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 my laboratory, Sujith Puthiyaveetil has 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.

 

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.

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.

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.