Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression

Chloroplasts and mitochondria are subcellular bioenergetic organelles with their own genomes and genetic systems. DNA replication and transmission to daughter organelles produces cytoplasmic inheritance of characters associated with primary events in photosynthesis and respiration. The prokaryotic a...

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2015-08, Vol.112 (33), p.10231-10238
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description Chloroplasts and mitochondria are subcellular bioenergetic organelles with their own genomes and genetic systems. DNA replication and transmission to daughter organelles produces cytoplasmic inheritance of characters associated with primary events in photosynthesis and respiration. The prokaryotic ancestors of chloroplasts and mitochondria were endosymbionts whose genes became copied to the genomes of their cellular hosts. These copies gave rise to nuclear chromosomal genes that encode cytosolic proteins and precursor proteins that are synthesized in the cytosol for import into the organelle into which the endosymbiont evolved. What accounts for the retention of genes for the complete synthesis within chloroplasts and mitochondria of a tiny minority of their protein subunits? One hypothesis is that expression of genes for protein subunits of energy-transducing enzymes must respond to physical environmental change by means of a direct and unconditional regulatory control—control exerted by change in the redox state of the corresponding gene product. This hypothesis proposes that, to preserve function, an entire redox regulatory system has to be retained within its original membrane-bound compartment. Colocation of gene and gene product for redox regulation of gene expression (CoRR) is a hypothesis in agreement with the results of a variety of experiments designed to test it and which seem to have no other satisfactory explanation. Here, I review evidence relating to CoRR and discuss its development, conclusions, and implications. This overview also identifies predictions concerning the results of experiments that may yet prove the hypothesis to be incorrect.
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genetics</topic><topic>Chloroplasts - physiology</topic><topic>CoRR hypothesis</topic><topic>cytoplasmic inheritance</topic><topic>cytosol</topic><topic>Cytosol - metabolism</topic><topic>DNA Replication</topic><topic>DNA, Plant - genetics</topic><topic>Electron Transport</topic><topic>endosymbionts</topic><topic>enzymes</topic><topic>Gene expression</topic><topic>gene expression regulation</topic><topic>Gene Expression Regulation, Plant</topic><topic>genes</topic><topic>Genome, Chloroplast</topic><topic>Genome, Mitochondrial</topic><topic>Genomes</topic><topic>hosts</topic><topic>Mitochondria</topic><topic>Mitochondria - genetics</topic><topic>Mitochondria - physiology</topic><topic>mitochondrion</topic><topic>Oxidation-Reduction</topic><topic>Oxidative Phosphorylation</topic><topic>Photosynthesis</topic><topic>Photosynthesis - physiology</topic><topic>Plants - genetics</topic><topic>prediction</topic><topic>protein subunits</topic><topic>proteins</topic><topic>Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles Sackler</topic><topic>Transcription, Genetic</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Allen, John F</creatorcontrib><collection>AGRIS</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Allen, John F</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>2015-08-18</date><risdate>2015</risdate><volume>112</volume><issue>33</issue><spage>10231</spage><epage>10238</epage><pages>10231-10238</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><abstract>Chloroplasts and mitochondria are subcellular bioenergetic organelles with their own genomes and genetic systems. 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This hypothesis proposes that, to preserve function, an entire redox regulatory system has to be retained within its original membrane-bound compartment. Colocation of gene and gene product for redox regulation of gene expression (CoRR) is a hypothesis in agreement with the results of a variety of experiments designed to test it and which seem to have no other satisfactory explanation. Here, I review evidence relating to CoRR and discuss its development, conclusions, and implications. This overview also identifies predictions concerning the results of experiments that may yet prove the hypothesis to be incorrect.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>26286985</pmid><doi>10.1073/pnas.1500012112</doi><tpages>8</tpages><oa>free_for_read</oa></addata></record>
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source MEDLINE; JSTOR Archive Collection A-Z Listing; PubMed Central; Alma/SFX Local Collection; Free Full-Text Journals in Chemistry
subjects ancestry
Biological Sciences
chloroplast
Chloroplasts
Chloroplasts - genetics
Chloroplasts - physiology
CoRR hypothesis
cytoplasmic inheritance
cytosol
Cytosol - metabolism
DNA Replication
DNA, Plant - genetics
Electron Transport
endosymbionts
enzymes
Gene expression
gene expression regulation
Gene Expression Regulation, Plant
genes
Genome, Chloroplast
Genome, Mitochondrial
Genomes
hosts
Mitochondria
Mitochondria - genetics
Mitochondria - physiology
mitochondrion
Oxidation-Reduction
Oxidative Phosphorylation
Photosynthesis
Photosynthesis - physiology
Plants - genetics
prediction
protein subunits
proteins
Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles Sackler
Transcription, Genetic
title Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression
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