Comparative Genomics of Plant Chromosomes

Abstract

Comparative genomics, the study of the similarities and differences in structure and function of hereditary information across taxa, uses molecular tools to investigate many notions that long preceded identification of DNA as the hereditary molecule. Vavilov’s (1922) law of homologous series in variation was an early suggestion of the similarities in the genetic blueprints of many (plant) species. Genetic analysis based on morphological and isoenzyme markers hinted at parallel arrangements of genes along the chromosomes of various taxa. These hints were later borne out at the DNA level, in seminal investigations of nightshades (Tanksley et al., 1988; Bonierbale et al., 1988) and grasses (Hulbert et al., 1990). Over the past two decades, multiple investigations of many additional taxa have delivered two broad messages: (1) In most plants, the evolution of the small but essential portion of the genome that actually encodes the organism’s genes has proceeded relatively slowly; as a result, taxa that have been reproductively isolated for millions of years have retained recognizable intragenic DNA sequences as well as similar arrangements of genes along the chromosomes. (2) A wide range of factors, such as ancient chromosomal or segmental duplications, mobility of DNA sequences, gene deletion, and localized rearrangements, has been superimposed on the relatively slow tempo of chromosomal evolution and causes many deviations from colinearity. The Brassicaceae comprise 360 genera, organized into 13 tribes (Shultz, 1936; Al-Shehbaz, 1973). The most economically important species are in the genus Brassica (tribe Brassiceae), six species of which are cultivated worldwide. Three of these species are considered diploid (B. rapa, A genome, 2n = 2x = 20; B. nigra, B genome, 2n = 2x = 16; B. oleracea, C genome, 2n = 2x = 18), and three are amphiploid derivatives of the diploids (B. juncea, AB, 2n = 4x = 36; B. napus, AC, 2n = 4x = 38; B. carinata, BC, 2n = 4x = 34). At least 15 molecular genetic maps have been constructed for Brassica that include all of the major cultivated species (Slocum et al., 1990; Landry et al., 1991, 1992; Song et al., 1991; Chyi et al., 1992; Kianian and Quiros, 1992; Figdore et al., 1993; Ferreira et al., 1994; Teutonico and Osborn, 1994; Uzunova et al., 1995; Lagercrantz and Lydiate, 1996; Truco et al., 1996; Lan et al., 2000a, 2000b; T.-H. Lan and A.H. Paterson, manuscript submitted). These maps include at least 935 different publicly available probes, with many shared by multiple maps. Within a species, the maps show almost complete colinearity (see Lydiate et al., 1993), except for small inversions that differ among some B. oleracea morphotypes (Kianian and Quiros, 1992; Lan et al., 2000a). Comparison of B. rapa with B. oleracea and B. napus supports the close evolutionary relationship between the two diploids but indicates that deletions and insertions may have occurred after divergence of the two species (Hoenecke and Chyi, 1991). The genome of the synthetic B. napus is essentially unrearranged with respect to its B. oleracea and B. rapa progenitors (Lydiate et al., 1993), although the evolution of wild B. napus (Cheung and Landry, 1996) has been accompanied by more complicated rearrangements. Extensive segmental duplications are found in both diploid and amphidiploid maps, supporting the hypothesis that diploid Brassica spp are derived from an ancestor with a lower original basic chromosome number; however, no duplications of whole linkage groups have been found. At least 22 chromosomal rearrangements differentiate B. oleracea homeologs from one another (Lan et al., 2000a) (see Figure 1). Most of the world’s food and feed crops are members of the family Poaceae, including rice, wheat, maize, sorghum, sugarcane, barley, oat, rye, millet, and others. Conservation across large chromosomal tracts, spanning ∼65 million years of evolution (Figure 2), is a recurring message from many investigations of diverse Poaceae (see Bennetzen and Freeling, 1993). Pioneering efforts in the comparative mapping of maize and sorghum (Hulbert et al., 1990) have been supported by more detailed studies (Whitkus et al., 1992; Berhan et al., 1993; Binelli et al., 1993; Chittenden et al., 1994; Pereira et al., 1994) and supplemented by the comparative organization of maize and rice (Ahn and Tanksley, 1993), wheat and rice (Kurata et al., 1994), and maize, wheat, and rice (Ahn et al., 1993). A host of investigations additionally encompasses many other cultivated Poaceae, with particular emphasis on the interrelationships among the homeologous chromosome sets of the Triticeae and their relatives (see Naranjo et al., 1987; Chao et al., 1989; Liu and Tsunewaki, 1991; Devos et al., 1992a, 1992b, 1993, 1995; Liu et al., 1992; Xie et al., 1993; Namuth et al., 1994; Hohmann et al., 1995; Marino et al., 1996; Mickelson-Young et al., 1995; Nelson et al., 1995a, 1995b, 1995c; Van Deynze et al., 1995). Curiously, even in the re