Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution

Chloroplast (cp) DNA is thought to originate from the ancestral endosymbiont genome and is compacted to form nucleoprotein complexes, cp nucleoids. The structure of cp nucleoids is ubiquitously observed in diverse plants from unicellular algae to flowering plants and is believed to be a multifunctio...

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Main Authors:	Kobayashi, Yusuke, Takusagawa, Mari, Harada, Naomi, Fukao, Yoichiro, Yamaoka, Shohei, Kohchi, Takayuki, Hori, Koichi, Ohta, Hiroyuki, Shikanai, Toshiharu, Nishimura, Yoshiki
Format:	Online
Language:	English
Published:	Oxford University Press 2015
Online Access:	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4758235/

id	pubmed-4758235
recordtype	oai_dc
spelling	pubmed-47582352016-03-04 Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution Kobayashi, Yusuke Takusagawa, Mari Harada, Naomi Fukao, Yoichiro Yamaoka, Shohei Kohchi, Takayuki Hori, Koichi Ohta, Hiroyuki Shikanai, Toshiharu Nishimura, Yoshiki Research Article Chloroplast (cp) DNA is thought to originate from the ancestral endosymbiont genome and is compacted to form nucleoprotein complexes, cp nucleoids. The structure of cp nucleoids is ubiquitously observed in diverse plants from unicellular algae to flowering plants and is believed to be a multifunctional platform for various processes, including cpDNA replication, repair/recombination, transcription, and inheritance. Despite its fundamental functions, the protein composition for cp nucleoids in flowering plants was suggested to be divergent from those of bacteria and algae, but the evolutionary process remains elusive. In this research, we aimed to reveal the evolutionary history of cp nucleoid organization by analyzing the key organisms representing the three evolutionary stages of eukaryotic phototrophs: the chlorophyte alga Chlamydomonas reinhardtii, the charophyte alga Klebsormidium flaccidum, and the most basal land plant Marchantia polymorpha. To clarify the core cp nucleoid proteins in C. reinhardtii, we performed an LC-MS/MS analysis using highly purified cp nucleoid fractions and identified a novel SAP domain-containing protein with a eukaryotic origin as a constitutive core component. Then, homologous genes for cp nucleoid proteins were searched for in C. reinhardtii, K. flaccidum, and M. polymorpha using the genome databases, and their intracellular localizations and DNA binding activities were investigated by cell biological/biochemical analyses. Based on these results, we propose a model that recurrent modification of cp nucleoid organization by eukaryotic factors originally related to chromatin organization might have been the driving force for the diversification of cp nucleoids since the early stage of green plant evolution. Oxford University Press 2015-11-25 /pmc/articles/PMC4758235/ /pubmed/26608058 http://dx.doi.org/10.1093/gbe/evv233 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
repository_type	Open Access Journal
institution_category	Foreign Institution
institution	US National Center for Biotechnology Information
building	NCBI PubMed
collection	Online Access
language	English
format	Online
author	Kobayashi, Yusuke Takusagawa, Mari Harada, Naomi Fukao, Yoichiro Yamaoka, Shohei Kohchi, Takayuki Hori, Koichi Ohta, Hiroyuki Shikanai, Toshiharu Nishimura, Yoshiki
spellingShingle	Kobayashi, Yusuke Takusagawa, Mari Harada, Naomi Fukao, Yoichiro Yamaoka, Shohei Kohchi, Takayuki Hori, Koichi Ohta, Hiroyuki Shikanai, Toshiharu Nishimura, Yoshiki Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution
author_facet	Kobayashi, Yusuke Takusagawa, Mari Harada, Naomi Fukao, Yoichiro Yamaoka, Shohei Kohchi, Takayuki Hori, Koichi Ohta, Hiroyuki Shikanai, Toshiharu Nishimura, Yoshiki
author_sort	Kobayashi, Yusuke
title	Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution
title_short	Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution
title_full	Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution
title_fullStr	Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution
title_full_unstemmed	Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution
title_sort	eukaryotic components remodeled chloroplast nucleoid organization during the green plant evolution
description	Chloroplast (cp) DNA is thought to originate from the ancestral endosymbiont genome and is compacted to form nucleoprotein complexes, cp nucleoids. The structure of cp nucleoids is ubiquitously observed in diverse plants from unicellular algae to flowering plants and is believed to be a multifunctional platform for various processes, including cpDNA replication, repair/recombination, transcription, and inheritance. Despite its fundamental functions, the protein composition for cp nucleoids in flowering plants was suggested to be divergent from those of bacteria and algae, but the evolutionary process remains elusive. In this research, we aimed to reveal the evolutionary history of cp nucleoid organization by analyzing the key organisms representing the three evolutionary stages of eukaryotic phototrophs: the chlorophyte alga Chlamydomonas reinhardtii, the charophyte alga Klebsormidium flaccidum, and the most basal land plant Marchantia polymorpha. To clarify the core cp nucleoid proteins in C. reinhardtii, we performed an LC-MS/MS analysis using highly purified cp nucleoid fractions and identified a novel SAP domain-containing protein with a eukaryotic origin as a constitutive core component. Then, homologous genes for cp nucleoid proteins were searched for in C. reinhardtii, K. flaccidum, and M. polymorpha using the genome databases, and their intracellular localizations and DNA binding activities were investigated by cell biological/biochemical analyses. Based on these results, we propose a model that recurrent modification of cp nucleoid organization by eukaryotic factors originally related to chromatin organization might have been the driving force for the diversification of cp nucleoids since the early stage of green plant evolution.
publisher	Oxford University Press
publishDate	2015
url	https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4758235/
_version_	1613540300861472768

Eukaryotic Components Remodeled Chloroplast Nucleoid Organization during the Green Plant Evolution

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