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Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana

The plastid evolved from a symbiotic cyanobacterial ancestor and is an essential organelle for plant life, but its developmental roles in roots have been largely overlooked. Here, we show that plastid translation is connected to the stem cell patterning in lateral root primordia. The RFC3 gene encod...

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Autores principales: Nakata, Miyuki T., Sato, Mayuko, Wakazaki, Mayumi, Sato, Nozomi, Kojima, Koji, Sekine, Akihiko, Nakamura, Shiori, Shikanai, Toshiharu, Toyooka, Kiminori, Tsukaya, Hirokazu, Horiguchi, Gorou
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Company of Biologists Ltd 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5861355/
https://www.ncbi.nlm.nih.gov/pubmed/29367414
http://dx.doi.org/10.1242/bio.028175
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author Nakata, Miyuki T.
Sato, Mayuko
Wakazaki, Mayumi
Sato, Nozomi
Kojima, Koji
Sekine, Akihiko
Nakamura, Shiori
Shikanai, Toshiharu
Toyooka, Kiminori
Tsukaya, Hirokazu
Horiguchi, Gorou
author_facet Nakata, Miyuki T.
Sato, Mayuko
Wakazaki, Mayumi
Sato, Nozomi
Kojima, Koji
Sekine, Akihiko
Nakamura, Shiori
Shikanai, Toshiharu
Toyooka, Kiminori
Tsukaya, Hirokazu
Horiguchi, Gorou
author_sort Nakata, Miyuki T.
collection PubMed
description The plastid evolved from a symbiotic cyanobacterial ancestor and is an essential organelle for plant life, but its developmental roles in roots have been largely overlooked. Here, we show that plastid translation is connected to the stem cell patterning in lateral root primordia. The RFC3 gene encodes a plastid-localized protein that is a conserved bacterial ribosomal protein S6 of β/γ proteobacterial origin. The rfc3 mutant developed lateral roots with disrupted stem cell patterning and associated with decreased leaf photosynthetic activity, reduced accumulation of plastid rRNAs in roots, altered root plastid gene expression, and changes in expression of several root stem cell regulators. These results suggest that deficiencies in plastid function affect lateral root stem cells. Treatment with the plastid translation inhibitor spectinomycin phenocopied the defective stem cell patterning in lateral roots and altered plastid gene expression observed in the rfc3 mutant. Additionally, when prps17 defective in a plastid ribosomal protein was treated with low concentrations of spectinomycin, it also phenocopied the lateral root phenotypes of rfc3. The spectinomycin treatment and rfc3 mutation also negatively affected symplasmic connectivity between primary root and lateral root primordia. This study highlights previously unrecognized functions of plastid translation in the stem cell patterning in lateral roots.
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spelling pubmed-58613552018-04-05 Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana Nakata, Miyuki T. Sato, Mayuko Wakazaki, Mayumi Sato, Nozomi Kojima, Koji Sekine, Akihiko Nakamura, Shiori Shikanai, Toshiharu Toyooka, Kiminori Tsukaya, Hirokazu Horiguchi, Gorou Biol Open Research Article The plastid evolved from a symbiotic cyanobacterial ancestor and is an essential organelle for plant life, but its developmental roles in roots have been largely overlooked. Here, we show that plastid translation is connected to the stem cell patterning in lateral root primordia. The RFC3 gene encodes a plastid-localized protein that is a conserved bacterial ribosomal protein S6 of β/γ proteobacterial origin. The rfc3 mutant developed lateral roots with disrupted stem cell patterning and associated with decreased leaf photosynthetic activity, reduced accumulation of plastid rRNAs in roots, altered root plastid gene expression, and changes in expression of several root stem cell regulators. These results suggest that deficiencies in plastid function affect lateral root stem cells. Treatment with the plastid translation inhibitor spectinomycin phenocopied the defective stem cell patterning in lateral roots and altered plastid gene expression observed in the rfc3 mutant. Additionally, when prps17 defective in a plastid ribosomal protein was treated with low concentrations of spectinomycin, it also phenocopied the lateral root phenotypes of rfc3. The spectinomycin treatment and rfc3 mutation also negatively affected symplasmic connectivity between primary root and lateral root primordia. This study highlights previously unrecognized functions of plastid translation in the stem cell patterning in lateral roots. The Company of Biologists Ltd 2018-01-24 /pmc/articles/PMC5861355/ /pubmed/29367414 http://dx.doi.org/10.1242/bio.028175 Text en © 2018. Published by The Company of Biologists Ltd http://creativecommons.org/licenses/by/3.0This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/3.0), which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
spellingShingle Research Article
Nakata, Miyuki T.
Sato, Mayuko
Wakazaki, Mayumi
Sato, Nozomi
Kojima, Koji
Sekine, Akihiko
Nakamura, Shiori
Shikanai, Toshiharu
Toyooka, Kiminori
Tsukaya, Hirokazu
Horiguchi, Gorou
Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana
title Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana
title_full Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana
title_fullStr Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana
title_full_unstemmed Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana
title_short Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana
title_sort plastid translation is essential for lateral root stem cell patterning in arabidopsis thaliana
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5861355/
https://www.ncbi.nlm.nih.gov/pubmed/29367414
http://dx.doi.org/10.1242/bio.028175
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