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

Abstract 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...

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Main Authors: Samy Carbonnel, Laurent Falquet, Ora Hazak
Format: Article
Language:English
Published: BMC 2022-11-01
Series:BMC Genomics
Subjects:
Online Access:https://doi.org/10.1186/s12864-022-08980-0
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author Samy Carbonnel
Laurent Falquet
Ora Hazak
author_facet Samy Carbonnel
Laurent Falquet
Ora Hazak
author_sort Samy Carbonnel
collection DOAJ
description Abstract 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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spelling doaj.art-83831b1c6d4b47e7803861b2b58a61932022-12-22T04:18:21ZengBMCBMC Genomics1471-21642022-11-0123111410.1186/s12864-022-08980-0Deeper genomic insights into tomato CLE genes repertoire identify new active peptidesSamy Carbonnel0Laurent Falquet1Ora Hazak2Department of Biology, University of FribourgDepartment of Biology, University of FribourgDepartment of Biology, University of FribourgAbstract 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.https://doi.org/10.1186/s12864-022-08980-0Tomato CLE genesPhylogenetic analysisExpression analysisRoot cell division arrestSlCLAVATA2
spellingShingle Samy Carbonnel
Laurent Falquet
Ora Hazak
Deeper genomic insights into tomato CLE genes repertoire identify new active peptides
BMC Genomics
Tomato CLE genes
Phylogenetic analysis
Expression analysis
Root cell division arrest
SlCLAVATA2
title Deeper genomic insights into tomato CLE genes repertoire identify new active peptides
title_full Deeper genomic insights into tomato CLE genes repertoire identify new active peptides
title_fullStr Deeper genomic insights into tomato CLE genes repertoire identify new active peptides
title_full_unstemmed Deeper genomic insights into tomato CLE genes repertoire identify new active peptides
title_short Deeper genomic insights into tomato CLE genes repertoire identify new active peptides
title_sort deeper genomic insights into tomato cle genes repertoire identify new active peptides
topic Tomato CLE genes
Phylogenetic analysis
Expression analysis
Root cell division arrest
SlCLAVATA2
url https://doi.org/10.1186/s12864-022-08980-0
work_keys_str_mv AT samycarbonnel deepergenomicinsightsintotomatoclegenesrepertoireidentifynewactivepeptides
AT laurentfalquet deepergenomicinsightsintotomatoclegenesrepertoireidentifynewactivepeptides
AT orahazak deepergenomicinsightsintotomatoclegenesrepertoireidentifynewactivepeptides