Predicting and Clustering Plant CLE Genes with a New Method Developed Specifically for Short Amino Acid Sequences

Zhang, Zhe; Liu, Lei; Kücükoglu, Melis; Tian, Dongdong; Larkin, Robert M.; Shi, Xueping; Zheng, Bo

doi:10.21203/rs.2.21530/v2

Cited by 5 publications

(9 citation statements)

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“…On the basis of a conserved functional C‐terminal CLE domain, our and others' phylogenetic analyses indicate that the mature CLV3 peptide shares the closest evolutionary relationship with CLE1 through CLE7, thereby constituting a single clade of closely‐related CLE peptides (Ito et al ., 2006; Kucukoglu & Nilsson, 2015; Yang et al ., 2017; Zhang et al ., 2020). Similar to CLV3 overexpression, overexpression of CLE1 to CLE7 results in wus ‐like phenotypes with plants exhibiting premature SAM termination (Strabala et al ., 2006; Meng et al ., 2010), implying that CLE1–CLE7 overexpression phenotypes are largely due to activation of the CLV‐WUS signaling pathway in the SAM.…”

Section: Resultsmentioning

confidence: 99%

“…Phylogenetic analysis revealed that CLE1–CLE7 and CLV3 group in the same clade if CLE motifs alone are evaluated (Ito et al ., 2006; Kucukoglu & Nilsson, 2015; Yang et al ., 2017; Zhang et al ., 2020). Mis‐expression of CLE1 – CLE7 from the CLV3 promoter can rescue the enlarged meristem phenotype of clv3 mutants, while their overexpression results in the premature loss of shoot stem cells (Ni & Clark, 2006; Strabala et al ., 2006; Meng et al ., 2010).…”

Section: Discussionmentioning

confidence: 99%

“…CLV1 and BAM1 are involved in de novo shoot regeneration and are required for CLE1-CLE7-mediated shoot regeneration signaling CLV1 and BAM1 are receptors for CLV3 (Ogawa et al, 2008;Shinohara & Matsubayashi, 2015), the mature CLE domain of which is most closely-related to those of CLE1-CLE7 (Ito et al, 2006;Kucukoglu & Nilsson, 2015;Yang et al, 2017;Zhang et al, 2020). Amongst these, CLE2 and CLE5 can physically bind to CLV1 (Ohyama et al, 2009;Guo et al, 2010).…”

Section: Cle1-cle7 Genes Are Induced Upon Cim Incubation and Dynamica...mentioning

confidence: 99%

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A group of CLE peptides regulates de novo shoot regeneration in Arabidopsis thaliana

et al. 2022

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Summary Known for their regulatory roles in stem cell homeostasis, CLAVATA3/ESR‐RELATED (CLE) peptides also function as mediators of external stimuli such as hormones. De novo shoot regeneration, representing the remarkable plant cellular plasticity, involves reconstitution of stem cells under control of stem‐cell regulators. Yet whether and how stem cell‐regulating CLE peptides are implicated in plant regeneration remains unknown. By CRISPR/Cas9‐induced loss‐of‐function studies, peptide application, precursor overexpression, and expression analyses, the role of CLE1–CLE7 peptides and their receptors in de novo shoot regeneration was studied in Arabidopsis thaliana. CLE1–CLE7 are induced by callus‐induction medium and dynamically expressed in pluripotent callus. Exogenously‐applied CLE1–CLE7 peptides or precursor overexpression effectively leads to shoot regeneration suppression, whereas their simultaneous mutation results in enhanced regenerative capacity, demonstrating that CLE1–CLE7 peptides redundantly function as negative regulators of de novo shoot regeneration. CLE1–CLE7‐mediated shoot regeneration suppression is impaired in loss‐of‐function mutants of callus‐expressed CLAVATA1 (CLV1) and BARELY ANY MERISTEM1 (BAM1) genes, indicating that CLV1/BAM1 are required for CLE1–CLE7‐mediated shoot regeneration signaling. CLE1–CLE7 signaling resulted in transcriptional repression of WUSCHEL (WUS), a stem cell‐promoting transcription factor known as a principal regulator of plant regeneration. Our results indicate that functionally‐redundant CLE1–CLE7 peptides genetically act through CLV1/BAM1 receptors and repress WUS expression to modulate shoot‐regeneration capacity, establishing the mechanistic basis for CLE1–CLE7‐mediated shoot regeneration and a novel role for CLE peptides in hormone‐dependent developmental plasticity.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Cle1-cle7 Genes Are Induced Upon Cim Incubation and Dynamica...mentioning

confidence: 99%

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A group of CLE peptides regulates de novo shoot regeneration in Arabidopsis thaliana

et al. 2022

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“…Motivated by uncovering the role of CLE peptides in tomato roots, we performed a re-analysis of the CLE peptide-encoding genes. The first genome-wide analysis in the tomato genome revealed only fifteen SlCLE genes [23] and further attempts failed to uncover additional genes [21, 22]. In our study, we applied a combined bioinformatic approach to identify additional SlCLE genes using the most recent versions of the tomato reference genome SL3.0 and SL4.0 [44].…”

Section: Resultsmentioning

confidence: 99%

New insights into tomato CLE peptide repertoire and perception mechanisms

Hazak

Carbonnel

Falquet

2022

Preprint

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Precision in sensing the environmental cues and adjusting the growth and the physiology of the root system is necessary for plant robustness. Plants achieve their phenotypic plasticity by tightly controlling and buffering developmental decisions. In addition to the classical plant hormones, the CLE peptides are exceptionally important in mediating development, and responses to environmental stresses. While the CLV3-CLV1 module appears to be highly conserved to control the proliferation of the shoot apical meristem stem cells, we do not know whether the function of root-specific CLEs that are implicated in vascular development, in mediating drought stress, sugar starvation, phosphate and nitrate deficit in Arabidopsis is also conserved in other plant species. Here we present a careful re-analysis of the CLE signaling components in the tomato genome and show that the mechanism of root-active CLE peptides is deeply conserved in Arabidopsis and tomato. Due to the small gene size and high sequence variability, it is extremely difficult to precisely annotate SlCLE genes in plant genomes. Our analysis of the SlCLE family, based on a combination of iterative tBLASTn and Hidden-Markov-Model (HMM), revealed thirty-seven new SlCLEs in addition to the fifteen reported previously. Analyzing publicly available RNAseq datasets, we found that the majority of SlCLE genes are preferentially expressed in root tissues. We could confirm the biological activities of selected SlCLE peptides which had a conserved potency like their Arabidopsis orthologs to suppress primary root growth. We show, that root responses are mediated by SlCLAVATA2, indicating the conservation of CLE perception mechanism.

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“…The genome-wide analyses of CLE genes have been performed in many plant genomes, including tomato, rice, wheat, maize, soybean, grape, potato and cucumber [19][20][21][22]. Due to the small gene size and high sequence variability, the annotation is challenging.…”

Section: Introductionmentioning

confidence: 99%

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

2022

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Background In eukaryotes, cell-to-cell communication relies on the activity of small signaling peptides. In plant genomes, many hundreds of genes encode for such short peptide signals. However, only few of them are functionally characterized and due to the small gene size and high sequence variability, the comprehensive identification of such peptide-encoded genes is challenging. The CLAVATA3 (CLV3)/EMBRYO SURROUNDING REGION-RELATED (CLE) gene family encodes for short peptides that have a role in plant meristem maintenance, vascular patterning and responses to environment. The full repertoire of CLE genes and the role of CLE signaling in tomato (Solanum lycopersicum)- one of the most important crop plants- has not yet been fully studied. Results By using a combined approach, we performed a genome-wide identification of CLE genes using the current tomato genome version SL 4.0. We identified 52 SlCLE genes, including 37 new non annotated before. By analyzing publicly available RNAseq datasets we could confirm the expression of 28 new SlCLE genes. We found that SlCLEs are often expressed in a tissue-, organ- or condition-specific manner. Our analysis shows an interesting gene diversification within the SlCLE family that seems to be a result of gene duplication events. Finally, we could show a biological activity of selected SlCLE peptides in the root growth arrest that was SlCLV2-dependent. Conclusions Our improved combined approach revealed 37 new SlCLE genes. These findings are crucial for better understanding of the CLE signaling in tomato. Our phylogenetic analysis pinpoints the closest homologs of Arabidopsis CLE genes in tomato genome and can give a hint about the function of newly identified SlCLEs. The strategy described here can be used to identify more precisely additional short genes in plant genomes. Finally, our work suggests that the mechanism of root-active CLE peptide perception is conserved between Arabidopsis and tomato. In conclusion, our work paves the way to further research on the CLE-dependent circuits modulating tomato development and physiological responses.

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Predicting and Clustering Plant CLE Genes with a New Method Developed Specifically for Short Amino Acid Sequences

Cited by 5 publications

References 9 publications

A group of CLE peptides regulates de novo shoot regeneration in Arabidopsis thaliana

A group of CLE peptides regulates de novo shoot regeneration in Arabidopsis thaliana

New insights into tomato CLE peptide repertoire and perception mechanisms

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

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