The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis

The Arabidopsis <i>PROSCOOP</i> genes belong to a family predicted to encode secreted pro-peptides, which undergo maturation steps to produce peptides named SCOOP. Some of them are involved in defence signalling through their perception by a receptor complex including MIK2, BAK1 and BKK1...

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Main Authors: Marie-Charlotte Guillou, Thierry Balliau, Emilie Vergne, Hervé Canut, Josiane Chourré, Claudia Herrera-León, Francisco Ramos-Martín, Masoud Ahmadi-Afzadi, Nicola D’Amelio, Eric Ruelland, Michel Zivy, Jean-Pierre Renou, Elisabeth Jamet, Sébastien Aubourg
Format: Article
Language:English
Published: MDPI AG 2022-12-01
Series:Plants
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Online Access:https://www.mdpi.com/2223-7747/11/24/3554
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author Marie-Charlotte Guillou
Thierry Balliau
Emilie Vergne
Hervé Canut
Josiane Chourré
Claudia Herrera-León
Francisco Ramos-Martín
Masoud Ahmadi-Afzadi
Nicola D’Amelio
Eric Ruelland
Michel Zivy
Jean-Pierre Renou
Elisabeth Jamet
Sébastien Aubourg
author_facet Marie-Charlotte Guillou
Thierry Balliau
Emilie Vergne
Hervé Canut
Josiane Chourré
Claudia Herrera-León
Francisco Ramos-Martín
Masoud Ahmadi-Afzadi
Nicola D’Amelio
Eric Ruelland
Michel Zivy
Jean-Pierre Renou
Elisabeth Jamet
Sébastien Aubourg
author_sort Marie-Charlotte Guillou
collection DOAJ
description The Arabidopsis <i>PROSCOOP</i> genes belong to a family predicted to encode secreted pro-peptides, which undergo maturation steps to produce peptides named SCOOP. Some of them are involved in defence signalling through their perception by a receptor complex including MIK2, BAK1 and BKK1. Here, we focused on the <i>PROSCOOP10</i> gene, which is highly and constitutively expressed in aerial organs. The MS/MS analyses of leaf apoplastic fluids allowed the identification of two distinct peptides (named SCOOP10#1 and SCOOP10#2) covering two different regions of PROSCOOP10. They both possess the canonical S-X-S family motif and have hydroxylated prolines. This identification in apoplastic fluids confirms the biological reality of SCOOP peptides for the first time. NMR and molecular dynamics studies showed that the SCOOP10 peptides, although largely unstructured in solution, tend to assume a hairpin-like fold, exposing the two serine residues previously identified as essential for the peptide activity. Furthermore, <i>PROSCOOP10</i> mutations led to an early-flowering phenotype and increased expression of the floral integrators <i>SOC1</i> and <i>LEAFY</i>, consistent with the de-regulated transcription of <i>PROSCOOP10</i> in several other mutants displaying early- or late-flowering phenotypes. These results suggest a role for <i>PROSCOOP10</i> in flowering time, highlighting the functional diversity within the <i>PROSCOOP</i> family.
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spelling doaj.art-da9bfc6e50724d4eab3366eaf5a0aabb2023-11-24T17:29:18ZengMDPI AGPlants2223-77472022-12-011124355410.3390/plants11243554The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in ArabidopsisMarie-Charlotte Guillou0Thierry Balliau1Emilie Vergne2Hervé Canut3Josiane Chourré4Claudia Herrera-León5Francisco Ramos-Martín6Masoud Ahmadi-Afzadi7Nicola D’Amelio8Eric Ruelland9Michel Zivy10Jean-Pierre Renou11Elisabeth Jamet12Sébastien Aubourg13Institut Agro, SFR QUASAV, IRHS, Université Angers, INRAE, F-49000 Angers, FranceAgroParisTech, GQE—Le Moulon, PAPPSO, Université Paris-Saclay, INRAE, CNRS, F-91190 Gif-sur-Yvette, FranceInstitut Agro, SFR QUASAV, IRHS, Université Angers, INRAE, F-49000 Angers, FranceLaboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, Toulouse INP, CNRS, F-31320 Auzeville-Tolosane, FranceLaboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, Toulouse INP, CNRS, F-31320 Auzeville-Tolosane, FranceUnité de Génie Enzymatique et Cellulaire UMR 7025 CNRS, Université de Picardie Jules Verne, F-80039 Amiens, FranceUnité de Génie Enzymatique et Cellulaire UMR 7025 CNRS, Université de Picardie Jules Verne, F-80039 Amiens, FranceInstitut Agro, SFR QUASAV, IRHS, Université Angers, INRAE, F-49000 Angers, FranceUnité de Génie Enzymatique et Cellulaire UMR 7025 CNRS, Université de Picardie Jules Verne, F-80039 Amiens, FranceUnité de Génie Enzymatique et Cellulaire UMR 7025 CNRS, Université de Technologie de Compiègne, F-60203 Compiègne, FranceAgroParisTech, GQE—Le Moulon, PAPPSO, Université Paris-Saclay, INRAE, CNRS, F-91190 Gif-sur-Yvette, FranceInstitut Agro, SFR QUASAV, IRHS, Université Angers, INRAE, F-49000 Angers, FranceLaboratoire de Recherche en Sciences Végétales, Université de Toulouse, UPS, Toulouse INP, CNRS, F-31320 Auzeville-Tolosane, FranceInstitut Agro, SFR QUASAV, IRHS, Université Angers, INRAE, F-49000 Angers, FranceThe Arabidopsis <i>PROSCOOP</i> genes belong to a family predicted to encode secreted pro-peptides, which undergo maturation steps to produce peptides named SCOOP. Some of them are involved in defence signalling through their perception by a receptor complex including MIK2, BAK1 and BKK1. Here, we focused on the <i>PROSCOOP10</i> gene, which is highly and constitutively expressed in aerial organs. The MS/MS analyses of leaf apoplastic fluids allowed the identification of two distinct peptides (named SCOOP10#1 and SCOOP10#2) covering two different regions of PROSCOOP10. They both possess the canonical S-X-S family motif and have hydroxylated prolines. This identification in apoplastic fluids confirms the biological reality of SCOOP peptides for the first time. NMR and molecular dynamics studies showed that the SCOOP10 peptides, although largely unstructured in solution, tend to assume a hairpin-like fold, exposing the two serine residues previously identified as essential for the peptide activity. Furthermore, <i>PROSCOOP10</i> mutations led to an early-flowering phenotype and increased expression of the floral integrators <i>SOC1</i> and <i>LEAFY</i>, consistent with the de-regulated transcription of <i>PROSCOOP10</i> in several other mutants displaying early- or late-flowering phenotypes. These results suggest a role for <i>PROSCOOP10</i> in flowering time, highlighting the functional diversity within the <i>PROSCOOP</i> family.https://www.mdpi.com/2223-7747/11/24/3554phytocytokineapoplasmpost-translational modificationfloweringArabidopsispeptidomics
spellingShingle Marie-Charlotte Guillou
Thierry Balliau
Emilie Vergne
Hervé Canut
Josiane Chourré
Claudia Herrera-León
Francisco Ramos-Martín
Masoud Ahmadi-Afzadi
Nicola D’Amelio
Eric Ruelland
Michel Zivy
Jean-Pierre Renou
Elisabeth Jamet
Sébastien Aubourg
The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis
Plants
phytocytokine
apoplasm
post-translational modification
flowering
Arabidopsis
peptidomics
title The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis
title_full The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis
title_fullStr The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis
title_full_unstemmed The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis
title_short The <i>PROSCOOP10</i> Gene Encodes Two Extracellular Hydroxylated Peptides and Impacts Flowering Time in Arabidopsis
title_sort i proscoop10 i gene encodes two extracellular hydroxylated peptides and impacts flowering time in arabidopsis
topic phytocytokine
apoplasm
post-translational modification
flowering
Arabidopsis
peptidomics
url https://www.mdpi.com/2223-7747/11/24/3554
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