Functional innovations of three chronological mesohexaploid Brassica rapa genomes
- Jungeun Kim†1, 2,
- Jeongyeo Lee†1,
- Jae-Pil Choi1,
- Inkyu Park1, 3,
- Kyungbong Yang1, 2,
- Min Keun Kim4,
- Young Han Lee4,
- Ill-Sup Nou5,
- Dae-Soo Kim1,
- Sung Ran Min1,
- Sang Un Park3 and
- HyeRan Kim1, 2Email author
© Kim et al.; licensee BioMed Central Ltd. 2014
Received: 25 February 2014
Accepted: 10 July 2014
Published: 18 July 2014
The Brassicaceae family is an exemplary model for studying plant polyploidy. The Brassicaceae knowledge-base includes the well-annotated Arabidopsis thaliana reference sequence; well-established evidence for three rounds of whole genome duplication (WGD); and the conservation of genomic structure, with 24 conserved genomic blocks (GBs). The recently released Brassica rapa draft genome provides an ideal opportunity to update our knowledge of the conserved genomic structures in Brassica, and to study evolutionary innovations of the mesohexaploid plant, B. rapa.
Three chronological B. rapa genomes (recent, young, and old) were reconstructed with sequence divergences, revealing a trace of recursive WGD events. A total of 636 fast evolving genes were unevenly distributed throughout the recent and young genomes. The representative Gene Ontology (GO) terms for these genes were ‘stress response’ and ‘development’ both through a change in protein modification or signaling, rather than by enhancing signal recognition. In retention patterns analysis, 98% of B. rapa genes were retained as collinear gene pairs; 77% of those were singly-retained in recent or young genomes resulting from death of the ancestral copies, while others were multi-retained as long retention genes. GO enrichments indicated that single retention genes mainly function in the interpretation of genetic information, whereas, multi-retention genes were biased toward signal response, especially regarding development and defense. In the recent genome, 13,302, 5,790, and 20 gene pairs were multi-retained following Brassica whole genome triplication (WGT) events with 2, 3, and 4 homoeologous copies, respectively. Enriched GO-slim terms from B. rapa homomoelogues imply that a major effect of the B. rapa WGT may have been to acquire environmental adaptability or to change the course of development. These homoeologues seem to more frequently undergo subfunctionalization with spatial expression patterns compared with other possible events including nonfunctionalization and neofunctionalization.
We refined Brassicaceae GB information using the latest genomic resources, and distinguished three chronologically ordered B. rapa genomes. B. rapa genes were categorized into fast evolving, single- and multi-retention genes, and long retention genes by their substitution rates and retention patterns. Representative functions of the categorized genes were elucidated, providing better understanding of B. rapa evolution and the Brassica genus.
KeywordsBrassica rapa Chronological genomes Fast-evolving genes Single-retention genes Multi-retention genes
The genus Brassica belongs to the Brassiceae tribe, Brassicaceae family, Brassicales order. The genus contains 38 species and several varieties, as well as numerous hybrids. The six major Brassica species are described by the “Triangle of U”: three diploid genomes of B. rapa (AA genome, 2n = 2x = 20), B. nigra (BB genome, 2n = 2x = 16), and B. oleracea (CC genome, 2n = 2x = 18), formed into the three amphidiploid plants B. juncea (AABB genome, 2n = 4x = 36), B. napus (AACC genome, 2n = 4x = 38), and B. carinata (BBCC genome, 2n = 4x = 34) through interspecific hybridization . Genomic orders are conserved between diploid and amphidiploid Brassica species according to marker-based studies [2–4]. Therefore, the construction of reference Brassica A, B, and C genomes provides a framework for many various Brassica species. The whole genome sequence (WGS) of Brassica A has been released with the B. rapa ssp. pekinensis line Chiifu-401-42  and the WGS of B. oleraceae (C genome) will be available in the near future . These valuable resources enable us to elucidate species identity as a consequence of whole genome triplication (WGT), to discover molecular markers useful in breeding, and to profile gene variants, all further enhancing our understanding of evolution within the group.
One of the more interesting outcomes of the increase in plant genomic research is the plethora of species expansion and diversification studies available. The polyploidy event, known as whole genome duplication (WGD), is a major contributor to genome evolution and species radiation through its ability to increase the odds of obtaining new functions in a genome [7–9]. The Brassicaceae (formerly Cruciferae) family is an exemplary model for studying polyploidy events because the well annotated Arabidopsis thaliana (A. thaliana) genome exists as a reference , with its well supported three rounds of WGD (At-α, At-β, and At-γ) . In addition, sub-classification of the Brassicaceae species is relatively clear for lineages I–III . The genus Brassica experienced an additional WGT around 13–17 million years ago (Mya) [13, 14]. The timing of this WGT makes Brassica an important model genus for evolutionary study because genomic collinearity among the species is maintained with their ancestral genome, a decisive factor in estimating ancestral genomes. The model plants, A. thaliana and B. rapa, belong to the core-Brassicaceae lineage I and II, respectively . Conservation of genomic structure from the Ancestral Crucifer Karyotype (ACK; n = 8) has been reported in Brassicaceae , and 24 conserved genomic blocks (GBs) based on A. thaliana loci have also been established . The common ancestor of lineage II in Brassicaceae (Proto-Calepineae Karyotype (PCK); n = 7) experienced chromosomal reduction . Additional translocation was also experienced translocation-PCK (tPCK) in several genera of the Brassicaceae lineage II, including the genus Brassica. Information about conserved GBs and their loci makes it easy to compare genomic structures as well as gene expansions related to Brassica diversity.
After WGD, a plant genome is reorganized via chromosomal rearrangements, excessive gene fractionation, and epigenetic changes [9, 19]. In Arabidopsis, 80 Mb and 33.2 Mb of the genome originated from recent (α-WGD), and from old (βγ-WGD) polyploidy events, respectively, according to a recent synonymous genomic blocks substitution analysis . After reorganization resulting from WGD, genomes preferentially retain genes or gene families [21–23]. In Arabidopsis these genes have been reported to be dosage sensitive and to be functionally involved in transcriptional and/or developmental regulation , biological networks and signal cascades [22, 24], as well as in protein complexes . Furthermore, longer retained genes contribute to species radiations by subfunctionalization or neofunctionalization after polyploidy . In the B. rapa genome multi-retained genes have been reported to be involved in environmental stress, hormone response, transcription factors (TFs), ribosome structure, cell wall, and cytoskeleton organization . Specifically, auxin-related gene families, which control a plant’s growth and morphological development, are over-retained in the B. rapa genome, which is an indicator that these genes are potential contributors to morphological diversification . Multi-retained genes possessing biased function are not specific to B. rapa, but are also common in other duplicated genomes . The innovative features of the B. rapa genome introduced by its recent WGT, and the major fate of those duplicated genes in the genome are not yet fully understood.
In this study we aim to refine GB information using the latest genomic data, and to distinguish the historic B. rapa genomes chronologically for further studies. Fast evolving and multi-retention genes have been elucidated, and genome innovations after the WGT event are discussed. This analysis will contribute to understanding B. rapa evolution in general, as well as suggest future experimental designs for studying Brassica diversity.
Reconstruction of three chronological B. rapagenomes with 24 refined genomic blocks
Classification of three chronological genomes by sequence divergence of the collinear gene pairs *
Syntenic segment information
No. of syntenic segments
No. of collinear protein pairs
Information of B. rapa genome segment
Size of genome segment
No. of integrated GBs
Average collinear gene pairs
No. of distinct A. thaliana genes
Reconstructed genomic blocks based on the synteny between A. thaliana and B. rapa
No of genes (%)
No of genes (%)
A total of 172 GBs were assigned to the recent genome, covering 250 Mb (98.69%) of the B. rapa genome by revealing 0.29 (“G” block) – 2.84 (“T” block) times of A. thaliana GB size (Additional file 2). There were 1,217 collinear gene pairs, preserving 53.48% of the Arabidopsis genome with collinearity (Table 1). The most conserved GB in terms of number of genes with collinearity was “R”, with 61.52% of the A. thaliana genes preserved in synteny, covering the A. thaliana “R” block 2.06 times. The B. rapa “G” block was the most fractionated, with 13.97% of the remaining collinear genes. The young genome was constructed with 203 Mb (79.24%) of B. rapa coverage, retaining 14.90% of A. thaliana collinear genes (Table 1). The most conserved and fractionated GBs in the young blocks were “A” and “Q” with 19.44% and 9.21% of A. thaliana genes, respectively (Additional file 2). The genomic block “G” was not detected in the young blocks. The old genome barely remained with 5.50 Mb of reconstructed blocks and 109 collinear gene pairs. The GB conservations were less intact in the older genome than in the younger genome, with 107, 37, and 10 collinear gene pairs per Mb in the recent, young, and old genomes, respectively (Table 1). Comparative analysis of GB arrangements in recent and young genomes showed that the “A”, “U”, and “F” GBs of the recent genome conservatively contained eight “O-V-J-I-C-D-L-K-E” blocks, eight “V-O-P-W-H-I-H-I” blocks, and seven “R-Q-R-W-R-C-T” block arrangements from the young genome, respectively (Figure 2). Three GBs (“H”, “K”, and “T”) in the recent genome consisted of only one GB (“U”, “A”, or “F”) from the young genome. The ancestral copies of the “G” block in the recent genome had been lost.
Fast evolving genes in B. rapagenome with recursive WGD
Functional bias according to gene retention patterns after recursive WGD
Classification of divergence time of B. rapa gene based on A. thaliana collinear pairs
Standard deviation of K s values
No. of B. rapaproteins (%)
Fate of homoeologues in the recent genome
Functional differentiation of the B. rapa homoeologues
Subfunctionalization of B. rapa genes involved in root and leaf developments
K a /K s
Absolute expression in A. thalianac
Extra-large G protein 3
Glycerophosphoryl diester phosphodiesterase-like protein (GDPD)
Auxin efflux carrier, root specific role
Germin-like protein 5 (GLP5)
flower, primary root, root, embryo, leaf, gynoecium, cotyledon,
Tryptophan aminotransferase of Arabidopsis 1 (TAA1)
root hair cell
Basic helix-loop-helix (bHLH)
root hair cell
seed, root, silique
root, seed, shoot, flower
RAN GTPase activating protein 2 (RANGAP2)
Lateral root primordium 1 (LRP1)
root, root cap, phloem, seedling
sepal, petal, senescent leaf
Regulatory particle AAA-ATPase 2A (RPT2A)
primary root, root
Response regulator 1 (RR1)
lateral root, leaf
sepal, senescent leaf
Protein phosphatase 2C like gene
root hair cell
Cysteine synthase isomer (CysC1)
PIN3, regulator of auxin efflux
Extra-large GTP-binding protein 2 (XLG2)
flower, lateral root, leaf
shoot, root flower,
Enhanced very-low-fluence responses 1 (EVE1)
lateral root, root
BRX, cell proliferation and elongation in the root
Cytosolic invertase 1
Proline-rich protein 3 (PRR3)
bHLH, root initiation
shoot, carpel, hypocotyl, flower
BDL, auxin-mediated processes
leaf, post-embryonic root, pollen
Multiubiquitin chain binding protein 1 (MCB1)
lateral root, stamen filament
IAA19, primary auxin-response genes
Plant invertase/pectin methylesterase inhibitor superfamily
Cycloidea and PCF transcription factor 2 (TCP2)
Extraction of three chronological genomic segments from the B. rapagenome
The mesohexaploid B. rapa genome underwent four rounds of polyploidy events after the diversification of the Eudicots . Three paleo-WGDs, known as At-γ, β, α events (in chronologic order) are shared with the entire core Brassicaceae family, whereas the last genome triplication is specific to the Brassica genus . Brassica WGT yielded three or six copies of genome colinearity in diploid and amphidiploid Brassica species, respectively [2–4, 26]. Advancements in next-generation sequencing (NGS) technology and bioinformatics analyses have increased the number of WGS projects for commercial and/or evolutionarily important plants. However, NGS based approaches often bias genome assembly toward gene rich regions, leaving most intergenic and repetitive regions unassembled . In this study, we used 283.8 Mb of B. rapa draft genome (several ‘N’s occur in unassembled regions and unanchored scaffolds), which covered 98% of gene space . This was of sufficient quality to allow our comparative analysis illuminating the effects of WGD/WGT events on Brassica gene and genome evolution. There must be some amount of gene loss and underestimation in our present data; however, that should not change the overall evidence leading to our conclusions. As a part of these studies, Cheng et al. (2013) showed that ten chromosomes of the B. rapa genome formed from an ancestral tPCK structure (n = 7), revealing one to three copies with GB associations conserved in the ancestral genome, and showing a trace of ancestral centromeres in the B. rapa genome . We rebuilt ancestral genomic segments based on the amount of synteny between A. thaliana and B. rapa, as measured by the average K s values of each syntenic segment (Figure 2). This was based on the assumption that genes in synteny should share similar substitution rates. These assessments clearly categorize syntenic segments into three chronologic classes: recent, young, and old genomes (Figure 1). The average K s value of the recent genomic segments (0.53; Table 1) indicate that the birth of the recent genome was concurrent with the split of A. thaliana and B. rapa (24–40 Mya) . The average K s value of young (1.16) and old (2.19) genomic segments in Brassica were similar to the paralogous gene sets in Arabidopsis recent (0.8–1 K s ) and old (2.0–2.2 K s ) segments . These values suggest that the birth of the young genome in Brassica is slightly older than the Arabidopsis recent polyploidy event, whereas the old Brassica genome is close in birth age to the old Arabidopsis polyploidy event (Table 1). Rare traces of the oldest paleo-WGD are explained by the broken collinearity resulting from recursive WGD and fractionation during 120 million years of evolutionary history after the emergence of the Eudicot plants .
Fast evolving genes may mediate stress response or development by changing protein metabolism
Genome-wide screening for fast evolving genes in plants has not been widely pursued. However, several proteins have been reported to belong to rapidly evolving gene families, including the nucleotide binding-leucine rich repeats (NB-LRRs) involved in plant resistance , and transcription factors (TFs) , as well as several protein-coding genes in plastids involved in RNA polymerase subunits and ribosomal proteins . In this study, a total of 636 potentially fast evolving genes were detected genome-wide. The distribution of the fast evolving genes was different among chronological genomes, chromosomes (Figure 3), and GBs (Additional file 3), suggesting a biased location of these genes. The fast evolving genes identified in our study had a high frequency of multi-retention suggesting that fast evolving genes may be affected by dosage-sensitive genes during recursive WGD events . Our GO terms and enrichment analysis of B. rapa fast evolving genes suggest that B. rapa has undergone positive evolution through rapid base substitution in these genes, enhancing environmental stress adaptability. The NB-LRR homologues in the whole-genome triplicated Brassica ancestor were deleted or lost quickly, and seem to have experienced species-specific amplification by tandem duplication [32, 33]. In our study, only three copies of NB-LRR genes were identified as fast evolving genes (Additional file 3) because tandem duplicated genes were filtered out based on our syntenic analysis criteria. Defense and developmental processes usually have three steps: recognition of signaling (biotic and abiotic stimulus for stress or hormones for development), signal transduction, and the expression of target genes. In our study, the GO-slim term ‘protein modification’ was enriched in fast evolving genes, and contained many sub-terms including the regulation of Ser/Thr signaling, effects on translation, and post-translational modifications enabling actual protein function (Figure 4B). These terms imply that defense and developmental processes may be enhanced in signaling levels and/or functional protein levels. Development and defense system signaling levels have been reported to be tightly linked . The results of our study suggest that stress response and developmental processes may have been enhanced by rapidly changing protein metabolism during the course of B. rapa evolution.
Evolutionary innovations of the recent B. rapagenome compared to its ancestral genome
We classified B. rapa genes into eight retention patterns (Table 3). The retention rates of B. rapa genes were similar to that of A. thaliana paralogs . The multiple collinear gene pairs in the recent and young genomes (Index 2) were older than genes specific to the recent genome with a higher standard deviation of K s values, although both gene sets were classified into the same category of recent genome. Based on this evidence, we estimated functional bias among seven patterns of gene sets in a step-wise manner, excluding genes with lost synteny (Index 5 in Table 3). The results of these analyses suggest that genes retained in specific chronological genomes (Indexes 1 and 6) were enriched with the function of genetic material interpretations, such as DNA/RNA/protein metabolism and transcription (Figure 5A). This functional bias was similar to the single retention genes of A. thaliana[24, 35]. However, genes with multiple synteny in different chronological genomes (Indexes 2–4) had frequent GO enrichments in ‘signal transducer’ or ‘transport’ mainly related to defense or development (Figure 5A), implying a more detailed process of adaptive evolution following WGD. Manual inspection of enriched GO terms mainly detected ‘development’ (Figure 5B) or ‘response to stimulus’ (Figure 5C) from the recent genome specific gene set. This data represented the functional innovative patterns following WGD or WGT events. Our study showed that the young genome was enriched with the GO-terms ‘reproductive structures (floral organs, seeds)’ , implying that reproductive organ development may be functionally diversified in the young genome . Interestingly, we observed that the GO terms ‘embryo’ and ‘embryo sac development’ were over-represented in genes specific to the recent genome, while ‘developments for vegetative tissues (leaf, root)’ were shared in two chronological genomes (Index 1 and 2). Embryos contain primordial tissue layers and drive morphogenetic diversity by regulating cell specification and cell-cell communication . Therefore, our GO enrichments cautiously suggest that the morphological diversity of B. rapa may be expanded during embryogenesis by concerted evolution. The specific GO enrichment patterns of signal response genes indicate that many pathogen (bacteria, fungi, and insects) or environmental stress (cold, heat, freezing, water deprivation) response genes were over-represented in both categories of Index 1 and 2 (Figure 5C), with duplicates continuously retained during recursive WGD events. Many phytohormones were also enriched in Index 2, which are important in regulating plant developments, as well as in defense by way of cross-talk signal transductions [34, 37, 38]. These retention patterns suggest that the B. rapa genome was more innovatively evolved to adapt to biotic/abiotic stress than to phytohormone stimuli.
Subfunctionalization is the primary fate of multi-retention genes in the recent genome
Functional diversification of surviving genes has been reported to be a major characteristic of long-term evolution in polyploids . Two times as many multi-retention genes were present in the B. rapa recent genome than there were in the A. thaliana recent genome, after the α-WGD event , in our study. There were 3.4 times as many two-copy retention genes than that of three copy retention genes. These results support the two-step theory of WGD events for the B. rapa mesohexaploid genome . GO functional annotation enrichments for single- and multi-retention gene sets were biased toward genetic control and the regulation of stress and/or development, respectively (Figure 6). In previous research duplicated genes were reported to acquire new functions via neofunctionalization or to alter their functions via subfunctionalization and pseudogenization . mRNA-Seq data have been published  providing tissue and developmental stage specific expression data, which enable us to study subfunctionalization for several developmental stages. We suggest that subfunctionalization is the major drive for the evolution of multi-retention genes (Table 4), because 34.27% of the homologues studied have spatially differentiated expression patterns, In previous research, 50% and 36–49% of homologous genes had undergone subfunctionalization in Glycine max and Triticum aestivum L., respectively [41, 42]. Comparatively lower distributions of B. rapa subfunctionalization were observed because of the limited number of the mRNA-Seq libraries used in this study. A. thaliana and B. rapa homoeologous gene expression patterns did not completely coincide in spite of their syntenic orthologous relationship (Table 5). Differences in expression patterns suggest a gain or alteration of function in duplicated B. rapa genes. Those genes, and/or their homologues, may have acquired new functions or altered their ancestral function after the Brassica WGT event. Several genes that we categorized as “dead” or “nonfunctionalization” classes could be expressed in other tissues or under specific conditions because of the dearth of public mRNA-seq data . Tissue-specific genes could be co-expressed in other tissues when expression conditions change. Our study shows a frequent subfunctionalization fate in duplicated genes, with small exceptions of nonfunctionalization via reciprocal gene loss after B. rapa WGD events. However, the mechanisms for gene loss, in both subfunctionalization and neofunctionalization, have not been fully resolved. Different duplicate retained gene expression levels were recently reported to be partially a result of epigenetic modifications such as methylation, histone modification, small RNAs, and transposable element genes (review in ). The patterns and processes driving gene retention and evolution in Brassica will be further elucidated through gene expression and function analysis, combined with epigenetic studies of the paralogous homologues.
Our interpretation of the B. rapa genome, based on sequence diversities, led to our construction of three chronological genomes. Furthermore, we identified fast evolving genes, and single- and multi-retention genes in the recent genome; long retention genes in young/old genomes; and three chronological genome specific genes. Both the fast evolving and the multi-retention genes were enriched with the GO terms ‘stress response’ and ‘development.’ However, detailed functions appeared to be related to the regulation of signal cascades and/or transport systems, rather than in recognition; while gene functions under ‘transcription and translation’ were highly enriched in recent or young genome specific gene sets. High numbers of multi-retention genes in the recent genome had undergone subfunctionalization, rather than neofunctionalization. The results of the present study will be useful in understanding innovative features of the B. rapa genome following Brassica WGT, and contribute to experimental design for studying Brassica diversity.
Construction of syntenic regions
We downloaded the model Brassicaceae plant A. thaliana’s genomics resource from The Arabidopsis Information Resource (TAIR, ver. 10) website (ftp://ftp.arabidopsis.org/Sequences/whole_chromosomes/), and the B. rapa genome from the BRAssica Database (BRAD, ftp://brassicadb.org/Bra_Chromosome_V1.2/). We identified all possible homologous proteins between A. thaliana and B. rapa using BLASTp, with a cut-off Expectation Value less than 1e-5, to build syntenic regions. After removing redundancies, the collinear gene-pairs within an adjacent 10 Kb were identified as syntenic segments using MCScan (ver. 0.8). MCScan is able to search for collinear protein pairs throughout a genome , and is downloaded from the Plant Genome Duplication Database (PGDD, http://chibba.agtec.uga.edu/duplication/mcscan/). The “mcl” algorithm in MCScan was used with the default parameters “--abc --abc-neg-log -abc-tf ‘mul (0.4343), ceil (200)’” to define syntenic segments.
Estimation of the levels of K s and K a
Protein sequences for each collinear protein pairs were aligned by clustalw2 and K s and K a were estimated using the maximum likelihood method in the PAML and PAL2NAL package [44, 45]. Finally, we applied the Yang-Nielson method.
Identification of fast evolving genes
where x i is K s for individual gene pairs in a syntenic block and is average Ks for a syntenic block. Z-score and its p-value were calculated with the scipy.stats module in the python package. We defined fast-evolving genes with a p-value less than 0.001.
GO enrichment analysis
GO terms for A. thaliana proteins were downloaded from TAIR web-site (ftp://ftp.arabidopsis.org/home/tair/Ontologies/Gene_Ontology/). GO and GO-Slim terms for B. rapa genes were assigned based on their A. thaliana syntenic counterpart. GO enrichments were analyzed by Fisher’s exact test (in the python module (ver.0.1.4)) specifying a p-value < 0.001 .
Identifying of B. rapahomoeologues and the fate of genes
Homologues were defined as those collinear gene pairs, as filtered by BLASTp and MCScan above, observed in both the B. rapa and A. thaliana genome. The fate of the B. rapa homologues was determined using gene expression pattern and sequence diversification rates compared to pivotal genes. To analyze gene expression patterns the mRNA-Seq data of B. rapa was downloaded from the BRAD database (http://brassicadb.org/brad/genomeDominanceData.php), including reads per kilobase of exon model per million mapped reads (RPKM) values as expression evidence from three tissues (leaf, root, and stem of B. rapa accession Chiifu-401-42), as well as two pooled mRNA libraries for B. rapa Chiifu-401-42, and a cultivar line L 58 . The genes with an RPKM value of “0” were defined as pseudo-genes without expression evidence. Based on RPKM, differentially expressed genes in specific libraries were analyzed using Audic’s test (p-value < 0.001) . Enrichment values were applied to define “subfunctionalization”. “Neofunctionalization” was defined as genes with K a /K s values larger than one.
This work was financially supported by grants from Cabbage Genomics assisted breeding supporting Center (CGC) research programs and Golden Seed Project (2013003-04-1-SB330) funded by the Ministry of Agriculture, Food and Rural Affairs, Republic of Korea.
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