Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis

Abstract 12-cis-oxo-phytodienoic acid (OPDA), a precursor of jasmonoyl-isoleucine (JA-Ile), is known to have distinct signaling roles in Arabidopsis, as shown in studies using the opr3 mutant, which lacks OPDA REDUCTASE3 (OPR3). This mutant, however, accumulates low levels of JA-Ile through an OPR2-...

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Main Authors: Khansa Mekkaoui, Ranjit Baral, Fiona Smith, Moritz Klein, Ivo Feussner, Bettina Hause
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-61832-9
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author Khansa Mekkaoui
Ranjit Baral
Fiona Smith
Moritz Klein
Ivo Feussner
Bettina Hause
author_facet Khansa Mekkaoui
Ranjit Baral
Fiona Smith
Moritz Klein
Ivo Feussner
Bettina Hause
author_sort Khansa Mekkaoui
collection DOAJ
description Abstract 12-cis-oxo-phytodienoic acid (OPDA), a precursor of jasmonoyl-isoleucine (JA-Ile), is known to have distinct signaling roles in Arabidopsis, as shown in studies using the opr3 mutant, which lacks OPDA REDUCTASE3 (OPR3). This mutant, however, accumulates low levels of JA-Ile through an OPR2-mediated bypass. To investigate OPDA signaling, the wound-induced transcriptome of the opr2opr3 mutant is compared to that of wild-type and allene oxide synthase mutant. Endogenous OPDA shows no unique transcriptional signature under control or wounding conditions, and previously identified OPDA-responsive genes are wound-induced independently of OPDA. Applying OPDA to opr2opr3 triggers a distinct response suggesting compartmentalization of endogenously formed OPDA. Trans-organellar complementation reveals that expression of OPR3 or OPR2 in opr2opr3 restores JA-Ile production regardless of localization, whereas mitochondrial targeted OPR1 exhibiting low OPDA/4,5-ddh-JA conversion activity does not. Our findings show that OPDA primarily serves as a JA precursor with limited independent signaling functions in the early wound response.
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spelling doaj-art-8f8a32b3dcbe40fbbb6562b53949887b2025-08-20T03:43:14ZengNature PortfolioNature Communications2041-17232025-07-0116111710.1038/s41467-025-61832-9Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in ArabidopsisKhansa Mekkaoui0Ranjit Baral1Fiona Smith2Moritz Klein3Ivo Feussner4Bettina Hause5Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Weinberg 3Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Weinberg 3Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Weinberg 3Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences and Goettingen Center for Molecular Biosciences (GZMB), University of Goettingen, Justus-von-Liebig-Weg 11Department of Plant Biochemistry, Albrecht-von-Haller-Institute for Plant Sciences and Goettingen Center for Molecular Biosciences (GZMB), University of Goettingen, Justus-von-Liebig-Weg 11Department of Cell and Metabolic Biology, Leibniz Institute of Plant Biochemistry, Weinberg 3Abstract 12-cis-oxo-phytodienoic acid (OPDA), a precursor of jasmonoyl-isoleucine (JA-Ile), is known to have distinct signaling roles in Arabidopsis, as shown in studies using the opr3 mutant, which lacks OPDA REDUCTASE3 (OPR3). This mutant, however, accumulates low levels of JA-Ile through an OPR2-mediated bypass. To investigate OPDA signaling, the wound-induced transcriptome of the opr2opr3 mutant is compared to that of wild-type and allene oxide synthase mutant. Endogenous OPDA shows no unique transcriptional signature under control or wounding conditions, and previously identified OPDA-responsive genes are wound-induced independently of OPDA. Applying OPDA to opr2opr3 triggers a distinct response suggesting compartmentalization of endogenously formed OPDA. Trans-organellar complementation reveals that expression of OPR3 or OPR2 in opr2opr3 restores JA-Ile production regardless of localization, whereas mitochondrial targeted OPR1 exhibiting low OPDA/4,5-ddh-JA conversion activity does not. Our findings show that OPDA primarily serves as a JA precursor with limited independent signaling functions in the early wound response.https://doi.org/10.1038/s41467-025-61832-9
spellingShingle Khansa Mekkaoui
Ranjit Baral
Fiona Smith
Moritz Klein
Ivo Feussner
Bettina Hause
Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis
Nature Communications
title Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis
title_full Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis
title_fullStr Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis
title_full_unstemmed Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis
title_short Transcriptomics and trans-organellar complementation reveal limited signaling of 12-cis-oxo-phytodienoic acid during early wound response in Arabidopsis
title_sort transcriptomics and trans organellar complementation reveal limited signaling of 12 cis oxo phytodienoic acid during early wound response in arabidopsis
url https://doi.org/10.1038/s41467-025-61832-9
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