CLAVATA signaling in plant-environment interactions

Article Agronomy

The effect of drought stress on nodulation, plant growth, and nitrogen fixation in soybean during early plant growth

Rhea Amor Lumactud et al.

Summary: Drought stress significantly reduced the nodulation, growth, and nitrogen fixation of soybeans, but increased the root-to-shoot ratio and nitrogen concentration in shoots.

JOURNAL OF AGRONOMY AND CROP SCIENCE (2023)

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Review Biochemistry & Molecular Biology

Single-cell and spatial multi-omics in the plant sciences: Technical advances, applications, and perspectives

Xiaole Yu et al.

Summary: Plants have diverse cell types and intricate regulatory mechanisms, which have been increasingly studied at the single-cell level. Single-cell transcriptomics, spatial transcriptomics, and spatial metabolomics techniques have been combined to analyze plant development. These techniques allow for the systematic exploration of gene expression and metabolism in specific tissues and cell types during defined developmental stages. This review provides an overview of significant advancements in spatial multi-omics in plants and discusses the potential essential roles of these approaches in plant research.

PLANT COMMUNICATIONS (2023)

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Article Plant Sciences

A Mutation in Mediator Subunit MED16A Suppresses Nodulation and Increases Arbuscule Density in Medicago truncatula

Diptee Chaulagain et al.

Summary: Nodulation in legumes is regulated by a negative feedback pathway called Autoregulation of Nodulation (AON), which suppresses further nodulation as early as 48-72 h post inoculation. By screening for suppressors of the hypernodulating mutant sunn-1, a new gene not associated with legume-rhizobia signaling was identified. This gene was found to restore normal nodule numbers in sunn-1 mutants.

JOURNAL OF PLANT GROWTH REGULATION (2023)

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Review Plant Sciences

The good, the bad, and the phosphate: regulation of beneficial and detrimental plant-microbe interactions by the plant phosphate status

Michael Paries et al.

Summary: Phosphate is vital for life, but it is poorly accessible for sessile land plants. To overcome this limitation, plants have developed various strategies for enhanced acquisition and recycling of phosphate. These strategies involve a conserved phosphate starvation response (PSR) system, as well as interactions with mycorrhiza fungi and other microbes. The PSR pathway not only regulates phosphate uptake but also influences plant immunity and can be manipulated by microbes.

NEW PHYTOLOGIST (2023)

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Article Multidisciplinary Sciences

Root-knot nematode modulates plant CLE3-CLV1 signaling as a long-distance signal for successful infection

Satoru Nakagami et al.

Summary: Parasitic nematodes manipulate host plant signaling to promote infection.

SCIENCE ADVANCES (2023)

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Article Biology

Mycorrhizas drive the evolution of plant adaptation to drought

Marco Cosme

Summary: This study reveals how the strategic association between plant roots and soil-borne symbiotic fungi has shaped the drought tolerance of plants throughout their evolution. The results show that ecto- and ericoid mycorrhizal species have gained and lost drought tolerance at a much faster rate compared to arbuscular mycorrhizal and non-mycorrhizal species, highlighting the crucial role of mycorrhizas in plant adaptation to global climate change.

COMMUNICATIONS BIOLOGY (2023)

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Article Biology

The CLE33 peptide represses phloem differentiation via autocrine and paracrine signaling in Arabidopsis

Samy Carbonnel et al.

Summary: Plant meristems require constant supply for dividing cells, and protophloem sieve elements deliver the necessary supply to the growing root. The formation of protophloem is regulated by genetic circuits involving positive regulators (DOF transcription factors, OCTOPUS and BREVIX RADIX) and negative regulators (CLE peptides, CLAVATA3/EMBRYO SURROUNDING REGION RELATED, and their receptors, BARELY ANY MERISTEM). The discovery of CLE33, a previously unidentified CLE gene, and its redundant function with CLE45 in protophloem formation, highlights its significance.

COMMUNICATIONS BIOLOGY (2023)

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Article Biochemistry & Molecular Biology

pH-dependent CLE peptide perception permits phloem differentiation in Arabidopsis roots

Nicholay Diaz-Ardila et al.

Summary: The differentiation of protophloem sieve elements (PPSEs) in the root meristem of A. thaliana is positively regulated by genetic factors. In loss-of-function mutants, the signaling of CLE45 peptide through BAM3 receptor interferes with PPSE differentiation. However, developing PPSEs escape the autocrine inhibitory CLE45 signal by desensitizing themselves to pH-dependent CLE45 response and transitioning to differentiation through an increase in apoplastic pH gradient.

CURRENT BIOLOGY (2023)

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Article Plant Sciences

Multiplexed single-cell 3D spatial gene expression analysis in plant tissue using PHYTOMap

Tatsuya Nobori et al.

Summary: PHYTOMap is a multiplexed fluorescence in situ hybridization method that allows for single-cell and spatial analysis of gene expression in whole-mount plant tissue, without the need for transgenes and at a low cost. This study demonstrates the successful application of PHYTOMap in identifying major cell types in Arabidopsis roots and its potential to accelerate the spatial mapping of marker genes in complex plant tissue.

NATURE PLANTS (2023)

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Article Plant Sciences

Integrated single-nucleus and spatial transcriptomics captures transitional states in soybean nodule maturation

Zhijian Liu et al.

Summary: Legumes form nitrogen-fixing nodules through symbiosis with rhizobium. By using single-nucleus and spatial transcriptomics, a cell atlas of soybean nodules and roots was established. In the central infected zones of nodules, uninfected cells specialize into functionally distinct subgroups during nodule development, and a transitional subtype of infected cells with enriched nodulation-related genes was identified. Overall, this study provides a single-cell perspective for understanding rhizobium-legume symbiosis.

NATURE PLANTS (2023)

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Review Biochemistry & Molecular Biology

Plant adaptation to low phosphorus availability: Core signaling, crosstalks, and applied implications

Javier Paz-Ares et al.

Summary: This article reviews the importance of phosphorus in plant growth and the adaptive mechanisms plants have developed to cope with phosphorus limitation. Research has identified several signaling molecules involved in the regulation of the phosphorus starvation rescue system, and complex interactions between phosphorus and other nutrients have been discovered. Improving phosphorus use efficiency can enhance plant uptake and utilization of phosphorus.

MOLECULAR PLANT (2022)

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Article Plant Sciences

A CLE-BAM-CIK signalling module controls root protophloem differentiation in Arabidopsis

Chong Hu et al.

Summary: The study identified CLE25/26/45 peptides as regulators of protophloem differentiation and showed their involvement in a genetic module with BAM1/3 and CIK2/3/4/5/6. Mutations in cle25 26 45 and cik2 3 4 5 6 rescued root defects in brx and ops mutants, suggesting their role in organ development downstream of BRX and OPS. The findings highlight the importance of CLE25/26/45 as a key factor in modulating organ development through genetic pathways.

NEW PHYTOLOGIST (2022)

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Review Plant Sciences

Root dynamic growth strategies in response to salinity

Yutao Zou et al.

Summary: Plants respond to salinity stress by remodelling root system architecture, with recent research focusing on the mechanisms of root growth responses under salt stress. The modulation of root branching, root tropisms, and root cell wall modifications under salinity stress provide insights into plant performance, with natural variation approaches revealing potential pathways for enhancing salt stress responses in crops. These findings enhance our understanding of how salt influences root phenotype and offer possibilities for engineering crops with improved yield and survival in saline soils.

PLANT CELL AND ENVIRONMENT (2022)

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Review Plant Sciences

CLE peptides: critical regulators for stem cell maintenance in plants

Xiu-Fen Song et al.

Summary: Plant CLE peptides play important roles in regulating stem cell maintenance and vascular bundle development in plants. They have different functions and regulatory mechanisms in different tissues and organs. However, the study of CLE peptides and their receptor kinases and signal transduction is still challenging due to genome-wide redundancies and rapid evolution.

PLANTA (2022)

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Article Multidisciplinary Sciences

HSL1 and BAM1/2 impact epidermal cell development by sensing distinct signaling peptides

Andra-Octavia Roman et al.

Summary: HAESA and HSL2 are receptors for IDA/IDL-family signaling peptides, while HSL1 recognizes CLE9. The binding affinity of HSL1 to IDA/IDL peptides is higher than CLE peptides. The receptor kinase BAM1 interacts with CLE9 with high affinity, regulating epidermal cell division homeostasis. These findings highlight the independent roles of HSL1-IDLs and BAM1/BAM2-CLEs in cell patterning in the leaf epidermal tissue.

NATURE COMMUNICATIONS (2022)

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Article Biochemistry & Molecular Biology

CLE14 functions as a brake signalto suppress age-dependent and stress-induced leaf senescence by promoting JUB1-mediated ROS scavenging in Arabidopsis

Zenglin Zhang et al.

Summary: CLE14 peptide suppresses leaf senescence by regulating ROS homeostasis and activating ROS scavenging genes through JUB1-mediated signaling.

MOLECULAR PLANT (2022)

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Article Plant Sciences

Long-distance translocation of CLAVATA3/ESR-related 2 peptide and its positive effect on roots sucrose status

Satoru Okamoto et al.

Summary: Shoot-to-root long-distance mobile peptide and its homologs positively affect sucrose levels and root growth, playing an important role in plant life. CLE genes have a positive effect on root sucrose levels, and mutations in CLE genes result in an increased shoot/root ratio.

PLANT PHYSIOLOGY (2022)

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Review Plant Sciences

A rulebook for peptide control of legume-microbe endosymbioses

Sonali Roy et al.

Summary: Plants engage in mutually beneficial relationships with microbes, regulated by plant nutrient status. Peptide hormones play a crucial role in symbiotic plant-microbe interactions and nutrient homeostasis.

TRENDS IN PLANT SCIENCE (2022)

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Article Agronomy

Nitrate-Induced MtCLE34 Gene Lacks the Ability to Reduce Symbiotic Nodule Number and Carries Nonsense Mutation in a Few Accessions of Medicago truncatula

Maria Lebedeva et al.

Summary: Legume plants form nitrogen-fixing nodules in symbiosis with rhizobia, controlled by autoregulation of nodulation (AON) mechanism. CLE peptides and CLV1-like receptor kinase play important roles in this process. This study analyzed the MtCLE34 gene in Medicago truncatula and found that it encodes functional products in most M. truncatula accession lines, despite having high sequence similarity to nodulation-suppressing CLE genes. Overexpression of MtCLE34 gene from the R108 line did not inhibit nodulation, suggesting differences in the ability to trigger AON.

AGRONOMY-BASEL (2022)

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Review Biochemistry & Molecular Biology

Progress in the Self-Regulation System in Legume Nodule Development-AON (Autoregulation of Nodulation)

Yuhe Li et al.

Summary: The development of legume nodules requires a significant amount of energy, and the AON system plays a crucial role in controlling nodule number and activity. The AON pathway involves a variety of signal transmission and transcriptional regulation mechanisms, contributing to nodule formation and development.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2022)

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Article Agronomy

CLAVATA3/EMBRYO SURROUNDING REGION Genes Involved in Symbiotic Nodulation in Pisum sativum

Maria A. A. Lebedeva et al.

Summary: CLE peptides play important regulatory roles in different aspects of plant development, especially in nodulation process of legumes. Nitrate-induced CLE genes mediate the inhibition of nodulation, and overexpression of PsCLE13 and PsCLE12 can reduce the nodule number in pea roots by inducing the expression of PsTML genes.

AGRONOMY-BASEL (2022)

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Review Plant Sciences

New Advances in the Regulation of Leaf Senescence by Classical and Peptide Hormones

Peixin Huang et al.

Summary: Leaf senescence is the final stage of leaf development controlled by a complex genetic network. Plant hormones and environmental stimuli play important roles in regulating leaf senescence, and recent research has shown the involvement of peptide hormones.

FRONTIERS IN PLANT SCIENCE (2022)

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Article Biochemistry & Molecular Biology

Arbuscular mycorrhizal fungi induce lateral root development in angiosperms via a conserved set of MAMP receptors

Chai Hao Chiu et al.

Summary: This study reveals that chitin-derived molecules, rather than symbiosis-specific signals, can trigger lateral root formation. The LysM receptors integrate MAMP perception with developmental responses, and their role in coordinating the interaction between roots and the rhizosphere biota is conserved across different plant species.

CURRENT BIOLOGY (2022)

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Review Plant Sciences

Spatial range, temporal span, and promiscuity of CLE-RLK signaling

Madhumitha Narasimhan et al.

Summary: CLE peptides regulate developmental transitions and responses to biotic and abiotic inputs through RLKs. CLE signaling ranges vary and are predominantly autocrine or paracrine. CLE-RLK-mediated signaling responses extend from cellular to whole organism level. Additionally, CLE-RLK signaling also mediates diverse non-developmental effects.

FRONTIERS IN PLANT SCIENCE (2022)

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Article Biotechnology & Applied Microbiology

Deeper genomic insights into tomato CLE genes repertoire identify new active peptides

Samy Carbonnel et al.

Summary: A comprehensive identification of CLE genes in tomato genome was conducted, revealing 37 new SlCLE genes. These new findings are crucial for understanding CLE signaling in tomato. The study also showed gene diversification within the SlCLE family and highlighted a conserved mechanism of root-active CLE peptide perception between Arabidopsis and tomato.

BMC GENOMICS (2022)

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Article Plant Sciences

A Dof-CLE circuit controls phloem organization

Pingping Qian et al.

Summary: This study reveals the role of Dof transcription factors in phloem development. It shows that Dof proteins induce phloem formation while also inhibiting excessive phloem cell formation through the secretion of CLE peptides. Furthermore, the study highlights the importance of positive feedback regulation in maintaining the balance of phloem differentiation.

NATURE PLANTS (2022)

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Article Plant Sciences

Genome-wide identification and functional characterization of the MdCLE peptide family in apple ( Malus x domestica )

Tianen Zhang et al.

Summary: This study identified 25 MdCLE genes in apple and found that they showed higher expression levels in leaves and root. Furthermore, MdCLE genes may play important roles in the acclimation of apple to abiotic stress. These findings provide valuable references for further investigation of the biological functions of MdCLE genes.

HORTICULTURAL PLANT JOURNAL (2022)

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Article Plant Sciences

Dynamic evolution of small signalling peptide compensation in plant stem cell control

Choon-Tak Kwon et al.

Summary: Gene duplications are important for plant genome evolution and genetic interactions that shape phenotypic diversity. This study used genomics and genome editing to investigate the evolution of compensating paralogues. The findings show that the compensation relationships can vary among different species, and in tomato, the compensation has partially degenerated.

NATURE PLANTS (2022)

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Article Plant Sciences

To the proteome and beyond: advances in single-cell omics profiling for plant systems

Natalie M. Clark et al.

Summary: Recent advances in single-cell proteomics can be applied to plants, increasing our understanding of plant development, response to stimuli, and cell-to-cell signaling.

PLANT PHYSIOLOGY (2022)

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Article Plant Sciences

Phytonematode peptide effectors exploit a host post-translational trafficking mechanism to the ER using a novel translocation signal

Jianying Wang et al.

Summary: A novel translocation signal within nematode CLE effectors has been identified, which can be recognized by plant cell secretory machinery to redirect these peptides from the cytoplasm to the apoplast of plant cells. This translocation signal is functionally conserved across nematode species and can traffic unrelated small peptides from the cytoplasm to the apoplast of host cells via an unknown post-translational mechanism of endoplasmic reticulum translocation.

NEW PHYTOLOGIST (2021)

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Editorial Material Plant Sciences

Plant-parasitic nematode secreted peptides hijack a plant secretory pathway

Nicolas Frei Dit Frey et al.

NEW PHYTOLOGIST (2021)

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Article Plant Sciences

Characterisation of Medicago truncatula CLE34 and CLE35 in nitrate and rhizobia regulation of nodulation

Celine Mens et al.

Summary: Novel nodulation-suppressing CLE peptides MtCLE34 and MtCLE35 were identified in legumes, showing different responses to rhizobia and nitrate. MtCLE12 and MtCLE13 are specific to autoregulation of nodulation, while MtCLE35 regulates nodule numbers in response to both rhizobia and nitrate. MtCLE34 was found to be a pseudogene with a non-functional CLE-domain due to a premature nonsense mutation.

NEW PHYTOLOGIST (2021)

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Article Biochemistry & Molecular Biology

CLAVATA Signaling Ensures Reproductive Development in Plants across Thermal Environments

Daniel S. Jones et al.

Summary: This passage discusses the necessity of integrating multiple signaling pathways to regulate plant reproduction development under different temperature conditions, highlighting the roles of CLAVATA2/CORYNE signaling at colder/ambient temperatures and the synergistic requirement of CLV2/CM signaling and heat-induced auxin biosynthesis at higher temperatures.

CURRENT BIOLOGY (2021)

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Review Biochemistry & Molecular Biology

The Regulation of Nodule Number in Legumes Is a Balance of Three Signal Transduction Pathways

Diptee Chaulagain et al.

Summary: Nitrogen is essential for plant growth and productivity, and legumes forming a symbiotic relationship with nitrogen-fixing rhizobia bacteria allows them to thrive in nitrogen-poor environments. However, hosting nitrogen-fixing bacteria comes with metabolic costs and requires regulation. The symbiosis is regulated through three signal transduction pathways, controlling the communication and organ formation of symbiotic signals.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Review Biochemistry & Molecular Biology

Mechanisms of Enhancer-Promoter Interactions in Higher Eukaryotes

Olga Kyrchanova et al.

Summary: Enhancers determine gene transcription activation in specific cell types and developmental stages by transforming signals from transcription factors. Developmental genes can be associated with multiple enhancers located at large distances, and the mechanisms underlying specific distance interactions between enhancers and promoters are not well understood.

INTERNATIONAL JOURNAL OF MOLECULAR SCIENCES (2021)

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Article Biology

Control of Arabidopsis shoot stem cell homeostasis by two antagonistic CLE peptide signalling pathways

Jenia Schlegel et al.

Summary: Researchers have found that in the shoot meristems of plants, the molecule CLE40 produced by peripheral zone cells increases the levels of WUS, thereby boosting the number of stem cells. WUS, in turn, reduces the production of CLE40 in the central zone and organizing center, allowing meristems to adapt to growing at different speeds. This balance between CLE40 and WUS helps regulate stem cell activity in meristems for plant growth and development.

ELIFE (2021)

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Review Plant Sciences

Cross-Talks Between Macro- and Micronutrient Uptake and Signaling in Plants

Xiaoning Fan et al.

Summary: This review explores the biochemical and physiological interactions between macro- and micro-mineral nutrients in plants, focusing on the cross-talks between N, Pi, S, Zn, and Fe uptake and homeostasis. The molecular mechanisms underlying these interactions in plants are still not well understood, highlighting the importance of further studies in this area for sustainable agriculture. The integrative study of multiple nutrient signaling cross-talks in plants is deemed crucial for better understanding mineral uptake and signaling in plants.

FRONTIERS IN PLANT SCIENCE (2021)

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Article Plant Sciences

Plasticity of rosette size in response to nitrogen availability is controlled by an RCC1-family protein

Gustavo Turqueto Duarte et al.

Summary: This study dissected the genetic architecture of plasticity in response to different nitrogen levels in Arabidopsis thaliana accessions. It was found that plasticity in levels of primary metabolites were related to the plasticities of the studied traits, and the gene At1g19880 was identified to confer plasticity of rosette diameter in response to nitrogen. Additionally, different genetic programs were shown to regulate growth and flowering-related traits in response to environmental cues.

PLANT CELL AND ENVIRONMENT (2021)

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Article Biochemistry & Molecular Biology

NLP1 reciprocally regulates nitrate inhibition of nodulation through SUNN-CRA2 signaling in Medicago truncatula

Zhenpeng Luo et al.

Summary: Most legume plants form nodules with rhizobia, regulated by signaling pathways involving CLE/SUNN and CEP/CRA2. Nitrate inhibits nodulation through local and systemic pathways, with NLP1 playing a key role. Further research is needed to understand the complex interactions between these pathways in mediating nodulation inhibition by nitrate.

PLANT COMMUNICATIONS (2021)

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Article Plant Sciences

Nitrate-induced CLE35 signaling peptides inhibit nodulation through the SUNN receptor and miR2111 repression

Corentin Moreau et al.

Summary: Studies have found that in high nitrogen environments, MtCLE35 inhibits nodule formation by affecting rhizobial infections, depending on the MtSUNN receptor and the miR2111 systemic effector.

PLANT PHYSIOLOGY (2021)

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Article Plant Sciences

The role of CLAVATA signalling in the negative regulation of mycorrhizal colonization and nitrogen response of tomato

Chenglei Wang et al.

Summary: Plants form mutualistic nutrient-acquiring symbioses with microbes like arbuscular mycorrhizal fungi, and employ a negative feedback loop called autoregulation of mycorrhizae (AOM) to limit the formation of these symbioses. Specific genes like FAB, FIN, and SlCLV2 have been identified as playing roles in negatively regulating arbuscular mycorrhizal formation in tomato. Furthermore, external nutrients such as phosphate and nitrate can strongly suppress arbuscular mycorrhizal formation, with FAB and FIN being required for nitrate suppression but not for phosphate suppression. This suggests a deep homology in the symbiotic role of these genes, potentially forming a common symbiotic toolkit for beneficial plant-microbe interactions.

JOURNAL OF EXPERIMENTAL BOTANY (2021)

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Article Plant Sciences

Enhancing grain-yield-related traits by CRISPR-Cas9 promoter editing of maize CLE genes

Lei Liu et al.

Summary: By using CRISPR-Cas9 genome editing, weak promoter alleles of CLE genes and a null allele of a partially redundant compensating CLE gene were engineered in maize to increase multiple maize grain-yield-related traits, demonstrating the potential of genomic editing in crop improvement.

NATURE PLANTS (2021)

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Review Biochemistry & Molecular Biology

Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation([OPEN])

Sonali Roy et al.

PLANT CELL (2020)

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Article Biochemistry & Molecular Biology

A Reservoir of Pluripotent Phloem Cells Safeguards the Linear Developmental Trajectory of Protophloem Sieve Elements

Bojan Gujas et al.

CURRENT BIOLOGY (2020)

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Article Biochemistry & Molecular Biology

Compact Root Architecture 2 Promotes Root Competence for Nodulation through the miR2111 Systemic Effector

Pierre Gautrat et al.

CURRENT BIOLOGY (2020)

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Review Plant Sciences

Signaling pathways underlying nitrogen-dependent changes in root system architecture: from model to crop species

Zhongtao Jia et al.

JOURNAL OF EXPERIMENTAL BOTANY (2020)

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Article Biochemistry & Molecular Biology

CLE-HAR1 Systemic Signaling and NIN-Mediated Local Signaling Suppress the Increased Rhizobial Infection in the daphne Mutant of Lotus japonicus

Emiko Yoro et al.

MOLECULAR PLANT-MICROBE INTERACTIONS (2020)

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Article Plant Sciences

CLE40 Signaling Regulates Root Stem Cell Fate(1)

Barbara Berckmans et al.

PLANT PHYSIOLOGY (2020)

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Article Plant Sciences

The CLE53-SUNN genetic pathway negatively regulates arbuscular mycorrhiza root colonization in Medicago truncatula

Magda Karlo et al.

JOURNAL OF EXPERIMENTAL BOTANY (2020)

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Article Plant Sciences

Inhibition of legume nodulation by Pi deficiency is dependent on the autoregulation of nodulation (AON) pathway

Mariel C. Isidra-Arellano et al.

PLANT JOURNAL (2020)

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Review Plant Sciences

Recent Advances in Arabidopsis CLE Peptide Signaling

Jennifer C. Fletcher

TRENDS IN PLANT SCIENCE (2020)

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Article Plant Sciences

Infection ofMedicago truncatulaby the Root-Knot NematodeMeloidogyne javanicaDoes Not Require Early Nodulation Genes

Sofia R. Costa et al.

FRONTIERS IN PLANT SCIENCE (2020)

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Review Genetics & Heredity

Nitrate Signaling, Functions, and Regulation of Root System Architecture: Insights fromArabidopsis thaliana

Muhammad Asim et al.

GENES (2020)

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Article Biotechnology & Applied Microbiology

Predicting and clustering plant CLE genes with a new method developed specifically for short amino acid sequences

Zhe Zhang et al.

BMC GENOMICS (2020)

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Review Plant Sciences

Connections in the cambium, receptors in the ring

Kristine S. Bagdassarian et al.

CURRENT OPINION IN PLANT BIOLOGY (2020)

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Article Plant Sciences

The role ofCLV1,CLV2andHPAThomologues in the nitrogen-regulation of root development

Chenglei Wang et al.

PHYSIOLOGIA PLANTARUM (2020)

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Article Biochemistry & Molecular Biology

CLE2regulates light-dependent carbohydrate metabolism in Arabidopsis shoots

Dichao Ma et al.

PLANT MOLECULAR BIOLOGY (2020)

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Article Multidisciplinary Sciences

MIR2111-5 locus and shoot-accumulated mature miR2111 systemically enhance nodulation depending on HAR1 in Lotus japonicus

Nao Okuma et al.

NATURE COMMUNICATIONS (2020)

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Article Plant Sciences

Nitrate-Induced CLE Peptide Systemically Inhibits Nodulation in Medicago truncatula

Maria Lebedeva et al.

PLANTS-BASEL (2020)

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Article Biochemistry & Molecular Biology

CLE25 peptide regulates phloem initiation in Arabidopsis through a CLERK-CLV2 receptor complex

Shi-Chao Ren et al.

JOURNAL OF INTEGRATIVE PLANT BIOLOGY (2019)

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Article Biochemistry & Molecular Biology

Regulation of Resource Partitioning Coordinates Nitrogen and Rhizobia Responses and Autoregulation of Nodulation in Medicago truncatula

Beatriz Lagunas et al.

MOLECULAR PLANT (2019)

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Article Genetics & Heredity

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

Daniel Rodriguez-Leal et al.

NATURE GENETICS (2019)

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Article Plant Sciences

Arbuscular Mycorrhizal Fungi Alleviate Drought Stress in C3 (Leymus chinensis) and C4 (Hemarthria altissima) Grasses via Altering Antioxidant Enzyme Activities and Photosynthesis

Junqin Li et al.

FRONTIERS IN PLANT SCIENCE (2019)

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Article Plant Sciences

CLE-CLAVATA1 Signaling Pathway Modulates Lateral Root Development under Sulfur Deficiency

Wei Dong et al.

PLANTS-BASEL (2019)

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Article Biotechnology & Applied Microbiology

Genome-wide identification of the CLAVATA3/EMBRYO SURROUNDING REGION (CLE) family in grape (Vitis vinifera L.)

Pengfei Wang et al.

BMC GENOMICS (2019)

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Review Plant Sciences

Phytohormones, miRNAs, and peptide signals integrate plant phosphorus status with arbuscular mycorrhizal symbiosis

Lena M. Mueller et al.

CURRENT OPINION IN PLANT BIOLOGY (2019)

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Editorial Material Plant Sciences

Sulfur nutrition: impacts on plant development, metabolism, and stress responses

Stanislav Kopriva et al.

JOURNAL OF EXPERIMENTAL BOTANY (2019)

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Article Genetics & Heredity

Natural variation in Arabidopsis shoot branching plasticity in response to nitrate supply affects fitness

Maaike de Jong et al.

PLOS GENETICS (2019)

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Review Plant Sciences

Interactions Between Phosphorus, Zinc, and Iron Homeostasis in Nonmycorrhizal and Mycorrhizal Plants

Xianan Xie et al.

FRONTIERS IN PLANT SCIENCE (2019)

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Article Genetics & Heredity

Systems genomics approaches provide new insights into Arabidopsis thaliana root growth regulation under combinatorial mineral nutrient limitation

Nadia Bouain et al.

PLOS GENETICS (2019)

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Article Plant Sciences

Arbuscular mycorrhizal fungi possess a CLAVATA3/embryo surrounding region-related gene that positively regulates symbiosis

Morgane Le Marquer et al.

NEW PHYTOLOGIST (2019)

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Article Plant Sciences

Genes controlling legume nodule numbers affect phenotypic plasticity responses to nitrogen in the presence and absence of rhizobia

Chooi-Hua Goh et al.

PLANT CELL AND ENVIRONMENT (2019)

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Article Plant Sciences

CLE9 peptide-induced stomatal closure is mediated by abscisic acid, hydrogen peroxide, and nitric oxide in Arabidopsis thaliana

Luosha Zhang et al.

PLANT CELL AND ENVIRONMENT (2019)

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Article Plant Sciences

A CLE-SUNN module regulates strigolactone content and fungal colonization in arbuscular mycorrhiza

Lena M. Mueller et al.

NATURE PLANTS (2019)

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Article Biochemistry & Molecular Biology

The Medicago truncatula CLAVATA3-LIKE CLE12/13 signaling peptides regulate nodule number depending on the CORYNE but not the COMPACT ROOT ARCHITECTURE2 receptor

Stephen Nowak et al.

PLANT SIGNALING & BEHAVIOR (2019)

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Article Biochemistry & Molecular Biology

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

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Cross-kingdom lipid transfer in arbuscular mycorrhiza symbiosis and beyond

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CURRENT OPINION IN PLANT BIOLOGY (2018)

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CLERK is a novel receptor kinase required for sensing of root-active CLE peptides in Arabidopsis

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Agrobacterial tumors interfere with nodulation and demonstrate the expression of nodulation-induced CLE genes in pea

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JOURNAL OF PLANT PHYSIOLOGY (2018)

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A NIN-LIKE PROTEIN mediates nitrate-induced control of root nodule symbiosis in Lotus japonicus

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NATURE COMMUNICATIONS (2018)

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The Soybean GmNARK Affects ABA and Salt Responses in Transgenic Arabidopsis thaliana

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FRONTIERS IN PLANT SCIENCE (2018)

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The Art of Self-Control - Autoregulation of Plant-Microbe Symbioses

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

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Systemic control of legume susceptibility to rhizobial infection by a mobile microRNA

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A group of receptor kinases are essential for CLAVATA signalling to maintain stem cell homeostasis

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The CLE9/10 secretory peptide regulates stomatal and vascular development through distinct receptors

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NIN interacts with NLPs to mediate nitrate inhibition of nodulation in Medicago truncatula

Jie-shun Lin et al.

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Comprehensive identification and clustering of CLV3/ESR-related (CLE) genes in plants finds groups with potentially shared function

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NEW PHYTOLOGIST (2017)

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A Collection of Mutants for CLE-Peptide-Encoding Genes in Arabidopsis Generated by CRISPR/Cas9-Mediated Gene Targeting

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PLANT AND CELL PHYSIOLOGY (2017)

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Genome-Wide Identification of Medicago Peptides Involved in Macronutrient Responses and Nodulation

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PLANT PHYSIOLOGY (2017)

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ROOT DETERMINED NODULATION1 Is Required for M. truncatula CLE12, But Not CLE13, Peptide Signaling through the SUNN Receptor Kinase

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Neodiversification of homeologous CLAVATA1-like receptor kinase genes in soybean leads to distinct developmental outcomes

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SCIENTIFIC REPORTS (2017)

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CLAVATA1 controls distinct signaling outputs that buffer shoot stem cell proliferation through a two-step transcriptional compensation loop

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Identification of cyst nematode B-type CLE peptides and modulation of the vascular stem cell pathway for feeding cell formation

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Interplay between Light and Plant Hormones in the Control of Arabidopsis Seedling Chlorophyll Biosynthesis

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Differential CLE peptide perception by plant receptors implicated from structural and functional analyses of TDIF-TDR interactions

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PLOS ONE (2017)

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Phosphate Starvation-Dependent Iron Mobilization Induces CLE14 Expression to Trigger Root Meristem Differentiation through CLV2/PEPR2 Signaling

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Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels

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Crystal structure of PXY-TDIF complex reveals a conserved recognition mechanism among CLE peptide-receptor pairs

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CELL RESEARCH (2016)

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CLAVATA-WUSCHEL signaling in the shoot meristem

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Expression of the CLE-RS3 gene suppresses root nodulation in Lotus japonicus

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JOURNAL OF PLANT RESEARCH (2016)

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Arabidopsis CLAVATA1 and CLAVATA2 receptors contribute to Ralstonia solanacearum pathogenicity through a miR169-dependent pathway

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The systemic nodule number regulation kinase SUNN in Medicago truncatula interacts with MtCLV2 and MtCRN

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CLE Peptide Signaling and Crosstalk with Phytohormones and Environmental Stimuli

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

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A cascade of arabinosyltransferases controls shoot meristem size in tomato

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RNA-seq Transcriptional Profiling of an Arbuscular Mycorrhiza Provides Insights into Regulated and Coordinated Gene Expression in Lotus japonicus and Rhizophagus irregularis

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PLANT AND CELL PHYSIOLOGY (2015)

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Enhanced resistance to soybean cyst nematode Heterodera glycines in transgenic soybean by silencing putative CLE receptors

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Arbuscular mycorrhizal symbiosis alters stomatal conductance of host plants more under drought than under amply watered conditions: a meta-analysis

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MYCORRHIZA (2015)

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Article Biochemistry & Molecular Biology

Shoot HAR1 mediates nitrate inhibition of nodulation in Lotus japonicus

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PLANT SIGNALING & BEHAVIOR (2015)

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The potential roles of strigolactones and brassinosteroids in the autoregulation of nodulation pathway

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ANNALS OF BOTANY (2014)

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Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice

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JOURNAL OF EXPERIMENTAL BOTANY (2014)

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Article Biotechnology & Applied Microbiology

The soybean (Glycine max) nodulation-suppressive CLE peptide, GmRIC1, functions interspecifically in common white bean (Phaseolus vulgaris), but not in a supernodulating line mutated in the receptor PvNARK

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Two CCAAT-box-binding transcription factors redundantly regulate early steps of the legume-rhizobia endosymbiosis

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CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner

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A Novel Pollen-Pistil Interaction Conferring High-Temperature Tolerance during Reproduction via CLE45 Signaling

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CURRENT BIOLOGY (2013)

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Review Biochemistry & Molecular Biology

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Structure-function analysis of the GmRIC1 signal peptide and CLE domain required for nodulation control in soybean

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Synergistic Interaction of CLAVATA1, CLAVATA2, and RECEPTOR-LIKE PROTEIN KINASE 2 in Cyst Nematode Parasitism of Arabidopsis

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Root-derived CLE glycopeptides control nodulation by direct binding to HAR1 receptor kinase

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Review Plant Sciences

Multiple control levels of root system remodeling in arbuscular mycorrhizal symbiosis

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Strigolactones Internal and external signals in plant symbioses?

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PLANT SIGNALING & BEHAVIOR (2013)

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Analyzing the soybean transcriptome during autoregulation of mycorrhization identifies the transcription factors GmNF-YA1a/b as positive regulators of arbuscular mycorrhization

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Physiological and molecular aspects of salt stress in plants

S. V. Isayenkov

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Direct and indirect influences of 8 yr of nitrogen and phosphorus fertilization on Glomeromycota in an alpine meadow ecosystem

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Strigolactones Are Involved in Root Response to Low Phosphate Conditions in Arabidopsis

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The Autoregulation Gene SUNN Mediates Changes in Root Organ Formation in Response to Nitrogen through Alteration of Shoot-to-Root Auxin Transport

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Review Plant Sciences

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Two CLE genes are induced by phosphate in roots of Lotus japonicus

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Identification of potential host plant mimics of CLAVATA3/ESR (CLE)-like peptides from the plant-parasitic nematode Heterodera schachtii

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Article Biochemistry & Molecular Biology

Inoculation- and Nitrate-Induced CLE Peptides of Soybean Control NARK-Dependent Nodule Formation

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Mitogen-Activated Protein Kinase Regulated by the CLAVATA Receptors Contributes to Shoot Apical Meristem Homeostasis

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Soybean Nodule-Enhanced CLE Peptides in Roots Act as Signals in GmNARK-Mediated Nodulation Suppression

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PLANT AND CELL PHYSIOLOGY (2011)

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Nematode CLE signaling in Arabidopsis requires CLAVATA2 and CORYNE

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PLANT JOURNAL (2011)

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The Clavata2 genes of pea and Lotus japonicus affect autoregulation of nodulation

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PLANT JOURNAL (2011)

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Strigolactones Are Transported through the Xylem and Play a Key Role in Shoot Architectural Response to Phosphate Deficiency in Nonarbuscular Mycorrhizal Host Arabidopsis

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Mechanisms of Molecular Mimicry of Plant CLE Peptide Ligands by the Parasitic Nematode Globodera rostochiensis

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ANNALS OF BOTANY (2010)

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The receptor-like kinase KLAVIER mediates systemic regulation of nodulation and non-symbiotic shoot development in Lotus japonicus

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DEVELOPMENT (2010)

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Review Plant Sciences

Temperature stress and plant sexual reproduction: uncovering the weakest links

Kelly E. Zinn et al.

JOURNAL OF EXPERIMENTAL BOTANY (2010)

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Dual roles for the variable domain in protein trafficking and host-specific recognition of Heterodera glycines CLE effector proteins

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NEW PHYTOLOGIST (2010)

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plenty, a Novel Hypernodulation Mutant in Lotus japonicus

Chie Yoshida et al.

PLANT AND CELL PHYSIOLOGY (2010)

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Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis

Yingfang Zhu et al.

PLANT JOURNAL (2010)

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

Andrea Bleckmann et al.

PLANT PHYSIOLOGY (2010)

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CLE Peptides Control Medicago truncatula Nodulation Locally and Systemically

Virginie Mortier et al.

PLANT PHYSIOLOGY (2010)

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Review Agronomy

Plant drought stress: effects, mechanisms and management

M. Farooq et al.

AGRONOMY FOR SUSTAINABLE DEVELOPMENT (2009)

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A glycopeptide regulating stem cell fate in Arabidopsis thaliana

Kentaro Ohyama et al.

NATURE CHEMICAL BIOLOGY (2009)

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Nod Factor/Nitrate-Induced CLE Genes that Drive HAR1-Mediated Systemic Regulation of Nodulation

Satoru Okamoto et al.

PLANT AND CELL PHYSIOLOGY (2009)

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Review Plant Sciences

Parasitism proteins in nematode-plant interactions

Eric L. Davis et al.

CURRENT OPINION IN PLANT BIOLOGY (2008)

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Article Cell Biology

Key divisions in the early Arabidopsis embryo require POL and PLL1 Phosphatases to establish the root stem cell organizer and vascular axis

Sang-Kee Song et al.

DEVELOPMENTAL CELL (2008)

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Article Developmental Biology

POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells

Sang-Kee Song et al.

DEVELOPMENT (2006)

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Defective long-distance auxin transport regulation in the Medicago truncatula super numeric nodules mutant

GE van Noorden et al.

PLANT PHYSIOLOGY (2006)

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The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis

BJ DeYoung et al.

PLANT JOURNAL (2006)

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Article Plant Sciences

Lack of mycorrhizal autoregulation and phytohormonal changes in the supernodulating soybean mutant nts1007

C Meixner et al.

PLANTA (2005)

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Article Biochemistry & Molecular Biology

The Medicago truncatula SUNN gene encodes a CLV1-like leucine-rich repeat receptor kinase that regulates nodule number and root length

E Schnabel et al.

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Nematodes. Sophisticated parasites of legumes

EL Davis et al.

PLANT PHYSIOLOGY (2005)

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A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana

XH Wang et al.

MOLECULAR PLANT PATHOLOGY (2005)

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Article Multidisciplinary Sciences

Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1

T Kinoshita et al.

NATURE (2005)

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Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana

L Sanchez-Calderon et al.

PLANT AND CELL PHYSIOLOGY (2005)

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WebLogo: A sequence logo generator

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GENOME RESEARCH (2004)

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Suppression of arbuscular mycorrhizal colonization and nodulation in split-root systems of alfalfa after pre-inoculation and treatment with Nod factors

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SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem

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GENES & DEVELOPMENT (2003)

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Letter Plant Sciences

Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3

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Long-distance signaling in nodulation directed by a CLAVATA1-like receptor kinase

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SCIENCE (2003)

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Shoot control of root development and nodulation is mediated by a receptor-like kinase

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NATURE (2002)

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An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine

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SCIENCE (2002)

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Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L.

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ANNALS OF BOTANY (2001)

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Short root mutant of Lotus japonicus with a dramatically altered symbiotic phenotype

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PLANT JOURNAL (2000)

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Influence of genes determining supernodulation on root colonization by the mycorrhizal fungus Glomus mosseae in Pisum sativum and Medicago truncatula mutants

D Morandi et al.

MYCORRHIZA (2000)

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Systemic suppression of mycorrhizal colonization of barley roots already colonized by AM fungi

H Vierheilig et al.

SOIL BIOLOGY & BIOCHEMISTRY (2000)

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CLAVATA signaling in plant-environment interactions

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