Genome Relationships: The Grass Model in Current Research

Abstract

Ten years ago, with the advent of comparative mapping, a new tool became available to plant geneticists. Comparative genome analyses demonstrated that gene orders among related plant species remained largely conserved over millions of years of evolution. This finding has revolutionized our thinking and formed the basis of a new science—comparative genomics. Since the first comparative mapping experiments, studies of genome relationships have included an ever wider range of plant species, and the focus has shifted from comparisons at the gross map level to studies of gene organization in small chromosomal regions and finally to the DNA sequence itself. To date, the most comprehensive data set comes from the grasses. The Poaceae family includes the staple cereals rice, maize, wheat, barley, sorghum, and the millets. For most of the past century, research has proceeded on each of these species individually. Mutants were produced, genetic maps were generated, and biochemical pathways were unraveled. Comparative genomics has provided the basis and stimulus to integrate this knowledge for application to all cereal crops. The realization of the power of a comparative approach has led to several plant genome initiatives and has promoted rice as a model for cereal crops. The rice genome, with only 400 million DNA base pairs (Mb), is the smallest among the major cereal crops and only approximately four times larger than that of the eudicot model plant Arabidopsis. Dense genetic maps, carrying some 2500 markers, have been constructed, and physical maps cover most of the genome. Additionally, large public collections of expressed sequence tags (ESTs) have become available, and it is clear that sequence data covering the entire rice genome will add a further vital dimension to comparative genomics in the near future. Views on the prospective applications of comparative genomics have developed as new insights have been gained into genome relationships and genome organization. At the same time, new opportunities have been envisaged and exploited. Below, we present an overview of the status of comparative genomics, with examples of ongoing research projects, focusing on wheat. Cereal crop species vary greatly in their DNA content, from ∼400 Mb in the small rice and foxtail millet genomes to 17,000 Mb in bread wheat. The bulk of the larger genomes consists of repetitive DNA sequences, most of which are species specific. Genes, on the other hand, tend to be highly conserved at the DNA sequence level. This conservation allows the use of heterologous probes in DNA gel blot experiments to identify orthologous DNA sequences even in species belonging to different tribes within the same taxonomic family. Therefore, cross-mapping of gene sequences is the first step to study genome relationships. An evolutionary analysis of closely related genomes is one immediate result of molecular mapping within allopolyploid species. Wheat, for example, arose through spontaneous hybridization of the diploid species Triticum urartu (AA genome) and an unknown species (BB genome), probably belonging to the Sitopsis group of Aegilops spp, to form tetraploid wheat (AABB). Further hybridization with a third ancestral species, Aegilops tauschii (DD), led, ∼10,000 years ago, to the production of hexaploid bread wheat (2n = 6x = 42; AABBDD). The finding that the three wheat genomes have a highly similar gene content and order was the first demonstration of colinearity in the grasses and a pivotal finding in the development of comparative genomics (Chao et al., 1989). Subsequently, it has become clear that the genomes are rearranged, relative to one another, through the occurrence of large reciprocal translocations involving chromosome arms 2BS and 6BS (Devos et al., 1993b) and chromosomes 4A, 5A, and 7B (Devos et al., 1995). The first translocation in this latter complex involved chromosome arms 4AL and 5AL and took place in the diploid ancestor. The remaining rearrangements probably arose at the tetraploid level. Comparisons at the genetic map level within the tribe Triticeae, which includes wheat, barley, rye, and wild relatives such as Aegilops spp, again show a high conservation of genome colinearity, which is only disrupted by gross chromosomal translocations. Interestingly, the number of rearrangements observed between different genomes varies greatly and appears to be unrelated to phylogenetic distance or evolutionary time. For example, the barley (Hordeum vulgare) genome is highly colinear with that of A. tauschii, differing only by two possible inversions (Dubcovsky et al., 1996), whereas the A. umbellulata and A. tauschii genomes differ by a minimum of 11 rearrangements (Zhang et al., 1998; Figure 1). Phylogenetic data have, however, indicated that A. umbellulata is more closely related to A. tauschii than is barley (Kellogg et al., 1996). Analyses of other Triticeae, such as rye (Secale cereale) (Devos et al., 1993a), A. longissima (Naranjo, 1