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 inMolecular Plant Vol. 8; no. 12; pp. 1751 - 1765
Main Authors Liu, Zhenhua, Boachon, Benoît, Lugan, Raphaël, Tavares, Raquel, Erhardt, Mathieu, Mutterer, Jérôme, Demais, Valérie, Pateyron, Stéphanie, Brunaud, Véronique, Ohnishi, Toshiyuki, Pencik, Ales, Achard, Patrick, Gong, Fan, Hedden, Peter, Werck-Reichhart, Danièle, Renault, Hugues
Format Journal Article
LanguageEnglish
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.
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
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  surname: Renault
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  organization: Institute of Plant Molecular Biology, Centre National de la Recherche Scientifique (CNRS), University of Strasbourg, 67084 Strasbourg, France
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ContentType Journal Article
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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)
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
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Copyright 2015 The Author
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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.
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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.
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PublicationTitle Molecular Plant
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Snippet Global inspection of plant genomes identifies genes maintained in low copies across taxa and under strong purifying selection, which are likely to have...
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SubjectTerms [SDV.BV]Life Sciences [q-bio]/Vegetal Biology
[SDV]Life Sciences [q-bio]
Arabidopsis
Arabidopsis - classification
Arabidopsis - enzymology
Arabidopsis - genetics
Arabidopsis - growth & development
Arabidopsis Proteins
Arabidopsis Proteins - chemistry
Arabidopsis Proteins - genetics
Arabidopsis Proteins - metabolism
biogenesis
biosynthesis
buds
cell walls
Conserved Sequence
cytochrome P-450
Cytochrome P-450 Enzyme System
Cytochrome P-450 Enzyme System - chemistry
Cytochrome P-450 Enzyme System - genetics
Cytochrome P-450 Enzyme System - metabolism
flower development
flowering
Flowers
Flowers - classification
Flowers - enzymology
Flowers - genetics
Flowers - growth & development
gene expression
gene expression regulation
Gene Expression Regulation, Developmental
Gene Expression Regulation, Plant
genes
gibberellic acid
gibberellins
homeostasis
jasmonate
jasmonic acid
Life Sciences
Molecular Biology
mutants
negative selection
phylogenomics
Phylogeny
Plant Science
Plants
Plants - classification
Plants - enzymology
Plants - genetics
pollen
Seeds
Seeds - classification
Seeds - enzymology
Seeds - genetics
Seeds - growth & development
sesquiterpenoids
Vegetal Biology
volatile compounds
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Title Conserved Cytochrome P450 Evolved in Seed Plants Regulates Flower Maturation
URI http://lib.cqvip.com/qk/90143B/201512/667237367.html
https://dx.doi.org/10.1016/j.molp.2015.09.002
https://cir.nii.ac.jp/crid/1871146592822379776
https://www.ncbi.nlm.nih.gov/pubmed/26388305
https://www.proquest.com/docview/1749612337
https://www.proquest.com/docview/2000313192
https://hal.science/hal-02437969
Volume 8
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