Eukaryotic non-coding DNA is functional: evidence from the differential scaling of cryptomonad genomes

Genic DNA functions are commonplace: coding for proteins and specifying non -messenger RNA structure. Yet most DNA in the biosphere is non-genic, exist ing in nuclei as non-coding or secondary DNA. Why so much secondary DNA exi sts and why its amount per genome varies over orders of magnitude (correlat ing positively with cell volume) are central biological problems. A novel p erspective on secondary DNA function comes from natural eukaryote-eukaryote chimaeras (cryptomonads and chlorarachneans) where two phylogenetically di stinct nuclei have coevolved within one cell for hundreds of millions of ye ars. By comparing cryptomonad species differing 13-fold in cell volume, we show that nuclear and nucleomorph genome sizes obey fundamentally different scaling laws. Following a more than 125-fold reduction in DNA content, nuc leomorph genomes exhibit little variation in size. Furthermore, the present lack of significant amounts of nucleomorph secondary DNA confirms that sel ection can readily eliminate functionless nuclear DNA, refuting 'selfish' a nd 'junk' theories of secondary DNA. Cryptomonad nuclear DNA content varied 12-fold: as in other eukaryotes, larger cells have extra DNA, which is alm ost certainly secondary DNA positively selected for a volume-related functi on. The skeletal DNA theory explains why nuclear genome size increases with cell volume and, using new evidence on nucleomorph gene functions, why nuc leomorph genomes do not.