Cargando…

A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity

Plants produce the volatile hormone ethylene to regulate many developmental processes and to deal with (a)biotic stressors. In seed plants, ethylene is synthesized from 1-aminocyclopropane-1-carboxylic acid (ACC) by the dedicated enzyme ACC oxidase (ACO). Ethylene biosynthesis is tightly regulated a...

Descripción completa

Detalles Bibliográficos
Autores principales: Vaughan-Hirsch, John, Li, Dongdong, Roig Martinez, Albert, Roden, Stijn, Pattyn, Jolien, Taira, Shu, Shikano, Hitomi, Miyama, Yoko, Okano, Yukari, Voet, Arnout, Van de Poel, Bram
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9510837/
https://www.ncbi.nlm.nih.gov/pubmed/36172554
http://dx.doi.org/10.3389/fpls.2022.995073
_version_ 1784797529670418432
author Vaughan-Hirsch, John
Li, Dongdong
Roig Martinez, Albert
Roden, Stijn
Pattyn, Jolien
Taira, Shu
Shikano, Hitomi
Miyama, Yoko
Okano, Yukari
Voet, Arnout
Van de Poel, Bram
author_facet Vaughan-Hirsch, John
Li, Dongdong
Roig Martinez, Albert
Roden, Stijn
Pattyn, Jolien
Taira, Shu
Shikano, Hitomi
Miyama, Yoko
Okano, Yukari
Voet, Arnout
Van de Poel, Bram
author_sort Vaughan-Hirsch, John
collection PubMed
description Plants produce the volatile hormone ethylene to regulate many developmental processes and to deal with (a)biotic stressors. In seed plants, ethylene is synthesized from 1-aminocyclopropane-1-carboxylic acid (ACC) by the dedicated enzyme ACC oxidase (ACO). Ethylene biosynthesis is tightly regulated at the level of ACC through ACC synthesis, conjugation and transport. ACC is a non-proteinogenic amino acid, which also has signaling roles independent from ethylene. In this work, we investigated the biological function of an uncharacterized ACC dipeptide. The custom-synthesized di-ACC molecule can be taken up by Arabidopsis in a similar way as ACC, in part via Lysine Histidine Transporters (e.g., LHT1). Using Nano-Particle Assisted Laser Desoprtion/Ionization (Nano-PALDI) mass-spectrometry imaging, we revealed that externally fed di-ACC predominantly localizes to the vasculature tissue, despite it not being detectable in control hypocotyl segments. Once taken up, the ACC dimer can evoke a triple response phenotype in dark-grown seedlings, reminiscent of ethylene responses induced by ACC itself, albeit less efficiently compared to ACC. Di-ACC does not act via ACC-signaling, but operates via the known ethylene signaling pathway. In vitro ACO activity and molecular docking showed that di-ACC can be used as an alternative substrate by ACO to form ethylene. The promiscuous nature of ACO for the ACC dimer also explains the higher ethylene production rates observed in planta, although this reaction occurred less efficiently compared to ACC. Overall, the ACC dipeptide seems to be transported and converted into ethylene in a similar way as ACC, and is able to augment ethylene production levels and induce subsequent ethylene responses in Arabidopsis.
format Online
Article
Text
id pubmed-9510837
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-95108372022-09-27 A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity Vaughan-Hirsch, John Li, Dongdong Roig Martinez, Albert Roden, Stijn Pattyn, Jolien Taira, Shu Shikano, Hitomi Miyama, Yoko Okano, Yukari Voet, Arnout Van de Poel, Bram Front Plant Sci Plant Science Plants produce the volatile hormone ethylene to regulate many developmental processes and to deal with (a)biotic stressors. In seed plants, ethylene is synthesized from 1-aminocyclopropane-1-carboxylic acid (ACC) by the dedicated enzyme ACC oxidase (ACO). Ethylene biosynthesis is tightly regulated at the level of ACC through ACC synthesis, conjugation and transport. ACC is a non-proteinogenic amino acid, which also has signaling roles independent from ethylene. In this work, we investigated the biological function of an uncharacterized ACC dipeptide. The custom-synthesized di-ACC molecule can be taken up by Arabidopsis in a similar way as ACC, in part via Lysine Histidine Transporters (e.g., LHT1). Using Nano-Particle Assisted Laser Desoprtion/Ionization (Nano-PALDI) mass-spectrometry imaging, we revealed that externally fed di-ACC predominantly localizes to the vasculature tissue, despite it not being detectable in control hypocotyl segments. Once taken up, the ACC dimer can evoke a triple response phenotype in dark-grown seedlings, reminiscent of ethylene responses induced by ACC itself, albeit less efficiently compared to ACC. Di-ACC does not act via ACC-signaling, but operates via the known ethylene signaling pathway. In vitro ACO activity and molecular docking showed that di-ACC can be used as an alternative substrate by ACO to form ethylene. The promiscuous nature of ACO for the ACC dimer also explains the higher ethylene production rates observed in planta, although this reaction occurred less efficiently compared to ACC. Overall, the ACC dipeptide seems to be transported and converted into ethylene in a similar way as ACC, and is able to augment ethylene production levels and induce subsequent ethylene responses in Arabidopsis. Frontiers Media S.A. 2022-09-12 /pmc/articles/PMC9510837/ /pubmed/36172554 http://dx.doi.org/10.3389/fpls.2022.995073 Text en Copyright © 2022 Vaughan-Hirsch, Li, Roig Martinez, Roden, Pattyn, Taira, Shikano, Miyama, Okano, Voet and Van de Poel. 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
Vaughan-Hirsch, John
Li, Dongdong
Roig Martinez, Albert
Roden, Stijn
Pattyn, Jolien
Taira, Shu
Shikano, Hitomi
Miyama, Yoko
Okano, Yukari
Voet, Arnout
Van de Poel, Bram
A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity
title A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity
title_full A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity
title_fullStr A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity
title_full_unstemmed A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity
title_short A 1-aminocyclopropane-1-carboxylic-acid (ACC) dipeptide elicits ethylene responses through ACC-oxidase mediated substrate promiscuity
title_sort 1-aminocyclopropane-1-carboxylic-acid (acc) dipeptide elicits ethylene responses through acc-oxidase mediated substrate promiscuity
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9510837/
https://www.ncbi.nlm.nih.gov/pubmed/36172554
http://dx.doi.org/10.3389/fpls.2022.995073
work_keys_str_mv AT vaughanhirschjohn a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT lidongdong a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT roigmartinezalbert a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT rodenstijn a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT pattynjolien a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT tairashu a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT shikanohitomi a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT miyamayoko a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT okanoyukari a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT voetarnout a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT vandepoelbram a1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT vaughanhirschjohn 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT lidongdong 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT roigmartinezalbert 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT rodenstijn 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT pattynjolien 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT tairashu 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT shikanohitomi 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT miyamayoko 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT okanoyukari 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT voetarnout 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity
AT vandepoelbram 1aminocyclopropane1carboxylicacidaccdipeptideelicitsethyleneresponsesthroughaccoxidasemediatedsubstratepromiscuity