Abstract
Eukaryotic genomes can vary at least 200,000-fold in size, although the number of genes probably differs by only little over a factor of 10. The extreme variation in genome size is mostly due to varying amounts of repetitive DNA. Most repetitive DNA is comprised of transposable elements (TEs), small genetic units with the ability to move and replicate in the genome. Because the wheat genome (and that of its close relatives such as barley) consists of at least 80% of TE sequences, I devoted much of my early research to classification and characterisation of TE sequences. When I started my research on genomics 10 years ago, very little was known about the molecular mechanisms that shape plant genomes. Data had just started to emerge that some plant genomes have expanded massively by the amplification of LTR retrotransposons. Our early studies showed that this was indeed a predominant mechanism in the wheat genome, providing an explanation for the very large size of the genomes of wheat and its close relatives. However, we and other research groups could show that this TE-driven genome expansion is permanently counteracted by the deletion of DNA through unequal crossing-over and illegitimate recombination. These two forces, expansion and contraction, lead to a constant genomic turnover of sequences that are not under selection pressure (i.e. TEs), making intergenic regions in plant genomes evolve very rapidly and dynamically. The increase/decrease model of genome size evolution is based on these observations and describes genome size as a result of the rate of DNA production through TEs and duplications and its removal through deletions. When whole genome sequences of grasses like sorghum and Brachypodium became available, my co-workers and I were intimately involved in the analysis and annotation of TEs in these genomes. We performed genome-wide comparisons of gene order in grass genomes, specifically focusing on regions with low numbers of colinear genes 3 and synteny breaks. This lead to the discovery that the different chromosome numbers in grasses can be explained by “nested” fusions where entire chromosomes insert into the centromeres of other chromosomes. Additionally, we found that in all grass genomes sequenced so far, one syntenic chromosome arm is extremely rich in repetitive DNA. This finding could not be explained with current models that predict that intergenic (i.e. repetitive) regions evolve rapidly and should therefore not be conserved between species. Our recent research was focused on specific contributions of TE sequences to genome evolution. When TEs insert into or excise from the genome, they can induce double- strand breaks (DSBs) which have to be repaired by the cell. This repair can lead to extensive deletions or the insertion of “filler” DNA. We could show that such DSB repair is a major mechanism responsible for gene movement and the erosion of gene colinearity that goes with it. Our future research will focus on genome-wide comparative analyses, search for additional mechanisms of genome evolution and the contribution of TEs to genome evolution. We are involved in the wheat and barley genome projects and have recently started an effort to completely sequence the genome of the wheat parasite powdery mildew. By expanding our range to larger and/or more diverse genomes, we hope to continue to identify fundamental principles that drive the evolution of eukaryotic genomes.
Wicker, Thomas