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Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis
Although mechanisms that activate organogenesis in plants are well established, much less is known about the subsequent fine-tuning of cell proliferation, which is crucial for creating properly structured and sized organs. Here we show, through analysis of temperature-dependent fasciation (TDF) muta...
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| Published in: | eLife 2021-01, Vol.10 |
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| creator | Otsuka, Kurataka Mamiya, Akihito Konishi, Mineko Nozaki, Mamoru Kinoshita, Atsuko Tamaki, Hiroaki Arita, Masaki Saito, Masato Yamamoto, Kayoko Hachiya, Takushi Noguchi, Ko Ueda, Takashi Yagi, Yusuke Kobayashi, Takehito Nakamura, Takahiro Sato, Yasushi Hirayama, Takashi Sugiyama, Munetaka |
| description | Although mechanisms that activate organogenesis in plants are well established, much less is known about the subsequent fine-tuning of cell proliferation, which is crucial for creating properly structured and sized organs. Here we show, through analysis of temperature-dependent fasciation (TDF) mutants of Arabidopsis,
(
),
, and
(
), that mitochondrial RNA processing is required for limiting cell division during early lateral root (LR) organogenesis. These mutants formed abnormally broadened (i.e. fasciated) LRs under high-temperature conditions due to extra cell division. All TDF proteins localized to mitochondria, where they were found to participate in RNA processing: RRD1 in mRNA deadenylation, and RRD2 and RID4 in mRNA editing. Further analysis suggested that LR fasciation in the TDF mutants is triggered by reactive oxygen species generation caused by defective mitochondrial respiration. Our findings provide novel clues for the physiological significance of mitochondrial activities in plant organogenesis. |
| doi_str_mv | 10.7554/eLife.61611 |
| format | article |
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(
),
, and
(
), that mitochondrial RNA processing is required for limiting cell division during early lateral root (LR) organogenesis. These mutants formed abnormally broadened (i.e. fasciated) LRs under high-temperature conditions due to extra cell division. All TDF proteins localized to mitochondria, where they were found to participate in RNA processing: RRD1 in mRNA deadenylation, and RRD2 and RID4 in mRNA editing. Further analysis suggested that LR fasciation in the TDF mutants is triggered by reactive oxygen species generation caused by defective mitochondrial respiration. Our findings provide novel clues for the physiological significance of mitochondrial activities in plant organogenesis.</description><identifier>ISSN: 2050-084X</identifier><identifier>EISSN: 2050-084X</identifier><identifier>DOI: 10.7554/eLife.61611</identifier><identifier>PMID: 33443014</identifier><language>eng</language><publisher>England: eLife Science Publications, Ltd</publisher><subject>Arabidopsis - genetics ; Arabidopsis - growth & development ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Cell division ; cell division control ; Cell growth ; Cell proliferation ; Developmental biology ; Gene expression ; lateral root ; Mitochondria ; mitochondrial RNA processing ; Morphogenesis ; mRNA ; Mutants ; Mutation ; Organogenesis ; Organogenesis, Plant ; pentatricopeptide repeat protein ; Physiological aspects ; Plant Biology ; Plant Roots - growth & development ; Plants ; poly(A)-specific ribonuclease ; Proteins ; Reactive oxygen species ; RNA ; RNA editing ; RNA processing ; RNA Processing, Post-Transcriptional ; RNA, Mitochondrial - metabolism ; Temperature ; temperature-dependent fasciation</subject><ispartof>eLife, 2021-01, Vol.10</ispartof><rights>2021, Otsuka et al.</rights><rights>COPYRIGHT 2021 eLife Science Publications, Ltd.</rights><rights>2021, Otsuka et al. This work is published under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>2021, Otsuka et al 2021 Otsuka et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c642t-e7cc1c94feca4e5f46acdc0aa4cf6ea795cab77f0c5789c3b318a952368af7cb3</citedby><cites>FETCH-LOGICAL-c642t-e7cc1c94feca4e5f46acdc0aa4cf6ea795cab77f0c5789c3b318a952368af7cb3</cites><orcidid>0000-0001-9095-389X ; 0000-0002-7050-8964 ; 0000-0003-3588-3643 ; 0000-0002-5190-892X ; 0000-0001-6492-7903</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/2595177723/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/2595177723?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,723,776,780,881,25732,27903,27904,36991,36992,44569,53770,53772,74873</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33443014$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Otsuka, Kurataka</creatorcontrib><creatorcontrib>Mamiya, Akihito</creatorcontrib><creatorcontrib>Konishi, Mineko</creatorcontrib><creatorcontrib>Nozaki, Mamoru</creatorcontrib><creatorcontrib>Kinoshita, Atsuko</creatorcontrib><creatorcontrib>Tamaki, Hiroaki</creatorcontrib><creatorcontrib>Arita, Masaki</creatorcontrib><creatorcontrib>Saito, Masato</creatorcontrib><creatorcontrib>Yamamoto, Kayoko</creatorcontrib><creatorcontrib>Hachiya, Takushi</creatorcontrib><creatorcontrib>Noguchi, Ko</creatorcontrib><creatorcontrib>Ueda, Takashi</creatorcontrib><creatorcontrib>Yagi, Yusuke</creatorcontrib><creatorcontrib>Kobayashi, Takehito</creatorcontrib><creatorcontrib>Nakamura, Takahiro</creatorcontrib><creatorcontrib>Sato, Yasushi</creatorcontrib><creatorcontrib>Hirayama, Takashi</creatorcontrib><creatorcontrib>Sugiyama, Munetaka</creatorcontrib><title>Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis</title><title>eLife</title><addtitle>Elife</addtitle><description>Although mechanisms that activate organogenesis in plants are well established, much less is known about the subsequent fine-tuning of cell proliferation, which is crucial for creating properly structured and sized organs. Here we show, through analysis of temperature-dependent fasciation (TDF) mutants of Arabidopsis,
(
),
, and
(
), that mitochondrial RNA processing is required for limiting cell division during early lateral root (LR) organogenesis. These mutants formed abnormally broadened (i.e. fasciated) LRs under high-temperature conditions due to extra cell division. All TDF proteins localized to mitochondria, where they were found to participate in RNA processing: RRD1 in mRNA deadenylation, and RRD2 and RID4 in mRNA editing. Further analysis suggested that LR fasciation in the TDF mutants is triggered by reactive oxygen species generation caused by defective mitochondrial respiration. Our findings provide novel clues for the physiological significance of mitochondrial activities in plant organogenesis.</description><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - growth & development</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Cell division</subject><subject>cell division control</subject><subject>Cell growth</subject><subject>Cell proliferation</subject><subject>Developmental biology</subject><subject>Gene expression</subject><subject>lateral root</subject><subject>Mitochondria</subject><subject>mitochondrial RNA processing</subject><subject>Morphogenesis</subject><subject>mRNA</subject><subject>Mutants</subject><subject>Mutation</subject><subject>Organogenesis</subject><subject>Organogenesis, Plant</subject><subject>pentatricopeptide repeat protein</subject><subject>Physiological aspects</subject><subject>Plant Biology</subject><subject>Plant Roots - growth & development</subject><subject>Plants</subject><subject>poly(A)-specific ribonuclease</subject><subject>Proteins</subject><subject>Reactive oxygen species</subject><subject>RNA</subject><subject>RNA editing</subject><subject>RNA processing</subject><subject>RNA Processing, Post-Transcriptional</subject><subject>RNA, Mitochondrial - metabolism</subject><subject>Temperature</subject><subject>temperature-dependent fasciation</subject><issn>2050-084X</issn><issn>2050-084X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>PIMPY</sourceid><sourceid>DOA</sourceid><recordid>eNptkt1rFDEUxQdRbKl98l0GfFFk12SSTDIvQil-LCwKtYJv4U7mZps6k6xJpir-86bdWrpi8pBw87sn3MOpqqeULKUQ_DWuncVlS1tKH1SHDRFkQRT_-vDe_aA6TumSlCW5UrR7XB0wxjkjlB9Wv89x2mKEPEdcDLhFP6DPtYVkHGQXfD3NGXxO9TaGKzdgDfXo_Le6x_wDsTy7HMxF8EN0MNZnH0-uQYMpOb-pwQ_1CLnoj3UMIddTiNuLsEGPyaUn1SMLY8Lj2_Oo-vLu7fnph8X60_vV6cl6YVre5AVKY6jpuEUDHIXlLZjBEABubIsgO2Ggl9ISI6TqDOsZVdCJhrUKrDQ9O6pWO90hwKXeRjdB_KUDOH1TCHGjIWZnRtSSYo8CFBOWciKs6pVtiLKK0Na2jBatNzut7dxPOJhiVhluT3T_xbsLvQlXWireNlIUgRe3AjF8nzFlPblkcBzBY5iTbrhUhEkiWUGf_4Nehjn6YpVuRCeolLK5R22gDOC8DeVfcy2qT1pBSKeUagu1_A9V9oCTM8GjdaW-1_Byr6EwGX_mDcwp6dXns3321Y41MaQU0d75QYm-jqm-iam-iWmhn9238I79G0r2B2BS5PI</recordid><startdate>20210114</startdate><enddate>20210114</enddate><creator>Otsuka, Kurataka</creator><creator>Mamiya, Akihito</creator><creator>Konishi, Mineko</creator><creator>Nozaki, Mamoru</creator><creator>Kinoshita, Atsuko</creator><creator>Tamaki, Hiroaki</creator><creator>Arita, Masaki</creator><creator>Saito, Masato</creator><creator>Yamamoto, Kayoko</creator><creator>Hachiya, Takushi</creator><creator>Noguchi, Ko</creator><creator>Ueda, Takashi</creator><creator>Yagi, Yusuke</creator><creator>Kobayashi, Takehito</creator><creator>Nakamura, Takahiro</creator><creator>Sato, Yasushi</creator><creator>Hirayama, Takashi</creator><creator>Sugiyama, Munetaka</creator><general>eLife Science Publications, Ltd</general><general>eLife Sciences Publications Ltd</general><general>eLife Sciences Publications, Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISR</scope><scope>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>88I</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2P</scope><scope>M7P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>Q9U</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-9095-389X</orcidid><orcidid>https://orcid.org/0000-0002-7050-8964</orcidid><orcidid>https://orcid.org/0000-0003-3588-3643</orcidid><orcidid>https://orcid.org/0000-0002-5190-892X</orcidid><orcidid>https://orcid.org/0000-0001-6492-7903</orcidid></search><sort><creationdate>20210114</creationdate><title>Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis</title><author>Otsuka, Kurataka ; Mamiya, Akihito ; Konishi, Mineko ; Nozaki, Mamoru ; Kinoshita, Atsuko ; Tamaki, Hiroaki ; Arita, Masaki ; Saito, Masato ; Yamamoto, Kayoko ; Hachiya, Takushi ; Noguchi, Ko ; Ueda, Takashi ; Yagi, Yusuke ; Kobayashi, Takehito ; Nakamura, Takahiro ; Sato, Yasushi ; Hirayama, Takashi ; Sugiyama, Munetaka</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c642t-e7cc1c94feca4e5f46acdc0aa4cf6ea795cab77f0c5789c3b318a952368af7cb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Arabidopsis - 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>eLife</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Otsuka, Kurataka</au><au>Mamiya, Akihito</au><au>Konishi, Mineko</au><au>Nozaki, Mamoru</au><au>Kinoshita, Atsuko</au><au>Tamaki, Hiroaki</au><au>Arita, Masaki</au><au>Saito, Masato</au><au>Yamamoto, Kayoko</au><au>Hachiya, Takushi</au><au>Noguchi, Ko</au><au>Ueda, Takashi</au><au>Yagi, Yusuke</au><au>Kobayashi, Takehito</au><au>Nakamura, Takahiro</au><au>Sato, Yasushi</au><au>Hirayama, Takashi</au><au>Sugiyama, Munetaka</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis</atitle><jtitle>eLife</jtitle><addtitle>Elife</addtitle><date>2021-01-14</date><risdate>2021</risdate><volume>10</volume><issn>2050-084X</issn><eissn>2050-084X</eissn><abstract>Although mechanisms that activate organogenesis in plants are well established, much less is known about the subsequent fine-tuning of cell proliferation, which is crucial for creating properly structured and sized organs. Here we show, through analysis of temperature-dependent fasciation (TDF) mutants of Arabidopsis,
(
),
, and
(
), that mitochondrial RNA processing is required for limiting cell division during early lateral root (LR) organogenesis. These mutants formed abnormally broadened (i.e. fasciated) LRs under high-temperature conditions due to extra cell division. All TDF proteins localized to mitochondria, where they were found to participate in RNA processing: RRD1 in mRNA deadenylation, and RRD2 and RID4 in mRNA editing. Further analysis suggested that LR fasciation in the TDF mutants is triggered by reactive oxygen species generation caused by defective mitochondrial respiration. Our findings provide novel clues for the physiological significance of mitochondrial activities in plant organogenesis.</abstract><cop>England</cop><pub>eLife Science Publications, Ltd</pub><pmid>33443014</pmid><doi>10.7554/eLife.61611</doi><orcidid>https://orcid.org/0000-0001-9095-389X</orcidid><orcidid>https://orcid.org/0000-0002-7050-8964</orcidid><orcidid>https://orcid.org/0000-0003-3588-3643</orcidid><orcidid>https://orcid.org/0000-0002-5190-892X</orcidid><orcidid>https://orcid.org/0000-0001-6492-7903</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 2050-084X |
| ispartof | eLife, 2021-01, Vol.10 |
| issn | 2050-084X 2050-084X |
| language | eng |
| recordid | cdi_doaj_primary_oai_doaj_org_article_71ebe5a835f1405f8b8f208f8016f631 |
| source | PubMed (Medline); Publicly Available Content (ProQuest) |
| subjects | Arabidopsis - genetics Arabidopsis - growth & development Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Cell division cell division control Cell growth Cell proliferation Developmental biology Gene expression lateral root Mitochondria mitochondrial RNA processing Morphogenesis mRNA Mutants Mutation Organogenesis Organogenesis, Plant pentatricopeptide repeat protein Physiological aspects Plant Biology Plant Roots - growth & development Plants poly(A)-specific ribonuclease Proteins Reactive oxygen species RNA RNA editing RNA processing RNA Processing, Post-Transcriptional RNA, Mitochondrial - metabolism Temperature temperature-dependent fasciation |
| title | Temperature-dependent fasciation mutants provide a link between mitochondrial RNA processing and lateral root morphogenesis |
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