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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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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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.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.1500012112</identifier><identifier>PMID: 26286985</identifier><language>eng</language><publisher>United States: National Academy of Sciences</publisher><subject>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</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 2015-08, Vol.112 (33), p.10231-10238</ispartof><rights>Volumes 1–89 and 106–112, copyright as a collective work only; author(s) retains copyright to individual articles</rights><rights>Copyright National Academy of Sciences Aug 18, 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c525t-cd5934470d9630ffff1c16159d6384640ab8fc3a9fa881082c195b43df5d0b113</citedby><cites>FETCH-LOGICAL-c525t-cd5934470d9630ffff1c16159d6384640ab8fc3a9fa881082c195b43df5d0b113</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/112/33.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/26464880$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/26464880$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26286985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Allen, John F</creatorcontrib><title>Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><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.</description><subject>ancestry</subject><subject>Biological Sciences</subject><subject>chloroplast</subject><subject>Chloroplasts</subject><subject>Chloroplasts - genetics</subject><subject>Chloroplasts - physiology</subject><subject>CoRR hypothesis</subject><subject>cytoplasmic inheritance</subject><subject>cytosol</subject><subject>Cytosol - metabolism</subject><subject>DNA Replication</subject><subject>DNA, Plant - genetics</subject><subject>Electron Transport</subject><subject>endosymbionts</subject><subject>enzymes</subject><subject>Gene expression</subject><subject>gene expression regulation</subject><subject>Gene Expression Regulation, Plant</subject><subject>genes</subject><subject>Genome, Chloroplast</subject><subject>Genome, Mitochondrial</subject><subject>Genomes</subject><subject>hosts</subject><subject>Mitochondria</subject><subject>Mitochondria - genetics</subject><subject>Mitochondria - physiology</subject><subject>mitochondrion</subject><subject>Oxidation-Reduction</subject><subject>Oxidative Phosphorylation</subject><subject>Photosynthesis</subject><subject>Photosynthesis - physiology</subject><subject>Plants - genetics</subject><subject>prediction</subject><subject>protein subunits</subject><subject>proteins</subject><subject>Symbioses Becoming Permanent: The Origins and Evolutionary Trajectories of Organelles Sackler</subject><subject>Transcription, Genetic</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkk2PFCEQhjtG446rZ08qiRcvs0vx0Q0eTMzEr2QTD7rxSBianmHSDSPQunP1l0vb47h6kgOQ4nnfVBVVVY8BXwBu6OXe63QBHGMMBIDcqRaAJSxrJvHdaoExaZaCEXZWPUhpVyjJBb5fnZGaiFoKvqh-fNkekNn2IYZ9r1NOSPsWDS4Hsw2-jU6jaLN2HuWtdRGF7x5trA-Dnclyt9kZlA4p2yG9RKvQB6OzCx51IRZxG27Kvhn7ORi6Xxpkb_bRplRCD6t7ne6TfXQ8z6vrt28-r94vrz6--7B6fbU0nPC8NC2XlLEGt7KmuCsLDNTAZVtTwWqG9Vp0hmrZaSEAC2JA8jWjbcdbvAag59Wr2Xc_rgfbGutz1L3aRzfoeFBBO_X3i3dbtQnfFOOsIUwWgxdHgxi-jjZlNbhkbN9rb8OYFDTQMEko4P9AMW9KNWxK6_k_6C6M0ZdOTFQ9YZwU6nKmTAwpRdud8gasplFQ0yioP6NQFE9vl3vif_99AdARmJQnOyCK0mJZ6ijIkxnZpRziLYvSbyGmMp_N750OSm-iS-r6E8FQl8nDQImgPwFmN87i</recordid><startdate>20150818</startdate><enddate>20150818</enddate><creator>Allen, John F</creator><general>National Academy of Sciences</general><general>National Acad Sciences</general><scope>FBQ</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20150818</creationdate><title>Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression</title><author>Allen, John F</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c525t-cd5934470d9630ffff1c16159d6384640ab8fc3a9fa881082c195b43df5d0b113</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>ancestry</topic><topic>Biological Sciences</topic><topic>chloroplast</topic><topic>Chloroplasts</topic><topic>Chloroplasts - 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 & 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. 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.</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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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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