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The physical map of wheat chromosome 5DS revealed gene duplications and small rearrangements.

Akpinar BA, Magni F, Yuce M, Lucas SJ, Šimková H, Šafář J, Vautrin S, Bergès H, Cattonaro F, Doležel J, Budak H - BMC Genomics (2015)

Bottom Line: Analysis of the gene space of 5DS suggested an increasing gradient of genes organized in islands towards the telomere, with the highest gene density of 5.17 genes/Mb in the 0.67-0.78 deletion bin, 1.4 to 1.6 times that of all other bins.Here, we provide a chromosome-specific view into the organization and evolution of the D genome of bread wheat, in comparison to one of its ancestors, revealing recent genome rearrangements.The high-quality physical map constructed in this study paves the way for the assembly of a reference sequence, from which breeding efforts will greatly benefit.

View Article: PubMed Central - PubMed

Affiliation: Sabanci University Nanotechnology Research and Application Centre (SUNUM), Sabanci University, Universite Cad. Orta Mah. No: 27, Tuzla, 34956, Istanbul, Turkey. balaani@sabanciuniv.edu.

ABSTRACT

Background: The substantially large bread wheat genome, organized into highly similar three sub-genomes, renders genomic research challenging. The construction of BAC-based physical maps of individual chromosomes reduces the complexity of this allohexaploid genome, enables elucidation of gene space and evolutionary relationships, provides tools for map-based cloning, and serves as a framework for reference sequencing efforts. In this study, we constructed the first comprehensive physical map of wheat chromosome arm 5DS, thereby exploring its gene space organization and evolution.

Results: The physical map of 5DS was comprised of 164 contigs, of which 45 were organized into 21 supercontigs, covering 176 Mb with an N50 value of 2,173 kb. Fifty-eight of the contigs were larger than 1 Mb, with the largest contig spanning 6,649 kb. A total of 1,864 molecular markers were assigned to the map at a density of 10.5 markers/Mb, anchoring 100 of the 120 contigs (>5 clones) that constitute ~95 % of the cumulative length of the map. Ordering of 80 contigs along the deletion bins of chromosome arm 5DS revealed small-scale breaks in syntenic blocks. Analysis of the gene space of 5DS suggested an increasing gradient of genes organized in islands towards the telomere, with the highest gene density of 5.17 genes/Mb in the 0.67-0.78 deletion bin, 1.4 to 1.6 times that of all other bins.

Conclusions: Here, we provide a chromosome-specific view into the organization and evolution of the D genome of bread wheat, in comparison to one of its ancestors, revealing recent genome rearrangements. The high-quality physical map constructed in this study paves the way for the assembly of a reference sequence, from which breeding efforts will greatly benefit.

No MeSH data available.


Related in: MedlinePlus

Blast2GO statistics and annotations for the syntenic read probes. a Top BLAST-hit species, x-axis species name, y-axis number of BLAST hits. b, c, d Blast2GO annotations for Biological Process, Molecular Function and Cellular Component, respectively
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Fig9: Blast2GO statistics and annotations for the syntenic read probes. a Top BLAST-hit species, x-axis species name, y-axis number of BLAST hits. b, c, d Blast2GO annotations for Biological Process, Molecular Function and Cellular Component, respectively

Mentions: To further explore the 5DS gene space, conserved read probes hybridizing to MTP clones were functionally assessed. Of the total 6,996 such probes, 1,306 giving positive signals under high stringency (see Materials and Methods) were annotated using the Blast2GO tool [42]. The remaining probes may have been eliminated due to the stringency measures applied to hybridization results or may have been located on singleton clones which were not included in the microarray experiments. Functional annotations of these conserved read probes gave insights into the gene space of 5DS (Fig. 9). Interestingly, the sequence comparison of the positive conserved probes to non-redundant Viridiplantae proteins yielded the most BLAST hits in Aegilops tauschii followed by Triticum urartu (Fig. 9a). This implies that, on the basis of the conserved microarray probes hybridizing to 5DS MTP clones, the 5DS chromosome arm shares extensive similarity with the D genome of Ae. tauschii. The relatively recent hybridization of Ae. tauschii with the AABB progenitor, giving rise to the hexaploid genome of Triticum aestivum, has allowed only restricted inter-chromosomal recombination compared to the A and B-genomes. This may explain why the majority of the syntenic probes on 5DS map yielded extensive homology to no species other than its ancestor, Ae. tauschii. There were also significant matches with the completely annotated proteomes of Oryza sativa and Brachypodium distachyon that emphasize the close evolutionary relationships among grasses. The GO terms assigned for Biological Process (BP), Molecular Function (MF) and Cellular Component (CC) terms revealed a range of processes, functions and locations mostly consistent with the annotations obtained from survey sequences generated from the whole of chromosome 5D [25]. BP terms for probes in conserved genes were enriched for transport, catabolic process and protein modification, among others (Fig. 9b). The 5DS gene space is likely to contribute to several processes to similar extents, rather than specializing on one or a few processes. In the case of MF terms, however, three functions appeared to dominate others. Nucleotide binding, hydrolase activity and kinase activity, together accounted for over 60 % of all MF terms (Fig. 9c). Intriguingly, hydrolase activity was also prominent in the secretome of an apple pathogen Venturia inaequalis closely related to the wheat pathogen Pyrenophora tritici-repentis [43] and was also central to the transcriptome of the wheat pest Heterodera avenae [44]. While the prominence of the hydrolase activity term among the probes may be reflected in the ‘catabolic process’ BP term (Fig. 9b), which accounts for a considerable portion of all BP term annotations, it could also be related to defense mechanisms, though in a general sense rather than specialized stress-response activities. From this perspective, genes involved in hydrolysis-related processes may be enriched on 5DS chromosome arm. CC terms revealed a higher than expected contribution of sequences to be related to the plastid or mitochondrion, which is also intriguing (Fig. 9d). As these organelles possess their own genetic material, it is tempting to speculate that 5DS was involved in the transfer of genes from the organellar DNA to the nucleus [45]. Considering that photosynthesis or energy-related process did not dominate BP terms, the large contribution of these organelles to CC terms is curious. Overall, while BP terms did not point to a specific process to which 5DS contributes to, the weighting of MF and CC terms may suggest that this chromosome arm includes families of genes devoted to carry out similar and specific functions, which would be consistent with the transcriptional autonomy of sub-genomes without the genome-wide dominance of one sub-genome over others [6].Fig. 9


The physical map of wheat chromosome 5DS revealed gene duplications and small rearrangements.

Akpinar BA, Magni F, Yuce M, Lucas SJ, Šimková H, Šafář J, Vautrin S, Bergès H, Cattonaro F, Doležel J, Budak H - BMC Genomics (2015)

Blast2GO statistics and annotations for the syntenic read probes. a Top BLAST-hit species, x-axis species name, y-axis number of BLAST hits. b, c, d Blast2GO annotations for Biological Process, Molecular Function and Cellular Component, respectively
© Copyright Policy - open-access
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4465308&req=5

Fig9: Blast2GO statistics and annotations for the syntenic read probes. a Top BLAST-hit species, x-axis species name, y-axis number of BLAST hits. b, c, d Blast2GO annotations for Biological Process, Molecular Function and Cellular Component, respectively
Mentions: To further explore the 5DS gene space, conserved read probes hybridizing to MTP clones were functionally assessed. Of the total 6,996 such probes, 1,306 giving positive signals under high stringency (see Materials and Methods) were annotated using the Blast2GO tool [42]. The remaining probes may have been eliminated due to the stringency measures applied to hybridization results or may have been located on singleton clones which were not included in the microarray experiments. Functional annotations of these conserved read probes gave insights into the gene space of 5DS (Fig. 9). Interestingly, the sequence comparison of the positive conserved probes to non-redundant Viridiplantae proteins yielded the most BLAST hits in Aegilops tauschii followed by Triticum urartu (Fig. 9a). This implies that, on the basis of the conserved microarray probes hybridizing to 5DS MTP clones, the 5DS chromosome arm shares extensive similarity with the D genome of Ae. tauschii. The relatively recent hybridization of Ae. tauschii with the AABB progenitor, giving rise to the hexaploid genome of Triticum aestivum, has allowed only restricted inter-chromosomal recombination compared to the A and B-genomes. This may explain why the majority of the syntenic probes on 5DS map yielded extensive homology to no species other than its ancestor, Ae. tauschii. There were also significant matches with the completely annotated proteomes of Oryza sativa and Brachypodium distachyon that emphasize the close evolutionary relationships among grasses. The GO terms assigned for Biological Process (BP), Molecular Function (MF) and Cellular Component (CC) terms revealed a range of processes, functions and locations mostly consistent with the annotations obtained from survey sequences generated from the whole of chromosome 5D [25]. BP terms for probes in conserved genes were enriched for transport, catabolic process and protein modification, among others (Fig. 9b). The 5DS gene space is likely to contribute to several processes to similar extents, rather than specializing on one or a few processes. In the case of MF terms, however, three functions appeared to dominate others. Nucleotide binding, hydrolase activity and kinase activity, together accounted for over 60 % of all MF terms (Fig. 9c). Intriguingly, hydrolase activity was also prominent in the secretome of an apple pathogen Venturia inaequalis closely related to the wheat pathogen Pyrenophora tritici-repentis [43] and was also central to the transcriptome of the wheat pest Heterodera avenae [44]. While the prominence of the hydrolase activity term among the probes may be reflected in the ‘catabolic process’ BP term (Fig. 9b), which accounts for a considerable portion of all BP term annotations, it could also be related to defense mechanisms, though in a general sense rather than specialized stress-response activities. From this perspective, genes involved in hydrolysis-related processes may be enriched on 5DS chromosome arm. CC terms revealed a higher than expected contribution of sequences to be related to the plastid or mitochondrion, which is also intriguing (Fig. 9d). As these organelles possess their own genetic material, it is tempting to speculate that 5DS was involved in the transfer of genes from the organellar DNA to the nucleus [45]. Considering that photosynthesis or energy-related process did not dominate BP terms, the large contribution of these organelles to CC terms is curious. Overall, while BP terms did not point to a specific process to which 5DS contributes to, the weighting of MF and CC terms may suggest that this chromosome arm includes families of genes devoted to carry out similar and specific functions, which would be consistent with the transcriptional autonomy of sub-genomes without the genome-wide dominance of one sub-genome over others [6].Fig. 9

Bottom Line: Analysis of the gene space of 5DS suggested an increasing gradient of genes organized in islands towards the telomere, with the highest gene density of 5.17 genes/Mb in the 0.67-0.78 deletion bin, 1.4 to 1.6 times that of all other bins.Here, we provide a chromosome-specific view into the organization and evolution of the D genome of bread wheat, in comparison to one of its ancestors, revealing recent genome rearrangements.The high-quality physical map constructed in this study paves the way for the assembly of a reference sequence, from which breeding efforts will greatly benefit.

View Article: PubMed Central - PubMed

Affiliation: Sabanci University Nanotechnology Research and Application Centre (SUNUM), Sabanci University, Universite Cad. Orta Mah. No: 27, Tuzla, 34956, Istanbul, Turkey. balaani@sabanciuniv.edu.

ABSTRACT

Background: The substantially large bread wheat genome, organized into highly similar three sub-genomes, renders genomic research challenging. The construction of BAC-based physical maps of individual chromosomes reduces the complexity of this allohexaploid genome, enables elucidation of gene space and evolutionary relationships, provides tools for map-based cloning, and serves as a framework for reference sequencing efforts. In this study, we constructed the first comprehensive physical map of wheat chromosome arm 5DS, thereby exploring its gene space organization and evolution.

Results: The physical map of 5DS was comprised of 164 contigs, of which 45 were organized into 21 supercontigs, covering 176 Mb with an N50 value of 2,173 kb. Fifty-eight of the contigs were larger than 1 Mb, with the largest contig spanning 6,649 kb. A total of 1,864 molecular markers were assigned to the map at a density of 10.5 markers/Mb, anchoring 100 of the 120 contigs (>5 clones) that constitute ~95 % of the cumulative length of the map. Ordering of 80 contigs along the deletion bins of chromosome arm 5DS revealed small-scale breaks in syntenic blocks. Analysis of the gene space of 5DS suggested an increasing gradient of genes organized in islands towards the telomere, with the highest gene density of 5.17 genes/Mb in the 0.67-0.78 deletion bin, 1.4 to 1.6 times that of all other bins.

Conclusions: Here, we provide a chromosome-specific view into the organization and evolution of the D genome of bread wheat, in comparison to one of its ancestors, revealing recent genome rearrangements. The high-quality physical map constructed in this study paves the way for the assembly of a reference sequence, from which breeding efforts will greatly benefit.

No MeSH data available.


Related in: MedlinePlus