Genome Relationships: The Grass Model in Current Research
Year: 2000
Type: article
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, 1995; Zhang et al., 2000), and A. speltoides (Maestra and Naranjo, 1998), provide further evidence that some genomes fix rearrangements more readily than others (Figure 1). These different rates of species divergence through chromosomal rearrangement do not appear to correlate to the breeding system, because high levels of evolutionary translocations are found in both rye, an outbreeder, and A. umbellulata, a predominantly self-pollinated species. A comparison of centromere positions allows us to infer the basic structure of the “ancestral” Triticeae chromosomes. Kimber (1967) observed the centromeres in Triticum and Aegilops spp to be generally located in submedian positions and suggested that subterminal centromere positions were the result of chromosomal rearrangements. The comparative maps indeed show that the subterminal positions of A. umbellulata chromosomes 2U and 7U are due to inversions and those of 3U and 6U to interchromosomal translocations (Figure 1). Gene content and order are also well maintained within taxonomic families, despite large differences between species in genome size and chromosome number. Cross-mapping of restriction fragment length polymorphism probes in a range of cereal crops has led to the widespread identification of chromosomal regions in which marker orders are highly conserved. It is now possible to describe all the genomes of grass crop species by their relationship to a single reference genome, rice. Regions of the rice genome that contain sets of markers that are colinear across other grass species have been termed linkage blocks. Figure 2depicts the genomes of foxtail millet (Setaria italica; 2n = 2x = 18; C = 0.45 pg) and pearl millet (Pennisetum glaucum; 2n = 2x = 14; C = 2.4 pg), two species belonging to the Paniceae tribe within the Panicoideae subfamily, in relation to rice (Oryza sativa; 2n = 2x = 24; C = 0.4 pg). The highly similar arrangement of linkage blocks in foxtail millet and rice demonstrates that these genomes have undergone few rearrangements since their divergence. The pearl millet genome, on the other hand, is highly rearranged relative to rice. Many of these rearrangements are not present in any of the other Panicoideae analyzed to date. Therefore, they are likely to be specific either to pearl millet or to the genus Pennisetum. A few chromosomal rearrangements, however, can be identified that are likely to have occurred before the speciation of the Panicoideae but after the Panicoideae–Oryzoideae divergence. Examples are the organization of rice linkage block 10, which is inserted into rice linkage block 3, and the insertion of rice linkage block 9 into 7 to form specific Panicoideae chromosomes (Figure 2). A different arrangement of rice linkage blocks, the insertion of linkage block 8 into 6 and linkage block 10 into 5, is present in wheat and oat and may characterize the Pooideae subfamily (Gale and Devos, 1998). Some rearrangements may reflect more ancient evolutionary events. A particularly interesting observation is that regions duplicated on rice chromosome arms 11S and 12S (Nagamura et al., 1995) have orthologs on foxtail millet chromosomes VII and VIII and pearl millet linkage groups 1 and 4 (Figure 2). The duplication event must therefore predate the divergence of the Panicoideae and rice from a common ancestor. This duplication has not been observed in members of the Pooideae subfamily; however, this does not preclude its presence even there. Duplications may go unnoticed when the marker density in the critical chromosome regions is low or when low polymorphism levels prohibit the mapping of both copies of duplicated probes. To date, genome relationships have been established between rice, wild rice (Zizania palustris; Kennard et al., 1999), foxtail millet, sugar cane, sorghum, pearl millet, maize, the Triticeae cereals wheat, barley, rye, and oats (for overview, see Gale and Devos, 1998), and a growing number of wild relatives of the domesticated cereal crop species. Despite a divergence time of some 60 million years, less than 30 rice linkage blocks are needed to represent all of these genomes. Significantly, the boundaries of the rice linkage blocks frequently coincide with the location of centromeres and telomeres, which implies that these sites may play a key role in chromosome evolution (Qumsiyeh, 1994; Moore et al., 1997). Other cereals that will be integrated into the grass consensus map in the near future include finger millet (Eleusine coracana) and tef (Eragrostis tef), two members of the Chloridoideae subfamily, and Lolium and Festuca spp, two members of the Pooideae subfamily. The Chloridoideae are a new subfamily not previously represented. In addition to assessing the overall levels of colinearity, it will be of interest to identify chromosomal arrangements that are present in both tef and finger millet. The presence of common rearrangements between subfamilies may provide evidence for taxonomic relationships. Preliminary data on the structural organization of the tetraploid finger millet genome have indicated the presence of the ancient interchromosomal R11S/R12S duplication previously observed in rice, foxtail, and pearl millet (M.M. Dida and K.M. Devos, unpublished data). Therefore, this duplication is predicted to be present also in tef. Phylogenetic and Genome Relationships among Six Triticeae Grasses. The D genome of A. tauschii has been chosen as the reference, and each of the seven chromosomes is represented by a different pattern. Open circles indicate centromere positions. Double-headed arrows indicate inversions. Vertical lines indicate evolutionary translocation breakpoints. The minimum number of chromosomal rearrangements necessary for the six present-day genomes to have evolved from the D genome format is for each species. Relationships among the of and C rice centromere positions. indicate and indicate and as to the rice which are with linkage blocks to entire chromosomes rice chromosomes and or chromosome and In foxtail and pearl millet, for which linkage groups have not been to and the and which to the maps (Devos et al., 2000), are millet chromosomes are with and pearl millet linkage groups are with For chromosomes that have to more than one rice are indicated with the chromosome number by indicate regions for which few comparative data are Double-headed arrows show arrows evolutionary translocations. In pearl millet, due to the large number of rearrangements relative to rice, the of arrows are can be from the chromosome for example, pearl millet linkage group is orthologous from to with rice linkage blocks arrows show evolutionary translocations that characterize all Panicoideae spp analyzed to date. The the rice the for The comparative of molecular markers can be for of the location of that key examples are those plant that are to In wheat, the are located on the arms of chromosomes and which to the duplicated regions on chromosome arms and carrying the and of and has that the and wheat are indeed In both were by that the of the et al., are few in which the of of has been by sequence the mapping of to orthologous regions a of as to the evolutionary of such The of for has involved the of one or more and in foxtail millet has been to two major on chromosomes and et al., Comparative analysis the on chromosome to to regions of chromosomes 1 and and linkage group which previously been to (Figure the on foxtail millet chromosome was orthologous to regions of rice chromosome pearl millet linkage group and chromosomes and all of which et al., 1995; et al., colinearity is likely to for most however, may be an in that they can a more et al., 1998). colinearity at the map level can be in and as a comparative gene highly conserved gene orders at the to level. the plant and eudicot species have similar of In maize, it has been demonstrated that genome is due to the the to 6 million of et al., 1998). In wheat and barley, of the genome consists of highly repetitive most of which is genome specific. these large of repetitive DNA may chromosome may be by a relative as a provided that the in the are present in the same order as those in the larger reference genome. which has a DNA content of and is closely related to = pg), is an to genome analysis in comparisons between and at the and sequence level are by Regions of and of the The chromosome regions are the of foxtail millet the of 1 the of and the of C which have been to the of the and indicate the at which the was observed in the of sorghum, the of a single maps are maps on the data by et and et = pg) has relatives for which genetic data and are Therefore, the use of rice as a model has been et a genetic map of a of the wheat chromosome that the gene that chromosome and in bread wheat. block analysis has that the wheat is orthologous to a of rice chromosome In a the marker order in the of wheat was with that in a rice chromosome the on rice chromosome marker orders were generally a small three markers was found to be duplicated in rice, with one in the and the from In of colinearity was observed the that of rice for gene in wheat may on the chromosome of rice DNA the location of the rice is et al., and have the barley, maize, and rice genomes for colinearity with a of the wheat genome the and This was found to be duplicated in wheat, with one located on the arms of the group 1 chromosomes and the on the arms of the group chromosomes. orthologous regions were found in rice and for the wheat group 1 A large family of related to was identified on rice chromosome 1 and on chromosome which to the on the wheat group chromosomes. of the number and organization of the in wheat, maize, and rice that the orthologous by and rearrangements and A similar comparative analysis at the level was between barley and rice in a for the barley gene et al., 1997). A map of the chromosome was constructed, and gene order was generally found to be conserved relative to a rice the as was observed in other a few markers to have to positions. a rice of not be found within the chromosome the the gene for a not be as a it is likely that is a to the conserved gene order of that in barley and rice et al., the data that the of colinearity observed between the Triticeae crops and rice may vary between chromosome regions and that even in regions in which gene orders are highly colinearity is not The gross chromosomal organization may have remained largely conserved for 60 million years, but small rearrangements and are a common of genome evolution. It again be that some of the observed rearrangements in gene order may in to This was also by a comparative analysis of the of rice with identified within a of rice were for their to to of these colinear orthologs on chromosome to a on chromosome further evidence that structural have occurred in most chromosomal regions after divergence from a common ancestor. rice several gene however, to to either sequence divergence or of these in et al., gene may not be to comparative gene It is also possible that gene is in because of the tetraploid of its genome. of gene in is well in hexaploid wheat the colinearity observed between genomes within the grass 60 million years of to which some million years from a common is a particularly because a large of the sequence is The of colinearity between and the even to small of the sequence for the identification of in the et suggested that to of those chromosomal have remained colinear over the evolutionary time the and from a however, has not this The mapping of rice identified through as to that were located on the same or closely to a of colinearity between rice and (Devos et al., Figure A similar comparative analysis of a from chromosome on the other hand, of a of the genome with to of the rice genome et al., only of the rice that to in the analyzed to a single rice the order of these in rice from that in by an The remaining were located in the rice genome because they not to common were probably not et al., of several with these for example, are not in when The from a may represent an or it may represent a of a gene family. It may even identify a gene that a similar sequence that contain a conserved for example, may be unrelated et al., To further the of colinearity between rice and we an analysis at the sequence level that included of sequence from rice chromosome 1 For four of the rice located within this the gene with the was located to a An 10 rice with in the genome. Interestingly, of these 10 also with within the with a Devos, unpublished data). The ancestral relationship between these at this but it is that they are Relationships between and A genetic map of an at the of chromosome 1 is with seven in three are rice their and map on rice chromosome arms and For in which between the rice and gene has been the are in restriction fragment length is needed in comparative data for genomes as as those of rice and Arabidopsis. The of colinearity found largely on the of the than the of colinearity, however, is the of the relationship between and rice for gene on at to only a few within Therefore, the of the genome to a gene for a of in crop on relative map to be for a in a markers that are to and a key wheat gene to is to the carrying the between wheat and rice, on the other hand, a of the high level of conserved colinearity between their genomes. The of the entire rice genome is therefore to into the staple cereals in A number of may of genome relationships. The use of such as for example, is in comparisons of genomes that are only the identification of on is on the by the In the between orthologous and sequences is when both are not available for in between and can also be in comparisons of closely related species for which genome colinearity has been established through the of conserved gene those probes that identify a gene for each of the genomes are likely to belonging to will to members of the gene but only those that restriction fragment length polymorphism in the mapping can be different members of a single family are in different species, the is that colinearity is For example, all probes that in a comparative study between the barley and A. tauschii genomes were in one or both of the species et al., in a comparison between foxtail millet and rice, of the probes that to all but one at two copies in the foxtail millet genome (Devos et al., 1998). It is possible to a in which an may a duplication event in a common one of the gene copies may be in each of two species after their divergence from the common ancestor. of copies to sequences that have positions in the two genomes. chromosome also may relationships. In diploid rice, have been identified between rice chromosome arms 11S and 12S (Nagamura et al., 1995) and of rice chromosomes 1 and et al., It is that more will be identified as the of the sequence of the genome, for example, has the presence of both and interchromosomal a of the predicted on chromosome were to have a to at one other on the same In large interchromosomal have been identified between two of chromosomes 1 and and between regions of chromosomes and 4 et al., Gene is a common event in genome it is not clear at this this through duplication of or larger chromosome gene copies are likely to be more to which may to gene It is that all will have undergone a level of chromosomal with large such as the Triticeae have been to gene by than of the wheat and barley genomes of highly repetitive which may in the as well as analysis of large are and of or for chromosome is et al., et al., 1996). the advent of comparative genomics and the realization that gene orders are highly conserved among grass the small rice genome has become a tool for gene It is however, that levels of colinearity are in highly the of gene order conservation may on the and is to be is comparative genomics the only in the of large particularly in the development of which have largely and the of have the and of of the entire wheat genome are available for several Triticeae species, et al., 1999), A. tauschii et al., 1999), and barley A barley is also available, and a hexaploid wheat has been in a chromosome et al., mapping of molecular markers a of wheat lines demonstrated the of regions in the wheat genome, that were not et al., 1996). A more of the organization of the wheat genome has been provided by analysis of large of an A. tauschii to the from the of chromosome to a identified six and a gene density the of at one gene and In other gene from one gene for the of chromosome and and one gene the on et al., to as high as one gene the on and The observed gene density in barley was with a of one gene the gene et al., and one gene the and These are seven to times than on a gene and they with the that are in of 60 of sequence the gene in barley the presence of three which of the Interestingly, only a single was for of the et al., 1998). This is different from the structural organization of the genome, in which are located between or blocks. analysis of of rice sequence that of the of repetitive of which was represented by and by In to the in maize, of the was et al., the sequence to gene in rice are found to be of the order of one gene to 10 et al., et al., 2000), which is also to times than data from plant species with large genomes are available data that in wheat and barley are within the genome. these gene can be gene be greatly The approach for gene is to identify molecular markers that are to a in large to to and the gene are to identify or the gene of approximately one gene it be to have both markers located on a of a few not within a single et al., et al., the years, has been a in our approach to large genomes. years ago, large genomes were This has the with the development of comparative The high of conservation of gene content and order between species within taxonomic groups the use of species with genomes as for crop at the of the century, are with more data become available, it is clear that the with which model can be will on our knowledge of the and the genome carrying the It is to the of conserved colinear relationships is the approach to crop plant research or we focus research on the crop plant genomes The in and our knowledge of the structural organization of crop genomes the latter as by the of the barley the other hand, the of the wheat the gene the that model species can to crop plant is comparative genomics will to play a major The of the entire rice genome and regions of other crop genomes will provide a of to both and evolutionary of grass genomes. It is however, that the in genome research be by in mapping and of the of genome data will only be possible when and and are
Source: The Plant Cell
DOI: 10.2307/3870991
Authors: Katrien M. Devos, Mike D. Gale
Institutions: John Innes Centre, Norwich Research Park
Language: English
Subfield: Genetics
Domain: Life Sciences
SDG: Zero hunger
Open Access status: green
OpenAlex ID: W2052009618