John F. Allen

Research

Redox signalling in cell evolution

Chloroplasts and mitochondria

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 chloroplast 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 has now found, in plants, 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. The Chloroplast Sensor Kinase. The figure shows a pair of guard cells forming one stoma of a tobacco leaf and viewed by fluorescence microscopy. In the picture at the top of the panel, individual chloroplasts in the cells are seen as their red chlorophyll fluorescence. The middle picture shows the same view, but the image is of fluorescence from green fluorescent protein, GFP, that has been imported into the chloroplasts as a passenger with the Chloroplast Sensor Kinase, CSK. CSK was discovered by Sujith Puthiyaveetil in his search for the redox sensor, predicted by CoRR to couple photosynthesis with chloroplast gene expression. The bottom picture shows an overlay of the other two pictures. The red and green fluorescence together give the colour orange. Only the lower of the two guard cells was transformed with tungsten particles coated with GFP-CSK, and shot into the leaf. Natural selection has retained bacterial sensor kinases in chloroplasts, but moved their genes to the nucleus of the plant cell. 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. | 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

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 era, between 2.8 and 3.5 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. Allen JF (2005) A redox switch hypothesis for the origin of two light reactions in photosynthesis. Febs Letters 579: 963-968. | Allen JF, Martin W (2007) Evolutionary biology - Out of thin air. Nature 445: 610-612.

Regulation of photosynthesis

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 yellow phosphorus atom joined to four red oxygen atoms. Without the phosphate group, the peptide chain is disordered. The addition and subtraction of phosphate regulates the conversion of energy from sunlight in photosynthesis. Slide the movie controller to gain an impression of depth. Graphic made from atomic coordinates of a model from NMR spectroscopy. Allen JF, Forsberg J (2001) Molecular recognition in thylakoid structure and function. Trends in Plant Science 6: 317-326. | Allen JF (2003) State transitions - a question of balance. Science 299: 1530-1532.

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