Whole genome comparisons of Fragaria, Prunus and Malus reveal different modes of evolution between Rosaceous subfamilies
- Sook Jung1Email author,
- Alessandro Cestaro2,
- Michela Troggio2,
- Dorrie Main1,
- Ping Zheng1,
- Ilhyung Cho3,
- Kevin M Folta4,
- Bryon Sosinski5,
- Albert Abbott6,
- Jean-Marc Celton7,
- Pere Arús8,
- Vladimir Shulaev9,
- Ignazio Verde10,
- Michele Morgante11,
- Daniel Rokhsar12,
- Riccardo Velasco2 and
- Daniel James Sargent2
© Jung et al; licensee BioMed Central Ltd. 2012
Received: 21 September 2011
Accepted: 4 April 2012
Published: 4 April 2012
Rosaceae include numerous economically important and morphologically diverse species. Comparative mapping between the member species in Rosaceae have indicated some level of synteny. Recently the whole genome of three crop species, peach, apple and strawberry, which belong to different genera of the Rosaceae family, have been sequenced, allowing in-depth comparison of these genomes.
Our analysis using the whole genome sequences of peach, apple and strawberry identified 1399 orthologous regions between the three genomes, with a mean length of around 100 kb. Each peach chromosome showed major orthology mostly to one strawberry chromosome, but to more than two apple chromosomes, suggesting that the apple genome went through more chromosomal fissions in addition to the whole genome duplication after the divergence of the three genera. However, the distribution of contiguous ancestral regions, identified using the multiple genome rearrangements and ancestors (MGRA) algorithm, suggested that the Fragaria genome went through a greater number of small scale rearrangements compared to the other genomes since they diverged from a common ancestor. Using the contiguous ancestral regions, we reconstructed a hypothetical ancestral genome for the Rosaceae 7 composed of nine chromosomes and propose the evolutionary steps from the ancestral genome to the extant Fragaria, Prunus and Malus genomes.
Our analysis shows that different modes of evolution may have played major roles in different subfamilies of Rosaceae. The hypothetical ancestral genome of Rosaceae and the evolutionary steps that lead to three different lineages of Rosaceae will facilitate our understanding of plant genome evolution as well as have a practical impact on knowledge transfer among member species of Rosaceae.
KeywordsRosaceae Comparative genomics Evolution
The Rosaceae is one of the most economically important and morphologically diverse plant families with over 90 genera containing more than 3000 species. The family contains three sub-families; the Dryadoideae, the Rosoideae and the Spireaeoideae, with the economically-important genera Prunus and Malus contained within the Spireaeoideae, whilst Fragaria is a member of the Rosoideae . The base chromosome number of the many genera within the family ranges from x = 7 to x = 17, and recent research has suggested that the ancestral chromosome number for Rosaceae may have been x = 9 [2, 3]. As in many other plant families, comparative genomics will enhance our understanding of genome structure and function and the evolutionary forces that have led to the current chromosomal configurations of the numerous Rosaceous species, and in turn to the mechanisms responsible for the wealth of morphological diversity encompassed by the family. An understanding of the degree of conservation of genome structure and function between related genera will enable inferences to be made about the genomic positions of genes controlling common traits among genera and permit information gained in one species to inform investigations in another.
The recent availability of whole genome sequences has permitted the delineation of syntenic blocks at high resolution and from this the evolutionary history in plant lineages can be inferred. In the grasses, paleogenomic modeling, using sequences of the maize, rice, and sorghum genomes as well as large sets of genetically mapped genes in wheat and barley, led to the proposal of an ancestral grass karyotype for the five ancestral chromosomes [4, 5] from which all modern grass genomes evolved. The recent sequencing of the Brachypodium genome  revealed a whole-genome paleo-duplication in Brachypodium chromosomes, whilst comparisons of the Brachypodium, rice and sorghum genome sequences revealed orthologous relationships that were consistent with the evolution of the extant Brachypodium genome from an ancestral genome containing five chromosomes.
Similarly, in the dicots, whole genome sequencing has revealed patterns of genome evolution that it had not been possible to detect using comparative mapping of orthologous markers. The sequencing of the grapevine genome  and its comparison to the genomes of Arabidopsis and poplar permitted the identification of a paleo-hexaploidisation event in the common lineage of the three species which occurred after the monocotyledonous and dicotyledenous plant lineages diverged. This hexaploidisation event had not previously been identified, despite the whole genome sequences of Arabidopsis and poplar being available for some time [8, 9]. This was primarily due to the subsequent polyploidisation events that had occurred in the genomes of these species (once in the case of poplar, and twice in the case of Arabidopsis) since they diverged from a common ancestor. Thus, analyses based on higher levels of resolution, particularly those based on whole genome sequence data, reveal evermore complex patterns of genome evolution between species, but at the same time provide compelling evidence to support models of genome evolution and deduced ancestral chromosomal configurations.
So far no studies have been performed that have compared whole genome sequences of plant species that belong to different genera of the same family. In Rosaceae, as well as in other economically important plant families including Poaceae, Solanaceae, Brassicaceae and Fabaceae [10–14], the comparative genomics studies have been performed using conserved genetic markers. Dirlewanger et al  first identified high levels of conservation of marker presence and order between three of the eight linkage groups of the Prunus reference map , and seven of the 17 linkage groups of the apple map , demonstrating that markers mapping to a single Prunus linkage group were located on two homeologous linkage groups on the Malus linkage map and that large conserved syntenic blocks were clearly identifiable within the two genera. A number of other studies were also performed using PCR-based markers that had been developed from both Malus and Fragaria, which were applied to comparative mapping between Prunus and these other members of the Rosaceae [18, 19]. High level of co-linearity within the sub-family Maloideae between the genomes of Malus and Pyrus has also shown by comparative mapping using simple sequence repeat (SSR) markers . Vilanova et al  reported a genome-wide inter-generic comparison of genetically mapped orthologous markers between diploid Fragaria and Prunus showing sufficiently well conserved macro-synteny to enable the reconstruction of a hypothetical ancestral genome for Rosaceae containing nine chromosomes. The study however also revealed a number of large-scale chromosomal rearrangements, including translocations of large syntenic blocks and numerous fusion-fission events that had occurred in the evolutionary history of the two genera. More recently, using the whole genome sequence from the apple cultivar 'Golden Delicious'  and sequence data from 1,473 markers mapped in Prunus and Fragaria, including Rosaceous conserved orthologous sequences (RosCOS) , Illa et al  performed a genome-wide comparison between all three genera. Analyses based on the positions of the 129 markers revealed clear, conserved, syntenic blocks that were common to all three genomes, with a single syntenic block in Prunus corresponding to one or two syntenic regions in Fragaria, and two or four syntenic regions in apple. Illa et al  reconstructed a hypothetical ancestral genome for the Rosaceae containing nine chromosomes (x = 9), consistent with the report of Vilanova et al . The data suggested that the resolution of studies based on modest numbers of markers was perhaps not sufficient to elucidate the true number of small scale genomic inversions that have taken place in genome evolution within the Rosaceae, which may have played an important role in speciation within the family. Thus, an evaluation of the conservation of synteny between Fragaria, Malus and Prunus based on whole genome sequence data may reveal much about sequence evolution in this closely-related, yet morphologically diverse family that has been hitherto undetected.
The genomes of three Rosaceous genera of significant economic importance, Fragaria, Malus and Prunus have recently been sequenced, presenting an exciting opportunity for high-resolution genome comparison. Here we report results from comparison of whole genome sequences of the three species of Rosaceae and the genome of Vitis vinifera, included as an outgroup species representing a basal rosid genome. We were able to identify the orthologous regions among the three Rosaceous species at a much higher-resolution than has previously been reported. This higher-resolution enabled us to detect different patterns of genome evolution between the sub-families of Rosaceae. Furthermore, we reconstructed a hypothetical Rosaceae ancestral genome using the Multiple Genome Rearrangements and Ancestors (MGRA) algorithm and further manual analyses.
Results and Discussion
Evaluation of orthologous regions between taxon pairs
The RosCOS markers used previously by  are a useful resource in comparative genome alignment and as such revealed insights into the patterns of genome evolution on a macro-syntenic scale in that study. Since the RosCOS are an important resource for future comparative studies, we anchored them to the orthologous regions (ORs) identified in this investigation (Additional file 3: Table S1). However, since orthologous genes in two species do not necessarily reside in large orthologous regions of the genome, using a relatively small set of orthologous sequences (as in the case of the RosCOS markers) in the detection of microsynteny would only be possible in genomic regions where the order of a large number of orthologs is conserved among related genomes. With only 800 mapped RosCOS available for study, it was difficult to detect orthologous regions at very high levels of resolution. Capitalising on the availability of whole genome sequences with many more predicted genes (27,243 in peach, 33,264 in strawberry and 43,335 in the primary assembly of apple), along with Mercator , which selects one to one orthologous regions based on the large numbers of exons available for study, meant that we were able to detect the conservation of synteny between the genomes at a much finer level in this investigation than in previous studies.
Number and length of orthologous regions (ORs) in two-genome and three genome comparisons
Mean No. Matching Exons
Mean Length in Kb (Prunus|Fragaria|Malus)
Largest Length in Mb (Prunus|Fragaria|Malus)
Prunus and Fragaria
Prunus and Malus
*Prunus and Malus (Split into two sub_genomes)
Prunus, Fragaria and Malus
Major orthologous chromosomes among Prunus, Fragaria and Malus
FC2, FC4, FC5
FC1, FC3, FC6
MC2/MC15, MC3/MC11, MC4/MC12
The analysis between Prunus and Malus produced fewer, but larger ORs with a greater number of matching exons. The smaller number of ORs may reflect the fact that the primary assembly of apple does not include all the predicted genes sequenced. A total of 349 ORs were obtained, with the longest region of 6.6 Mb of PC3 and 7.5 Mb of MC9 (Table 1). The mean number of matching exons in ORs was 23 and the mean lengths of ORs were 200.9 kb in Prunus and 260.5 kb in Malus (Table 1). At the chromosome level, the analysis revealed more complex relationships between the two genera than between Prunus and Fragaria. ORs on PC3 and PC5 each corresponded to ORs on two major Malus chromosomes, MC9 and MC17, and MC6 and MC14, respectively. The two sets of Malus chromosomes, MC9/MC17 and MC6/MC14, were two of the chromosome doublets that contain large syntenic regions indicative of the recent WGD in Malus lineage which agrees with previous hypotheses that the Malus genome went through relatively recent Pyreae-specific WGD [3, 21], that occurred following the divergence of the Malus and Prunus lineages, as no evidence of such a WGD is present in the strawberry and peach genomes [23, 24]. Orthologous regions in PC2 corresponded to major ORs on three Malus chromosomes, MC1, MC2 and MC7. ORs on PC1, PC4, and PC7 each corresponded to ORs on four Malus chromosomes, whilst ORs on PC6 corresponded to ORs on multiple Malus chromosomes (Figure 1B, Table 2). The observation that each chromosome of Prunus corresponded to ORs in two or more chromosomes of Malus, even though Mercator detects ORs in one to one relationships, suggests both sets of chromosomes generated by WGD retained orthologous relationships to their corresponding Prunus chromosomes. It also suggests that both of the two sub-genomic regions generated by WGD have retained a similar level of conservation of orthology. When the Malus chromosomes were divided into sub-genome 1 and 2 prior to the analyses (see Materials and Methods) so that Mercator could find ORs in each Malus subgenome, 706 ORs were detected (Table 1). The whole genome duplication of Malus alone however does not account for the higher number of rearrangements that occurred since Prunus and Malus diverged from a common ancestor. Since the ancestor of the genus Fragaria diverged from a common ancestor shared by both Malus and Prunus, it is more likely that there have been more instances of large-scale chromosomal fission in the Malus lineage than the occurrence of multiple, yet independent fusion events in the Prunus and Fragaria lineages to derive the extant genome structure that is evident in the three genera today. More instances of large-scale chromosomal fission may be a consequence of, or related to, the WGD that occurred in Malus lineage. Some of the rearrangements, however, may have resulted from the potential errors during genome sequencing and assembly.
Evaluation of orthologous regions between Fragaria, Malus and Prunus
The evolutionary relationships among the three Rosaceous species studied were analysed further by investigating ORs shared amongst all three genera in addition to those detected in each taxon pair. In total 1399 regions that were orthologous in all three genera were identified. The list of ORs with their positions and orientations in each genome are given in Table S1. Table S2 lists the size of ORs and the number of exons in each genome. The ORs contained 667 out of 855 RosCOS that have been anchored to the peach genome and 616 of the total 1399 ORs contained anchored RosCOS markers. The list of RosCOS markers, their anchored positions and their matching ORs are provided in Table S3. The longest OR in Prunus and Fragaria was OR 627 spanning 3.5 Mb in PC8 and 1.3 Mb in FC2 with an OR in MC9. The longest OR in Malus was 2.6 Mb in MC4 with ORs in PC6 and FC6 (Table 1). OR 627 contained 1318 exons and 316 genes in Prunus, 998 exons and 200 genes in Fragaria, and 92 exons and 21 genes in Malus, respectively. The numbers of sequences in OR 627 with matches in other genomes were 125 exons and 62 genes in Prunus, 121 exons and 57 genes in Fragaria, and 21 exons and 6 genes in Malus, respectively. Table S4 lists all the genes and exons in OR 627 in each genome with their positions. The longest ORs in each genome and size distributions of the ORs are given in Table S5.
Comparison of orthologous regions in major orthologous and non-orthologous chromosomes
Comparisons of orthologous regions (ORs) in major orthologous chromosomes with those in non-orthologous chromosomes
Mean length in kb (Prunus| Fragaria)
Mean No. Exons
Mean No. Matching Exons
Mean Syntenic Quality (%)
Mean PID (%)
Mean Bit Score
Orthologous chromosomes between Prunus and Fragaria
Mean length in kb ( Prunus | Malus )
Mean No. Exons ( Prunus | Malus )
Mean No. Matching Exons
Mean Syntenic Quality (%)
Mean PID (%)
Mean Bit Score
Orthologous chromosomes between Prunus and Malus
Detection of conserved ancestral regions
Number of breaks between chromosomal regions that are originated from different CARs
Avg. (per 10 Mbp)
Avg. (per chromosome)
Reconstruction of hypothetical Rosaceae ancestral genome
The availability of whole genome sequence data has permitted for the first time a detailed evaluation of the conservation of macro- and micro-synteny in the Rosaceae which has demonstrated that the genomes of Fragaria, Malus and Prunus have undergone different modes of evolution since they diverged from a common ancestor. This study has revealed that a greater number of small scale rearrangements have occurred in Fragaria than in either Malus or Prunus and has indicated that Malus went through more translocations potentially as a consequence of the WGD event in the lineage of the genus. The results of this investigation suggest that Prunus has the most conserved karyotype at both the macro- and micro-syntenic level in relation to the ancestral genome configuration for the Rosaceae, which in concordance with other studies is hypothesised to have had nine chromosomes. The resolution obtained in this comparison of genome structure demonstrates the utility of whole genome sequencing data to the elucidation of mechanisms driving genome evolution between related organisms at a level of resolution that would not have been possible through conventional comparative mapping endeavours.
Materials and methods
Detection of orthologous regions
To detect orthologous regions between the peach and grape genomes, the whole genome sequence and annotation data of grape were downloaded from Genoscope . Whole genome sequence of Prunus persica v1.0, primary assembly of Malus domestica and Fragaria vesca beta version FvH4 pseudochromosomes were downloaded from GDR, Genome Database for Rosaceae [37, 38]. The annotation data that includes the prediction of exons and genes were also downloaded from the databases above. All the sequence and annotation files that have been used in this study are available from GDR http://www.rosaceae.org/BMC_rosaceae_Genome_paper. The whole genome sequences of peach and grape were masked for repeats using RepeatMasker , as well as the nmerge, WU-BLAST distribution, and faSoftMask distribution utilities of Mercator . Mercator identifies orthologous regions with one to one ortholgy relationships, rather than producing any syntenic regions in which one region can have many syntenic regions. Mercator employs BLAT-similar anchor pairs to identify orthologous segments in a modified k-way reciprocal best hit algorithm . Translated sequences of exons, provided by the annotation data, have been used as anchors in these analyses. Two exons from each genome were determined to be similar if the BLAT  score of the pair was below 1e -10. BLAT scores were computed in protein space. To select the optimal criteria to assess conservation of synteny between Rosaceous genomes, Mercator parameters were varied from between a minimum of 30 exons and a maximum distance of 300 kbp between exons, to a minimum of two exons and a maximum distance of 3 Mbp between exons. As the parameters become less stringent, we observed a sudden increase of the number of orthologous regions without the accompanying increase of the percent geonome coverage. Parameters selected for further analysis were a minimum of ten exons and a maximum distance of 300 kbp between exons as these parameters gave high percentage coverage within the genomes but reduced small-size syntenic regions that are potentially artefactual. With the exception of the analysis shown in Figure 1, the Malus genome was split into two arbitrary 'sub-genomes' based on the data of Velasco et al ; sub-genome 1 consisted of chromosomes 1, 2, 3, 4, 5, 8, 9, 13 and 14, whilst sub-genome 2 was composed of chromosomes 6, 7, 10, 11, 12, 15, 16 and 17 to use as an input for the Mercator program. This was done to detect orthologous regions in each of the homeologous Malus chromosomes. The anchored position of RosCOS markers in the peach genome were downloaded from GDR [37, 38]. RosCOS markers were anchored to orthologous regions when their anchored positions in peach belong to the corresponding positions of ORs.
Reconstruction of hypothetical ancestral genome
We used the Multiple Genome Rearrangements and Ancestors (MGRA) algorithm  to predict Contiguous Ancestral Regions (CARs) that existed in a common ancestor. The orthology map of Prunus, Fragaria and Vitis genomes, produced by Mercator, was used as an input for the MGRA program. The Vitis genome was included in the analysis as anoutgroup. The hypothetical ancestral genome was manually constructed using CARs generated from MGRA, as written in the Result and discussion section above.
Contiguous ancestral regions
Multiple genome rearrangements and ancestors
Rosaceous conserved orthologous sequences
Simple sequence repeat
Whole genome duplication.
We thank Colin Dewey (University of Wisconsin-Madison), Max Alekseyev (University of South Carolina), and Martin Krzywinski (Genome Sciences Center) for their advice on using programs, Mercator, MGRA and Circos, respectively. This project has been supported by the USDA NIFA SCRI grant # 2010-2010-03255. We acknowledge International Peach Genome Initiative for the permission to use the peach genome in this study.
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