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SUPPRESSOR OF LLP1 1‐mediated C–terminal processing is critical for CLE19 peptide activity

Summary Cell‐to‐cell communication is essential for the coordinated development of multicellular organisms. Members of the CLAVATA3/EMBRYO‐SURROUNDING REGION‐RELATED (CLE) family, a group of small secretory peptides, are involved in these processes in plants. Although post‐translational modification...

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Published in:The Plant journal : for cell and molecular biology 2013-12, Vol.76 (6), p.970-981
Main Authors: Tamaki, Takayuki, Betsuyaku, Shigeyuki, Fujiwara, Masayuki, Fukao, Yoichiro, Fukuda, Hiroo, Sawa, Shinichiro
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container_title The Plant journal : for cell and molecular biology
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creator Tamaki, Takayuki
Betsuyaku, Shigeyuki
Fujiwara, Masayuki
Fukao, Yoichiro
Fukuda, Hiroo
Sawa, Shinichiro
description Summary Cell‐to‐cell communication is essential for the coordinated development of multicellular organisms. Members of the CLAVATA3/EMBRYO‐SURROUNDING REGION‐RELATED (CLE) family, a group of small secretory peptides, are involved in these processes in plants. Although post‐translational modifications are considered to be indispensable for their activity, the detailed mechanisms governing these modifications are not well understood. Here, we report that SUPPRESSOR OF LLP1 1 (SOL1), a putative Zn2+ carboxypeptidase previously isolated as a suppressor of the CLE19 over‐expression phenotype, functions in C–terminal processing of the CLE19 proprotein to produce the functional CLE19 peptide. Newly isolated sol1 mutants are resistant to CLE19 over‐expression, consistent with the previous report (Casamitjana‐Martinez, E., Hofhuis, H.F., Xu, J., Liu, C.M., Heidstra, R. and Scheres, B. (2003) Curr. Biol. 13, 1435–1441). As expected, our experiment using synthetic CLE19 peptide revealed that the sol1 mutation does not compromise CLE signal transduction pathways per se. SOL1 possesses enzymatic activity to remove the C–terminal arginine residue of CLE19 proprotein in vitro, and SOL1‐dependent cleavage of the C–terminal arginine residue is necessary for CLE19 activity in vivo. Additionally, the endosomal localization of SOL1 suggests that this processing occurs in endosomes in the secretory pathway. Thus, our data indicate the importance of C–terminal processing of CLE proproteins to ensure CLE activities.
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Members of the CLAVATA3/EMBRYO‐SURROUNDING REGION‐RELATED (CLE) family, a group of small secretory peptides, are involved in these processes in plants. Although post‐translational modifications are considered to be indispensable for their activity, the detailed mechanisms governing these modifications are not well understood. Here, we report that SUPPRESSOR OF LLP1 1 (SOL1), a putative Zn2+ carboxypeptidase previously isolated as a suppressor of the CLE19 over‐expression phenotype, functions in C–terminal processing of the CLE19 proprotein to produce the functional CLE19 peptide. Newly isolated sol1 mutants are resistant to CLE19 over‐expression, consistent with the previous report (Casamitjana‐Martinez, E., Hofhuis, H.F., Xu, J., Liu, C.M., Heidstra, R. and Scheres, B. (2003) Curr. Biol. 13, 1435–1441). As expected, our experiment using synthetic CLE19 peptide revealed that the sol1 mutation does not compromise CLE signal transduction pathways per se. SOL1 possesses enzymatic activity to remove the C–terminal arginine residue of CLE19 proprotein in vitro, and SOL1‐dependent cleavage of the C–terminal arginine residue is necessary for CLE19 activity in vivo. Additionally, the endosomal localization of SOL1 suggests that this processing occurs in endosomes in the secretory pathway. Thus, our data indicate the importance of C–terminal processing of CLE proproteins to ensure CLE activities.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.12349</identifier><identifier>PMID: 24118638</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject><![CDATA[Amino Acid Sequence ; Arabidopsis - cytology ; Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - isolation & purification ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; carboxypeptidase ; Carboxypeptidases - genetics ; Carboxypeptidases - isolation & purification ; Carboxypeptidases - metabolism ; Cellular biology ; CLE peptide ; CLE19 ; Endosomes - enzymology ; Estrogens - pharmacology ; Gene Expression ; Gene Expression Regulation, Enzymologic ; Gene Expression Regulation, Plant ; Genes, Reporter ; intercellular signaling ; Meristem - cytology ; Meristem - enzymology ; Meristem - genetics ; Meristem - growth & development ; Molecular Sequence Data ; Mutagenesis, Insertional ; Nicotiana - enzymology ; Nicotiana - genetics ; Peptides ; Phenotype ; Plant biology ; Plant Roots - cytology ; Plant Roots - enzymology ; Plant Roots - genetics ; Plant Roots - growth & development ; Plant Shoots - cytology ; Plant Shoots - enzymology ; Plant Shoots - genetics ; Plant Shoots - growth & development ; Plants, Genetically Modified ; post‐translational processing ; Protein Processing, Post-Translational ; Signal Transduction ; SOL1]]></subject><ispartof>The Plant journal : for cell and molecular biology, 2013-12, Vol.76 (6), p.970-981</ispartof><rights>2013 The Authors. 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Members of the CLAVATA3/EMBRYO‐SURROUNDING REGION‐RELATED (CLE) family, a group of small secretory peptides, are involved in these processes in plants. Although post‐translational modifications are considered to be indispensable for their activity, the detailed mechanisms governing these modifications are not well understood. Here, we report that SUPPRESSOR OF LLP1 1 (SOL1), a putative Zn2+ carboxypeptidase previously isolated as a suppressor of the CLE19 over‐expression phenotype, functions in C–terminal processing of the CLE19 proprotein to produce the functional CLE19 peptide. Newly isolated sol1 mutants are resistant to CLE19 over‐expression, consistent with the previous report (Casamitjana‐Martinez, E., Hofhuis, H.F., Xu, J., Liu, C.M., Heidstra, R. and Scheres, B. (2003) Curr. Biol. 13, 1435–1441). As expected, our experiment using synthetic CLE19 peptide revealed that the sol1 mutation does not compromise CLE signal transduction pathways per se. SOL1 possesses enzymatic activity to remove the C–terminal arginine residue of CLE19 proprotein in vitro, and SOL1‐dependent cleavage of the C–terminal arginine residue is necessary for CLE19 activity in vivo. Additionally, the endosomal localization of SOL1 suggests that this processing occurs in endosomes in the secretory pathway. 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Members of the CLAVATA3/EMBRYO‐SURROUNDING REGION‐RELATED (CLE) family, a group of small secretory peptides, are involved in these processes in plants. Although post‐translational modifications are considered to be indispensable for their activity, the detailed mechanisms governing these modifications are not well understood. Here, we report that SUPPRESSOR OF LLP1 1 (SOL1), a putative Zn2+ carboxypeptidase previously isolated as a suppressor of the CLE19 over‐expression phenotype, functions in C–terminal processing of the CLE19 proprotein to produce the functional CLE19 peptide. Newly isolated sol1 mutants are resistant to CLE19 over‐expression, consistent with the previous report (Casamitjana‐Martinez, E., Hofhuis, H.F., Xu, J., Liu, C.M., Heidstra, R. and Scheres, B. (2003) Curr. Biol. 13, 1435–1441). As expected, our experiment using synthetic CLE19 peptide revealed that the sol1 mutation does not compromise CLE signal transduction pathways per se. SOL1 possesses enzymatic activity to remove the C–terminal arginine residue of CLE19 proprotein in vitro, and SOL1‐dependent cleavage of the C–terminal arginine residue is necessary for CLE19 activity in vivo. Additionally, the endosomal localization of SOL1 suggests that this processing occurs in endosomes in the secretory pathway. Thus, our data indicate the importance of C–terminal processing of CLE proproteins to ensure CLE activities.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>24118638</pmid><doi>10.1111/tpj.12349</doi><tpages>12</tpages></addata></record>
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subjects Amino Acid Sequence
Arabidopsis - cytology
Arabidopsis - enzymology
Arabidopsis - genetics
Arabidopsis - growth & development
Arabidopsis Proteins - genetics
Arabidopsis Proteins - isolation & purification
Arabidopsis Proteins - metabolism
Arabidopsis thaliana
carboxypeptidase
Carboxypeptidases - genetics
Carboxypeptidases - isolation & purification
Carboxypeptidases - metabolism
Cellular biology
CLE peptide
CLE19
Endosomes - enzymology
Estrogens - pharmacology
Gene Expression
Gene Expression Regulation, Enzymologic
Gene Expression Regulation, Plant
Genes, Reporter
intercellular signaling
Meristem - cytology
Meristem - enzymology
Meristem - genetics
Meristem - growth & development
Molecular Sequence Data
Mutagenesis, Insertional
Nicotiana - enzymology
Nicotiana - genetics
Peptides
Phenotype
Plant biology
Plant Roots - cytology
Plant Roots - enzymology
Plant Roots - genetics
Plant Roots - growth & development
Plant Shoots - cytology
Plant Shoots - enzymology
Plant Shoots - genetics
Plant Shoots - growth & development
Plants, Genetically Modified
post‐translational processing
Protein Processing, Post-Translational
Signal Transduction
SOL1
title SUPPRESSOR OF LLP1 1‐mediated C–terminal processing is critical for CLE19 peptide activity
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