Why chloroplasts and mitochondria retain their own genomes and genetic systems: Colocation for redox regulation of gene expression

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.

Keywords: CoRR hypothesis; chloroplast; mitochondrion; oxidative phosphorylation; photosynthesis.

Fig. 1.

Two-component redox regulatory control of transcription. The bioenergetic membrane is a diagrammatic composite of photosynthetic and respiratory membranes that couple electron transport with ATP synthesis/hydrolysis by means of a transmembrane gradient of hydrogen ion (H⁺) concentration and electrical potential difference between the outer, positive aqueous phase (P-phase) and the inner, negative aqueous phase (N-phase). A redox sensor responds, by autophosphorylation, to a change in the redox state of an electron carrier. Phosphoryl transfer to a specific response regulator then initiates or inhibits a DNA-dependent RNA polymerase through the action of a regulatory sigma factor that is specific to a particular promoter. Transcription, translation, and assembly of an electron carrier then serve to regulate electron transfer at a specific point in the chain, optimizing it in response to a change in environmental conditions. Adapted from ref. .

Fig. 2.

(A) The CoRR hypothesis outlined—ancestral prokaryote. Genes A, B, and C are transcribed and translated to give proteins A, B, and C. Protein A is a membrane-intrinsic component of the prokaryote’s bioenergetic (energy-transducing) membrane; its redox state regulates its own synthesis by the action of a two-component regulatory system on transcription of gene A. (B) The CoRR hypothesis outlined—endosymbiont. Genes A, B, and C are copied from the endosymbiont to the genome of the host cell. They are transcribed and translated, on host ribosomes, to give precursor proteins that are exported from the host into the endosymbiont. Each of proteins A, B, and C then has two possible sites of synthesis. Natural selection determines which of these sites is maintained. (C) The CoRR hypothesis outlined—bioenergetic organelle. Genes B and C are lost from their original location whereas a continued requirement for regulation of gene A by the redox state of protein A maintains colocation of gene A with gene product. The endosymbiont has become a bioenergetic organelle. Adapted from ref. .

Fig. 3.

Two-component redox regulation of chloroplast transcription. Chloroplast sensor kinase (CSK) selectively switches on and off chloroplast genes in response to perturbations in the photosynthetic electron transport chain (depicted as electron flow from H₂O to NADP⁺) within the thylakoid membrane. CSK is a redox sensor and reports on electron flow through plastoquinone (PQ). A response regulator (RR) mediates CSK’s control over transcription of genes for reaction center apoproteins of photosystem I and photosystem II, giving autoregulatory adjustment of photosystem stoichiometry. Chloroplast genes and gene products are shown in green. The nuclearly encoded components, imported into the chloroplast, are shown in light brown. Adapted from ref. .

Fig. 4.

Convergent evolution of gene content in mitochondria and chloroplasts. The ancestors of both organelles were prokaryotes with genomes encoding around 5,000 genes. During the course of endosymbiosis, genes are transferred from each organelle to the hosts’ nuclear genome, and the corresponding gene products are imported back to the organelles. The initial genome size of around 5,000 genes decreased to 3–67 genes in mitochondria and 23–200 genes in chloroplasts. The color coding within compartments in the lower part of the figure illustrates the convergent evolution of genes retained in the two bioenergetic organelles: genes for components of oxidative phosphorylation, photosynthesis, and proteins of 50S and 30S ribosomal subunits. Organellar-encoded genes are colored brown for mitochondria and green for plastids. TIC/TOC, protein translocator of the inner/outer chloroplast membrane; TIM/TOM, protein translocator of the inner/outer mitochondrial membrane. Schemes for oxidative phosphorylation and photosynthesis are adapted from ref. . Reproduced from ref. .