Repeated big bangs and the expanding universe: Directionality in plant genome size evolution

The lack of correlation between genome size and organismal complexity has long been a topic of great interest. Over the last decade it has become clear that transposable elements play a dominant role in genome size growth, and that most of the observed genome size variation in plants can be ascribed to differential accumulation of transposable elements, particularly long terminal repeat retrotransposons, which often massively proliferate over exceptionally short evolutionary time-scales. In the absence of one or more counterbalancing forces, Bennetzen and Kellogg previously suggested that growth via transposable element accumulation would create a “one-way ticket to genomic obesity”. Phylogenetic evidence, however, indicates that lineages may experience genomic downsizing, notwithstanding the relative paucity of experimental evidence on mechanisms capable of eliminating massive amounts of DNA. Thus, genome size evolution in plants may involve both feast and famine. Here we review recent insights into the molecular mechanisms and evolutionary dynamics of genome size evolution in plants. These include mechanisms that contribute to genome size expansion, i.e. polyploidy and transposable element proliferation, in addition to the counteracting forces that act to remove DNA, particularly intra-strand homologous recombination and illegitimate recombination. We argue that extant genome sizes reflect myriad competing forces of genomic expansion and contraction, but that current evidence pertaining to rates and amounts of DNA loss prove insufficient to overcome transposable element proliferation in most lineages. Accordingly, the directionality of plant genome size evolution in most cases is biased toward growth, with mechanisms of DNA loss acting to attenuate (but not reverse) the march toward obesity.