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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doaj-7f474a6b1a63412e9ca458a31939e6022021-06-02T15:57:14ZengThe Company of BiologistsBiology Open2046-63902018-02-017210.1242/bio.028175028175Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thalianaMiyuki T. Nakata0Mayuko Sato1Mayumi Wakazaki2Nozomi Sato3Koji Kojima4Akihiko Sekine5Shiori Nakamura6Toshiharu Shikanai7Kiminori Toyooka8Hirokazu Tsukaya9Gorou Horiguchi10 Research Center for Life Science, College of Science, Rikkyo University, Toshima, Tokyo 171-8501, Japan Center for Sustainable Resource Science, RIKEN, Tsurumi, Yokohama, Kanagawa 230-0045, Japan Center for Sustainable Resource Science, RIKEN, Tsurumi, Yokohama, Kanagawa 230-0045, Japan Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan Department of Life Science, College of Science, Rikkyo University, Toshima, Tokyo 171-8501, Japan Department of Life Science, College of Science, Rikkyo University, Toshima, Tokyo 171-8501, Japan Department of Life Science, College of Science, Rikkyo University, Toshima, Tokyo 171-8501, Japan Graduate School of Science, Kyoto University, Sakyo, Kyoto 606-8502, Japan Center for Sustainable Resource Science, RIKEN, Tsurumi, Yokohama, Kanagawa 230-0045, Japan Graduate school of Science, The University of Tokyo, Bunkyo, Tokyo 113-0033, Japan Research Center for Life Science, College of Science, Rikkyo University, Toshima, Tokyo 171-8501, Japan 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.http://bio.biologists.org/content/7/2/bio028175Lateral rootPlastidRFC3RibosomeSpectinomycinStem cell |
collection |
DOAJ |
language |
English |
format |
Article |
sources |
DOAJ |
author |
Miyuki T. Nakata Mayuko Sato Mayumi Wakazaki Nozomi Sato Koji Kojima Akihiko Sekine Shiori Nakamura Toshiharu Shikanai Kiminori Toyooka Hirokazu Tsukaya Gorou Horiguchi |
spellingShingle |
Miyuki T. Nakata Mayuko Sato Mayumi Wakazaki Nozomi Sato Koji Kojima Akihiko Sekine Shiori Nakamura Toshiharu Shikanai Kiminori Toyooka Hirokazu Tsukaya Gorou Horiguchi Plastid translation is essential for lateral root stem cell patterning in Arabidopsis thaliana Biology Open Lateral root Plastid RFC3 Ribosome Spectinomycin Stem cell |
author_facet |
Miyuki T. Nakata Mayuko Sato Mayumi Wakazaki Nozomi Sato Koji Kojima Akihiko Sekine Shiori Nakamura Toshiharu Shikanai Kiminori Toyooka Hirokazu Tsukaya Gorou Horiguchi |
author_sort |
Miyuki T. Nakata |
title |
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_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_sort |
plastid translation is essential for lateral root stem cell patterning in arabidopsis thaliana |
publisher |
The Company of Biologists |
series |
Biology Open |
issn |
2046-6390 |
publishDate |
2018-02-01 |
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. |
topic |
Lateral root Plastid RFC3 Ribosome Spectinomycin Stem cell |
url |
http://bio.biologists.org/content/7/2/bio028175 |
work_keys_str_mv |
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