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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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 |
work_keys_str_mv |
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