Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for
Posttranscriptional and Translational Gene Regulation in
Arabidopsis

J 2020

Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis

RAXWAL, Vivek Kumar, C.G. SIMPSON, J. GLOGGNITZER, J.C. ENTINZE, W.B. GUO et. al.

Basic information

Original name

Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis

Authors

RAXWAL, Vivek Kumar (356 India, belonging to the institution), C.G. SIMPSON, J. GLOGGNITZER, J.C. ENTINZE, W.B. GUO, R.X. ZHANG, J.W.S. BROWN and Karel ŘÍHA (203 Czech Republic, guarantor, belonging to the institution)

Edition

Plant Cell, ROCKVILLE, AMER SOC PLANT BIOLOGISTS, 2020, 1040-4651

Other information

Language

English

Type of outcome

Článek v odborném periodiku

Field of Study

10611 Plant sciences, botany

Country of publisher

United States of America

Confidentiality degree

není předmětem státního či obchodního tajemství

References:

URL

Impact factor

Impact factor: 11.277

RIV identification code

RIV/00216224:14740/20:00114761

Organization unit

Central European Institute of Technology

DOI

http://dx.doi.org/10.1105/tpc.20.00244

UT WoS

000578504100015

Keywords in English

MESSENGER-RNA; TRIGGERED IMMUNITY; COMPLEX; NMD; IDENTIFICATION; TERMINATION; EXPRESSION; TRANSCRIPTOME; SURVEILLANCE; DEGRADATION

Abstract

V originále

Nonsense-mediated RNA decay (NMD) is an RNA control mechanism that has also been implicated in the broader regulation of gene expression. Nevertheless, a role for NMD in genome regulation has not yet been fully assessed, partially because NMD inactivation is lethal in many organisms. Here, we performed an in-depth comparative analysis of Arabidopsis (Arabidopsis thaliana) mutants lacking the NMD-related proteins UPF3, UPF1, and SMG7. We found different impacts of these proteins on NMD and the Arabidopsis transcriptome, with UPF1 having the biggest effect. Transcriptome assembly in UPF1-null plants revealed genome-wide changes in alternative splicing, suggesting that UPF1 functions in splicing. The inactivation of UPF1 led to translational repression, as manifested by a global shift in mRNAs from polysomes to monosomes and the downregulation of genes involved in translation and ribosome biogenesis. Despite these global changes, NMD targets and mRNAs expressed at low levels with short half-lives were enriched in the polysomes ofupf1mutants, indicating that UPF1/NMD suppresses the translation of aberrant RNAs. Particularly striking was an increase in the translation of TIR domain-containing, nucleotide binding, leucine-rich repeat (TNL) immune receptors. The regulation of TNLs via UPF1/NMD-mediated mRNA stability and translational derepression offers a dynamic mechanism for the rapid activation of TNLs in response to pathogen attack. The RNA helicase and ATPase UPF1 affects transcriptome homeostasis and gene expression through nonsense-mediated RNA decay, splicing, and translation in Arabidopsis.

Links

EF15_003/0000479, research and development project

Name: Regulace rostlinné meiózy

GA16-18578S, research and development project

Name: Funkce UPF1 helikázy v procesech odehrávajících se v buněčném jádře

Investor: Czech Science Foundation

Citovat

RAXWAL, Vivek Kumar, C.G. SIMPSON, J. GLOGGNITZER, J.C. ENTINZE, W.B. GUO, R.X. ZHANG, J.W.S. BROWN and Karel ŘÍHA. Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis. Plant Cell. ROCKVILLE: AMER SOC PLANT BIOLOGISTS, 2020, vol. 32, No 9, p. 2725-2741. ISSN 1040-4651. Available from: https://dx.doi.org/10.1105/tpc.20.00244.

@article{1749838,
   author = {Raxwal, Vivek Kumar and Simpson, C.G. and Gloggnitzer, J. and Entinze, J.C. and Guo, W.B. and Zhang, R.X. and Brown, J.W.S. and Říha, Karel},
   article_location = {ROCKVILLE},
   article_number = {9},
   doi = {http://dx.doi.org/10.1105/tpc.20.00244},
   keywords = {MESSENGER-RNA; TRIGGERED IMMUNITY; COMPLEX; NMD; IDENTIFICATION; TERMINATION; EXPRESSION; TRANSCRIPTOME; SURVEILLANCE; DEGRADATION},
   language = {eng},
   issn = {1040-4651},
   journal = {Plant Cell},
   title = {Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis},
   url = {https://academic.oup.com/plcell/article/32/9/2725/6115658},
   volume = {32},
   year = {2020}
}

TY  - JOUR
ID  - 1749838
AU  - Raxwal, Vivek Kumar - Simpson, C.G. - Gloggnitzer, J. - Entinze, J.C. - Guo, W.B. - Zhang, R.X. - Brown, J.W.S. - Říha, Karel
PY  - 2020
TI  - Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis
JF  - Plant Cell
VL  - 32
IS  - 9
SP  - 2725-2741
EP  - 2725-2741
PB  - AMER SOC PLANT BIOLOGISTS
SN  - 10404651
KW  - MESSENGER-RNA
KW  - TRIGGERED IMMUNITY
KW  - COMPLEX
KW  - NMD
KW  - IDENTIFICATION
KW  - TERMINATION
KW  - EXPRESSION
KW  - TRANSCRIPTOME
KW  - SURVEILLANCE
KW  - DEGRADATION
UR  - https://academic.oup.com/plcell/article/32/9/2725/6115658
N2  - Nonsense-mediated RNA decay (NMD) is an RNA control mechanism that has also been implicated in the broader regulation of gene expression. Nevertheless, a role for NMD in genome regulation has not yet been fully assessed, partially because NMD inactivation is lethal in many organisms. Here, we performed an in-depth comparative analysis of Arabidopsis (Arabidopsis thaliana) mutants lacking the NMD-related proteins UPF3, UPF1, and SMG7. We found different impacts of these proteins on NMD and the Arabidopsis transcriptome, with UPF1 having the biggest effect. Transcriptome assembly in UPF1-null plants revealed genome-wide changes in alternative splicing, suggesting that UPF1 functions in splicing. The inactivation of UPF1 led to translational repression, as manifested by a global shift in mRNAs from polysomes to monosomes and the downregulation of genes involved in translation and ribosome biogenesis. Despite these global changes, NMD targets and mRNAs expressed at low levels with short half-lives were enriched in the polysomes ofupf1mutants, indicating that UPF1/NMD suppresses the translation of aberrant RNAs. Particularly striking was an increase in the translation of TIR domain-containing, nucleotide binding, leucine-rich repeat (TNL) immune receptors. The regulation of TNLs via UPF1/NMD-mediated mRNA stability and translational derepression offers a dynamic mechanism for the rapid activation of TNLs in response to pathogen attack. The RNA helicase and ATPase UPF1 affects transcriptome homeostasis and gene expression through nonsense-mediated RNA decay, splicing, and translation in Arabidopsis.
ER  -

RAXWAL, Vivek Kumar, C.G. SIMPSON, J. GLOGGNITZER, J.C. ENTINZE, W.B. GUO, R.X. ZHANG, J.W.S. BROWN and Karel ŘÍHA. Nonsense-Mediated RNA Decay Factor UPF1 Is Critical for Posttranscriptional and Translational Gene Regulation in Arabidopsis. \textit{Plant Cell}. ROCKVILLE: AMER SOC PLANT BIOLOGISTS, 2020, vol.~32, No~9, p.~2725-2741. ISSN~1040-4651. Available from: https://dx.doi.org/10.1105/tpc.20.00244.

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