The skeletal function of non-genic nuclear DNA: new evidence from ancient cell chimaeras

DNA can be divided functionally into three categories: (1) genes - which co de for proteins or specify non-messenger RNAs; (2) semons - short specific sequences involved in the replication, segregation, recombination or specif ic attachments of chromosomes, or chromosome regions (e.g. loops or domains ) or selfish genetic elements; (3) secondary DNA - which does not function by means of specific sequences. Probably more than 90% of DNA in the biosph ere is secondary DNA present in the nuclei of plants and phytoplankton. The amount of genic DNA is related to the complexity of the organism, whereas the amount of secondary DNA increases proportionally with cell volume, and not with complexity. This correlation is most simply explained by the skele tal DNA hypothesis, according to which nuclear DNA functions as the basic f ramework for the assembly of the nucleus and the total genomic DNA content functions (together with relatively invariant folding rules) in determining nuclear volumes. Balanced growth during the cell cycle requires the cytonu clear ratio to be basically constant, irrespective of cell volume; thus nuc lear volumes, and therefore the overall genome size, have to be evolutionar ily adjusted to changing cell volumes for optimal function. Bacteria, mitoc hondria, chloroplasts and viruses have no nuclear envelope; and the skeleta l DNA hypothesis simply explains why secondary DNA is essentially absent fr om them but present in large cell nuclei. Hitherto it has been difficult to refute the alternative hypothesis that nuclear secondary DNA (whether 'jun k' or selfish DNA) accumulates merely by mutation pressure, and that select ion for economy is not strong enough to eliminate it, whereas accumulation in mitochondria and plastids is prevented by intracellular replicative comp etition between their multiple genomes. New data that discriminate clearly between these explanations for secondary DNA come from cryptomonads and chl orarachneans, two groups of algae that originated independently by secondar y symbiogenesis (i.e., the merger of two radically different eukaryote cell s) several hundred million years ago. In both groups the nucleus and plasma membrane of the former algal symbiont persist as the nucleomorphs and peri plastid membrane, respectively. The fact that nucleomorphs have undergone a 200- to 1000-fold reduction in genome size and have virtually no secondary DNA shows that selection against non-functional nuclear DNA is strong enou gh to eliminate it very efficiently; therefore, the large amounts of second ary DNA in the former host nuclei of these chimaeras, and in nuclei general ly, must be being maintained by positive selection. The divergent selection for secondary DNA in the nucleus and against it in nucleomorphs is readily explicable by the skeletal DNA hypothesis, given the different spectrum of gene functions that it encodes.