A BAC-based physical map of Brachypodium distachyon and its comparative analysis with rice and wheat
© Gu et al; licensee BioMed Central Ltd. 2009
Received: 28 April 2009
Accepted: 27 October 2009
Published: 27 October 2009
Brachypodium distachyon (Brachypodium) has been recognized as a new model species for comparative and functional genomics of cereal and bioenergy crops because it possesses many biological attributes desirable in a model, such as a small genome size, short stature, self-pollinating habit, and short generation cycle. To maximize the utility of Brachypodiu m as a model for basic and applied research it is necessary to develop genomic resources for it. A BAC-based physical map is one of them. A physical map will facilitate analysis of genome structure, comparative genomics, and assembly of the entire genome sequence.
A total of 67,151 Brachypodium BAC clones were fingerprinted with the SNaPshot HICF fingerprinting method and a genome-wide physical map of the Brachypodium genome was constructed. The map consisted of 671 contigs and 2,161 clones remained as singletons. The contigs and singletons spanned 414 Mb. A total of 13,970 gene-related sequences were detected in the BAC end sequences (BES). These gene tags aligned 345 contigs with 336 Mb of rice genome sequence, showing that Brachypodium and rice genomes are generally highly colinear. Divergent regions were mainly in the rice centromeric regions. A dot-plot of Brachypodium contigs against the rice genome sequences revealed remnants of the whole-genome duplication caused by paleotetraploidy, which were previously found in rice and sorghum. Brachypodium contigs were anchored to the wheat deletion bin maps with the BES gene-tags, opening the door to Brachypodium-Triticeae comparative genomics.
The construction of the Brachypodium physical map, and its comparison with the rice genome sequence demonstrated the utility of the SNaPshot-HICF method in the construction of BAC-based physical maps. The map represents an important genomic resource for the completion of Brachypodium genome sequence and grass comparative genomics. A draft of the physical map and its comparisons with rice and wheat are available at http://phymap.ucdavis.edu/brachypodium/.
Model systems play an important role in studies of genome structure and evolution, and are invaluable in gene isolation and functional characterization. The application of model systems toward the study of both basic and applied problems in plant biology has become routine. The model dicot Arabidopsis thaliana has been used in studies ranging from nutrient uptake and metabolism to plant-pathogen interactions. Unfortunately, due to its distant relationship to monocots, Arabidopsis is not an ideal model for grasses. Rice is being currently used as a grass model , but its primary adaptation to semi-aquatic, subtropical environments limits its usefulness. The large sizes of rice plants and long generation time make experiments requiring large numbers of plants grown under controlled conditions costly. It is also challenging to grow rice under the conditions prevailing in greenhouses in northern climates.
Brachypodium distachyon has numerous attributes expected to find in a genetic model and interest in using it as a model system for wheat and other temperate grasses is growing rapidly [2–8]. Diploid B. distachyon is closely related to the Triticeae [9, 10] but in contrast to the Triticeae, it possesses a very small genome (x = 5) of approximately 355 Mb [9, 11]. The recent release of 8× B. distachyon genome sequence showed that the genome is 271 Mb in size (assembled sequences, http://www.brachypodium.org). It is a small temperate grass with simple growth requirements, short generation time, and self-pollinating habit [2, 6, 7, 9]. Highly efficient transformation of B. distachyon via Agrobacterium tumefaciens has been developed, which will facilitate its functional genomics and biotechnological applications [12–14]. These characteristics make B. distachyon superbly suitable for both functional and comparative genomic research.
Several genomic regions of B. distachyon and B. sylvaticum, a close relative of B. distachyon with a larger genome, have been compared with wheat and rice. In general, good colinearity was observed reflecting general conservation of synteny across the grass family [15–19]. To foster the development of B. distachyon as a grass model and coordinate the development of its genomics resources, the International Brachypodium Initiative was formed http://www.brachypodium.org. The Initiative placed a high priority on the development of a global physical map of diploid B. distachyon composed of large genomic fragments cloned in a bacterial artificial chromosome vector (BAC) http://www.brachypodium.org/node/8. A high resolution BAC-based physical map has many genomics applications including analyzing genome structure, conducting genome-wide comparisons, and facilitating the assembly of B. distachyon genome sequence.
The development of a Brachypodium BAC-based physical map is reported here. Also reported is a global comparison of the map with rice genome sequence  and wheat deletion bin maps  with the goal to obtain a clearer picture of B. distachyon genome structure and evolutionary history and their relationships to those of rice and wheat.
Results and Discussion
BAC source, fingerprinting, and contig assembly
Cross-contamination and low quality fingerprinting data interfere with accurate contig assembly . Contaminated clones, empty clones, small insert clones, and clones with fingerprints below specified quality threshold were eliminated with the GenoProfiler program . Of the 67,151 fingerprinted clones, 52,343 clones (78%) were suitable for contig assembly. An average fingerprint had 79.4 restriction fragments in this population of fingerprints. Since the average insert size was 100 kb , there was on the average a restriction fragment every 1.26 kb.
The 52,343 fingerprints representing 14× B. distachyon genome equivalents were used for an initial automated contig assembly using the FPC software . The initial assembly was performed at a relatively high stringency (1 × 10-45) to minimize faulty contig assembly of clones from unrelated regions of the genome. The "DQer" function was used to dissemble contigs containing more than 10% questionable (Q) clones. The "End to End" FPC function was then repeatedly employed to merge contigs with successively less stringent Sulston score cutoff values [24, 25, 28]. In the end, the FPC assembly resulted in 648 contigs containing a total of 50,182 BAC clones. In this "Phase I" physical map, 177 contigs had more than 100 clones each, 73 contigs had 50 - 99 clones each, 72 contigs had 10 - 49 clones, and the rest had 9 clones or less. A total of 2,161 singletons remained. The cumulative, contiguous, non-redundant fragment count across all contigs was equivalent to approximately 410 Mb, which was 15.5% more than the estimated size of B. distachyon genome (355 Mb) [9, 11]; if the genome size of 271 Mb based on the recent release of 8× genome sequence assembly http://www.brachypodium.org is used, the fragment count would be equivalent to 51.3% more of the estimated genome size. This indicated that many contigs actually overlapped other contigs, but the overlaps were below contig joining threshold. Such overestimation has been reported in physical maps of other plant genomes [25, 29].
Editing of contigs by alignments with the rice genome sequence
Integration of molecular markers into contigs is crucial for their anchoring on genetic maps and ultimate alignment of a physical map and genome sequence. This task can be accomplished by screening BAC libraries with pools of labeled probes derived from EST clones or mapped genetic markers or screening of multidimensional pools of BAC clones by PCR or highly parallel Illumina GoldenGate assays [30–33]. BAC end sequences (BESs), in addition to other genomic applications [34–37], can facilitate initial genome characterization [3, 28, 34, 35] and anchoring of contigs onto the genetic map. BESs are particularly useful for contig anchoring in small, gene-dense genomes. Their utility is diminished in large and complex genomes due to a low gene density. For example, in wheat, over 80% of the genome consists of repetitive DNA (reviewed in ). Akhunov et al.  reported that coding sequences accounted for only 5.8, 4.5, and 4.8% of BES in T. uratu, Ae. speltoides, and Ae. tauschii BAC libraries, respectively. A total of 38 Mb of random B. distachyon genomic sequence was generated by sequencing 64,694 BAC ends from the two BAC libraries, representing ~14.0% of the genome sequence on the basis of a genome size of 271 Mb http://www.brachypodium.org. This was equivalent to one sequence tag every 4.2 kb (considering 271 Mb of the genome size). A total of 25.3% of repeat-masked B. distachyon BESs had matches to the rice genome sequence (E < 10-25). Among them, 13,970 also matched wheat ESTs . Therefore, the integration of B. distachyon BES into the contigs immediately anchored a large number of contigs onto the rice genome sequence and wheat deletion maps (see discussion below).
Comparison of B. distachyon contigs with the rice genome
The alignment of contigs of the Phase II B. distachyon physical map to the rice genome sequence estimated the genome coverage. A total of 345 contigs (51.4%) could be aligned to the rice genome sequence. They covered 336 Mb (88%) of the rice genome sequence (using 382 Mb as 1C rice genome size, ) and represented 88% of the total B. distachyon FPC map as measured by CB units. When only contigs with more than 10 clones were used, 331 out of 364 (90.9%) could be aligned to the rice genome. Although 326 contigs could not be anchored, these contigs were generally small, and the total number of clones in them equaled to only 2,489 (5.0%) out of the total 50,182 clones, indicating that only a small portion of the clones could not been anchored onto the rice genome. The data suggested a general conservation of synteny between rice and B. distachyon genomes, which confirms previous conclusions made on the basis of sequencing a few B. sylvaticum BAC clones and their sequence comparisons with the orthologous regions in rice and wheat .
Most plant genomes are paleopolyploid with ancient whole-genome duplications [43–48]. The radiation of grasses was preceded by paleotetraploidy resulting in a whole-genome duplication , which was followed by diploidization by deletions. Therefore, in regions that are still duplicated in the B. distachyon genome, a rice region will align strongly with one B. distachyon contig block and weakly with another. This is evident in Figure 5B, where two B. distachyon syntenic contig blocks can be identified for several rice chromosomes. These data show that the B. distachyon genome has a similar set of duplications derived from the ancient paleotetraploid as does rice.
Alignment of wheat EST deletion bin map to B. distachyon contigs
The 1C nucleus of hexaploid T. aestivum contains 16,000 Mb DNA , which makes map-based cloning of wheat genes very difficult. Because B. distachyon diverged from the wheat phylogenetic lineage only about 30 million years ago (MYA) , B. distachyon physical map and ultimately genome sequence can facilitate wheat map-based cloning and other genomic applications.
A total of 7,104 expressed sequence tag (EST) unigenes were previously mapped into 156 deletion bins, providing a genome-wide framework for wheat mapping and identifying agronomically important genes . However, a disadvantage of the deletion bin map is that loci are not ordered within the bins. Given the general colinearity among the grass genomes, this problems can be partially overcome by in silico ordering of wheat ESTs using rice genomic sequence . Brachypodium is expected to show better synteny with wheat than rice because it diverged from wheat more recently than rice , Brachypodium is therefore expected to be more useful in comparative mapping applications than rice.
To assess the utility of B. distachyon physical map for wheat genomics, we compared the Brachypodium contigs with the wheat deletion bin map . Of 7,104 deletion bin mapped wheat ESTs, 985 matched Brachypodium BESs at an e-value cutoff of 1× 10-10. These matches were derived from BESs associated with 216 contigs (32% of total Brachypodium contigs). Such analysis allowed us to align Brachypodium contigs onto individual chromosomes based on wheat deletion bin map data http://phymap.ucdavis.edu/brachypodium/.
ESTs BF473313 and BE446475 homologous to BES sequences of Contig138 also have no match in the rice genome, but were mapped on long arms of wheat chromosomes of homeologous groups 1 and 7, respectively. These genes are only present in Brachypodium and wheat but are not located in colinear positions in the two genomes. Another EST locus, BM138418, is colinear only between Brachypodium and rice since this EST was mapped to the chromosome 3B in wheat based on the wheat deletion bin map result. Two ESTs, BF484988 and BG313703, at the top of Contig138 were mapped to the short arm on wheat chromosomes of homeologous group 5. In rice, they matched sequences on chromosome 1. Other examples of noncolinear genes among the three genomes were observed. Occasional perturbations of synteny between Brachypodium, rice and wheat must therefore be expected and taken into account in comparative genomic applications. Since synteny of wheat chromosomes has been eroded faster in the distal regions than in proximal regions , perturbed synteny should be expected particularly in genomic comparisons with Brachypodium involving distal regions of wheat chromosomes. Synteny perturbations observed in contig 138 exemplify this reality since the contig is orthologous to a distal region of the short arm of chromosome 1.
To further expand the utility of the Brachypodium physical map, we integrated wheat ESTs that have not been placed into wheat deletion bins into Brachypodium contigs. There are over one million wheat ESTs in Genbank, and they have been assembled into 42,848 unigene sets http://www.ncbi.nlm.nih.gov/unigene. Using BLAT, 5,421 different unigenes were integrated to the Brachypodium contigs. They were homologous to a total of 5,910 BES in the physical map. These wheat EST markers will further facilitate comparative mapping in wheat. The comparison of Brachypodium contigs with wheat deletion maps and integration of wheat unigenes into Brachypodium contigs can be accessed at http://phymap.ucdavis.edu/brachypodium/.
A whole-genome, BAC-based physical map for the new grass model species, Brachypodium, was constructed. The map facilitated a variety of genomic applications. Comparison of contigs with rice revealed high colinearity between rice and Brachypodium chromosomes. Additionally, many Brachypodium BAC contigs could be anchored on the wheat deletion bin maps. Both outcomes support the anticipated utility of Brachypodium for wheat comparative genomics and practical applications in map-based cloning of wheat genes. Another application of the physical map is in the Brachypodium genome sequencing project. The phase II physical map can be aligned with shotgun sequence contigs via BES and provide scaffolds for ordering shotgun sequence contigs and estimating gap sizes. The BAC-based physical map reported here was provided to the Brachypodium distachyon sequence assembly team and has helped produce a high quality final sequence assembly http://www.brachypodium.org/node/18. The physical map can also identify BACs spanning sequence gaps and has served as sequencing template to fill them. Brachypodium is expected to serve as a surrogate to assist gene discovery and functional characterization in the large and complex crop genomes, such as wheat and bioenergy crops. All the data and resources developed in this study are available at the http://phymap.ucdavis.edu/brachypodium/ website for community use.
Bacterial artificial chromosomal (BAC) libraries
The B. distachyon BAC libraries used in this study were previously constructed using partial digests with Hin dIII and Bam HI restriction enzymes from an inbred diploid line of B. distachyon, Bd21, the same line selected for complete sequencing by the US Department of Energy Joint Genome Institute through its "Community Sequencing Program" http://www.jgi.doe.gov/sequencing/why/51281.html . These BAC libraries represent ~29.2-fold haploid genome equivalents and were employed for BAC fingerprinting and contig assembly.
BAC fingerprinting and fragment sizing
The BAC clones were fingerprinted as described by  with minor modifications. From each 384-well plate, four 96-well blocks containing 1.2 ml of 2× YT medium plus 12.5 μg/ml chloramphenicol were inoculated with a 96-well replicator. Two pins were removed from the replicator to allow the insertion of control clones into the 96-well plate. Two control BAC clones were inserted manually in wells E07 and H12 in each 96-well block. The plates were covered with Airpore gas permeable plate sealant (Qiagen) and shaken on an orbital shaker agitated at 400 rpm at 37°C for 20 hours. BAC DNA was isolated with the Qiagen R.E.A.L 96-Prep kit (Qiagen, Valencia, California). The following minor modifications of the fingerprinting method were made to accommodate the use of ABI3730XL (Applied Biosystems, Foster City, California) instead of ABI3100 for capillary electrophoresis. The more sensitive laser of the ABI3730XL instrument improved fingerprinting resolution and made it possible to reduce the amount of BAC DNA sample for electrophoresis, thus lowering fingerprinting costs. To reduce sample size, 0.5-1.2 μg instead of 1.0-2.0 μg of BAC DNA was simultaneously digested with 2.0 instead of 5.0 units each Bam HI, Eco RI, Xba I, Xho I and Hae III (New England Biolabs, Beverly, Massachusetts) at 37°C for 3 hrs. The DNA was labeled with 0.4 μl instead of 1.0 μl of the SNaPshot kit (Applied Biosystems, Foster City, California) at 65°C for 1 hr and precipitated with ethanol. The labeled DNA was dissolved in 9.9 μl of Hi-Di formamide, and 0.3 μl of GeneScan 1200 LIZ (Applied Biosystems, Foster City, California) was added to each sample as an internal size standard. Restriction fragments were sized with ABI3730XL using 50 cm capillaries and POP7 (Applied Biosystems, Foster City, California). The fragment size calling was accomplished with the GeneMaper software (Applied Biosystems, Foster City, California) with the help of FP Pipeliner http://www.bioinforsoft.com/.
Fingerprints editing and contig assembly
The fingerprint profiles for each BAC clone were collected by GeneMapper v3.7 (Applied Biosystems). The GeneMaper output data was edited with the GenoProfiler program . The two control BAC clones inserted in each 96-well plate were used to check for the correct orientation of the plate. Fragments in the size range of 100 - 1,000 bp were measured. For the data quality control, vector bands and clones failing fingerprinting or lacking inserts were removed using GenoProfiler program. In addition, samples with less than 40 or more than 150 fragments were also eliminated. Fingerprints of cross-contaminated samples were detected using a module in the GenoProfiler  and removed from the data set. The cross-contamination was defined as clones residing in neighboring wells either in 384-well format or 96-well format (quadrants) share 30% or more of the mean number of fragments, the formula is shared bands*2/(bands1 + bands2).
A total of 52,343 BAC clones that passed quality check were used to assemble contigs using the FPC v8.5.3 . The initial assembly used a Sulston score of 1× 10-45 and a tolerance 0.4 bp. The contig assembly was processed through the DQ function of FPC to break up contigs having more than 10% Q-clones in a contig. The assembly was further refined using "Single-to-End" and "End-to-End" merging by stepwise decreasing of assembly stringency of Sulston score cutoff values (down to 1× 10-14).
Alignment of FPC contig with the rice genome and wheat deletion bin map
There were 64,697 BAC end sequences generated from the fingerprinted B. distachyon BAC clones  which were compared using BLAT  against the rice pseudomolecules build 4.0 http://rgp.dna.affrc.go.jp/IRGSP/Build4/build4.html. The results were used as input into Synteny Mapping and Analysis Program (SyMap) , which computed the synteny blocks. The results can be viewed from the SyMAP Java based dot-plot, synteny block to chromosome, and close-up views.
To anchor B. distachyon physical contigs to the wheat deletion bin map, BAC-end sequence data from the B. distachyon BACs were compared against sequences of the mapped wheat EST probe sets using BLAT (parameters minScore = 50, minIdentity = 80%) and links to the wheat deletion bin map constructed [20, 52]. The BLAT alignments and FPC anchoring were carried out using FPC modules BSS, which is designed for this purpose . The CMAP http://gmod.org/wiki/Cmap tool allowed for comparative analysis between the B. distachyon physical contigs and wheat deletion bin map.
The authors thank Daniel Hayden, Devin Coleman and Theresa Hill for assistance in BAC DNA extraction; Charles H. Wang and Rana Nederi for assistance in generating BAC fingerprints. This work was supported in part by the United State Department of Agriculture, Agriculture Research Service CRIS 532502100-010, 533502100-011, and 532502100-013; and by the Department of Plant Sciences, University of California, Davis.
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