Many conserved eukaryotic traits, including apoptosis, two sexes, speciation and ageing, can be causally linked to a bioenergetic requirement for mitochondrial genes. Mitochondrial genes encode proteins involved in cell respiration, which interact closely with proteins encoded by nuclear genes. Functional respiration requires the coadaptation of mitochondrial and nuclear genes, despite divergent tempi and modes of evolution. Free‐radical signals emerge directly from the biophysics of mosaic respiratory chains encoded by two genomes prone to mismatch, with apoptosis being the default penalty for (...) compromised respiration. Selection for genomic matching is facilitated by two sexes, and optimizes fitness, adaptability and fertility in youth. Mismatches cause infertility, low fitness, hybrid breakdown, and potentially speciation. The dynamics of selection for mitonuclear function optimize fitness over generations, but the same selective processes also operate within generations, driving ageing and age‐related diseases. This coherent view of eukaryotic energetics offers striking insights into infertility and age‐related diseases. (shrink)

During evolution, the genomes of eukaryotic cells have undergone major restructuring to meet the new regulatory challenges associated with compartmentalization of the genetic material in the nucleus and the organelles acquired by endosymbiosis (mitochondria and plastids). Restructuring involved the loss of dispensable or redundant genes and the massive translocation of genes from the ancestral organelles to the nucleus. Genomics and bioinformatic data suggest that the process of DNA transfer from organelles to the nucleus still continues, providing raw material for evolutionary (...) tinkering in the nuclear genome. Recent reconstruction of these events in the laboratory has provided a unique tool to observe genome evolution in real time and to study the molecular mechanisms by which plastid genes are converted into functional nuclear genes. Here, we summarize current knowledge about plastid‐to‐nuclear gene transfer in the context of genome evolution and discuss new insights gained from experiments that recapitulate endosymbiotic gene transfer in the laboratory. BioEssays 30:556–566, 2008. © 2008 Wiley Periodicals, Inc. (shrink)

Early in the 20th century, Charles Manning Child attributed organismal gradients in metabolism to interactions among groups of cells. Metabolic gradients are now firmly grounded in redox chemistry, yet modern work on metabolic signaling has consistently focused on the cellular level. Multicellular redox regulation, however, may occur when redox state is determined by the behavior of a group of cells. For instance, typically an abundance of substrate will shift the redox state of mitochondria in the direction of reduction, leading to (...) increased reactive oxygen species (ROS). These ROS, in turn, may modify the conformation and activity of proteins involved in signaling pathways, resulting in phenotypic changes. In contrast, if substrate triggers the contractions of a muscular structure comprising mitochondrion‐rich cells, the resulting metabolic demand may shift the redox state in the direction of oxidation, with a corresponding decrease of ROS and different phenotypic effects. Indeed, colonial hydroids exemplify this process. Parallel examples may occur whenever mitochondria are concentrated in cells of structures that can respond to environmental perturbations with increased metabolic demand. In these circumstances, predicting the direction of metabolic signaling may require an understanding of events at the organismal level. BioEssays 28:72–77, 2006. © 2005 Wiley Periodicals, Inc. (shrink)