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Functional innovations of three chronological mesohexaploid Brassica rapa genomes.

Kim J, Lee J, Choi JP, Park I, Yang K, Kim MK, Lee YH, Nou IS, Kim DS, Min SR, Park SU, Kim H - BMC Genomics (2014)

Bottom Line: 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.Representative functions of the categorized genes were elucidated, providing better understanding of B. rapa evolution and the Brassica genus.

View Article: PubMed Central - PubMed

Affiliation: Korea Research Institute of Bioscience and Biotechnology (KRIBB), 125 Gwahangno, Yuseong-gu, Daejeon 305-806, Republic of Korea. kimhr@kribb.re.kr.

ABSTRACT

Background: 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.

Results: 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.

Conclusion: 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.

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GO slim analysis of fast evolving genes. A. Frequency of GO-slim terms. The x-axis represents GO-slim terms classified into the biological process (BP), cellular component (CC) and molecular function (MF) while the y-axis represents % of fast evolving genes assigned to specific GO-slim categories. B. GO-slim enrichment analysed by fisher’s exact test and p-values estimating fisher’s exact test under the description. The x-axis represents fold ratio between the frequency of fast evolving gene in recent or young genome categorized in certain GO-slim terms and background frequency (total B. rapa gene are not detected in fast evolving genes) in that term. The y-axis represents GO-slim terms. Different levels of p-value (< 0.05, < 0.01, < 0.001) are represented by *, **, ***, respectively.
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Fig4: GO slim analysis of fast evolving genes. A. Frequency of GO-slim terms. The x-axis represents GO-slim terms classified into the biological process (BP), cellular component (CC) and molecular function (MF) while the y-axis represents % of fast evolving genes assigned to specific GO-slim categories. B. GO-slim enrichment analysed by fisher’s exact test and p-values estimating fisher’s exact test under the description. The x-axis represents fold ratio between the frequency of fast evolving gene in recent or young genome categorized in certain GO-slim terms and background frequency (total B. rapa gene are not detected in fast evolving genes) in that term. The y-axis represents GO-slim terms. Different levels of p-value (< 0.05, < 0.01, < 0.001) are represented by *, **, ***, respectively.

Mentions: We selected fast evolving genes in the syntenic segments based on nucleotide substitution rates. A total of 636 fast evolving genes were identified from 265 syntenic segments by selecting genes with Ks values significantly higher than the average Ks value of their syntenic segments (p < 0.001). Among them 543 (85.38%) and 93 (14.62%) fast evolving genes were detected, from 181 recent and 84 young syntenic segments, respectively, whereas no fast evolving genes were identified in old syntenic segments (Additional file 3). The fast evolving genes were unevenly distributed throughout the B. rapa genome (Figure 3). In the “recent” genome, A03 chromosome had the highest number of fast evolving genes with 78 genes, while A04 had the lowest with 29 genes, not including scaffolds. In “young” genomes, A01 and A08 were the chromosomes with the most (17 genes) and the least (3 genes) fast evolving genes, respectively. The quantity of fast evolving genes in the 24 GBs were varied, with 1 (0.18% in “G”) – 67 (12.34% in “F”) genes/GB in recent blocks, and 0–11 (11.83% in “A”) genes/GB in young blocks (Additional file 3). No fast evolving genes were detected in the “G”, “L”, and “Q” GBs in the young genome. Only five genes were commonly identified as fast evolving genes in both the recent and young genomes. Fast evolving gene function was estimated using Gene Ontology (GO) annotation. A total of 631 fast evolving genes were assigned to GO terms in all hierarchies; 555 biological processes (BP), 244 molecular functions (MF) and 103 cellular components (CC) (Additional file 3). To simplify the presentation, GO terms were re-categorized into GO-slim terms. High proportions of fast evolving genes remained unknown (Figure 4A). Nevertheless, four BP-terms show moderate frequencies (>15%), ‘protein metabolism’ , ‘response to abiotic or biotic stimulus’ , ‘developmental process’ , and ‘cell organization and biogenesis.’ These genes function in ‘binding (to protein, DNA, RNA, nucleotide)’ , or as ‘enzymes (hydrolase, transferase, kinase)’ , and a small number of them are involved as ‘transporters’ or ‘receptors’ in MF-terms. In CC terms, fast evolving genes mainly localized at the ‘nucleus’ , ‘cytoplasmic’ , and ‘intracellular regions.’ To understand the representative functions of the fast evolving genes, an enrichment test was performed based on GO-slim. Despite many functions that remained unclear, several notable functions were identified such as ‘protein metabolism’ and ‘structural molecule activity’ (Figure 4B). The BP term ‘protein metabolism’ included ‘protein folding’ , ‘translation’ , ‘post-translational protein modification (myristoylation, phosphorylation, methylation, glycosylation, ubiquitination, dephosphorylation, deubiquitination, autophosphorylation)’ , ‘proteolysis’ , and ‘positive and negative regulation of serine/threonine kinase activity’. The ‘structural molecule activity’ MF terms contains ‘constituent of ribosome.’ Despite high frequencies of ‘stress’ and ‘biotic/abiotic response’ genes, terms such as ‘receptor binding/activity’ and ‘transporter’ , which facilitate the recognition and transportation of environmental signals, were observed at relatively lower frequencies in MF terms (Figure 4A). The term ‘plasma membrane’ , which indicates a recognition function, was not represented (Figure 4B).Figure 3


Functional innovations of three chronological mesohexaploid Brassica rapa genomes.

Kim J, Lee J, Choi JP, Park I, Yang K, Kim MK, Lee YH, Nou IS, Kim DS, Min SR, Park SU, Kim H - BMC Genomics (2014)

GO slim analysis of fast evolving genes. A. Frequency of GO-slim terms. The x-axis represents GO-slim terms classified into the biological process (BP), cellular component (CC) and molecular function (MF) while the y-axis represents % of fast evolving genes assigned to specific GO-slim categories. B. GO-slim enrichment analysed by fisher’s exact test and p-values estimating fisher’s exact test under the description. The x-axis represents fold ratio between the frequency of fast evolving gene in recent or young genome categorized in certain GO-slim terms and background frequency (total B. rapa gene are not detected in fast evolving genes) in that term. The y-axis represents GO-slim terms. Different levels of p-value (< 0.05, < 0.01, < 0.001) are represented by *, **, ***, respectively.
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4117954&req=5

Fig4: GO slim analysis of fast evolving genes. A. Frequency of GO-slim terms. The x-axis represents GO-slim terms classified into the biological process (BP), cellular component (CC) and molecular function (MF) while the y-axis represents % of fast evolving genes assigned to specific GO-slim categories. B. GO-slim enrichment analysed by fisher’s exact test and p-values estimating fisher’s exact test under the description. The x-axis represents fold ratio between the frequency of fast evolving gene in recent or young genome categorized in certain GO-slim terms and background frequency (total B. rapa gene are not detected in fast evolving genes) in that term. The y-axis represents GO-slim terms. Different levels of p-value (< 0.05, < 0.01, < 0.001) are represented by *, **, ***, respectively.
Mentions: We selected fast evolving genes in the syntenic segments based on nucleotide substitution rates. A total of 636 fast evolving genes were identified from 265 syntenic segments by selecting genes with Ks values significantly higher than the average Ks value of their syntenic segments (p < 0.001). Among them 543 (85.38%) and 93 (14.62%) fast evolving genes were detected, from 181 recent and 84 young syntenic segments, respectively, whereas no fast evolving genes were identified in old syntenic segments (Additional file 3). The fast evolving genes were unevenly distributed throughout the B. rapa genome (Figure 3). In the “recent” genome, A03 chromosome had the highest number of fast evolving genes with 78 genes, while A04 had the lowest with 29 genes, not including scaffolds. In “young” genomes, A01 and A08 were the chromosomes with the most (17 genes) and the least (3 genes) fast evolving genes, respectively. The quantity of fast evolving genes in the 24 GBs were varied, with 1 (0.18% in “G”) – 67 (12.34% in “F”) genes/GB in recent blocks, and 0–11 (11.83% in “A”) genes/GB in young blocks (Additional file 3). No fast evolving genes were detected in the “G”, “L”, and “Q” GBs in the young genome. Only five genes were commonly identified as fast evolving genes in both the recent and young genomes. Fast evolving gene function was estimated using Gene Ontology (GO) annotation. A total of 631 fast evolving genes were assigned to GO terms in all hierarchies; 555 biological processes (BP), 244 molecular functions (MF) and 103 cellular components (CC) (Additional file 3). To simplify the presentation, GO terms were re-categorized into GO-slim terms. High proportions of fast evolving genes remained unknown (Figure 4A). Nevertheless, four BP-terms show moderate frequencies (>15%), ‘protein metabolism’ , ‘response to abiotic or biotic stimulus’ , ‘developmental process’ , and ‘cell organization and biogenesis.’ These genes function in ‘binding (to protein, DNA, RNA, nucleotide)’ , or as ‘enzymes (hydrolase, transferase, kinase)’ , and a small number of them are involved as ‘transporters’ or ‘receptors’ in MF-terms. In CC terms, fast evolving genes mainly localized at the ‘nucleus’ , ‘cytoplasmic’ , and ‘intracellular regions.’ To understand the representative functions of the fast evolving genes, an enrichment test was performed based on GO-slim. Despite many functions that remained unclear, several notable functions were identified such as ‘protein metabolism’ and ‘structural molecule activity’ (Figure 4B). The BP term ‘protein metabolism’ included ‘protein folding’ , ‘translation’ , ‘post-translational protein modification (myristoylation, phosphorylation, methylation, glycosylation, ubiquitination, dephosphorylation, deubiquitination, autophosphorylation)’ , ‘proteolysis’ , and ‘positive and negative regulation of serine/threonine kinase activity’. The ‘structural molecule activity’ MF terms contains ‘constituent of ribosome.’ Despite high frequencies of ‘stress’ and ‘biotic/abiotic response’ genes, terms such as ‘receptor binding/activity’ and ‘transporter’ , which facilitate the recognition and transportation of environmental signals, were observed at relatively lower frequencies in MF terms (Figure 4A). The term ‘plasma membrane’ , which indicates a recognition function, was not represented (Figure 4B).Figure 3

Bottom Line: 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.Representative functions of the categorized genes were elucidated, providing better understanding of B. rapa evolution and the Brassica genus.

View Article: PubMed Central - PubMed

Affiliation: Korea Research Institute of Bioscience and Biotechnology (KRIBB), 125 Gwahangno, Yuseong-gu, Daejeon 305-806, Republic of Korea. kimhr@kribb.re.kr.

ABSTRACT

Background: 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.

Results: 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.

Conclusion: 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.

Show MeSH