RETRACTED ARTICLE: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation

Mark Bailey; Aiste Ivanauskaite; Julia Grimmer; Oluwatunmise Akintewe; Adrienne C Payne; Rory Osborne; Anne-Marie Labandera; Ross D Etherington; Marjaana Rantala; Sacha Baginsky; Paula Mulo; Daniel J Gibbs

doi:10.1038/s41467-020-20506-4

RETRACTED ARTICLE: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation

Mark Bailey, Aiste Ivanauskaite, Julia Grimmer, Oluwatunmise Akintewe, Adrienne C Payne, Rory Osborne, Anne-Marie Labandera, Ross D Etherington, Marjaana Rantala, Sacha Baginsky, Paula Mulo, Daniel J Gibbs^*

^*Corresponding author for this work

Biosciences

Research output: Contribution to journal › Article › peer-review

2 Citations (Scopus)

165 Downloads (Pure)

Abstract

Chloroplast function requires the coordinated action of nuclear- and chloroplast-derived proteins, including several hundred nuclear-encoded pentatricopeptide repeat (PPR) proteins that regulate plastid mRNA metabolism. Despite their large number and importance, regulatory mechanisms controlling PPR expression are poorly understood. Here we show that the Arabidopsis NOT4A ubiquitin-ligase positively regulates the expression of PROTON GRADIENT REGULATION 3 (PGR3), a PPR protein required for translating several thylakoid-localised photosynthetic components and ribosome subunits within chloroplasts. Loss of NOT4A function leads to a strong depletion of cytochrome b6f and NAD(P)H dehydrogenase (NDH) complexes, as well as plastid 30 S ribosomes, which reduces mRNA translation and photosynthetic capacity, causing pale-yellow and slow-growth phenotypes. Quantitative transcriptome and proteome analysis of the not4a mutant reveal it lacks PGR3 expression, and that its molecular defects resemble those of a pgr3 mutant. Furthermore, we show that normal plastid function is restored to not4a through transgenic PGR3 expression. Our work identifies NOT4A as crucial for ensuring robust photosynthetic function during development and stress-response, through promoting PGR3 production and chloroplast translation.

Original language	English
Article number	251
Number of pages	15
Journal	Nature Communications
Volume	12
Issue number	1
Early online date	11 Jan 2021
DOIs	https://doi.org/10.1038/s41467-020-20506-4
Publication status	Published - Dec 2021

Bibliographical note

Funding Information:
This work was supported by Biotechnology and Biological Sciences Research Council grants [BB/M020568/1 and BB/T004002/1] and a European Research Council grant [ERC Starting Grant 715441-GasPlaNt] to D.J.G., an EMBO Short-Term Fellowship [Grant number 8104] to M.B., Academy of Finland grants [307335 and 321616] for A.I., M.R. and P.M., and the Doctoral Programme in Molecular Life Sciences at the University of Turku (A.I.). We would like to thank Laura Laihonen for her assistance within the PM group. S.B. gratefully acknowledges support from the DFG with grant number BA 1902/ 3-2. Collaboration between D.J.G. and P.M. was facilitated via the European Research Area Network for Coordinating Action in Plant Sciences (ERA-CAPS) project “KatNat”. We thank Dr Alessandro Di Mio and the BALM facility at the University of Birmingham for support with confocal analyses.

Publisher Copyright:
© 2021, The Author(s).

Keywords

Arabidopsis Proteins/chemistry
Arabidopsis/genetics
Chloroplasts/metabolism
Gene Expression Regulation, Plant
Gene Ontology
Mutation/genetics
Photosynthesis
Protein Biosynthesis
Protein Domains
RNA, Messenger/genetics
RNA-Binding Proteins/chemistry
Ribosomes/metabolism
Seedlings/growth & development
Ubiquitin-Protein Ligases/chemistry

ASJC Scopus subject areas

General Physics and Astronomy
General Chemistry
General Biochemistry,Genetics and Molecular Biology

Access to Document

10.1038/s41467-020-20506-4Licence: Creative Commons: Attribution (CC BY)

BaileyM2021ArabidopsisFinal published version, 4.4 MBLicence: Creative Commons: Attribution (CC BY)

2 Citations
1 Comment/debate

Retraction Note: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation
Bailey, M., Ivanauskaite, A., Grimmer, J., Akintewe, O., Payne, A. C., Osborne, R., Labandera, A.-M., Etherington, R. D., Rantala, M., Baginsky, S., Mulo, P. & Gibbs, D. J., 20 May 2022, In: Nature Communications. 13, 15 p., 2913.
Research output: Contribution to journal › Comment/debate

Open Access

2 Finished

H2020_ERC_GASPLANT_COORDINATOR
Gibbs, D. (Principal Investigator)
European Commission
1/03/17 → 30/06/23
Project: EU
N-terminal acetylation as a signal for protein degradation controlling plant development and stress responses
Gibbs, D. (Principal Investigator)
Biotechnology & Biological Sciences Research Council
1/09/15 → 31/08/18
Project: Research Councils

Cite this

Bailey, M., Ivanauskaite, A., Grimmer, J., Akintewe, O., Payne, A. C., Osborne, R., Labandera, A.-M., Etherington, R. D., Rantala, M., Baginsky, S., Mulo, P., & Gibbs, D. J. (2021). RETRACTED ARTICLE: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation. Nature Communications, 12(1), Article 251. https://doi.org/10.1038/s41467-020-20506-4

@article{46d54d82de9d464c85f9b01f5a59230f,

title = "RETRACTED ARTICLE: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation",

abstract = "Chloroplast function requires the coordinated action of nuclear- and chloroplast-derived proteins, including several hundred nuclear-encoded pentatricopeptide repeat (PPR) proteins that regulate plastid mRNA metabolism. Despite their large number and importance, regulatory mechanisms controlling PPR expression are poorly understood. Here we show that the Arabidopsis NOT4A ubiquitin-ligase positively regulates the expression of PROTON GRADIENT REGULATION 3 (PGR3), a PPR protein required for translating several thylakoid-localised photosynthetic components and ribosome subunits within chloroplasts. Loss of NOT4A function leads to a strong depletion of cytochrome b6f and NAD(P)H dehydrogenase (NDH) complexes, as well as plastid 30 S ribosomes, which reduces mRNA translation and photosynthetic capacity, causing pale-yellow and slow-growth phenotypes. Quantitative transcriptome and proteome analysis of the not4a mutant reveal it lacks PGR3 expression, and that its molecular defects resemble those of a pgr3 mutant. Furthermore, we show that normal plastid function is restored to not4a through transgenic PGR3 expression. Our work identifies NOT4A as crucial for ensuring robust photosynthetic function during development and stress-response, through promoting PGR3 production and chloroplast translation.",

keywords = "Arabidopsis Proteins/chemistry, Arabidopsis/genetics, Chloroplasts/metabolism, Gene Expression Regulation, Plant, Gene Ontology, Mutation/genetics, Photosynthesis, Protein Biosynthesis, Protein Domains, RNA, Messenger/genetics, RNA-Binding Proteins/chemistry, Ribosomes/metabolism, Seedlings/growth & development, Ubiquitin-Protein Ligases/chemistry",

author = "Mark Bailey and Aiste Ivanauskaite and Julia Grimmer and Oluwatunmise Akintewe and Payne, {Adrienne C} and Rory Osborne and Anne-Marie Labandera and Etherington, {Ross D} and Marjaana Rantala and Sacha Baginsky and Paula Mulo and Gibbs, {Daniel J}",

note = "Funding Information: This work was supported by Biotechnology and Biological Sciences Research Council grants [BB/M020568/1 and BB/T004002/1] and a European Research Council grant [ERC Starting Grant 715441-GasPlaNt] to D.J.G., an EMBO Short-Term Fellowship [Grant number 8104] to M.B., Academy of Finland grants [307335 and 321616] for A.I., M.R. and P.M., and the Doctoral Programme in Molecular Life Sciences at the University of Turku (A.I.). We would like to thank Laura Laihonen for her assistance within the PM group. S.B. gratefully acknowledges support from the DFG with grant number BA 1902/ 3-2. Collaboration between D.J.G. and P.M. was facilitated via the European Research Area Network for Coordinating Action in Plant Sciences (ERA-CAPS) project “KatNat”. We thank Dr Alessandro Di Mio and the BALM facility at the University of Birmingham for support with confocal analyses. Publisher Copyright: {\textcopyright} 2021, The Author(s).",

year = "2021",

month = dec,

doi = "10.1038/s41467-020-20506-4",

language = "English",

volume = "12",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Springer",

number = "1",

}

TY - JOUR

T1 - RETRACTED ARTICLE

T2 - The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation

AU - Bailey, Mark

AU - Ivanauskaite, Aiste

AU - Grimmer, Julia

AU - Akintewe, Oluwatunmise

AU - Payne, Adrienne C

AU - Osborne, Rory

AU - Labandera, Anne-Marie

AU - Etherington, Ross D

AU - Rantala, Marjaana

AU - Baginsky, Sacha

AU - Mulo, Paula

AU - Gibbs, Daniel J

N1 - Funding Information: This work was supported by Biotechnology and Biological Sciences Research Council grants [BB/M020568/1 and BB/T004002/1] and a European Research Council grant [ERC Starting Grant 715441-GasPlaNt] to D.J.G., an EMBO Short-Term Fellowship [Grant number 8104] to M.B., Academy of Finland grants [307335 and 321616] for A.I., M.R. and P.M., and the Doctoral Programme in Molecular Life Sciences at the University of Turku (A.I.). We would like to thank Laura Laihonen for her assistance within the PM group. S.B. gratefully acknowledges support from the DFG with grant number BA 1902/ 3-2. Collaboration between D.J.G. and P.M. was facilitated via the European Research Area Network for Coordinating Action in Plant Sciences (ERA-CAPS) project “KatNat”. We thank Dr Alessandro Di Mio and the BALM facility at the University of Birmingham for support with confocal analyses. Publisher Copyright: © 2021, The Author(s).

PY - 2021/12

Y1 - 2021/12

N2 - Chloroplast function requires the coordinated action of nuclear- and chloroplast-derived proteins, including several hundred nuclear-encoded pentatricopeptide repeat (PPR) proteins that regulate plastid mRNA metabolism. Despite their large number and importance, regulatory mechanisms controlling PPR expression are poorly understood. Here we show that the Arabidopsis NOT4A ubiquitin-ligase positively regulates the expression of PROTON GRADIENT REGULATION 3 (PGR3), a PPR protein required for translating several thylakoid-localised photosynthetic components and ribosome subunits within chloroplasts. Loss of NOT4A function leads to a strong depletion of cytochrome b6f and NAD(P)H dehydrogenase (NDH) complexes, as well as plastid 30 S ribosomes, which reduces mRNA translation and photosynthetic capacity, causing pale-yellow and slow-growth phenotypes. Quantitative transcriptome and proteome analysis of the not4a mutant reveal it lacks PGR3 expression, and that its molecular defects resemble those of a pgr3 mutant. Furthermore, we show that normal plastid function is restored to not4a through transgenic PGR3 expression. Our work identifies NOT4A as crucial for ensuring robust photosynthetic function during development and stress-response, through promoting PGR3 production and chloroplast translation.

AB - Chloroplast function requires the coordinated action of nuclear- and chloroplast-derived proteins, including several hundred nuclear-encoded pentatricopeptide repeat (PPR) proteins that regulate plastid mRNA metabolism. Despite their large number and importance, regulatory mechanisms controlling PPR expression are poorly understood. Here we show that the Arabidopsis NOT4A ubiquitin-ligase positively regulates the expression of PROTON GRADIENT REGULATION 3 (PGR3), a PPR protein required for translating several thylakoid-localised photosynthetic components and ribosome subunits within chloroplasts. Loss of NOT4A function leads to a strong depletion of cytochrome b6f and NAD(P)H dehydrogenase (NDH) complexes, as well as plastid 30 S ribosomes, which reduces mRNA translation and photosynthetic capacity, causing pale-yellow and slow-growth phenotypes. Quantitative transcriptome and proteome analysis of the not4a mutant reveal it lacks PGR3 expression, and that its molecular defects resemble those of a pgr3 mutant. Furthermore, we show that normal plastid function is restored to not4a through transgenic PGR3 expression. Our work identifies NOT4A as crucial for ensuring robust photosynthetic function during development and stress-response, through promoting PGR3 production and chloroplast translation.

KW - Arabidopsis Proteins/chemistry

KW - Arabidopsis/genetics

KW - Chloroplasts/metabolism

KW - Gene Expression Regulation, Plant

KW - Gene Ontology

KW - Mutation/genetics

KW - Photosynthesis

KW - Protein Biosynthesis

KW - Protein Domains

KW - RNA, Messenger/genetics

KW - RNA-Binding Proteins/chemistry

KW - Ribosomes/metabolism

KW - Seedlings/growth & development

KW - Ubiquitin-Protein Ligases/chemistry

UR - http://www.scopus.com/inward/record.url?scp=85099222263&partnerID=8YFLogxK

U2 - 10.1038/s41467-020-20506-4

DO - 10.1038/s41467-020-20506-4

M3 - Article

C2 - 33431870

SN - 2041-1723

VL - 12

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 251

ER -

RETRACTED ARTICLE: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation

Abstract

Bibliographical note

Keywords

ASJC Scopus subject areas

Access to Document

Fingerprint

Research output

Retraction Note: The Arabidopsis NOT4A E3 ligase promotes PGR3 expression and regulates chloroplast translation

Projects

H2020_ERC_GASPLANT_COORDINATOR

N-terminal acetylation as a signal for protein degradation controlling plant development and stress responses

Cite this