The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria
Abstract Gene expression in plant mitochondria is mainly regulated by nuclear-encoded proteins on a post-transcriptional level. Pentatricopeptide repeat (PPR) proteins play a major role by participating in mRNA stability, splicing, RNA editing, and translation initiation. PPR proteins were also show...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Nature Portfolio
2022-07-01
|
| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-16812-0 |
| _version_ | 1811287626607493120 |
|---|---|
| author | Stefanie Grüttner Tan-Trung Nguyen Anika Bruhs Hakim Mireau Frank Kempken |
| author_facet | Stefanie Grüttner Tan-Trung Nguyen Anika Bruhs Hakim Mireau Frank Kempken |
| author_sort | Stefanie Grüttner |
| collection | DOAJ |
| description | Abstract Gene expression in plant mitochondria is mainly regulated by nuclear-encoded proteins on a post-transcriptional level. Pentatricopeptide repeat (PPR) proteins play a major role by participating in mRNA stability, splicing, RNA editing, and translation initiation. PPR proteins were also shown to be part of the mitochondrial ribosome (rPPR proteins), which may act as regulators of gene expression in plants. In this study, we focus on a mitochondrial-located P-type PPR protein—DWEORG1—from Arabidopsis thaliana. Its abundance in mitochondria is high, and it has a similar expression pattern as rPPR proteins. Mutant dweorg1 plants exhibit a slow-growth phenotype. Using ribosome profiling, a decrease in translation efficiency for cox2, rps4, rpl5, and ccmF N2 was observed in dweorg1 mutants, correlating with a reduced accumulation of the Cox2 protein in these plants. In addition, the mitochondrial rRNA levels are significantly reduced in dweorg1 compared with the wild type. DWEORG1 co-migrates with the ribosomal proteins Rps4 and Rpl16 in sucrose gradients, suggesting an association of DWEORG1 with the mitoribosome. Collectively, this data suggests that DWEORG1 encodes a novel rPPR protein that is needed for the translation of cox2, rps4, rpl5, and ccmF N2 and provides a stabilizing function for mitochondrial ribosomes. |
| first_indexed | 2024-04-13T03:21:54Z |
| format | Article |
| id | doaj.art-5326a8d22b3f4cef8baf220b0bdb6973 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-13T03:21:54Z |
| publishDate | 2022-07-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-5326a8d22b3f4cef8baf220b0bdb69732022-12-22T03:04:46ZengNature PortfolioScientific Reports2045-23222022-07-0112111410.1038/s41598-022-16812-0The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondriaStefanie Grüttner0Tan-Trung Nguyen1Anika Bruhs2Hakim Mireau3Frank Kempken4Abteilung Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universität zu KielInstitut Jean-Pierre Bourgin INRA, AgroParisTech, CNRS, Université Paris-SaclayAbteilung Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universität zu KielInstitut Jean-Pierre Bourgin INRA, AgroParisTech, CNRS, Université Paris-SaclayAbteilung Botanische Genetik und Molekularbiologie, Botanisches Institut und Botanischer Garten, Christian-Albrechts-Universität zu KielAbstract Gene expression in plant mitochondria is mainly regulated by nuclear-encoded proteins on a post-transcriptional level. Pentatricopeptide repeat (PPR) proteins play a major role by participating in mRNA stability, splicing, RNA editing, and translation initiation. PPR proteins were also shown to be part of the mitochondrial ribosome (rPPR proteins), which may act as regulators of gene expression in plants. In this study, we focus on a mitochondrial-located P-type PPR protein—DWEORG1—from Arabidopsis thaliana. Its abundance in mitochondria is high, and it has a similar expression pattern as rPPR proteins. Mutant dweorg1 plants exhibit a slow-growth phenotype. Using ribosome profiling, a decrease in translation efficiency for cox2, rps4, rpl5, and ccmF N2 was observed in dweorg1 mutants, correlating with a reduced accumulation of the Cox2 protein in these plants. In addition, the mitochondrial rRNA levels are significantly reduced in dweorg1 compared with the wild type. DWEORG1 co-migrates with the ribosomal proteins Rps4 and Rpl16 in sucrose gradients, suggesting an association of DWEORG1 with the mitoribosome. Collectively, this data suggests that DWEORG1 encodes a novel rPPR protein that is needed for the translation of cox2, rps4, rpl5, and ccmF N2 and provides a stabilizing function for mitochondrial ribosomes.https://doi.org/10.1038/s41598-022-16812-0 |
| spellingShingle | Stefanie Grüttner Tan-Trung Nguyen Anika Bruhs Hakim Mireau Frank Kempken The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria Scientific Reports |
| title | The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria |
| title_full | The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria |
| title_fullStr | The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria |
| title_full_unstemmed | The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria |
| title_short | The P-type pentatricopeptide repeat protein DWEORG1 is a non-previously reported rPPR protein of Arabidopsis mitochondria |
| title_sort | p type pentatricopeptide repeat protein dweorg1 is a non previously reported rppr protein of arabidopsis mitochondria |
| url | https://doi.org/10.1038/s41598-022-16812-0 |
| work_keys_str_mv | AT stefaniegruttner theptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT tantrungnguyen theptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT anikabruhs theptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT hakimmireau theptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT frankkempken theptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT stefaniegruttner ptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT tantrungnguyen ptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT anikabruhs ptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT hakimmireau ptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria AT frankkempken ptypepentatricopeptiderepeatproteindweorg1isanonpreviouslyreportedrpprproteinofarabidopsismitochondria |