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Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions

BACKGROUND: Shifts in dynamic equilibria of the abundance of cellular molecules in plant-pathogen interactions need further exploration. We induced PTI in optimally growing Arabidopsis thaliana seedlings for 16 h, returning them to growth conditions for another 16 h. METHODS: Turn-over and abundance...

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Autores principales: Abukhalaf, Mohammad, Proksch, Carsten, Thieme, Domenika, Ziegler, Jörg, Hoehenwarter, Wolfgang
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634109/
https://www.ncbi.nlm.nih.gov/pubmed/37940940
http://dx.doi.org/10.1186/s12915-023-01739-3
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author Abukhalaf, Mohammad
Proksch, Carsten
Thieme, Domenika
Ziegler, Jörg
Hoehenwarter, Wolfgang
author_facet Abukhalaf, Mohammad
Proksch, Carsten
Thieme, Domenika
Ziegler, Jörg
Hoehenwarter, Wolfgang
author_sort Abukhalaf, Mohammad
collection PubMed
description BACKGROUND: Shifts in dynamic equilibria of the abundance of cellular molecules in plant-pathogen interactions need further exploration. We induced PTI in optimally growing Arabidopsis thaliana seedlings for 16 h, returning them to growth conditions for another 16 h. METHODS: Turn-over and abundance of 99 flg22 responding proteins were measured chronologically using a stable heavy nitrogen isotope partial labeling strategy and targeted liquid chromatography coupled to mass spectrometry (PRM LC–MS). These experiments were complemented by measurements of mRNA and phytohormone levels. RESULTS: Changes in synthesis and degradation rate constants (K(s) and K(d)) regulated tryptophane and glucosinolate, IAA transport, and photosynthesis-associated protein (PAP) homeostasis in growth/PTI transitions independently of mRNA levels. K(s) values increased after elicitation while protein and mRNA levels became uncorrelated. mRNA returned to pre-elicitation levels, yet protein abundance remained at PTI levels even 16 h after media exchange, indicating protein levels were robust and unresponsive to transition back to growth. The abundance of 23 PAPs including FERREDOXIN-NADP( +)-OXIDOREDUCTASE (FNR1) decreased 16 h after PAMP exposure, their depletion was nearly abolished in the myc234 mutant. FNR1 K(d) increased as mRNA levels decreased early in PTI, its K(s) decreased in prolonged PTI. FNR1 K(d) was lower in myc234, mRNA levels decreased as in wild type. CONCLUSIONS: Protein K(d) and K(s) values change in response to flg22 exposure and constitute an additional layer of protein abundance regulation in growth defense transitions next to changes in mRNA levels. Our results suggest photosystem remodeling in PTI to direct electron flow away from the photosynthetic carbon reaction towards ROS production as an active defense mechanism controlled post-transcriptionally and by MYC2 and homologs. Target proteins accumulated later and PAP and auxin/IAA depletion was repressed in myc234 indicating a positive effect of the transcription factors in the establishment of PTI. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01739-3.
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spelling pubmed-106341092023-11-10 Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions Abukhalaf, Mohammad Proksch, Carsten Thieme, Domenika Ziegler, Jörg Hoehenwarter, Wolfgang BMC Biol Research Article BACKGROUND: Shifts in dynamic equilibria of the abundance of cellular molecules in plant-pathogen interactions need further exploration. We induced PTI in optimally growing Arabidopsis thaliana seedlings for 16 h, returning them to growth conditions for another 16 h. METHODS: Turn-over and abundance of 99 flg22 responding proteins were measured chronologically using a stable heavy nitrogen isotope partial labeling strategy and targeted liquid chromatography coupled to mass spectrometry (PRM LC–MS). These experiments were complemented by measurements of mRNA and phytohormone levels. RESULTS: Changes in synthesis and degradation rate constants (K(s) and K(d)) regulated tryptophane and glucosinolate, IAA transport, and photosynthesis-associated protein (PAP) homeostasis in growth/PTI transitions independently of mRNA levels. K(s) values increased after elicitation while protein and mRNA levels became uncorrelated. mRNA returned to pre-elicitation levels, yet protein abundance remained at PTI levels even 16 h after media exchange, indicating protein levels were robust and unresponsive to transition back to growth. The abundance of 23 PAPs including FERREDOXIN-NADP( +)-OXIDOREDUCTASE (FNR1) decreased 16 h after PAMP exposure, their depletion was nearly abolished in the myc234 mutant. FNR1 K(d) increased as mRNA levels decreased early in PTI, its K(s) decreased in prolonged PTI. FNR1 K(d) was lower in myc234, mRNA levels decreased as in wild type. CONCLUSIONS: Protein K(d) and K(s) values change in response to flg22 exposure and constitute an additional layer of protein abundance regulation in growth defense transitions next to changes in mRNA levels. Our results suggest photosystem remodeling in PTI to direct electron flow away from the photosynthetic carbon reaction towards ROS production as an active defense mechanism controlled post-transcriptionally and by MYC2 and homologs. Target proteins accumulated later and PAP and auxin/IAA depletion was repressed in myc234 indicating a positive effect of the transcription factors in the establishment of PTI. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12915-023-01739-3. BioMed Central 2023-11-09 /pmc/articles/PMC10634109/ /pubmed/37940940 http://dx.doi.org/10.1186/s12915-023-01739-3 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Abukhalaf, Mohammad
Proksch, Carsten
Thieme, Domenika
Ziegler, Jörg
Hoehenwarter, Wolfgang
Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
title Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
title_full Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
title_fullStr Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
title_full_unstemmed Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
title_short Changing turn-over rates regulate abundance of tryptophan, GS biosynthesis, IAA transport and photosynthesis proteins in Arabidopsis growth defense transitions
title_sort changing turn-over rates regulate abundance of tryptophan, gs biosynthesis, iaa transport and photosynthesis proteins in arabidopsis growth defense transitions
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10634109/
https://www.ncbi.nlm.nih.gov/pubmed/37940940
http://dx.doi.org/10.1186/s12915-023-01739-3
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