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Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme

Jasmonic acid (JA) and its biologically active form jasmonoyl-L-isoleucine (JA-Ile) regulate defense responses to various environmental stresses and developmental processes in plants. JA and JA-Ile are synthesized from α-linolenic acids derived from membrane lipids via 12-oxo-phytodienoic acid (OPDA...

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Autores principales: Inagaki, Hideo, Miyamoto, Koji, Ando, Noriko, Murakami, Kohei, Sugisawa, Koki, Morita, Shion, Yumoto, Emi, Teruya, Miyu, Uchida, Kenichi, Kato, Nobuki, Kaji, Takuya, Takaoka, Yousuke, Hojo, Yuko, Shinya, Tomonori, Galis, Ivan, Nozawa, Akira, Sawasaki, Tatsuya, Nojiri, Hideaki, Ueda, Minoru, Okada, Kazunori
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8201998/
https://www.ncbi.nlm.nih.gov/pubmed/34135933
http://dx.doi.org/10.3389/fpls.2021.688565
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author Inagaki, Hideo
Miyamoto, Koji
Ando, Noriko
Murakami, Kohei
Sugisawa, Koki
Morita, Shion
Yumoto, Emi
Teruya, Miyu
Uchida, Kenichi
Kato, Nobuki
Kaji, Takuya
Takaoka, Yousuke
Hojo, Yuko
Shinya, Tomonori
Galis, Ivan
Nozawa, Akira
Sawasaki, Tatsuya
Nojiri, Hideaki
Ueda, Minoru
Okada, Kazunori
author_facet Inagaki, Hideo
Miyamoto, Koji
Ando, Noriko
Murakami, Kohei
Sugisawa, Koki
Morita, Shion
Yumoto, Emi
Teruya, Miyu
Uchida, Kenichi
Kato, Nobuki
Kaji, Takuya
Takaoka, Yousuke
Hojo, Yuko
Shinya, Tomonori
Galis, Ivan
Nozawa, Akira
Sawasaki, Tatsuya
Nojiri, Hideaki
Ueda, Minoru
Okada, Kazunori
author_sort Inagaki, Hideo
collection PubMed
description Jasmonic acid (JA) and its biologically active form jasmonoyl-L-isoleucine (JA-Ile) regulate defense responses to various environmental stresses and developmental processes in plants. JA and JA-Ile are synthesized from α-linolenic acids derived from membrane lipids via 12-oxo-phytodienoic acid (OPDA). In the presence of JA-Ile, the COI1 receptor physically interacts with JAZ repressors, leading to their degradation, resulting in the transcription of JA-responsive genes by MYC transcription factors. Although the biosynthesis of JA-Ile is conserved in vascular plants, it is not recognized by COI1 in bryophytes and is not biologically active. In the liverwort Marchantia polymorpha, dinor-OPDA (dn-OPDA), a homolog of OPDA with two fewer carbons, and its isomer dn-iso-OPDA accumulate after wounding and are recognized by COI1 to activate downstream signaling. The moss Calohypnum plumiforme produces the antimicrobial-specialized metabolites, momilactones. It has been reported that JA and JA-Ile are not detected in C. plumiforme and that OPDA, but not JA, can induce momilactone accumulation and the expression of these biosynthetic genes, suggesting that OPDA or its derivative is a biologically active molecule in C. plumiforme that induces chemical defense. In the present study, we investigated the biological functions of OPDA and its derivatives in C. plumiforme. Searching for the components potentially involving oxylipin signaling from transcriptomic and genomic data revealed that two COI1, three JAZ, and two MYC genes were present. Quantification analyses revealed that OPDA and its isomer iso-OPDA accumulated in larger amounts than dn-OPDA and dn-iso-OPDA after wounding. Moreover, exogenously applied OPDA, dn-OPDA, or dn-iso-OPDA induced the transcription of JAZ genes. These results imply that OPDA, dn-OPDA, and/or their isomers potentially act as biologically active molecules to induce the signaling downstream of COI1-JAZ. Furthermore, co-immunoprecipitation analysis showed the physical interaction between JAZs and MYCs, indicating the functional conservation of JAZs in C. plumiforme with other plants. These results suggest that COI1-JAZ-MYC mediated signaling is conserved and functional in C. plumiforme.
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spelling pubmed-82019982021-06-15 Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme Inagaki, Hideo Miyamoto, Koji Ando, Noriko Murakami, Kohei Sugisawa, Koki Morita, Shion Yumoto, Emi Teruya, Miyu Uchida, Kenichi Kato, Nobuki Kaji, Takuya Takaoka, Yousuke Hojo, Yuko Shinya, Tomonori Galis, Ivan Nozawa, Akira Sawasaki, Tatsuya Nojiri, Hideaki Ueda, Minoru Okada, Kazunori Front Plant Sci Plant Science Jasmonic acid (JA) and its biologically active form jasmonoyl-L-isoleucine (JA-Ile) regulate defense responses to various environmental stresses and developmental processes in plants. JA and JA-Ile are synthesized from α-linolenic acids derived from membrane lipids via 12-oxo-phytodienoic acid (OPDA). In the presence of JA-Ile, the COI1 receptor physically interacts with JAZ repressors, leading to their degradation, resulting in the transcription of JA-responsive genes by MYC transcription factors. Although the biosynthesis of JA-Ile is conserved in vascular plants, it is not recognized by COI1 in bryophytes and is not biologically active. In the liverwort Marchantia polymorpha, dinor-OPDA (dn-OPDA), a homolog of OPDA with two fewer carbons, and its isomer dn-iso-OPDA accumulate after wounding and are recognized by COI1 to activate downstream signaling. The moss Calohypnum plumiforme produces the antimicrobial-specialized metabolites, momilactones. It has been reported that JA and JA-Ile are not detected in C. plumiforme and that OPDA, but not JA, can induce momilactone accumulation and the expression of these biosynthetic genes, suggesting that OPDA or its derivative is a biologically active molecule in C. plumiforme that induces chemical defense. In the present study, we investigated the biological functions of OPDA and its derivatives in C. plumiforme. Searching for the components potentially involving oxylipin signaling from transcriptomic and genomic data revealed that two COI1, three JAZ, and two MYC genes were present. Quantification analyses revealed that OPDA and its isomer iso-OPDA accumulated in larger amounts than dn-OPDA and dn-iso-OPDA after wounding. Moreover, exogenously applied OPDA, dn-OPDA, or dn-iso-OPDA induced the transcription of JAZ genes. These results imply that OPDA, dn-OPDA, and/or their isomers potentially act as biologically active molecules to induce the signaling downstream of COI1-JAZ. Furthermore, co-immunoprecipitation analysis showed the physical interaction between JAZs and MYCs, indicating the functional conservation of JAZs in C. plumiforme with other plants. These results suggest that COI1-JAZ-MYC mediated signaling is conserved and functional in C. plumiforme. Frontiers Media S.A. 2021-05-31 /pmc/articles/PMC8201998/ /pubmed/34135933 http://dx.doi.org/10.3389/fpls.2021.688565 Text en Copyright © 2021 Inagaki, Miyamoto, Ando, Murakami, Sugisawa, Morita, Yumoto, Teruya, Uchida, Kato, Kaji, Takaoka, Hojo, Shinya, Galis, Nozawa, Sawasaki, Nojiri, Ueda and Okada. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Inagaki, Hideo
Miyamoto, Koji
Ando, Noriko
Murakami, Kohei
Sugisawa, Koki
Morita, Shion
Yumoto, Emi
Teruya, Miyu
Uchida, Kenichi
Kato, Nobuki
Kaji, Takuya
Takaoka, Yousuke
Hojo, Yuko
Shinya, Tomonori
Galis, Ivan
Nozawa, Akira
Sawasaki, Tatsuya
Nojiri, Hideaki
Ueda, Minoru
Okada, Kazunori
Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
title Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
title_full Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
title_fullStr Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
title_full_unstemmed Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
title_short Deciphering OPDA Signaling Components in the Momilactone-Producing Moss Calohypnum plumiforme
title_sort deciphering opda signaling components in the momilactone-producing moss calohypnum plumiforme
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8201998/
https://www.ncbi.nlm.nih.gov/pubmed/34135933
http://dx.doi.org/10.3389/fpls.2021.688565
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