeptide signaling gene family in plant growth and development

Ke Wan et al.

Summary: The CLE gene family encodes important short peptide hormones involved in plant shoot apical meristem division and root and vascular bundle development regulation. Studies on the GhCLE gene family in cotton show functional conservation in apical shoot development regulation.

SCIENTIFIC REPORTS (2021)

Article Plant Sciences

Genome-wide identification of CLE gene family and their potential roles in bolting and fruit bearing in cucumber (Cucumis sativus L.)

Nannan Qin et al.

Summary: Signal peptides play vital roles in plant growth and development, with CLE genes being crucial in maintaining the balance between cell proliferation and differentiation. A total of 26 CLE genes were identified in Chinese long '9930' cucumber, showing close relationships with Arabidopsis and melon. Specific expression of these genes was observed in different growth stages, and the overexpression of the representative gene CLV3 in Arabidopsis affected bolting and fruit bearing in cucumber.

BMC PLANT BIOLOGY (2021)

Article Biochemistry & Molecular Biology

In vitro and in vivo activity analysis of poplar CLE dodecapeptides that are most divergent from Arabidopsis counterparts

Yawen Song et al.

Summary: Intercellular communication mediated by the plant-specific CLE family members is a fundamental mechanism coordinating the development of plant bodies, with sequence variations in CLE peptides affecting their functional characteristics.

PLANT SCIENCE (2021)

Article Multidisciplinary Sciences

Structural variation at the maize WUSCHEL1 locus alters stem cell organization in inflorescences

Zongliang Chen et al.

Summary: The study reveals the crucial role of ZmWUS1 in WUSCHEL function in maize, and demonstrates how structural variation can impact plant morphology. Structural variations in plant genomes are significant drivers of crop domestication and productivity, affecting important traits for crop improvement.

NATURE COMMUNICATIONS (2021)

Article Plant Sciences

An Evolutionarily Conserved Coreceptor Gene Is Essential for CLAVATA Signaling in Marchantia polymorpha

Go Takahashi et al.

Summary: Research has shown that peptide hormones MpCLE1 and MpCLE2 in Marchantia polymorpha play crucial roles in cell division and sexual reproduction by interacting with specific receptors at the apical meristem. Compared to other plants, Marchantia polymorpha possesses a minimal set of CLE family peptides, exhibiting higher conservation in evolutionary terms.

FRONTIERS IN PLANT SCIENCE (2021)

Review Biochemistry & Molecular Biology

CLAVATA3, a plant peptide controlling stem cell fate in the meristem

Yuki Hirakawa

Summary: CLAVATA3 (CLV3) is a peptide signal regulating meristem homeostasis and floral organ numbers in plants, with homologs widely conserved in land plants. Studies have shown the involvement of leucin-rich repeat receptor-like kinases (LRR-RLKs) in CLV3 signaling, although the full mechanisms are still largely unknown. Recent research on bryophyte model species offers insights into the evolution and ancestral function of CLV signaling.

PEPTIDES (2021)

Article Biotechnology & Applied Microbiology

A xylem-produced peptide PtrCLE20 inhibits vascular cambium activity in Populus

Yingying Zhu et al.

PLANT BIOTECHNOLOGY JOURNAL (2020)

Article Multidisciplinary Sciences

RGF1 controls root meristem size through ROS signalling

Masashi Yamada et al.

NATURE (2020)

Article Plant Sciences

Peptide Signaling Pathways in Vascular Differentiation([OPEN])

Hiroo Fukuda et al.

PLANT PHYSIOLOGY (2020)

Article Plant Sciences

CLE40 Signaling Regulates Root Stem Cell Fate(1)

Barbara Berckmans et al.

PLANT PHYSIOLOGY (2020)

Article Biochemistry & Molecular Biology

Local and Systemic Effects of Brassinosteroid Perception in Developing Phloem

Moritz Graeff et al.

CURRENT BIOLOGY (2020)

Review Plant Sciences

Recent Advances in Arabidopsis CLE Peptide Signaling

Jennifer C. Fletcher

TRENDS IN PLANT SCIENCE (2020)

Article Biochemistry & Molecular Biology

Induction of Multichotomous Branching by CLAVATA Peptide in Marchantia polymorpha

Yuki Hirakawa et al.

CURRENT BIOLOGY (2020)

Article Multidisciplinary Sciences

Plant stem-cell organization and differentiation at single-cell resolution

James W. Satterlee et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2020)

Article Genetics & Heredity

Evolution of buffering in a genetic circuit controlling plant stem cell proliferation

Daniel Rodriguez-Leal et al.

NATURE GENETICS (2019)

Review Plant Sciences

Sulfated plant peptide hormones

Christine Kaufmann et al.

JOURNAL OF EXPERIMENTAL BOTANY (2019)

Article Biochemistry & Molecular Biology

A Cellular Insulator against CLE45 Peptide Signaling

Alice S. Breda et al.

CURRENT BIOLOGY (2019)

Article Biochemistry & Molecular Biology

Identification and Functional Analysis of the CLAVATA3/EMBRYO SURROUNDING REGION (CLE) Gene Family in Wheat

Zheng Li et al.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2019)

Review Plant Sciences

Cytokinin and CLE signaling are highly intertwined developmental regulators across tissues and species

Joseph Cammarata et al.

CURRENT OPINION IN PLANT BIOLOGY (2019)

Review Plant Sciences

Look Closely, the Beautiful May Be Small: Precursor-Derived Peptides in Plants

Vilde Olsson et al.

ANNUAL REVIEW OF PLANT BIOLOGY, VOL 70 (2019)

Article Biochemistry & Molecular Biology

CLAVATA Was a Genetic Novelty for the Morphological Innovation of 3D Growth in Land Plants

Chris D. Whitewoods et al.

CURRENT BIOLOGY (2018)

Article Multidisciplinary Sciences

Regulation of the stability of RGF1 receptor by the ubiquitin-specific proteases UBP12/UBP13 is critical for root meristem maintenance

Zhichao An et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2018)

Article Multidisciplinary Sciences

A small peptide modulates stomatal control via abscisic acid in long-distance signalling

Fuminori Takahashi et al.

NATURE (2018)

Article Plant Sciences

Dual CLAVATA3 peptides in Arabidopsis shoot stem cell signaling

Hyeon-Ji Kim et al.

JOURNAL OF PLANT BIOLOGY (2017)

Article Biochemistry & Molecular Biology

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

Ora Hazak et al.

EMBO REPORTS (2017)

Article Biochemistry & Molecular Biology

Arabidopsis MAKR5 is a positive effector of BAM3-dependent CLE45 signaling

Yeon Hee Kang et al.

EMBO REPORTS (2016)

Article Biochemistry & Molecular Biology

SERK Family Receptor-like Kinases Function as Co-receptors with PXY for Plant Vascular Development

Heqiao Zhang et al.

MOLECULAR PLANT (2016)

Article Multidisciplinary Sciences

Identification of three LRR-RKs involved in perception of root meristem growth factor in Arabidopsis

Hidefumi Shinohara et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2016)

Article Developmental Biology

Plant stem cell maintenance by transcriptional cross-regulation of related receptor kinases

Zachary L. Nimchuk et al.

DEVELOPMENT (2015)

Article Plant Sciences

Mathematical modelling of WOX5- and CLE40-mediated columella stem cell homeostasis in Arabidopsis

Sarah Richards et al.

JOURNAL OF EXPERIMENTAL BOTANY (2015)

Article Multidisciplinary Sciences

Allosteric receptor activation by the plant peptide hormone phytosulfokine

Jizong Wang et al.

NATURE (2015)

Article Genetics & Heredity

A cascade of arabinosyltransferases controls shoot meristem size in tomato

Cao Xu et al.

NATURE GENETICS (2015)

Article Biochemistry & Molecular Biology

Heterotrimeric G proteins control stem cell proliferation through CLAVATA signaling in Arabidopsis

Takashi Ishida et al.

EMBO REPORTS (2014)

Article Biochemistry & Molecular Biology

The CLE40 and CRN/CLV2 Signaling Pathways Antagonistically Control Root Meristem Growth in Arabidopsis

Helge Pallakies et al.

MOLECULAR PLANT (2014)

Article Multidisciplinary Sciences

Molecular genetic framework for protophloem formation

Antia Rodriguez-Villalon et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2014)

Article Multidisciplinary Sciences

Plant GSK3 proteins regulate xylem cell differentiation downstream of TDIF-TDR signalling

Yuki Kondo et al.

NATURE COMMUNICATIONS (2014)

Article Biochemistry & Molecular Biology

Moderation of Arabidopsis Root Sternness by CLAVATA1 and ARABIDOPSIS CRINKLY4 Receptor Kinase Complexes

Yvonne Stahl et al.

CURRENT BIOLOGY (2013)

Article Biochemistry & Molecular Biology

Identification of three hydroxyproline O-arabinosyltransferases in Arabidopsis thaliana

Mari Ogawa-Ohnishi et al.

NATURE CHEMICAL BIOLOGY (2013)

Article Multidisciplinary Sciences

Suppression of Arabidopsis protophloem differentiation and root meristem growth by CLE45 requires the receptor-like kinase BAM3

Stephen Depuydt et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2013)

Article Multidisciplinary Sciences

CLE-like (CLEL) peptides control the pattern of root growth and lateral root development in Arabidopsis

Ling Meng et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2012)

Article Cell Biology

WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex

Ram Kishor Yadav et al.

GENES & DEVELOPMENT (2011)

Article Plant Sciences

CLE Peptides can Negatively Regulate Protoxylem Vessel Formation via Cytokinin Signaling

Yuki Kondo et al.

PLANT AND CELL PHYSIOLOGY (2011)

Article Plant Sciences

Expression and Functional Analysis of a CLV3-Like Gene in the Model Legume Lotus japonicus

Satoru Okamoto et al.

PLANT AND CELL PHYSIOLOGY (2011)

Article Developmental Biology

RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis

Atsuko Kinoshita et al.

DEVELOPMENT (2010)

Article Plant Sciences

Stem Cell Signaling in Arabidopsis Requires CRN to Localize CLV2 to the Plasma Membrane

Andrea Bleckmann et al.

PLANT PHYSIOLOGY (2010)

Article Biochemistry & Molecular Biology

A Signaling Module Controlling the Stem Cell Niche in Arabidopsis Root Meristems

Yvonne Stahl et al.

CURRENT BIOLOGY (2009)

Article Developmental Biology

Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX

Emanuele Scacchi et al.

DEVELOPMENT (2009)

Article Biochemistry & Molecular Biology

A glycopeptide regulating stem cell fate in Arabidopsis thaliana

Kentaro Ohyama et al.

NATURE CHEMICAL BIOLOGY (2009)

Article Plant Sciences

The Receptor-Like Kinase SOL2 Mediates CLE Signaling in Arabidopsis

Hiroki Miwa et al.

PLANT AND CELL PHYSIOLOGY (2008)

Article Biochemistry & Molecular Biology

Functional diversification of CLAVATA3-related CLE proteins in meristem maintenance in rice

Takuya Suzaki et al.

PLANT CELL (2008)

Article Multidisciplinary Sciences

Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system

Yuki Hirakawa et al.

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA (2008)

Article Multidisciplinary Sciences

Arabidopsis CLV3 peptide directly binds CLV1 ectodomain

Mari Ogawa et al.

SCIENCE (2008)

Article Biochemistry & Molecular Biology

PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development

Kate Fisher et al.

CURRENT BIOLOGY (2007)

Article Plant Sciences

Protophloem differentiation in early Arabidopsis thaliana development

Helene Bauby et al.

PLANT AND CELL PHYSIOLOGY (2007)

Article Multidisciplinary Sciences

A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis

Tatsuhiko Kondo et al.

SCIENCE (2006)

Article Plant Sciences

A large family of genes that share homology with CLAVATA3

JM Cock et al.

PLANT PHYSIOLOGY (2001)