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Grass Genomic Synteny Illuminates Plant Genome Function and Evolution

Grass Genomic Synteny Illuminates Plant Genome Function and Evolution Rice (2008) 1:109–118 DOI 10.1007/s12284-008-9015-6 REVIEW Grass Genomic Synteny Illuminates Plant Genome Function and Evolution Jeffrey L. Bennetzen & Mingsheng Chen Received: 1 October 2008 /Accepted: 21 October 2008 /Published online: 12 November 2008 Springer Science + Business Media, LLC 2008 Abstract The genic colinearity of grass genetic maps, Introduction physical maps, and contiguous genomic sequences has been a major contributor to almost two decades of study into the Two of the central questions in biology are what are the structure and evolution of grass genomes. This research has genetic foundations that underlie the similarities between led to the discovery of all of the major phenomena different species or individuals within a species and what are responsible for the rapid evolution of flowering plant the genetic variations responsible for the observed differ- genomes. These processes include polyploidy, transposable ences. Even from the first days of comparative genomics, it element (TE) amplification, TE-driven genome rearrange- was surprising to many that humans, fruit flies, nematodes, ment, and DNA removal by unequal homologous recom- and yeast shared a large percentage of their genes [2, 85]. bination and illegitimate recombination. The great variety Given our human-centered worldview, it was to be expected in angiosperm genome structure is largely an outcome of that many would be shocked by the fact that humans and our differences in the specificities, frequencies, and amplitudes closest surviving relative, the chimpanzee, share ~98% of these common genome-altering processes. Future em- sequence identity and an even higher similarity in gene phasis now needs to shift to harnessing an even broader content [81]. In plants, haplotypic differences in genome range of studied species, and to use this phylogenomic sequence within a species like maize can greatly outstrip perspective to uncover the nature and functions of the genes these interspecies primate variations. Of course, not all that are shared by particular lineages and those that set each sequence change is equally significant, and work on the individual species apart as a unique biological entity. evolution of maize has shown that tiny changes in regulatory loci can dramatically alter morphology and behavior [24]. . . Keywords Comparative genomics Genome evolution The field of comparative genomics was founded on the . . Microcolinearity Recombination Transposable elements idea that comprehensive analyses and comparison of whole genomes could uncover the essential conserved, and the importantly variable, components of any set of genomes. In plants, this comparative analysis proved to be particularly challenging for several reasons, including (1) the small number of species that were investigated, (2) their large and complex genomes, and (3) their high rate of structural rearrangement. The observation that closely related plants J. L. Bennetzen (*) sometimes exhibited regions of DNA-marker colinearity Department of Genetics, University of Georgia, [11, 38] provided a key point of constancy in these Athens, GA 30602-7223, USA e-mail: maize@uga.edu comparisons because genetic map relatedness was simple to determine with robust techniques that were not dramatically M. Chen affected by genome size or the overall quality of the genetic State Key Laboratory of Plant Genomics, Institute of Genetics and toolkit for that species [8]. The first demonstrations of Developmental Biology, Chinese Academy of Sciences, microcolinearity (also called microsynteny) by comparative Beijing 100101, China 110 Rice (2008) 1:109–118 sequencing of orthologous chromosomal regions [17, 84] Gale and Tanksley groups [3, 4, 20]. These studies indicated that overall genomic similarity could be converted indicated a good deal of similarity in gene content and into very local analyses of the evolved structure and function colinearity, with a low frequency of small and large of genes that were all derived from a known ancestral locus exceptions. Moore et al. [67] provided a major conceptual at attributable dates. Hence, both whole genome and leap when they identified a series of conserved grass individual gene analyses could be made in a comprehensive genome segments and then assembled them into a comparative manner across many species, as first proposed and illustrated circle map. in the grasses. The comparative circular map of the grasses, also known Another enduring question that was illuminated by a as the crop circle, has allowed identification of the major comparative genome analysis strategy was the nature of the rearrangements that differentiate grass genomes, and has DNA in the eukaryotic nucleus. For many decades, it has provided insight into the timing of these events during grass been known that nuclear genomes vary dramatically in size, descent from a common ancestor more than 50 mya. As even between closely related species, and the mystery shown in Fig. 1, gene order and telomere location are behind this “unexplained” or presumed “excess” DNA was largely conserved at this scale, although the number of termed the “C-value paradox” by Thomas [82]. Research in chromosomes is quite variable across species. Maize yields flowering plants, where the differences in nuclear DNA two concentric circles, suggestive of a whole genome content varies more than one thousand fold, has explained polyploidy event, which has been confirmed by extensive this C-value variation [10]. We now know that the differ- orthologous DNA sequence analysis [80]. Two specific ences in C-value across flowering plants are very dynamic translocations, shown at 3 o’clock and 7 o’clock on the outcomes of occasional polyploidy along with great circle map, are shared by all investigated members of the variability in transposable element (TE) amplification and Panicoid subfamily but not by rice or the Triticeae. Most of processes for DNA removal. However, we do not know the other detected rearrangements are inversions that are how often these changes (especially those caused by TEs or limited to only one or two of the species depicted (Fig. 1). other small indels) generate selectable variation that can In addition, this circular map allowed the easily lead to changed capabilities within a species or to visualized (and thus conceptualized and transmitted) dis- speciation. covery that some important genes involved in domestica- This plant genome review will discuss the discovery of tion or other important traits appeared to be the same genomic colinearity and synteny, its biological origins, its orthologous loci across multiple grass species (Fig. 1)[72]. numerous exceptions, and its uses for genome analysis. We This, in turn, helped encourage the use of surrogate plant will focus on the grasses because this is our area of greatest chromosomes like the relatively small genome of rice to expertise and because this is also the source of the most assist in the map-based cloning of genes in large-genome comprehensive sets of data and analyses in plants. We have species like barley, wheat, or sugarcane [14, 33, 19]. every reason to believe that much of what is discussed Three major conclusions that were clear from the herein for the grasses will also be true in other plants, and comparative circular maps were (1) the relatively low in more distantly related eukaryotes. frequency of large genomic rearrangements, (2) the pres- ence of inversions, translocations and duplications, and (3) the uneven distribution of such events, with many at Genetic map colinearity in the grasses: rules boundaries near current centromere locations (Fig. 1). and exceptions Among the many issues not resolved by this analysis, however, was whether the frequencies of these major The crop circle rearrangements were in any way predictive or mechanisti- cally similar to the frequencies and types of local rearrange- The first comparative genetic map in the grasses was a ments. More detailed physical and genetic maps would be miniscule maize::sorghum comparison in a study meant to needed to address these questions. test whether restriction fragment length polymorphism (RFLP) markers generated in one species (e.g., maize) Physical maps, genetic maps and their comparison could be used to help generate a genetic map in other species (e.g., sorghum) [38]. This project indicated that Early studies by comparative genetic mapping revealed the maize RFLP probes could be used routinely for species as extent of conservation of gene content and gross gene order far distant as foxtail millet, a lineage that last shared a among different grass species, but did not give many common ancestor with the maize lineage about 30 million insights into the likelihood or nature of small rearrange- years ago (mya) [48]. Serious grass genome comparisons ments. In these first studies [38], it was observed that most were then generated by expert mapping labs, especially the maize RFLP probes hybridized strongly to sorghum DNA, Rice (2008) 1:109–118 111 111 Fig. 1 Synteny of five crop genomes. Different color bars represent the chromosomes in different grass genomes, with their telomeres indicated by red triangles. Arrows show rear- rangements relative to rice. Arrows with a single arrowhead are translocations, and those with two arrowheads are inver- sions. Arrows at 3 o'clock and 7 o'clock indicate rearrangements that are shared by the subfamily Panicoideae (foxtail millet, sor- ghum, and maize). Dotted bars indicate regions where insuffi- cient data were available at the time of the analysis undertaken by Gale and Devos [30]. The dotted internal line indicates a duplication shared by chromo- somes 11 and 12 of rice [69]. Red dots are orthologous genes controlling semi-dwarf pheno- types that are located on rice chromosome 3, wheat chromo- some 4 and maize chromosome 1[22, 73]. pt Part of a chromosome. but the repetitive DNA sequences in maize usually did not recombination-poor heterochromatin, such as pericentromeric hybridize to sorghum. This suggested that repetitive DNA regions [12]. This phenomenon was also apparent in sequences evolved much faster than genes, and that comparison of homoeologous chromosomal regions in rice heterologous probes could thus provide some advantages derived from the ancient duplication at the origin of the over homologous probes from a repeat-rich genome. grasses, where little colinearity was retained in pericentro- Comparative genetic mapping between closely related meric regions [83]. In addition, the heterochromatic regions grasses, such as sorghum and sugarcane, whose separate of sorghum have been preferentially expanded relative to lineages diverged from each other about 8 mya, show rice, as compared to euchromatic regions [51]. Future striking map colinearity [35]. In contrast, detailed compar- detailed studies of microcolinearity in heterochromatin are ative genetic mapping among more distantly related species, needed to uncover the dynamics and mechanisms for macro- such as maize and rice, identified numerous chromosomal and micro-rearrangements in these crossover-deficient parts rearrangements, such as telomeric fusions, nested insertions, of grass genomes [61, 63]. inversions and translocations [92], although about 2/3 of these genomes appeared to still be colinear. Many of the detected rearrangements were confirmed by comparative Microcolinearity physical mapping, such as (from a rice perspective) the fusion of rice chromosomes 3 and 10 and chromosomes 7 Across the grasses (and a bit beyond) and 9 into single chromosomes in the Panicoideae lineage [88]. In addition, comparative physical mapping also Even from the start, comparisons of genomic sequence in uncovered the ancient grass genome duplication shared by orthologous regions of different grass species examined a maize [88], wheat [77], and other grasses [71]. very large time frame, such as rice versus sorghum [17]or Comparative physical mapping between sorghum and rice versus various Triticeae [28, 37, 26], all comparisons rice revealed different genome components with very different where the investigated species last shared a common degrees of microcolinearity. In euchromatic regions, where ancestor ~50 mya. In this time frame, the sequences most meiotic recombination occurs, greater microcolinearity between genes appeared to be completely different, was observed; however, less microcolinearity was observed in although very tiny “conserved non-coding sequences” 112 Rice (2008) 1:109–118 (CNS) were later discovered [45, 36]. Even introns of to the eudicots, >220 million years of independent descent, orthologous genes, although largely consistent in location only rare segments of genic colinearity are observed at either across all flowering plants, contained obvious conserved full genome or local genome scales [58]. sequences only at the boundaries needed to specify The most frequent type of structural change in all appropriate RNA processing. Hence, the general conclusion investigated angiosperm nuclear genomes has been ob- could be reached that anything still conserved after 50 served to be the differential insertion and subsequent million years of grass genome divergence was likely to instability of transposable elements (TEs). In large-genome have an important function. species like maize and barley, most of the DNA between Gene content and order, on the other hand, were mostly genes is comprised of TEs, especially long terminal repeat conserved on segments of a few dozen to a few hundred kb (LTR) retrotransposons [78, 86, 89, 75]. These elements even after 50 million years of independent grass genome transpose by reverse transcription of an RNA transcript and evolution. Comparisons to rice have been particularly insertion of the resultant DNA, so transposition does not useful in this regard because (1) it is evolutionarily quite involve excision. Because LTR retrotransposons make up distant from the other important grasses like maize, wheat, more than 50% of most or all large flowering plant barley, and sorghum [48], (2) it has a relatively small genomes and their high content varies somewhat propor- genome (~400 Mb) with a high gene density, (3) it’s tionally with angiosperm genome size, it is clear that these genome was an early target for comprehensive sequence TEs are the most important factor responsible for genome analysis [41], and (4) it has proven to be more stable vis- size variation in flowering plants [10]. Because these TEs à-vis small local rearrangements than other grasses like (and all other unselected DNAs) are fragmented and maize, sorghum, wheat or barley [9]. removed so rapidly by accumulated small deletions (see In the most comprehensive comparisons to date, between below), all of the insertions appear to be very recent, rice and two panicoid grasses, sorghum and maize, the usually within the last 2–6 million years [87]. This accounts frequency of gene movement over the last fifty million for the near-complete lack of homology of the intergenic years was calculated as at least 5%, and possibly as high as regions in orthologous genome segments with grass 25%, between sorghum and rice [53]. This number does not lineages that last shared a common ancestor more than include the gain or loss of tandemly repeated gene copies, a 50 mya. very common phenomenon in all grass lineages investigat- We currently lack a vocabulary to precisely describe the ed. Most of the genic rearrangements in maize compared to degree of conservation of genic content and colinearity either rice or sorghum are apparent gene losses on one of between any two species, much less across multiple two maize homoeologues [40, 53], an expected outcome of species, although a gene-pair conservation terminology is the polyploidization event about five mya that gave rise to currently in development (L. Feng and J. Bennetzen, the Zea lineage [80]. However, too little data yet exist to unpub. res.). However, it is clear that some lineages are identify possible subtle patterns in types of rearrangement. very unstable (e.g., pearl millet, sorghum, maize) and others Moreover, rearrangements involving genes are likely to be are much more stable (e.g., rice and foxtail millet) at the under selective pressure, so the events currently observed in level of compared genetic maps and/or microcolinearity any species are a combined outcome of those events that [23, 75, 9, 40]. We do not yet know the reasons for these have occurred, minus those that were subsequently differences, nor whether high conservation at one scale removed by chance or by selection against some specific (e.g., genetic map) in any way correlates with high changes. conservation at other scales (e.g., physical map or micro- In more distant comparisons, with longer ancestral colinearity). It is clear, though, that certain types of gene divergence times, colinearity across orthologous regions rearrangement are rare (e.g., movement of a gene to a appears to be much more rare than within the grasses. In the wholly different chromosome) while others are relatively rice flatsedge, Cyperus iria, the near-adjacent Sh2 and A1 common (tandem duplication, deletion or inversion of small homologues appear to be conserved in order and orienta- genic segments). tion, but one of the two genes in between in the grasses is Analysis of microcolinearity and gene content conserva- missing in the sedge (A. Pontaroli and J. Bennetzen, unpub. tion at long time frames has the advantage of the obs.). However, this is the only comparison that has been accumulation of multiple events for analysis, but this is done to the grasses in this ~110-million-years-of-divergence more than counterbalanced by three negative aspects of window [13]. Similarly, Musa (e.g., banana) genomes show concentrating on such ancient rearrangements. First, natural some colinearity with the grasses after >115 million years of selection has had a great deal of time to remove any events divergence from their last shared ancestor, but more than that had even a minor organismal disadvantage, so one only 50% of the annotated genes were non-colinear in a observes certain classes of tolerated or advantageous events comparison to rice [56]. With even more distant comparison that might not be proportional to the true spectrum of de Rice (2008) 1:109–118 11 113 3 novo rearrangements. Second, the components of the [40, 53, 64], wheat [27, 46, 90, 34, 16, 15] and sugarcane genome responsible for the rearrangement have had ample [42], have revealed interesting features of gene and genome time to decay into a state where they are invisible to current evolution in recent polyploids. LTR retrotransposon ampli- annotation approaches. And, third, individual events may be fication and altered regulation (e.g., silencing) or loss of buried underneath second, third or more layers of events at duplicated genes are repeated themes. Inactivation and the same location. For all of these reasons, investigations of eventual elimination of duplicated genes can be mediated orthologous regions in closely related lineages are justified, by altered epigenetic regulation, deletions, TE insertions, and are expected to be “there to discover” because of the and/or point mutations causing premature stop codons. relatively high rate of local chromosomal rearrangement in Some evidence suggests that specific alterations recur in the grasses. independent polyploidizations in wheat [27, 46]and Brassica napus [59]. However, most eventually fixed changes do not Colinearity dynamics within a 0–15 million year window occur instantly in post-polyploid genome rearrangements, at of grass genome evolution least not in maize. In adh1-homoeologous regions, for instance, fragments of partially deleted genes remain, Orthologous sequence comparisons across short time indicating the incomplete status of removal several million frames has the potential to reveal both the rate and the years after polyploidy, and showing that these gene losses mechanisms for disruption of colinearity. In a sequence are primarily by the accumulation of multiple small deletions comparison of the adh1-orthologous regions of maize and [40]. Another example of reasonably stable polyploid gene sorghum, two species that last shared a common ancestor copies comes from a comparative study of the adh1- about 12 mya [80], a 212-kb maize sequence was found to orthologous regions of maize, sorghum and sugarcane [42]. be largely collinear with a 66-kb sorghum sequence [84]. The two sugarcane homoeologous haplotypes show perfect The more than three-fold size difference is mainly due to genic colinearity. In addition, two maize homoeologous nested LTR retrotransposon insertions in the maize genome regions yielded the same gene content, order and orientation [78, 84]. In the original annotation, orthologs of nine maize as in sugarcane. Our data on comparative analysis in the genes were detected in the sorghum region in perfect Oryza genus also reveals excellent stability of polyploid colinear order; however, three additional genes in this genomes formed less than two million years ago (Chen et al., sorghum segment were not found in the maize adh1 region. unpub. res.). In subsequent analyses, one of the “missing” maize genes The Oryza genus contains about 24 species that belongs was found to be located in the adh1-homoeologous region to ten different genome types [31]. A project, entitled the of maize [40]. This has now turned out to be a routine Oryza MAP Alignment Project (OMAP), was launched to situation in the maize genome, where two maize segments build a framework for comparative biology in the Oryza represent each sorghum region due to a polyploidy event in genus [93]. Representative species, ranging from closely the Zea lineage within the last few million years [80]. Gene related species/subspecies, such as those with AA deletion (usually of only one homoeologous copy) subse- genomes, which diverged from their common ancestor quent to polyploidization has now reduced the originally less than a million years ago, to more distantly related doubled copy number of genes (2×) to less than 1.5× [53]. species, such as O. brachyantha and O. granulata,whose The other two non-colinear genes in the adh1-orthologous ancestors diverged about 10 mya, were chosen for regions of sorghum are found elsewhere in the genomes of bacterial artificial chromosome (BAC) library construc- maize and other grasses and are hypothesized to have been tion, BAC end sequencing, and physical map construction caused by the insertion of two unlinked genes, either as two [5, 49]. The initial analyses revealed excellent gene subsequent events or by a single event involving three colinearity both in their physical maps [50]and in chromatids. In dramatic contrast, a comparison of the adh1- sequence comparisons [96]. Genome size variations in orthologous regions between sorghum and sugarcane, both the Oryza genus were found to be mainly caused by gene colinearity and strong homology of non-coding lineage-specific amplifications of LTR retrotransposons regions were observed [42], indicating greater stability in [74, 6]. Our systematic comparative analysis of the these lineages over this shorter (~8 million year) time frame sequence of the MONOCLUM1-ortholgous regions across of divergence. the Oryza genus not only revealed high gene colinearity In at least some genomes, polyploidization is followed but also identified new genes that appear to have by extensive genomic change resulting in the silencing and originated de novo in the AA genomes (Fig. 2 and Chen elimination of duplicated genes [1]. In grasses, polyploidy et al., unpub. res.), which highlights the advantage of has been a recurrent theme, with many lineages exhibiting multiple species comparisons. full genome duplications over the last few million years. Intraspecific local sequence comparisons have also Local sequence comparisons in these species, such as maize identified interesting features of grass genome structure 114 Rice (2008) 1:109–118 Fig. 2 Microcolinearity in the MONOCULM1-orthologous regions across the Oryza genus. Black boxes represent genes. Red boxes indicate retrotranspo- sons. Fuchsia boxes symbolize DNA transposons. Orthologous genes are connected by lines. and evolution. A detailed sequence comparison of the discovery of more cases of TE components being co-opted bronze region of maize inbred lines McC and B73 found for organismal functions in plants, as in the recent that LTR retrotransposon clusters differed one hundred identification of transcription factors in Arabidopsis derived from the Mutator transposase [57]. percent in location relative to the genes in the bronze region between these two lines [29]. This suggests an amazingly Even if TE-vectored gene fragments are rarely if ever rapid process both for TE insertion and for removal of true genes with a selected host function, they certainly are a ancestral TEs. In addition, the first annotation of these two complication to genome annotation. Even without internal regions suggested that the genes themselves differed gene fragments, low-copy-number TEs are often mis- between these lines in this region. An apparent four-gene annotated as genes, giving rise to as much as two-fold over cluster was detected in McC but not in the orthologous estimations of gene numbers [7]. This type of over- position in B73 [29]. Later, these sequences were found to estimation in gene number can play particular havoc with be comprised of four gene fragments within Helitrons,a assessment of genic colinearity, as evidenced by studies in new type of eukaryotic transposon [44, 54, 52, 68]. This rice showing hundreds of gene differences between differ- phenomenon resembles Pack-MULEs, a type of TE first ent races of O. sativa that were later shown to all be named and comprehensively described in rice, that also explained by mis-annotated TEs [9]. Hence, many early capture and mobilize gene fragments [43]. Although neither publications showing numerous genic exceptions to micro- Helitrons nor Pack-MULEs usually mobilize intact genes, colinearity are incorrect because of this routine annotation they do commonly acquire more than one gene fragment in error. the same element. When transcribed, these internal frag- Sequence comparisons in closely related haplotypes in ments are often fused (via intron processing) into transcripts Arabidopsis, in rice and in wheat have demonstrated that that could encode novel protein products [43, 68]. This unequal homologous recombination and illegitimate recom- process of exon shuffling, first proposed by Gilbert [32]as bination are the major forces that remove DNA from the reason for the existence of introns, could be creating flowering plant genomes [16, 21, 60, 90, 91]. These new genes in plants at an amazing rate. The maize nuclear activities can remove >100 Mb of DNA from a plant genome, for instance, has more than 4,000 Helitrons that genome in just one million years [62], but the rate of contain inserted gene fragments [68] (L. Yang and J. removal appears to be much faster in some angiosperms Bennetzen, unpub. res.). However, there is not yet a proven than in others [87]. Most of the removed DNA is derived case of any of these Helitron- or Pack-MULE-generated from TEs, but other intergenic DNA and extra gene copies “new” genes having actually acquired a genetic function are also removed by these processes [60]. essential to its host. Given the rapid rate of unselected DNA Several recent studies have accentuated the fact that not loss from plant genomes (see below), it is unlikely that all genomic regions evolve at the same rate. Disease conversion of these chimeric gene candidates into true resistance gene clusters are known to be unstable even in genes will occur commonly, but even rates as low as one in map position [55], and to also undergo high rates of a million would be significant. Other than the standard unequal recombination [76], including some recombination route of gene duplication, which primarily creates sub- events that are delimited to specific sites that can optimize functionalized or (rarely) mildly modified new gene novel pathogen recognition specificities [70]. Ribosomal functions (reviewed in [39]), there is no known aggressive RNA gene clusters also appear to vary in map position even process for the generation of new genes. Perhaps Pack- in close relatives [25]. Perhaps most surprising, the MULEs and Helitrons will eventually be proven to provide composition and arrangement of sequences in centromeres this process. At the very least, we expect to see the have been found to be hyper-variable, primarily by the Rice (2008) 1:109–118 11 115 5 process of unequal homologous recombination [61, 63, 65]. provide an unprecedented opportunity to study grass This rapid rearrangement by recombination in a region that genome function and evolution. Because maize is derived is deficient in crossovers suggests a very tight control over from a fairly recent tetraploid [80], identifying the homoe- the outcomes of recombination, especially a powerful bias ologous segments and subsequent comparisons of these toward non-crossover, intrastrand and/or sister chromatid segments will illustrate how genome duplication has shaped outcomes [61]. This core centromeric instability has been the maize genome, and reveal the evolutionary fate of this argued to yield centromeres that have the potential to out- type of duplicated gene [47, 94]. Because all grass genomes compete other centromeres for choice as the germinal are derived from a shared paleopolyploid [71, 83, 95], nucleus in egg development [66]. identication and comparison of two sets of homoeologous In summary, local sequence comparisons of closely chromosomal segments in rice and four sets of homoeolo- related grass genomes and of intraspecific haplotypes have gous chromosomal segments in maize will reveal common begun to reveal the major mechanisms driving genome and lineage-specific patterns of conservation [77], suggest evolution. These include gene and genome duplication, mechanisms for gene movement [40, 53], and possibly gene silencing and eventual deletion of duplicated genes identify signatures of cases where these movements led to subsequent to polyploidization, transposable element am- significant biological outcomes. plification, gene movement mediated by transposition of The exciting next few years of grass genome compara- mobile elements, unequal homologous recombination, and tive genomics, with great emphasis on the Oryzae and on illegitimate recombination. All of these processes are quite maize and its relatives (e.g., sorghum and sugarcane), will variable even when comparing closely related species, so provide a framework for the next generation of plant genome their differences in levels of activity (and, possibly, analyses. At the technical level, comparative genome specificity) are responsible for the very different genomes analysis on a few model species like rice, maize, sorghum, found in flowering plants. and Brachypodium has opened up avenues to the highly leveraged study of any other grass. No single species is more enriched for “interesting” genes than any other species, but The past, present, and future of plant genome the traditional tractability of studying these interesting genes comparisons was centered on the model species with excellent molecular, physiological, biochemical, cell biological and genetic Perhaps the most valuable insight gained from comparative toolkits. Because of comparative genomics, this historical genomic analyses in rice and related grasses has been the limitation no longer holds true. astounding instability of genome structure against a fairly With highly conserved gene content across the grasses, conserved set of biological functions. As mentioned above, small-genome surrogates (or, even better, those surrogates at a local genome level, two maize plants are often more with sequenced genomes) can be used to provide facile different from each other than a human is from a access to any shared grass gene. Moreover, the discovery of chimpanzee, or even from a macaque. The grasses and novel genes or modified gene functions that make each other angiosperms obviously insulate their gene functions species unique can now be performed by simple EST from the great majority of this genome change, in manners analysis or trait mapping. Once these candidate genes for that we do not now understand at even the most minimal family- or genus- or species-specific gene functions are level. identified, they can now be easily isolated and tested for the As shown in Drosophila, pursuit of full genome analyses ability to condition novel biological function by introduction in several species within a dense phylogenetic framework into easily-transformed model species. can be exceptionally productive [18, 79]. In plants, the Oryza Despite, perhaps because of, the many important genus provides such a unique opportunity to investigate discoveries that have been made over the last 15–20 years various aspects of gene and genome evolution with the of plant comparative genomics, we have more questions to availability of a robust phylogenetic framework [31, 97], rich answer now than we did at the outset. Because of the genomic resources [5, 49], and a near-perfect reference continued extraordinary increases in throughput and genome [41]. The ongoing sequence comparisons in the decreases in cost of nucleic acid sequence analyses, many Oryza genus will provide dramatic and lineage-oriented more plant species will be investigated with a much broader insights into the creation of new genes, the evolution of gene (and better-conceived) set of phylogenetic justifications. structure and function, conserved non-coding sequences, the Genetic maps, physical maps and EST analyses are all evolutionary dynamics of duplicated gene in polyploid needed for hundreds or thousands of plant species to identify species, centromere drive and a wealth of other issues. shared and novel traits. Every one of these genes can be As maize genome sequencing nears completion of its tested for function in a few model species (by forward first draft, whole genome comparison of maize and rice will genetic, reverse genetic and transgenic technologies), so the 116 Rice (2008) 1:109–118 16. Chantret N, Salse J, Sabot F, Rahman S, Bellec A, et al. Molecular orthologues, paralogues and “new” genes can also be basis of evolutionary events that shaped the hardness locus in compared and “uncovered” in a conductive genetic back- diploid and polyploid wheat species (Triticum and Aegilops). ground or backgrounds. With such torrents of data on the Plant Cell 2005;17:1033–45. horizon, better tools for sorting the gold from the grit will be 17. Chen M, SanMiguel P, Bennetzen JL. Sequence organization and conservation in sh2/a1-homologous regions of sorghum and rice. needed. 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Grass Genomic Synteny Illuminates Plant Genome Function and Evolution

Rice , Volume 1 (2) – Dec 1, 2008

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Springer Journals
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Copyright © Springer Science + Business Media, LLC 2008
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Life Sciences; Plant Sciences; Plant Genetics & Genomics; Plant Breeding/Biotechnology; Agriculture; Plant Ecology
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1939-8425
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10.1007/s12284-008-9015-6
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Abstract

Rice (2008) 1:109–118 DOI 10.1007/s12284-008-9015-6 REVIEW Grass Genomic Synteny Illuminates Plant Genome Function and Evolution Jeffrey L. Bennetzen & Mingsheng Chen Received: 1 October 2008 /Accepted: 21 October 2008 /Published online: 12 November 2008 Springer Science + Business Media, LLC 2008 Abstract The genic colinearity of grass genetic maps, Introduction physical maps, and contiguous genomic sequences has been a major contributor to almost two decades of study into the Two of the central questions in biology are what are the structure and evolution of grass genomes. This research has genetic foundations that underlie the similarities between led to the discovery of all of the major phenomena different species or individuals within a species and what are responsible for the rapid evolution of flowering plant the genetic variations responsible for the observed differ- genomes. These processes include polyploidy, transposable ences. Even from the first days of comparative genomics, it element (TE) amplification, TE-driven genome rearrange- was surprising to many that humans, fruit flies, nematodes, ment, and DNA removal by unequal homologous recom- and yeast shared a large percentage of their genes [2, 85]. bination and illegitimate recombination. The great variety Given our human-centered worldview, it was to be expected in angiosperm genome structure is largely an outcome of that many would be shocked by the fact that humans and our differences in the specificities, frequencies, and amplitudes closest surviving relative, the chimpanzee, share ~98% of these common genome-altering processes. Future em- sequence identity and an even higher similarity in gene phasis now needs to shift to harnessing an even broader content [81]. In plants, haplotypic differences in genome range of studied species, and to use this phylogenomic sequence within a species like maize can greatly outstrip perspective to uncover the nature and functions of the genes these interspecies primate variations. Of course, not all that are shared by particular lineages and those that set each sequence change is equally significant, and work on the individual species apart as a unique biological entity. evolution of maize has shown that tiny changes in regulatory loci can dramatically alter morphology and behavior [24]. . . Keywords Comparative genomics Genome evolution The field of comparative genomics was founded on the . . Microcolinearity Recombination Transposable elements idea that comprehensive analyses and comparison of whole genomes could uncover the essential conserved, and the importantly variable, components of any set of genomes. In plants, this comparative analysis proved to be particularly challenging for several reasons, including (1) the small number of species that were investigated, (2) their large and complex genomes, and (3) their high rate of structural rearrangement. The observation that closely related plants J. L. Bennetzen (*) sometimes exhibited regions of DNA-marker colinearity Department of Genetics, University of Georgia, [11, 38] provided a key point of constancy in these Athens, GA 30602-7223, USA e-mail: maize@uga.edu comparisons because genetic map relatedness was simple to determine with robust techniques that were not dramatically M. Chen affected by genome size or the overall quality of the genetic State Key Laboratory of Plant Genomics, Institute of Genetics and toolkit for that species [8]. The first demonstrations of Developmental Biology, Chinese Academy of Sciences, microcolinearity (also called microsynteny) by comparative Beijing 100101, China 110 Rice (2008) 1:109–118 sequencing of orthologous chromosomal regions [17, 84] Gale and Tanksley groups [3, 4, 20]. These studies indicated that overall genomic similarity could be converted indicated a good deal of similarity in gene content and into very local analyses of the evolved structure and function colinearity, with a low frequency of small and large of genes that were all derived from a known ancestral locus exceptions. Moore et al. [67] provided a major conceptual at attributable dates. Hence, both whole genome and leap when they identified a series of conserved grass individual gene analyses could be made in a comprehensive genome segments and then assembled them into a comparative manner across many species, as first proposed and illustrated circle map. in the grasses. The comparative circular map of the grasses, also known Another enduring question that was illuminated by a as the crop circle, has allowed identification of the major comparative genome analysis strategy was the nature of the rearrangements that differentiate grass genomes, and has DNA in the eukaryotic nucleus. For many decades, it has provided insight into the timing of these events during grass been known that nuclear genomes vary dramatically in size, descent from a common ancestor more than 50 mya. As even between closely related species, and the mystery shown in Fig. 1, gene order and telomere location are behind this “unexplained” or presumed “excess” DNA was largely conserved at this scale, although the number of termed the “C-value paradox” by Thomas [82]. Research in chromosomes is quite variable across species. Maize yields flowering plants, where the differences in nuclear DNA two concentric circles, suggestive of a whole genome content varies more than one thousand fold, has explained polyploidy event, which has been confirmed by extensive this C-value variation [10]. We now know that the differ- orthologous DNA sequence analysis [80]. Two specific ences in C-value across flowering plants are very dynamic translocations, shown at 3 o’clock and 7 o’clock on the outcomes of occasional polyploidy along with great circle map, are shared by all investigated members of the variability in transposable element (TE) amplification and Panicoid subfamily but not by rice or the Triticeae. Most of processes for DNA removal. However, we do not know the other detected rearrangements are inversions that are how often these changes (especially those caused by TEs or limited to only one or two of the species depicted (Fig. 1). other small indels) generate selectable variation that can In addition, this circular map allowed the easily lead to changed capabilities within a species or to visualized (and thus conceptualized and transmitted) dis- speciation. covery that some important genes involved in domestica- This plant genome review will discuss the discovery of tion or other important traits appeared to be the same genomic colinearity and synteny, its biological origins, its orthologous loci across multiple grass species (Fig. 1)[72]. numerous exceptions, and its uses for genome analysis. We This, in turn, helped encourage the use of surrogate plant will focus on the grasses because this is our area of greatest chromosomes like the relatively small genome of rice to expertise and because this is also the source of the most assist in the map-based cloning of genes in large-genome comprehensive sets of data and analyses in plants. We have species like barley, wheat, or sugarcane [14, 33, 19]. every reason to believe that much of what is discussed Three major conclusions that were clear from the herein for the grasses will also be true in other plants, and comparative circular maps were (1) the relatively low in more distantly related eukaryotes. frequency of large genomic rearrangements, (2) the pres- ence of inversions, translocations and duplications, and (3) the uneven distribution of such events, with many at Genetic map colinearity in the grasses: rules boundaries near current centromere locations (Fig. 1). and exceptions Among the many issues not resolved by this analysis, however, was whether the frequencies of these major The crop circle rearrangements were in any way predictive or mechanisti- cally similar to the frequencies and types of local rearrange- The first comparative genetic map in the grasses was a ments. More detailed physical and genetic maps would be miniscule maize::sorghum comparison in a study meant to needed to address these questions. test whether restriction fragment length polymorphism (RFLP) markers generated in one species (e.g., maize) Physical maps, genetic maps and their comparison could be used to help generate a genetic map in other species (e.g., sorghum) [38]. This project indicated that Early studies by comparative genetic mapping revealed the maize RFLP probes could be used routinely for species as extent of conservation of gene content and gross gene order far distant as foxtail millet, a lineage that last shared a among different grass species, but did not give many common ancestor with the maize lineage about 30 million insights into the likelihood or nature of small rearrange- years ago (mya) [48]. Serious grass genome comparisons ments. In these first studies [38], it was observed that most were then generated by expert mapping labs, especially the maize RFLP probes hybridized strongly to sorghum DNA, Rice (2008) 1:109–118 111 111 Fig. 1 Synteny of five crop genomes. Different color bars represent the chromosomes in different grass genomes, with their telomeres indicated by red triangles. Arrows show rear- rangements relative to rice. Arrows with a single arrowhead are translocations, and those with two arrowheads are inver- sions. Arrows at 3 o'clock and 7 o'clock indicate rearrangements that are shared by the subfamily Panicoideae (foxtail millet, sor- ghum, and maize). Dotted bars indicate regions where insuffi- cient data were available at the time of the analysis undertaken by Gale and Devos [30]. The dotted internal line indicates a duplication shared by chromo- somes 11 and 12 of rice [69]. Red dots are orthologous genes controlling semi-dwarf pheno- types that are located on rice chromosome 3, wheat chromo- some 4 and maize chromosome 1[22, 73]. pt Part of a chromosome. but the repetitive DNA sequences in maize usually did not recombination-poor heterochromatin, such as pericentromeric hybridize to sorghum. This suggested that repetitive DNA regions [12]. This phenomenon was also apparent in sequences evolved much faster than genes, and that comparison of homoeologous chromosomal regions in rice heterologous probes could thus provide some advantages derived from the ancient duplication at the origin of the over homologous probes from a repeat-rich genome. grasses, where little colinearity was retained in pericentro- Comparative genetic mapping between closely related meric regions [83]. In addition, the heterochromatic regions grasses, such as sorghum and sugarcane, whose separate of sorghum have been preferentially expanded relative to lineages diverged from each other about 8 mya, show rice, as compared to euchromatic regions [51]. Future striking map colinearity [35]. In contrast, detailed compar- detailed studies of microcolinearity in heterochromatin are ative genetic mapping among more distantly related species, needed to uncover the dynamics and mechanisms for macro- such as maize and rice, identified numerous chromosomal and micro-rearrangements in these crossover-deficient parts rearrangements, such as telomeric fusions, nested insertions, of grass genomes [61, 63]. inversions and translocations [92], although about 2/3 of these genomes appeared to still be colinear. Many of the detected rearrangements were confirmed by comparative Microcolinearity physical mapping, such as (from a rice perspective) the fusion of rice chromosomes 3 and 10 and chromosomes 7 Across the grasses (and a bit beyond) and 9 into single chromosomes in the Panicoideae lineage [88]. In addition, comparative physical mapping also Even from the start, comparisons of genomic sequence in uncovered the ancient grass genome duplication shared by orthologous regions of different grass species examined a maize [88], wheat [77], and other grasses [71]. very large time frame, such as rice versus sorghum [17]or Comparative physical mapping between sorghum and rice versus various Triticeae [28, 37, 26], all comparisons rice revealed different genome components with very different where the investigated species last shared a common degrees of microcolinearity. In euchromatic regions, where ancestor ~50 mya. In this time frame, the sequences most meiotic recombination occurs, greater microcolinearity between genes appeared to be completely different, was observed; however, less microcolinearity was observed in although very tiny “conserved non-coding sequences” 112 Rice (2008) 1:109–118 (CNS) were later discovered [45, 36]. Even introns of to the eudicots, >220 million years of independent descent, orthologous genes, although largely consistent in location only rare segments of genic colinearity are observed at either across all flowering plants, contained obvious conserved full genome or local genome scales [58]. sequences only at the boundaries needed to specify The most frequent type of structural change in all appropriate RNA processing. Hence, the general conclusion investigated angiosperm nuclear genomes has been ob- could be reached that anything still conserved after 50 served to be the differential insertion and subsequent million years of grass genome divergence was likely to instability of transposable elements (TEs). In large-genome have an important function. species like maize and barley, most of the DNA between Gene content and order, on the other hand, were mostly genes is comprised of TEs, especially long terminal repeat conserved on segments of a few dozen to a few hundred kb (LTR) retrotransposons [78, 86, 89, 75]. These elements even after 50 million years of independent grass genome transpose by reverse transcription of an RNA transcript and evolution. Comparisons to rice have been particularly insertion of the resultant DNA, so transposition does not useful in this regard because (1) it is evolutionarily quite involve excision. Because LTR retrotransposons make up distant from the other important grasses like maize, wheat, more than 50% of most or all large flowering plant barley, and sorghum [48], (2) it has a relatively small genomes and their high content varies somewhat propor- genome (~400 Mb) with a high gene density, (3) it’s tionally with angiosperm genome size, it is clear that these genome was an early target for comprehensive sequence TEs are the most important factor responsible for genome analysis [41], and (4) it has proven to be more stable vis- size variation in flowering plants [10]. Because these TEs à-vis small local rearrangements than other grasses like (and all other unselected DNAs) are fragmented and maize, sorghum, wheat or barley [9]. removed so rapidly by accumulated small deletions (see In the most comprehensive comparisons to date, between below), all of the insertions appear to be very recent, rice and two panicoid grasses, sorghum and maize, the usually within the last 2–6 million years [87]. This accounts frequency of gene movement over the last fifty million for the near-complete lack of homology of the intergenic years was calculated as at least 5%, and possibly as high as regions in orthologous genome segments with grass 25%, between sorghum and rice [53]. This number does not lineages that last shared a common ancestor more than include the gain or loss of tandemly repeated gene copies, a 50 mya. very common phenomenon in all grass lineages investigat- We currently lack a vocabulary to precisely describe the ed. Most of the genic rearrangements in maize compared to degree of conservation of genic content and colinearity either rice or sorghum are apparent gene losses on one of between any two species, much less across multiple two maize homoeologues [40, 53], an expected outcome of species, although a gene-pair conservation terminology is the polyploidization event about five mya that gave rise to currently in development (L. Feng and J. Bennetzen, the Zea lineage [80]. However, too little data yet exist to unpub. res.). However, it is clear that some lineages are identify possible subtle patterns in types of rearrangement. very unstable (e.g., pearl millet, sorghum, maize) and others Moreover, rearrangements involving genes are likely to be are much more stable (e.g., rice and foxtail millet) at the under selective pressure, so the events currently observed in level of compared genetic maps and/or microcolinearity any species are a combined outcome of those events that [23, 75, 9, 40]. We do not yet know the reasons for these have occurred, minus those that were subsequently differences, nor whether high conservation at one scale removed by chance or by selection against some specific (e.g., genetic map) in any way correlates with high changes. conservation at other scales (e.g., physical map or micro- In more distant comparisons, with longer ancestral colinearity). It is clear, though, that certain types of gene divergence times, colinearity across orthologous regions rearrangement are rare (e.g., movement of a gene to a appears to be much more rare than within the grasses. In the wholly different chromosome) while others are relatively rice flatsedge, Cyperus iria, the near-adjacent Sh2 and A1 common (tandem duplication, deletion or inversion of small homologues appear to be conserved in order and orienta- genic segments). tion, but one of the two genes in between in the grasses is Analysis of microcolinearity and gene content conserva- missing in the sedge (A. Pontaroli and J. Bennetzen, unpub. tion at long time frames has the advantage of the obs.). However, this is the only comparison that has been accumulation of multiple events for analysis, but this is done to the grasses in this ~110-million-years-of-divergence more than counterbalanced by three negative aspects of window [13]. Similarly, Musa (e.g., banana) genomes show concentrating on such ancient rearrangements. First, natural some colinearity with the grasses after >115 million years of selection has had a great deal of time to remove any events divergence from their last shared ancestor, but more than that had even a minor organismal disadvantage, so one only 50% of the annotated genes were non-colinear in a observes certain classes of tolerated or advantageous events comparison to rice [56]. With even more distant comparison that might not be proportional to the true spectrum of de Rice (2008) 1:109–118 11 113 3 novo rearrangements. Second, the components of the [40, 53, 64], wheat [27, 46, 90, 34, 16, 15] and sugarcane genome responsible for the rearrangement have had ample [42], have revealed interesting features of gene and genome time to decay into a state where they are invisible to current evolution in recent polyploids. LTR retrotransposon ampli- annotation approaches. And, third, individual events may be fication and altered regulation (e.g., silencing) or loss of buried underneath second, third or more layers of events at duplicated genes are repeated themes. Inactivation and the same location. For all of these reasons, investigations of eventual elimination of duplicated genes can be mediated orthologous regions in closely related lineages are justified, by altered epigenetic regulation, deletions, TE insertions, and are expected to be “there to discover” because of the and/or point mutations causing premature stop codons. relatively high rate of local chromosomal rearrangement in Some evidence suggests that specific alterations recur in the grasses. independent polyploidizations in wheat [27, 46]and Brassica napus [59]. However, most eventually fixed changes do not Colinearity dynamics within a 0–15 million year window occur instantly in post-polyploid genome rearrangements, at of grass genome evolution least not in maize. In adh1-homoeologous regions, for instance, fragments of partially deleted genes remain, Orthologous sequence comparisons across short time indicating the incomplete status of removal several million frames has the potential to reveal both the rate and the years after polyploidy, and showing that these gene losses mechanisms for disruption of colinearity. In a sequence are primarily by the accumulation of multiple small deletions comparison of the adh1-orthologous regions of maize and [40]. Another example of reasonably stable polyploid gene sorghum, two species that last shared a common ancestor copies comes from a comparative study of the adh1- about 12 mya [80], a 212-kb maize sequence was found to orthologous regions of maize, sorghum and sugarcane [42]. be largely collinear with a 66-kb sorghum sequence [84]. The two sugarcane homoeologous haplotypes show perfect The more than three-fold size difference is mainly due to genic colinearity. In addition, two maize homoeologous nested LTR retrotransposon insertions in the maize genome regions yielded the same gene content, order and orientation [78, 84]. In the original annotation, orthologs of nine maize as in sugarcane. Our data on comparative analysis in the genes were detected in the sorghum region in perfect Oryza genus also reveals excellent stability of polyploid colinear order; however, three additional genes in this genomes formed less than two million years ago (Chen et al., sorghum segment were not found in the maize adh1 region. unpub. res.). In subsequent analyses, one of the “missing” maize genes The Oryza genus contains about 24 species that belongs was found to be located in the adh1-homoeologous region to ten different genome types [31]. A project, entitled the of maize [40]. This has now turned out to be a routine Oryza MAP Alignment Project (OMAP), was launched to situation in the maize genome, where two maize segments build a framework for comparative biology in the Oryza represent each sorghum region due to a polyploidy event in genus [93]. Representative species, ranging from closely the Zea lineage within the last few million years [80]. Gene related species/subspecies, such as those with AA deletion (usually of only one homoeologous copy) subse- genomes, which diverged from their common ancestor quent to polyploidization has now reduced the originally less than a million years ago, to more distantly related doubled copy number of genes (2×) to less than 1.5× [53]. species, such as O. brachyantha and O. granulata,whose The other two non-colinear genes in the adh1-orthologous ancestors diverged about 10 mya, were chosen for regions of sorghum are found elsewhere in the genomes of bacterial artificial chromosome (BAC) library construc- maize and other grasses and are hypothesized to have been tion, BAC end sequencing, and physical map construction caused by the insertion of two unlinked genes, either as two [5, 49]. The initial analyses revealed excellent gene subsequent events or by a single event involving three colinearity both in their physical maps [50]and in chromatids. In dramatic contrast, a comparison of the adh1- sequence comparisons [96]. Genome size variations in orthologous regions between sorghum and sugarcane, both the Oryza genus were found to be mainly caused by gene colinearity and strong homology of non-coding lineage-specific amplifications of LTR retrotransposons regions were observed [42], indicating greater stability in [74, 6]. Our systematic comparative analysis of the these lineages over this shorter (~8 million year) time frame sequence of the MONOCLUM1-ortholgous regions across of divergence. the Oryza genus not only revealed high gene colinearity In at least some genomes, polyploidization is followed but also identified new genes that appear to have by extensive genomic change resulting in the silencing and originated de novo in the AA genomes (Fig. 2 and Chen elimination of duplicated genes [1]. In grasses, polyploidy et al., unpub. res.), which highlights the advantage of has been a recurrent theme, with many lineages exhibiting multiple species comparisons. full genome duplications over the last few million years. Intraspecific local sequence comparisons have also Local sequence comparisons in these species, such as maize identified interesting features of grass genome structure 114 Rice (2008) 1:109–118 Fig. 2 Microcolinearity in the MONOCULM1-orthologous regions across the Oryza genus. Black boxes represent genes. Red boxes indicate retrotranspo- sons. Fuchsia boxes symbolize DNA transposons. Orthologous genes are connected by lines. and evolution. A detailed sequence comparison of the discovery of more cases of TE components being co-opted bronze region of maize inbred lines McC and B73 found for organismal functions in plants, as in the recent that LTR retrotransposon clusters differed one hundred identification of transcription factors in Arabidopsis derived from the Mutator transposase [57]. percent in location relative to the genes in the bronze region between these two lines [29]. This suggests an amazingly Even if TE-vectored gene fragments are rarely if ever rapid process both for TE insertion and for removal of true genes with a selected host function, they certainly are a ancestral TEs. In addition, the first annotation of these two complication to genome annotation. Even without internal regions suggested that the genes themselves differed gene fragments, low-copy-number TEs are often mis- between these lines in this region. An apparent four-gene annotated as genes, giving rise to as much as two-fold over cluster was detected in McC but not in the orthologous estimations of gene numbers [7]. This type of over- position in B73 [29]. Later, these sequences were found to estimation in gene number can play particular havoc with be comprised of four gene fragments within Helitrons,a assessment of genic colinearity, as evidenced by studies in new type of eukaryotic transposon [44, 54, 52, 68]. This rice showing hundreds of gene differences between differ- phenomenon resembles Pack-MULEs, a type of TE first ent races of O. sativa that were later shown to all be named and comprehensively described in rice, that also explained by mis-annotated TEs [9]. Hence, many early capture and mobilize gene fragments [43]. Although neither publications showing numerous genic exceptions to micro- Helitrons nor Pack-MULEs usually mobilize intact genes, colinearity are incorrect because of this routine annotation they do commonly acquire more than one gene fragment in error. the same element. When transcribed, these internal frag- Sequence comparisons in closely related haplotypes in ments are often fused (via intron processing) into transcripts Arabidopsis, in rice and in wheat have demonstrated that that could encode novel protein products [43, 68]. This unequal homologous recombination and illegitimate recom- process of exon shuffling, first proposed by Gilbert [32]as bination are the major forces that remove DNA from the reason for the existence of introns, could be creating flowering plant genomes [16, 21, 60, 90, 91]. These new genes in plants at an amazing rate. The maize nuclear activities can remove >100 Mb of DNA from a plant genome, for instance, has more than 4,000 Helitrons that genome in just one million years [62], but the rate of contain inserted gene fragments [68] (L. Yang and J. removal appears to be much faster in some angiosperms Bennetzen, unpub. res.). However, there is not yet a proven than in others [87]. Most of the removed DNA is derived case of any of these Helitron- or Pack-MULE-generated from TEs, but other intergenic DNA and extra gene copies “new” genes having actually acquired a genetic function are also removed by these processes [60]. essential to its host. Given the rapid rate of unselected DNA Several recent studies have accentuated the fact that not loss from plant genomes (see below), it is unlikely that all genomic regions evolve at the same rate. Disease conversion of these chimeric gene candidates into true resistance gene clusters are known to be unstable even in genes will occur commonly, but even rates as low as one in map position [55], and to also undergo high rates of a million would be significant. Other than the standard unequal recombination [76], including some recombination route of gene duplication, which primarily creates sub- events that are delimited to specific sites that can optimize functionalized or (rarely) mildly modified new gene novel pathogen recognition specificities [70]. Ribosomal functions (reviewed in [39]), there is no known aggressive RNA gene clusters also appear to vary in map position even process for the generation of new genes. Perhaps Pack- in close relatives [25]. Perhaps most surprising, the MULEs and Helitrons will eventually be proven to provide composition and arrangement of sequences in centromeres this process. At the very least, we expect to see the have been found to be hyper-variable, primarily by the Rice (2008) 1:109–118 11 115 5 process of unequal homologous recombination [61, 63, 65]. provide an unprecedented opportunity to study grass This rapid rearrangement by recombination in a region that genome function and evolution. Because maize is derived is deficient in crossovers suggests a very tight control over from a fairly recent tetraploid [80], identifying the homoe- the outcomes of recombination, especially a powerful bias ologous segments and subsequent comparisons of these toward non-crossover, intrastrand and/or sister chromatid segments will illustrate how genome duplication has shaped outcomes [61]. This core centromeric instability has been the maize genome, and reveal the evolutionary fate of this argued to yield centromeres that have the potential to out- type of duplicated gene [47, 94]. Because all grass genomes compete other centromeres for choice as the germinal are derived from a shared paleopolyploid [71, 83, 95], nucleus in egg development [66]. identication and comparison of two sets of homoeologous In summary, local sequence comparisons of closely chromosomal segments in rice and four sets of homoeolo- related grass genomes and of intraspecific haplotypes have gous chromosomal segments in maize will reveal common begun to reveal the major mechanisms driving genome and lineage-specific patterns of conservation [77], suggest evolution. These include gene and genome duplication, mechanisms for gene movement [40, 53], and possibly gene silencing and eventual deletion of duplicated genes identify signatures of cases where these movements led to subsequent to polyploidization, transposable element am- significant biological outcomes. plification, gene movement mediated by transposition of The exciting next few years of grass genome compara- mobile elements, unequal homologous recombination, and tive genomics, with great emphasis on the Oryzae and on illegitimate recombination. All of these processes are quite maize and its relatives (e.g., sorghum and sugarcane), will variable even when comparing closely related species, so provide a framework for the next generation of plant genome their differences in levels of activity (and, possibly, analyses. At the technical level, comparative genome specificity) are responsible for the very different genomes analysis on a few model species like rice, maize, sorghum, found in flowering plants. and Brachypodium has opened up avenues to the highly leveraged study of any other grass. No single species is more enriched for “interesting” genes than any other species, but The past, present, and future of plant genome the traditional tractability of studying these interesting genes comparisons was centered on the model species with excellent molecular, physiological, biochemical, cell biological and genetic Perhaps the most valuable insight gained from comparative toolkits. Because of comparative genomics, this historical genomic analyses in rice and related grasses has been the limitation no longer holds true. astounding instability of genome structure against a fairly With highly conserved gene content across the grasses, conserved set of biological functions. As mentioned above, small-genome surrogates (or, even better, those surrogates at a local genome level, two maize plants are often more with sequenced genomes) can be used to provide facile different from each other than a human is from a access to any shared grass gene. Moreover, the discovery of chimpanzee, or even from a macaque. The grasses and novel genes or modified gene functions that make each other angiosperms obviously insulate their gene functions species unique can now be performed by simple EST from the great majority of this genome change, in manners analysis or trait mapping. Once these candidate genes for that we do not now understand at even the most minimal family- or genus- or species-specific gene functions are level. identified, they can now be easily isolated and tested for the As shown in Drosophila, pursuit of full genome analyses ability to condition novel biological function by introduction in several species within a dense phylogenetic framework into easily-transformed model species. can be exceptionally productive [18, 79]. In plants, the Oryza Despite, perhaps because of, the many important genus provides such a unique opportunity to investigate discoveries that have been made over the last 15–20 years various aspects of gene and genome evolution with the of plant comparative genomics, we have more questions to availability of a robust phylogenetic framework [31, 97], rich answer now than we did at the outset. Because of the genomic resources [5, 49], and a near-perfect reference continued extraordinary increases in throughput and genome [41]. The ongoing sequence comparisons in the decreases in cost of nucleic acid sequence analyses, many Oryza genus will provide dramatic and lineage-oriented more plant species will be investigated with a much broader insights into the creation of new genes, the evolution of gene (and better-conceived) set of phylogenetic justifications. structure and function, conserved non-coding sequences, the Genetic maps, physical maps and EST analyses are all evolutionary dynamics of duplicated gene in polyploid needed for hundreds or thousands of plant species to identify species, centromere drive and a wealth of other issues. shared and novel traits. 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Journal

RiceSpringer Journals

Published: Dec 1, 2008

Keywords: Comparative genomics; Genome evolution; Microcolinearity; Recombination; Transposable elements

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