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The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid

BACKGROUND: Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO(2)-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including with the...

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Autores principales: Matsuzaki, Ryo, Suzuki, Shigekatsu, Yamaguchi, Haruyo, Kawachi, Masanobu, Kanesaki, Yu, Yoshikawa, Hirofumi, Mori, Toshiyuki, Nozaki, Hisayoshi
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7853309/
https://www.ncbi.nlm.nih.gov/pubmed/33514317
http://dx.doi.org/10.1186/s12862-020-01733-1
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author Matsuzaki, Ryo
Suzuki, Shigekatsu
Yamaguchi, Haruyo
Kawachi, Masanobu
Kanesaki, Yu
Yoshikawa, Hirofumi
Mori, Toshiyuki
Nozaki, Hisayoshi
author_facet Matsuzaki, Ryo
Suzuki, Shigekatsu
Yamaguchi, Haruyo
Kawachi, Masanobu
Kanesaki, Yu
Yoshikawa, Hirofumi
Mori, Toshiyuki
Nozaki, Hisayoshi
author_sort Matsuzaki, Ryo
collection PubMed
description BACKGROUND: Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO(2)-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including with the origin of land plants. The molecular basis of the evolutionary loss of pyrenoids is a major topic in evolutionary biology. Recently, it was hypothesized that pyrenoid formation is controlled by the hydrophobicity of the two helices on the surface of the Rubisco small subunit (RBCS), but the relationship between hydrophobicity and pyrenoid loss during the evolution of closely related algal/plant lineages has not been examined. Here, we focused on, the Reticulata group of the unicellular green algal genus Chloromonas, within which pyrenoids are present in some species, although they are absent in the closely related species. RESULTS: Based on de novo transcriptome analysis and Sanger sequencing of cloned reverse transcription-polymerase chain reaction products, rbcS sequences were determined from 11 strains of two pyrenoid-lacking and three pyrenoid-containing species of the Reticulata group. We found that the hydrophobicity of the RBCS helices was roughly correlated with the presence or absence of pyrenoids within the Reticulata group and that a decrease in the hydrophobicity of the RBCS helices may have primarily caused pyrenoid loss during the evolution of this group. CONCLUSIONS: Although we suggest that the observed correlation may only exist for the Reticulata group, this is still an interesting study that provides novel insight into a potential mechanism determining initial evolutionary steps of gain and loss of the pyrenoid.
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spelling pubmed-78533092021-02-09 The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid Matsuzaki, Ryo Suzuki, Shigekatsu Yamaguchi, Haruyo Kawachi, Masanobu Kanesaki, Yu Yoshikawa, Hirofumi Mori, Toshiyuki Nozaki, Hisayoshi BMC Ecol Evol Research Article BACKGROUND: Pyrenoids are protein microcompartments composed mainly of Rubisco that are localized in the chloroplasts of many photosynthetic organisms. Pyrenoids contribute to the CO(2)-concentrating mechanism. This organelle has been lost many times during algal/plant evolution, including with the origin of land plants. The molecular basis of the evolutionary loss of pyrenoids is a major topic in evolutionary biology. Recently, it was hypothesized that pyrenoid formation is controlled by the hydrophobicity of the two helices on the surface of the Rubisco small subunit (RBCS), but the relationship between hydrophobicity and pyrenoid loss during the evolution of closely related algal/plant lineages has not been examined. Here, we focused on, the Reticulata group of the unicellular green algal genus Chloromonas, within which pyrenoids are present in some species, although they are absent in the closely related species. RESULTS: Based on de novo transcriptome analysis and Sanger sequencing of cloned reverse transcription-polymerase chain reaction products, rbcS sequences were determined from 11 strains of two pyrenoid-lacking and three pyrenoid-containing species of the Reticulata group. We found that the hydrophobicity of the RBCS helices was roughly correlated with the presence or absence of pyrenoids within the Reticulata group and that a decrease in the hydrophobicity of the RBCS helices may have primarily caused pyrenoid loss during the evolution of this group. CONCLUSIONS: Although we suggest that the observed correlation may only exist for the Reticulata group, this is still an interesting study that provides novel insight into a potential mechanism determining initial evolutionary steps of gain and loss of the pyrenoid. BioMed Central 2021-01-25 /pmc/articles/PMC7853309/ /pubmed/33514317 http://dx.doi.org/10.1186/s12862-020-01733-1 Text en © The Author(s) 2021 Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research Article
Matsuzaki, Ryo
Suzuki, Shigekatsu
Yamaguchi, Haruyo
Kawachi, Masanobu
Kanesaki, Yu
Yoshikawa, Hirofumi
Mori, Toshiyuki
Nozaki, Hisayoshi
The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
title The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
title_full The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
title_fullStr The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
title_full_unstemmed The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
title_short The Rubisco small subunits in the green algal genus Chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
title_sort rubisco small subunits in the green algal genus chloromonas provide insights into evolutionary loss of the eukaryotic carbon-concentrating organelle, the pyrenoid
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7853309/
https://www.ncbi.nlm.nih.gov/pubmed/33514317
http://dx.doi.org/10.1186/s12862-020-01733-1
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