Increasing biological complexity is positively correlated with the relative genome-wide expansion of non-protein-coding DNA sequences

Abstract

Prior to the current genomic era it was suggested that the number of protein-coding genes that an organism made use of was a valid measure of its complexity. It is now clear, however, that major incongruities exist and that there is only a weak relationship between biological complexity and the number of protein coding genes. For example, using the protein-coding gene number as a basis for evaluating biological complexity would make urochordates and insects less complex than nematodes, and humans less complex than rice. We analyzed the ratio of noncoding to total genomic DNA (ncDNA/tgDNA) for 85 sequenced species and found that this ratio correlates well with increasing biological complexity. The ncDNA/tgDNA ratio is generally contained within the bandwidth of 0.05 - 0.24 for prokaryotes, but rises to 0.26 - 0.52 in unicellular eukaryotes, and to 0.62 - 0.985 for developmentally complex multicellular organisms. Significantly, prokaryotic species display a non-uniform species distribution approaching the mean of 0.1177 ncDNA/tgDNA (p = 1.58 x 10-13), and a nonlinear ncDNA/tgDNA relationship to genome size (r = 0.15). Importantly, the ncDNA/tgDNA ratio corrects for ploidy, and is not substantially affected by variable loads of repetitive sequences. We suggest that the observed noncoding DNA increases and compositional patterns are primarily a function of increased information content. It is therefore possible that introns, intergenic sequences, repeat elements, and genomic DNA previously regarded as genetically inert may be far more important to the evolution and functional repertoire of complex organisms than has been previously appreciated.