Conserved Cytochrome P450 Evolved in Seed Plants Regulates Flower Maturation
Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared ea...
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Published in | Molecular Plant Vol. 8; no. 12; pp. 1751 - 1765 |
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Main Authors | , , , , , , , , , , , , , , , |
Format | Journal Article |
Language | English |
Published |
England
Elsevier Inc
07.12.2015
Elsevier BV Cell Press/Oxford UP |
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Abstract | Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A 1 showed a restricted tissue-specific expres- sion in the tapetum of flower buds and in the anther filaments upon anthesis, cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expres- sion analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modi- fication of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expan- sion and volatile emission. It is thus expected to be an important determinant of flower-insect interaction. |
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AbstractList | Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A1 showed a restricted tissue-specific expression in the tapetum of flower buds and in the anther filaments upon anthesis. cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expression analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modification of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expansion and volatile emission. It is thus expected to be an important determinant of flower-insect interaction. Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A1 showed a restricted tissue-specific expression in the tapetum of flower buds and in the anther filaments upon anthesis. cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expression analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modification of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expansion and volatile emission. It is thus expected to be an important determinant of flower–insect interaction. This article proposes a new phylogenomic approach to identify genes with essential functions in plant signaling metabolism. CYP715, a candidate selected based on its high conservation in plant genomes, is shown to regulate flower maturation. Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A1 showed a restricted tissue-specific expression in the tapetum of flower buds and in the anther filaments upon anthesis. cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expression analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modification of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expansion and volatile emission. It is thus expected to be an important determinant of flower-insect interaction.Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A1 showed a restricted tissue-specific expression in the tapetum of flower buds and in the anther filaments upon anthesis. cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expression analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modification of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expansion and volatile emission. It is thus expected to be an important determinant of flower-insect interaction. Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A 1 showed a restricted tissue-specific expres- sion in the tapetum of flower buds and in the anther filaments upon anthesis, cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expres- sion analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modi- fication of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expan- sion and volatile emission. It is thus expected to be an important determinant of flower-insect interaction. |
Author | Zhenhua Liu Benoit Boachon RaphaelLugan Raquel Tavares Mathieu Erhardt Jerome Mutterer Valerie Demais Stephanie Pateyron Veronique Brunaud Toshiyuki Ohnishi Ales Pencik Patrick Achard Fan Gong Peter Hedden Daniele Werck-Reichhart Hugues Renault |
AuthorAffiliation | Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France Laboratoire de Biometrie et Biologie Evolutive, Universite Lyon 1, CNRS, 69622 Villeurbanne, France plateforme d'lmagerie In Vitro, IFR 37 de Neurosciences, 67084 Strasbourg, France Transcriptomic Platform, Unite de Recherche en Genomique Vegetale (URGV), INRA, Universite d'Evry Val d'Essonne, CNRS, 91057 Evry, France Bioinformatics for Predictive Genomics, URGV, INRA, Universite d'Evry Val d'Essonne, CNRS, 91057 Evry, France Graduate School of Agriculture, Shizuoka University, Shizuoka, 422-8529 Japan Laboratory of Growth Regulators & Department of Chemical Biology and Genetics, Centre of the Region Hana for Biotechnological and Agricultural Research, Faculty of Science, Palacky University & Institute of Experimental Botany AS CR, 771 47 Olomouc, Czech Republic Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK University of Strasbourg In |
Author_xml | – sequence: 1 givenname: Zhenhua surname: Liu fullname: Liu, Zhenhua organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 2 givenname: Benoît surname: Boachon fullname: Boachon, Benoît organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 3 givenname: Raphaël surname: Lugan fullname: Lugan, Raphaël organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 4 givenname: Raquel surname: Tavares fullname: Tavares, Raquel organization: Laboratoire de Biométrie et Biologie Évolutive, Université Lyon 1, CNRS, 69622 Villeurbanne, France – sequence: 5 givenname: Mathieu surname: Erhardt fullname: Erhardt, Mathieu organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 6 givenname: Jérôme surname: Mutterer fullname: Mutterer, Jérôme organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 7 givenname: Valérie surname: Demais fullname: Demais, Valérie organization: Plateforme d’Imagerie In Vitro, IFR 37 de Neurosciences, 67084 Strasbourg, France – sequence: 8 givenname: Stéphanie surname: Pateyron fullname: Pateyron, Stéphanie organization: Transcriptomic Platform, Unité de Recherche en Génomique Végétale (URGV), INRA, Université d'Evry Val d'Essonne, CNRS, 91057 Evry, France – sequence: 9 givenname: Véronique surname: Brunaud fullname: Brunaud, Véronique organization: Bioinformatics for Predictive Genomics, URGV, INRA, Université d'Evry Val d'Essonne, CNRS, 91057 Evry, France – sequence: 10 givenname: Toshiyuki surname: Ohnishi fullname: Ohnishi, Toshiyuki organization: Graduate School of Agriculture, Shizuoka University, Shizuoka, 422-8529 Japan – sequence: 11 givenname: Ales surname: Pencik fullname: Pencik, Ales organization: Laboratory of Growth Regulators & Department of Chemical Biology and Genetics, Centre of the Region Haná for Biotechnological and Agricultural Research, Faculty of Science, Palacký University & Institute of Experimental Botany AS CR, 771 47 Olomouc, Czech Republic – sequence: 12 givenname: Patrick surname: Achard fullname: Achard, Patrick organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 13 givenname: Fan surname: Gong fullname: Gong, Fan organization: Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK – sequence: 14 givenname: Peter surname: Hedden fullname: Hedden, Peter organization: Rothamsted Research, Harpenden, Hertfordshire AL5 2JQ, UK – sequence: 15 givenname: Danièle surname: Werck-Reichhart fullname: Werck-Reichhart, Danièle email: daniele.werck@ibmp-cnrs.unistra.fr organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France – sequence: 16 givenname: Hugues surname: Renault fullname: Renault, Hugues organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France |
BackLink | https://cir.nii.ac.jp/crid/1871146592822379776$$DView record in CiNii https://www.ncbi.nlm.nih.gov/pubmed/26388305$$D View this record in MEDLINE/PubMed https://hal.science/hal-02437969$$DView record in HAL |
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ContentType | Journal Article |
Contributor | China Scholarship Council ; Region Alsace ; Agence Nationale pour la Recherche via the PHENOWALL ANR-10-BLAN-1528 ; Freiburg Institute for Advanced Studies (FRIAS) ;University of Strasbourg Institute for Advanced Study (USIAS) ; Ministry of Education, Youth and Sport of the Czech Republic LO1204 ; European Fund for Regional Development Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE) Sexe et évolution ; Département PEGASE [LBBE] (PEGASE) ; Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetA |
Contributor_xml | – sequence: 1 fullname: Institut de Biologie Moléculaire des Plantes (IBMP) ; Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS) – sequence: 2 fullname: Sexe et évolution [LBBE] ; Département PEGASE [LBBE] (PEGASE) ; Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS) – sequence: 3 fullname: Plateforme d'Imagerie In Vitro ; Université de Strasbourg (UNISTRA)-Institut Fédératif de Recherche 37 des Neurosciences – sequence: 4 fullname: Institut des Sciences des Plantes de Paris-Saclay (IPS2 (UMR_9213 / UMR_1403)) ; Institut National de la Recherche Agronomique (INRA)-Université Paris-Sud - Paris 11 (UP11)-Université Paris Diderot - Paris 7 (UPD7)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS) – sequence: 5 fullname: Unité Mathématique Informatique et Génome (MIG) ; 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Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Laboratoire de Biométrie et Biologie Evolutive - UMR 5558 (LBBE) ; Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Institut National de Recherche en Informatique et en Automatique (Inria)-VetAgro Sup - Institut national d'enseignement supérieur et de recherche en alimentation, santé animale, sciences agronomiques et de l'environnement (VAS)-Centre National de la Recherche Scientifique (CNRS) – sequence: 9 fullname: Institut de biologie moléculaire des plantes (IBMP) ; 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Copyright | 2015 The Author Copyright © 2015 The Author. Published by Elsevier Inc. All rights reserved. Distributed under a Creative Commons Attribution 4.0 International License |
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DocumentTitleAlternate | Conserved Cytochrome P450 Evolved in Seed Plants Regulates Flower Maturation |
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Issue | 12 |
Keywords | volatile compounds flower development gibberellins negative selection jasmonate phylogenomics |
Language | English |
License | http://www.elsevier.com/open-access/userlicense/1.0 https://www.elsevier.com/tdm/userlicense/1.0 Copyright © 2015 The Author. Published by Elsevier Inc. All rights reserved. Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0 |
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Notes | 31-2013/Q flower development, phylogenomics, negative selection, jasmonate, gibberellins, volatile compounds Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have essential functions. Based on this rationale, we investigated the function of the low-duplicated CYP715 cytochrome P450 gene family that appeared early in seed plants and evolved under strong negative selection. Arabidopsis CYP715A 1 showed a restricted tissue-specific expres- sion in the tapetum of flower buds and in the anther filaments upon anthesis, cyp715a1 insertion lines showed a strong defect in petal development, and transient alteration of pollen intine deposition. Comparative expres- sion analysis revealed the downregulated expression of genes involved in pollen development, cell wall biogenesis, hormone homeostasis, and floral sesquiterpene biosynthesis, especially TPS21 and several key genes regulating floral development such as MYB21, MYB24, and MYC2. Accordingly, floral sesquiterpene emission was suppressed in the cyp715a1 mutants. Flower hormone profiling, in addition, indicated a modi- fication of gibberellin homeostasis and a strong disturbance of the turnover of jasmonic acid derivatives. Petal growth was partially restored by the active gibberellin GA3 or the functional analog of jasmonoyl-isoleucine, coronatine. CYP715 appears to function as a key regulator of flower maturation, synchronizing petal expan- sion and volatile emission. It is thus expected to be an important determinant of flower-insect interaction. ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
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Title | Conserved Cytochrome P450 Evolved in Seed Plants Regulates Flower Maturation |
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