N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis

Abstract After transcription, a messenger RNA (mRNA) is further post‐transcriptionally regulated by several features including RNA secondary structure and covalent RNA modifications (specifically N6‐methyladenosine, m6A). Both RNA secondary structure and m6A have been demonstrated to regulate mRNA s...

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Main Authors: Marianne C. Kramer, Kevin A. Janssen, Kyle Palos, Andrew D. L. Nelson, Lee E. Vandivier, Benjamin A. Garcia, Eric Lyons, Mark A. Beilstein, Brian D. Gregory
Format: Article
Language:English
Published: Wiley 2020-07-01
Series:Plant Direct
Subjects:
Online Access:https://doi.org/10.1002/pld3.239
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spelling doaj-80905837322145e8b608b1550305e4672021-05-02T20:21:55ZengWileyPlant Direct2475-44552020-07-0147n/an/a10.1002/pld3.239N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in ArabidopsisMarianne C. Kramer0Kevin A. Janssen1Kyle Palos2Andrew D. L. Nelson3Lee E. Vandivier4Benjamin A. Garcia5Eric Lyons6Mark A. Beilstein7Brian D. Gregory8Department of Biology University of Pennsylvania Philadelphia PA USADepartment of Biochemistry and Biophysics Perelman School of Medicine University of Pennsylvania Philadelphia PA USASchool of Plant Sciences University of Arizona Tucson AZ USABoyce Thompson Institute Cornell University Ithaca NY USADepartment of Biology University of Pennsylvania Philadelphia PA USADepartment of Biochemistry and Biophysics Perelman School of Medicine University of Pennsylvania Philadelphia PA USASchool of Plant Sciences University of Arizona Tucson AZ USASchool of Plant Sciences University of Arizona Tucson AZ USADepartment of Biology University of Pennsylvania Philadelphia PA USAAbstract After transcription, a messenger RNA (mRNA) is further post‐transcriptionally regulated by several features including RNA secondary structure and covalent RNA modifications (specifically N6‐methyladenosine, m6A). Both RNA secondary structure and m6A have been demonstrated to regulate mRNA stability and translation and have been independently linked to plant responses to soil salinity levels. However, the effect of m6A on regulating RNA secondary structure and the combinatorial interplay between these two RNA features during salt stress response has yet to be studied. Here, we globally identify RNA‐protein interactions and RNA secondary structure during systemic salt stress. This analysis reveals that RNA secondary structure changes significantly during salt stress, and that it is independent of global changes in RNA‐protein interactions. Conversely, we find that m6A is anti‐correlated with RNA secondary structure in a condition‐dependent manner, with salt‐specific m6A correlated with a decrease in mRNA secondary structure during salt stress. Taken together, we suggest that salt‐specific m6A deposition and the associated loss of RNA secondary structure results in increases in mRNA stability for transcripts encoding abiotic stress response proteins and ultimately increases in protein levels from these stabilized transcripts. In total, our comprehensive analyses reveal important post‐transcriptional regulatory mechanisms involved in plant long‐term salt stress response and adaptation.https://doi.org/10.1002/pld3.239non‐coding RNAspost‐transcriptional regulationRNA covalent modificationsRNA processingRNA stabilityRNA‐binding proteins
collection DOAJ
language English
format Article
sources DOAJ
author Marianne C. Kramer
Kevin A. Janssen
Kyle Palos
Andrew D. L. Nelson
Lee E. Vandivier
Benjamin A. Garcia
Eric Lyons
Mark A. Beilstein
Brian D. Gregory
spellingShingle Marianne C. Kramer
Kevin A. Janssen
Kyle Palos
Andrew D. L. Nelson
Lee E. Vandivier
Benjamin A. Garcia
Eric Lyons
Mark A. Beilstein
Brian D. Gregory
N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis
Plant Direct
non‐coding RNAs
post‐transcriptional regulation
RNA covalent modifications
RNA processing
RNA stability
RNA‐binding proteins
author_facet Marianne C. Kramer
Kevin A. Janssen
Kyle Palos
Andrew D. L. Nelson
Lee E. Vandivier
Benjamin A. Garcia
Eric Lyons
Mark A. Beilstein
Brian D. Gregory
author_sort Marianne C. Kramer
title N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis
title_short N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis
title_full N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis
title_fullStr N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis
title_full_unstemmed N6‐methyladenosine and RNA secondary structure affect transcript stability and protein abundance during systemic salt stress in Arabidopsis
title_sort n6‐methyladenosine and rna secondary structure affect transcript stability and protein abundance during systemic salt stress in arabidopsis
publisher Wiley
series Plant Direct
issn 2475-4455
publishDate 2020-07-01
description Abstract After transcription, a messenger RNA (mRNA) is further post‐transcriptionally regulated by several features including RNA secondary structure and covalent RNA modifications (specifically N6‐methyladenosine, m6A). Both RNA secondary structure and m6A have been demonstrated to regulate mRNA stability and translation and have been independently linked to plant responses to soil salinity levels. However, the effect of m6A on regulating RNA secondary structure and the combinatorial interplay between these two RNA features during salt stress response has yet to be studied. Here, we globally identify RNA‐protein interactions and RNA secondary structure during systemic salt stress. This analysis reveals that RNA secondary structure changes significantly during salt stress, and that it is independent of global changes in RNA‐protein interactions. Conversely, we find that m6A is anti‐correlated with RNA secondary structure in a condition‐dependent manner, with salt‐specific m6A correlated with a decrease in mRNA secondary structure during salt stress. Taken together, we suggest that salt‐specific m6A deposition and the associated loss of RNA secondary structure results in increases in mRNA stability for transcripts encoding abiotic stress response proteins and ultimately increases in protein levels from these stabilized transcripts. In total, our comprehensive analyses reveal important post‐transcriptional regulatory mechanisms involved in plant long‐term salt stress response and adaptation.
topic non‐coding RNAs
post‐transcriptional regulation
RNA covalent modifications
RNA processing
RNA stability
RNA‐binding proteins
url https://doi.org/10.1002/pld3.239
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