John F. Allen


The origin of atmospheric oxygen | Chloroplasts and mitochondria | Mitochondria, ageing, separate sexes | Regulation of photosynthesis | ORCID

The origin of atmospheric oxygen

I propose that oxygen-evolving photosynthesis arose from a simple mutation that produced constitutive expression of two sets of reaction centre genes, otherwise expressed at different times and in different places in an anaerobic bacterium. Shared electron carriers then connected the two, newly co-existing photosystems, giving rise to photosystem I and photosystem II and to the first cyanobacterium. The electrical connection allowed indefinitely renewable generation of electrochemical potentials high enough to oxidise water to oxygen. This testable hypothesis provides an insight into the origin of oxygenic photosynthesis - the profound evolutionary and geochemical transition that paved the way for aerobic respiration, eukaryotes, multicellularity, plants and animals, and colonisation of the land.

A world without oxygen. An artist's impression of a sea-shore in the Archaean aeon, between 2.5 and 3.6 thousand million years ago. The hydrothermal springs in the foreground and stromatolites in the littoral zone are still with us today. Without atmospheric oxygen there is no ozone layer. The weak sunlight is rich in ultraviolet light, and life is confined to seas, rivers, lakes, and rock-pools. Stromatolites are today built by oxygen-evolving cyanobacteria. In the Archaean they may have been built, instead, by their anaerobic ancestors, with their redox switch to adapt photosynthesis to the changing environment.

A detail from Archaean Landscape by Peter Sawyer of the Smithsonian Institution, Washington.

pdf Allen JF, Thake B, Martin WF (2019) Nitrogenase inhibition limited oxygenation of Earth’s Proterozoic atmosphere. Trends in Plant Science. doi:10.1016/j.tplants.2019.07.007 | pdf Allen JF (2016) A proposal for formation of Archaean stromatolites before the advent of oxygenic photosynthesis. Frontiers in Microbiology 7: 1784. | pdf Allen JF, Martin W (2007) Evolutionary biology - Out of thin air. Nature 445: 610-612. | pdf Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. FEBS Letters 579: 963-968.

Dawn of the water eaters: How Earth got its oxygen – New Scientist
Archaean Landscape

Chloroplasts and mitochondria

Chloroplast Sensor Kinase Why do chloroplasts and mitochondria contain distinct genetic systems to make a small but constant sub-set of their own proteins? I propose that redox control of gene expression explains the function of the genomes of chloroplasts and mitochondria and their retention, in evolution, as extra-nuclear genetic systems. This hypothesis is named CoRR for Co-location for Redox Regulation. CoRR states that redox regulation of gene expression repays, on its own, the huge cost of maintaining genetic systems in the chloroplasts and mitochondria of eukaryotic cells. For animal mitochondria, this cost includes ageing and death of the individual. Template mitochondria are rescued and granted immortality by means of maternal inheritance and sex. Redox chemistry is thus a key to understanding both cell evolution and biological energy transduction.

In our laboratory, Sujith Puthiyaveetil found the conserved, ancestral, bacterial sensor kinase that couples electron transport to chloroplast gene transcription, and whose existence and properties are predicted by CoRR. Numerous experimental predictions flow from this key discovery.

Chloroplast Sensor Kinase acts on the transcriptional regulators Plastid Transcription Kinase (PTK) and Sigma Factor 1 (Sig-1). Changes in incident light energy produce photosystem stoichiometry adjustment in the chloroplast thylakoid membrane. Plastoquinone carries electrons between the photosystems, and its redox state depends on the rate of each photosystem relative to the other. Plastoquinone redox state is information. This information is communicated to the RNA polymerase at the promoter regions of genes for the reaction centres of the two photosystems, where their relative rates of transcription are determined by the phosphorylation state of Chloroplast Sensor Kinase. Natural selection has retained bacterial sensor kinases in chloroplasts, but moved their genes to the nucleus of the cell. Chloroplasts inherit a typically bacterial mode of gene expression that must act on a typically bacterial genome. Thus, in photosynthetic eukaryotes, chloroplasts retain genomes, and genes for photosynthetic reaction centres are always found only in chloroplast DNA.

pdf Allen JF (2017) The CoRR hypothesis for genes in organelles. Journal of Theoretical Biology 434: 50-57. | pdf 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 | pdf 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. | pdf 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. |

Co-location for Redox Regulation – CoRR

Mitochondria, ageing, separate sexes

There is no greater mystery in the whole world, as it seems to me, than the existence of the sexes, – more especially since the discovery of Parthenogenesis. The origination of the sexes seems beyond all speculation.Charles Darwin: Letter to J. S. Henslow, 16 July 1860.

Fertilization of an egg by a sperm, like all life processes, requires energy, which is provided in the form of ATP. ATP is made in mitochondria. However, there is a price to pay – mitochondria also contain DNA, which becomes progressively degraded by the chemistry required for ATP synthesis. We show that egg mitochondria are radically different from all others by being in a state of suspended animation – unable to use the information in their DNA to make the protein machinery of respiration. Sperm mitochondria wear out and are discarded when their job is done. But, in their germ-lines, females carry mitochondria that never grow old.

A fluorescent image of three consecutive stages of oogenesis in the fruit fly Drosophila melanogaster. Cells are stained to reveal reactive oxygen species in green and DNA in blue. Oocytes and nurse cells have quiescent mitochondria, and their nuclear DNA gives them their blue colour. In contrast, mitochondria of the surrounding diploid follicle cells, active in respiration, produce reactive oxygen species, and so green predominates. We find that female germline mitochondria in fruit fly, zebrafish and jellyfish suppress transcription and oxidative phosphorylation. This suppression may protect the mitochondrial genetic template from free radical-mediated mutation. We propose that complementary properties of mitochondria of male and female gametes, serving motility and hereditary functions, respectively, explain the origin and function of sexual dimorphism in multicellular animals. This hypothesis, after Allen (1996), predicts that the female germ line forms an indefinitely replicating vehicle for accurate transmission of mitochondrial DNA between generations.

pdf de Paula WBM, Lucas CH, Agip A-NA, Vizcay-Barrena G, Allen JF (2013) Energy, ageing, fidelity and sex. Oocyte mitochondrial DNA as a protected genetic template. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences 368: 20120267. | pdf de Paula WBM, Agip A-NA, Missirlis F, Ashworth R, Vizcay-Barrena G, Lucas CH, Allen JF (2013) Female and male gamete mitochondria are distinct and complementary in transcription, structure, and genome function. Genome Biology and Evolution 5: 1969-1977. | pdf Allen JF, de Paula WBM (2013) Mitochondrial genome function and maternal inheritance. Biochemical Society Transactions 41: 1298-1304.

Why are there two sexes? – YouTube – Presentation with audio
Separate sexes and maternal transmission of DNA in quiescent, template mitochondria – animated graphic
Mitochondria and separate sexes – Faculti – Wilson de Paula
On the Origin of the Sexes – Highlight in Genome Biology and Evolution – Danielle Venton
Damage and Fidelity: The Role of the Female Germline in mtDNA Inheritance – Claire Asher
Genome Biology and Evolution | Cover April 2014

Regulation of photosynthesis

N-terminus of LHC II In photosynthesis, the redox state of the electron carrier plastoquinone controls phosphorylation of proteins of the chloroplast light-harvesting pigment-protein complex, LHC II. This control explains the phenomenon of state 1-state 2 transitions in plants and algae. Our results that first suggested this hypothesis have been corroborated in many laboratories and experimental systems. Light-harvesting function of chloroplast chlorophyll-proteins is universally regulated to restore redox poise within the photosynthetic electron transport chain. A major goal is an atomic-resolution structural description of the effects of phosphorylation of LHC II on its interactions with chloroplast photosystem I and photosystem II.

The amino-terminal segment of LHC II, the protein that harvests sunlight. The peptide chain adopts a compact, helix-like structure - but only when a phosphate group is attached. The phosphate group is depicted as a phosphorus atom (in yellow) joined to red oxygen atoms (in red). Without the phosphate group, the peptide chain is disordered. The addition and subtraction of phosphate regulates the conversion of energy from sunlight in photosynthesis.

Graphic from atomic coordinates of a model derived from NMR spectroscopy.

pdf Allen JF, Nield J, Krauß N (2019) Molecular recognition: how photosynthesis anchors the mobile antenna. Trends in Plant Science 24: 388-392. doi:10.1016/j.tplants.2019.03.003 | pdf Allen JF (2017) Why we need to know the structure of phosphorylated chloroplast light-harvesting complex II. Physiologia Plantarum 161: 28-44. | pdf Allen JF (2003) State transitions - a question of balance. Science 299: 1530-1532.

In our time – Photosynthesis | Podcast

The origin of atmospheric oxygen | Chloroplasts and mitochondria | Mitochondria, ageing, separate sexes | Regulation of photosynthesis | Head of this page | ORCID

Publications | John F. Allen web page