Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation

Abstract The phenylpropanoid cinnamic acid (CA) is a plant metabolite that can occur under a trans‐ or cis‐form. In contrast to the proven bioactivity of the cis‐form (c‐CA), the activity of trans‐CA (t‐CA) is still a matter of debate. We tested both compounds using a submerged rice coleoptile assay...

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Main Authors: Lena Vlaminck, Brix De Rouck, Sandrien Desmet, Thijs Van Gerrewey, Geert Goeminne, Lien De Smet, Veronique Storme, Tina Kyndt, Kristof Demeestere, Godelieve Gheysen, Dirk Inzé, Bartel Vanholme, Stephen Depuydt
Format: Article
Language:English
Published: Wiley 2022-12-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.465
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author Lena Vlaminck
Brix De Rouck
Sandrien Desmet
Thijs Van Gerrewey
Geert Goeminne
Lien De Smet
Veronique Storme
Tina Kyndt
Kristof Demeestere
Godelieve Gheysen
Dirk Inzé
Bartel Vanholme
Stephen Depuydt
author_facet Lena Vlaminck
Brix De Rouck
Sandrien Desmet
Thijs Van Gerrewey
Geert Goeminne
Lien De Smet
Veronique Storme
Tina Kyndt
Kristof Demeestere
Godelieve Gheysen
Dirk Inzé
Bartel Vanholme
Stephen Depuydt
author_sort Lena Vlaminck
collection DOAJ
description Abstract The phenylpropanoid cinnamic acid (CA) is a plant metabolite that can occur under a trans‐ or cis‐form. In contrast to the proven bioactivity of the cis‐form (c‐CA), the activity of trans‐CA (t‐CA) is still a matter of debate. We tested both compounds using a submerged rice coleoptile assay and demonstrated that they have opposite effects on cell elongation. Notably, in the tip of rice coleoptile t‐CA showed an inhibiting and c‐CA a stimulating activity. By combining transcriptomics and (untargeted) metabolomics with activity assays and genetic and pharmacological experiments, we aimed to explain the underlying mechanistic processes. We propose a model in which c‐CA treatment activates proton pumps and stimulates acidification of the apoplast, which in turn leads to the loosening of the cell wall, necessary for elongation. We hypothesize that c‐CA also inactivates auxin efflux transporters, which might cause a local auxin accumulation in the tip of the coleoptile. For t‐CA, the phenotype can partially be explained by a stimulation of cell wall polysaccharide feruloylation, leading to a more rigid cell wall. Metabolite profiling also demonstrated that salicylic acid (SA) derivatives are increased upon t‐CA treatment. As SA is a known antagonist of auxin, the shift in SA homeostasis provides an additional explanation of the observed t‐CA‐mediated restriction on cell growth.
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spelling doaj.art-9d87d8396a7447ea820c8014c8d6d92b2022-12-27T02:44:34ZengWileyPlant Direct2475-44552022-12-01612n/an/a10.1002/pld3.465Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongationLena Vlaminck0Brix De Rouck1Sandrien Desmet2Thijs Van Gerrewey3Geert Goeminne4Lien De Smet5Veronique Storme6Tina Kyndt7Kristof Demeestere8Godelieve Gheysen9Dirk Inzé10Bartel Vanholme11Stephen Depuydt12Department of Plant Biotechnology and Bioinformatics Ghent University Ghent BelgiumLaboratory of Plant Growth Analysis Ghent University Global Campus Incheon South KoreaVIB Metabolomics Core Ghent Ghent BelgiumLaboratory of Plant Growth Analysis Ghent University Global Campus Incheon South KoreaVIB Metabolomics Core Ghent Ghent BelgiumDepartment of Biotechnology Ghent University Ghent BelgiumDepartment of Plant Biotechnology and Bioinformatics Ghent University Ghent BelgiumDepartment of Biotechnology Ghent University Ghent BelgiumDepartment of Green Chemistry and Technology Ghent University Ghent BelgiumDepartment of Biotechnology Ghent University Ghent BelgiumDepartment of Plant Biotechnology and Bioinformatics Ghent University Ghent BelgiumDepartment of Plant Biotechnology and Bioinformatics Ghent University Ghent BelgiumDepartment of Plant Biotechnology and Bioinformatics Ghent University Ghent BelgiumAbstract The phenylpropanoid cinnamic acid (CA) is a plant metabolite that can occur under a trans‐ or cis‐form. In contrast to the proven bioactivity of the cis‐form (c‐CA), the activity of trans‐CA (t‐CA) is still a matter of debate. We tested both compounds using a submerged rice coleoptile assay and demonstrated that they have opposite effects on cell elongation. Notably, in the tip of rice coleoptile t‐CA showed an inhibiting and c‐CA a stimulating activity. By combining transcriptomics and (untargeted) metabolomics with activity assays and genetic and pharmacological experiments, we aimed to explain the underlying mechanistic processes. We propose a model in which c‐CA treatment activates proton pumps and stimulates acidification of the apoplast, which in turn leads to the loosening of the cell wall, necessary for elongation. We hypothesize that c‐CA also inactivates auxin efflux transporters, which might cause a local auxin accumulation in the tip of the coleoptile. For t‐CA, the phenotype can partially be explained by a stimulation of cell wall polysaccharide feruloylation, leading to a more rigid cell wall. Metabolite profiling also demonstrated that salicylic acid (SA) derivatives are increased upon t‐CA treatment. As SA is a known antagonist of auxin, the shift in SA homeostasis provides an additional explanation of the observed t‐CA‐mediated restriction on cell growth.https://doi.org/10.1002/pld3.465bioactivitycinnamic acidcoleoptile elongationOryza sativa
spellingShingle Lena Vlaminck
Brix De Rouck
Sandrien Desmet
Thijs Van Gerrewey
Geert Goeminne
Lien De Smet
Veronique Storme
Tina Kyndt
Kristof Demeestere
Godelieve Gheysen
Dirk Inzé
Bartel Vanholme
Stephen Depuydt
Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation
Plant Direct
bioactivity
cinnamic acid
coleoptile elongation
Oryza sativa
title Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation
title_full Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation
title_fullStr Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation
title_full_unstemmed Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation
title_short Opposing effects of trans‐ and cis‐cinnamic acid during rice coleoptile elongation
title_sort opposing effects of trans and cis cinnamic acid during rice coleoptile elongation
topic bioactivity
cinnamic acid
coleoptile elongation
Oryza sativa
url https://doi.org/10.1002/pld3.465
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