Co-location for Redox Regulation - CoRR
Why are there genes in organelles?
Chloroplasts and mitochondria are energy-converting organelles in the cytoplasm of eukaryotic cells. Chloroplasts in plant cells perform photosynthesis; the capture and conversion of the energy of sunlight. Mitochondria in both plant and animal cells perform respiration; the release of this stored energy when work is done. Photosynthesis and respiration are chemical redox reactions.
Chloroplasts and mitochondria also contain small, specialised, and complete genetic systems to make their own proteins. Both the genetic and the energy-converting systems of chloroplasts and mitochondria are descended, with little modification, from those of the free-living bacteria that these organelles once were.
The great majority of genes for the proteins of chloroplasts and mitochondria are, however, now located elsewhere. They are found in the nuclei of eukaryotic cells. There they code for precursor proteins that are made in the cytosol for subsequent import into organelles. So why, in evolution, did some genes move to the cell nucleus, while others did not?
The CoRR Hypothesis. Ten principles, axioms, predictions
The principle of endosymbiotic origin.
Bioenergetic organelles - mitochondria and chloroplasts - evolved from free-living bacteria.
The principle of unselective gene transfer.
Gene transfer between the symbiont or organelle and the nucleus of the host cell may occur in either direction and is not selective for particular genes.
The principle of unselective protein import.
There is no barrier to the successful import into the organelles of any precursor protein, nor to its processing and assembly into a functional, mature form.
The principle of continuity of redox control.
Direct redox control of expression of certain genes was present in the bacterial progenitors of chloroplasts and mitochondria, and was vital for cell function before, during, and after the transition from bacterium to organelle. The mechanisms of this control have been conserved.
The principle of the selective value of redox control.
For each gene under direct redox control, it is selectively advantageous for that gene to be retained and expressed only within the organelle.
The principle of the selective value of nuclear location for genes not under redox control.
For each bacterial gene that survives and is not under direct redox control, it is selectively advantageous for that gene to be located in the nucleus and expressed only in the nucleus and cytosol. If the mature gene product functions in chloroplasts or mitochondria, the gene is first expressed in the form of a precursor for import.
The principle of contemporary operation of selection on gene location.
For any species, the distribution of genes between organelle and nucleus is the result of selective forces that continue to operate.
The principle of primary involvement in energy transduction.
Those genes for which direct redox control is always vital to cell function have gene products involved in, or closely connected with, primary electron transfer. These genes are always contained within the organelle.
The principle of secondary involvement in energy transduction.
Genes whose products contribute to the organelle genetic system itself, or whose products are associated with secondary events in energy transduction, may be contained in the organelle in one group of organisms, but not in another.
The principle of the nuclear encoding of redox signalling components.
Components of the redox-signalling pathways upon which co-location for redox regulation depends are themselves not involved in primary electron transfer, and so their genes have been relocated to the nucleus.
The CoRR Hypothesis. Summary
- Vectorial electron and proton transfer exerts regulatory control over expression of genes encoding proteins directly involved in, or affecting, redox poise.
- This regulatory coupling requires co-location of such genes with their gene products.
- Co-location for Redox Regulation - CoRR - operated continuously before, during, and after the transition from prokaryote to eukaryotic organelle.
- Mitochondria and chloroplasts are “intelligent” energy-transducing devices. They make their own decisions on the basis of environmental changes affecting redox poise.
- CoRR operates today and will continue to operate. CoRR is a necessary condition for the compatibility of energy conversion with genome function in living cells.
- Allen JF (1993) Control of Gene-Expression by Redox Potential and the Requirement for Chloroplast and Mitochondrial Genomes. Journal of Theoretical Biology 165: 609-631.
- Allen JF (1993) Redox Control of Gene-Expression and the Function of Chloroplast Genomes - an Hypothesis. Photosynthesis Research 36: 95-102.
- Allen JF (1993) Redox Control of Transcription - Sensors, Response Regulators, Activators and Repressors. FEBS Letters 332: 203-207.
- Pfannschmidt T, Nilsson A, Allen JF (1999) Photosynthetic control of chloroplast gene expression. Nature 397: 625-628.
- Allen JF (2003) The function of genomes in bioenergetic organelles. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 358: 19-37.
- Allen JF (2003) Why chloroplasts and mitochondria contain genomes. Comparative and Functional Genomics 4: 31-36.
- Allen JF, Puthiyaveetil S, Strom J, Allen CA (2005) Energy transduction anchors genes in organelles. Bioessays 27: 426-435.
- Puthiyaveetil S, Kavanagh TA, Cain P, Sullivan JA, Newell CA, Gray JC, Robinson C, van der Giezen M, Rogers MB, Allen JF (2008) The ancestral symbiont sensor kinase CSK links photosynthesis with gene expression in chloroplasts. Proceedings of the National Academy of Sciences of the United States of America 105: 10061-10066. | Supporting information.
- Puthiyaveetil S, Allen JF (2009) Chloroplast two-component systems: evolution of the link between photosynthesis and gene expression. Proceedings of the Royal Society B-Biological Sciences 276: 2133-2145.
- Puthiyaveetil S, Ibrahim IM, Jeličić B, Tomašić A, Fulgosi H, Allen JF (2010) Transcriptional control of photosynthesis genes: the evolutionarily conserved regulatory mechanism in plastid genome function. Genome Biology and Evolution 2: 888-896. | Supplementary material.
- Allen JF, de Paula WBM, Puthiyaveetil S, Nield J (2011) A structural phylogenetic map for chloroplast photosynthesis. Trends in Plant Science 16(12): 645-655 | Supplemental Data.
- de Paula WBM, Allen JF, van der Giezen M (2012) Mitochondria, hydrogenosomes and mitosomes in relation to the CoRR hypothesis for genome function and evolution. In: Bullerwell CE (ed) Organelle Genetics. Springer, Berlin and Heidelberg, pp. 105-119.
- Puthiyaveetil S, Ibrahim IM, Allen JF (2013) Evolutionary rewiring: a modified prokaryotic gene regulatory pathway in chloroplasts. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 368: 20120260. doi:10.1098/rstb.2012.0260.
- Maier U-G, Zauner S, Woehle C, Bolte K, Hempel F, Allen JF, Martin WF (2013) Massively convergent evolution for ribosomal protein gene content in plastid and mitochondrial genomes. Genome Biology and Evolution. First published online: November 19, 2013. doi:10.1093/gbe/evt181 | Supplementary material.
- Allen JF (2015) Why chloroplasts and mitochondria retain their own genomes and genetic systems: colocation for redox regulation of gene expression. Proceedings of the National Academy of Sciences of the United States of America 112: 10231–10238. doi:10.1073/pnas.1500012112
- Allen JF (2017) The CoRR hypothesis for genes in organelles. Journal of Theoretical Biology, in press. doi:10.1016/j.jtbi.2017.04.008
Summary of Research | Publications | John F. Allen web page