Comparative genomics in the grass family: molecular characterization of grass genome structure and evolution

Abstract

The genomes of grasses are very different in terms of size, ploidy level and chromosome number. Despite these significant differences, it was found by comparative mapping that the linear order (colinearity) of genetic markers and genes is very well conserved between different grass genomes. The potential of such conservation has been exploited in several directions, e.g. in defining rice as a model genome for grasses and in designing better strategies for positional cloning in large genomes. Recently, the development of large insert libraries in species such as maize, rice, barley and diploid wheat has allowed the study of large stretches of DNA sequence and has provided insight into gene organization in grasses. It was found that genes are not distributed randomly along the chromosomes and that there are clusters of high gene density in species with large genomes. Comparative analysis performed at the DNA sequence level has demonstrated that colinearity between the grass genomes is retained at the molecular level (microcolinearity) in most cases. However, detailed analysis has also revealed a number of exceptions to microcolinearity, which have given insight into mechanisms that are involved in grass-genome evolution. In some cases, the use of rice as a model to support gene isolation from other grass genomes will be complicated by local rearrangements. In this Botanical Briefing, we present recent progress and future prospects of comparative genomics in grasses.

Fig. 1. Different types of micro‐rearrangements observed in grass genomes at the microcolinearity level: deletion and/or translocation of small DNA fragments to another chromosome (A) (Kilian et al., 1997; Tikhonov et al., 1999; Tarchiniet al., 2000); gene inversion (B) or gene duplication (C) (Chen et al., 1997; Dubcovsky et al., 2001) or a combination of these rearrangements. Genetic mapping using probes corresponding to the adjacent sequences would indicate colinearity in this region. However, some of these micro‐rearrangements (e.g. translocations) will complicate the analysis and limit the use of colinearity in cross genome map‐based cloning strategies. Different genes are indicated by coloured boxes and the orientation of the transcription is indicated by an arrow below the genes.

Fig. 2. Different types of gene organization observed in grass genomes. A, Coding regions are conserved between maize and rice but the size of the intergenic region varies according to the genome size (Chen et al., 1997). B, Similar high‐gene density regions are found at orthologous loci in genomes which size can differ by a factor > 12 (Feuillet et al., 1999). C, Both high‐gene density regions and genes interspersed by large intergenic regions coexist on the same DNA fragment (Tikhonov et al., 1999; Wicker et al., 2001). D, Model for the large scale gene organization and evolution of large grass genomes. Gene‐rich regions, which are composed of both high‐gene density islands (one gene every 5–20 kb) and single genes interspersed by less than 150 kb distances, are distributed along the chromosomes. The question mark indicates that the presence of genes in the large regions located in‐between the gene‐rich regions has not yet been demonstrated. Genes are represented by different coloured boxes.

Fig. 3. Possible mechanisms of genome expansion in the grass genomes. A, Insertion of retroelements in the intergenic regions is a major driving force of genome expansion. Several waves of retroelement invasions can occur leading to the insertion of retrotransposons within each other (nested retroelements; SanMiguel et al., 1996; Wicker et al., 2001). B, Local duplications and insertion of sequences that do not show features of retroelements can also contribute to genome size increase (Feuillet et al., 2001; Wicker et al., 2001). Genes are indicated as black and white patterned boxes. Retrotransposons are represented by coloured chevrons flanked by black chevrons representing the long terminal repeats (LTRs).

Fig. 4. Possible mechanisms leading to genome contraction. Genome contraction can be due to unequal crossing‐over or intra‐element recombination between nearby long terminal repeats (LTRs). Such recombination leads to the removal of the internal part of the retroelement (in blue) leaving a solo LTR (Vicient et al., 1999; Shirasu et al., 2000). Deletions of large DNA fragments consisting of different types of retroelements involve a mechanism independent from retrotransposon activity and are also responsible for DNA loss (Wicker et al., 2001). Genes are indicated by black and white patterned boxes, retroelements are indicated by coloured chevrons delimited by LTRs represented as black chevrons.