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.

The Roles of Mutation, Selection, and Expression in Determining Relative Rates of Evolution in Mitochondrial versus Nuclear Genomes

“…Specifically, a mixture of nuclear-and mt-encoded products physically interact to form the multisubunit oxidative phosphorylation (OXPHOS) enzyme complexes (Allen 2015) and components of the mt translational machinery (particularly ribosomes; Maier et al 2013). The nuclear and mt genomes are replicated and inherited in fundamentally different ways, resulting in fascinating coevolutionary dynamics that have important consequences for health, aging, and eukaryotic diversification (Dowling 2014;Hill 2015).…”

Mitochondrial depolarization in yeast zygotes inhibits clonal expansion of selfish mtDNA

“…Yeast cells also possess a mechanism for mitophagy, but so far this machinery was reported to be used mainly for non-selective, bulk removal of mitochondria in the stationary phase or under nitrogen starvation (for a review, see Müller et al, 2015) and was not shown to be activated by uncouplers (Mendl et al, 2011). At the same time, it was suggested that mitochondrial inner membrane region can be enriched with the proteins encoded by the mtDNA adjacent to this region (the CoRR hypothesis, see Allen, 2015 for a review). Therefore, coupling of mitochondria quality control and negative selection of mutated mtDNAs is theoretically possible.…”

Symbiogenesis, gradualism, and mitochondrial energy in eukaryote origin

“…Current debate on symbiogenesis has focused on the role of mitochondria at the origin of eukaryotes. Proponents of symbiogenesis, or endosymbiotic theory, have it that symbiosis is a rare but crucial mechanism of evolution (7,8,9,10,11,12,13,14). Proponents of the opposing gradualist view admit that endosymbiosis occurred when mitochondria arose, but hold that it had no impact on the evolutionary process (15,16,17).…”

“…ii) One more symbiogenic association gave rise to the first cell with plastids (7,9,10,11), from which all plants (now called archaeplastida) descend. iii) Secondary symbioses occurred among eukaryotes to give rise to algae with secondary plastids (83).…”