When it comes to genomes, size matters

Genome size and angiosperms

Of any eukaryotic group, angiosperms (the flowering plants) deserve special mention, as they display the largest range in genome size (GS) known to date, with approximately a 2,400-fold difference between the smallest and largest genomes. At the lower end of the scale, the minute genome of the carnivorous plant Genlisea aurea (Lentibulariaceae) contains just 64 Mb of DNA. At the other extreme, the Japanese canopy plant (Paris japonica, Melanthiaceae) holds the current record, with a staggering 149,000 Mb of DNA packed into each gametic nucleus. Indeed, its genome is so large that if its chromosomes were uncoiled and placed end to end they would be taller that the tower of Big Ben!

Despite this huge range, the distribution of GS in angiosperms is strongly skewed towards small sizes (see graph below), and those species with giant genomes are considerably restricted to just a few lineages. The limited occurrence of very large genomes could be influenced by the fact that carrying such a large amount of DNA has many consequences at the level of individual cells. For example, genome size places restrictions on cell size, the amount of phosphates and nitrates needed to build nucleic acids and the time that it takes for cells to divide. Such effects also have knock-on impacts at the whole-plant level.

Comparing data from many different plant species has demonstrated that those with the largest genomes are less able to live in polluted soils and are less likely to adapt to, and tolerate, extreme environmental conditions. Consequently, species with giant genomes might be at greater risk of extinction. 

So how did the genomes become so large in Parideae?

Most of our understanding of the processes generating GS change comes from studies of model plants with small or very small genomes. These studies have shown that polyploidy (numerous copies of the genome) and the presence of repetitive DNA sequences (eg transposable elements (TEs) and DNA satellites) are primarily responsible for promoting GS diversity. Transposable elements are bits of DNA that move around the genome, often duplicating themselves as part of the process, which therefore have the potential to contribute hugely to genome size. Likewise, DNA satellites are long stretches of repetitive non-coding DNA up to several thousand base pairs in length.

However, polyploidy is largely absent in Parideae, so another explanation for the large genome size needs to be sought. Here we propose that it is the amplification of repetitive DNA which may have played an important role in governing these changes in genome size. Genome size increase could therefore be explained by bursts of DNA amplification coupled with lower rates of DNA removal, as illustrated by the great size of chromosomes in the tribe. Certainly, this has been observed in other organisms with large genomes, not only in land plants such as in the closely related fritillaries (with the largest diploid genomes of any angiosperm group) and in the Norway spruce (Picea abies), but also in animals (eg salamanders), where several types of repetitive DNA have been amplified and lower rates and smaller DNA deletions are prevalent.