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Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems

Due to their sessile nature, plants rely on root systems to mediate many biotic and abiotic cues. To overcome these challenges, the root proteome is shaped to specific responses. Proteome-wide reprogramming events are magnified in meristems due to their active protein production. Using meristems as...

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Autores principales: Martinez-Seidel, Federico, Suwanchaikasem, Pipob, Nie, Shuai, Leeming, Michael G., Pereira Firmino, Alexandre Augusto, Williamson, Nicholas A., Kopka, Joachim, Roessner, Ute, Boughton, Berin A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8121087/
https://www.ncbi.nlm.nih.gov/pubmed/33995454
http://dx.doi.org/10.3389/fpls.2021.656683
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author Martinez-Seidel, Federico
Suwanchaikasem, Pipob
Nie, Shuai
Leeming, Michael G.
Pereira Firmino, Alexandre Augusto
Williamson, Nicholas A.
Kopka, Joachim
Roessner, Ute
Boughton, Berin A.
author_facet Martinez-Seidel, Federico
Suwanchaikasem, Pipob
Nie, Shuai
Leeming, Michael G.
Pereira Firmino, Alexandre Augusto
Williamson, Nicholas A.
Kopka, Joachim
Roessner, Ute
Boughton, Berin A.
author_sort Martinez-Seidel, Federico
collection PubMed
description Due to their sessile nature, plants rely on root systems to mediate many biotic and abiotic cues. To overcome these challenges, the root proteome is shaped to specific responses. Proteome-wide reprogramming events are magnified in meristems due to their active protein production. Using meristems as a test system, here, we study the major rewiring that plants undergo during cold acclimation. We performed tandem mass tag-based bottom-up quantitative proteomics of two consecutive segments of barley seminal root apexes subjected to suboptimal temperatures. After comparing changes in total and ribosomal protein (RP) fraction-enriched contents with shifts in individual protein abundances, we report ribosome accumulation accompanied by an intricate translational reprogramming in the distal apex zone. Reprogramming ranges from increases in ribosome biogenesis to protein folding factors and suggests roles for cold-specific RP paralogs. Ribosome biogenesis is the largest cellular investment; thus, the vast accumulation of ribosomes and specific translation-related proteins during cold acclimation could imply a divergent ribosomal population that would lead to a proteome shift across the root. Consequently, beyond the translational reprogramming, we report a proteome rewiring. First, triggered protein accumulation includes spliceosome activity in the root tip and a ubiquitous upregulation of glutathione production and S-glutathionylation (S-GSH) assemblage machineries in both root zones. Second, triggered protein depletion includes intrinsically enriched proteins in the tip-adjacent zone, which comprise the plant immune system. In summary, ribosome and translation-related protein accumulation happens concomitantly to a proteome reprogramming in barley root meristems during cold acclimation. The cold-accumulated proteome is functionally implicated in feedbacking transcript to protein translation at both ends and could guide cold acclimation.
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spelling pubmed-81210872021-05-15 Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems Martinez-Seidel, Federico Suwanchaikasem, Pipob Nie, Shuai Leeming, Michael G. Pereira Firmino, Alexandre Augusto Williamson, Nicholas A. Kopka, Joachim Roessner, Ute Boughton, Berin A. Front Plant Sci Plant Science Due to their sessile nature, plants rely on root systems to mediate many biotic and abiotic cues. To overcome these challenges, the root proteome is shaped to specific responses. Proteome-wide reprogramming events are magnified in meristems due to their active protein production. Using meristems as a test system, here, we study the major rewiring that plants undergo during cold acclimation. We performed tandem mass tag-based bottom-up quantitative proteomics of two consecutive segments of barley seminal root apexes subjected to suboptimal temperatures. After comparing changes in total and ribosomal protein (RP) fraction-enriched contents with shifts in individual protein abundances, we report ribosome accumulation accompanied by an intricate translational reprogramming in the distal apex zone. Reprogramming ranges from increases in ribosome biogenesis to protein folding factors and suggests roles for cold-specific RP paralogs. Ribosome biogenesis is the largest cellular investment; thus, the vast accumulation of ribosomes and specific translation-related proteins during cold acclimation could imply a divergent ribosomal population that would lead to a proteome shift across the root. Consequently, beyond the translational reprogramming, we report a proteome rewiring. First, triggered protein accumulation includes spliceosome activity in the root tip and a ubiquitous upregulation of glutathione production and S-glutathionylation (S-GSH) assemblage machineries in both root zones. Second, triggered protein depletion includes intrinsically enriched proteins in the tip-adjacent zone, which comprise the plant immune system. In summary, ribosome and translation-related protein accumulation happens concomitantly to a proteome reprogramming in barley root meristems during cold acclimation. The cold-accumulated proteome is functionally implicated in feedbacking transcript to protein translation at both ends and could guide cold acclimation. Frontiers Media S.A. 2021-04-30 /pmc/articles/PMC8121087/ /pubmed/33995454 http://dx.doi.org/10.3389/fpls.2021.656683 Text en Copyright © 2021 Martinez-Seidel, Suwanchaikasem, Nie, Leeming, Pereira Firmino, Williamson, Kopka, Roessner and Boughton. 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
Martinez-Seidel, Federico
Suwanchaikasem, Pipob
Nie, Shuai
Leeming, Michael G.
Pereira Firmino, Alexandre Augusto
Williamson, Nicholas A.
Kopka, Joachim
Roessner, Ute
Boughton, Berin A.
Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems
title Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems
title_full Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems
title_fullStr Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems
title_full_unstemmed Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems
title_short Membrane-Enriched Proteomics Link Ribosome Accumulation and Proteome Reprogramming With Cold Acclimation in Barley Root Meristems
title_sort membrane-enriched proteomics link ribosome accumulation and proteome reprogramming with cold acclimation in barley root meristems
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8121087/
https://www.ncbi.nlm.nih.gov/pubmed/33995454
http://dx.doi.org/10.3389/fpls.2021.656683
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