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Genomic compartments in barley

Nature volume 544, pages 424425 (27 April 2017) | Download Citation

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A high-quality barley genome reveals a surprising compartmentalization of genes and repetitive sequences in chromosomes. This advance paves the way for improved genetic optimization of cereals. See Article p.427

The produce of members of the plant tribe Triticeae can be enjoyed in many ways — as freshly baked bread, perfectly cooked spaghetti or a cool beer, for example. The Triticeae includes important cereal species such as barley, bread wheat, durum wheat and rye. But most Triticeae species have been unamenable to many of the modern molecular-breeding approaches routinely used for other crops, because their large genomes have prevented the production of high-quality DNA sequences that can be used as a reference for study. On page 427, Mascher et al.1 report the first high-quality reference sequence of barley (Hordeum vulgare). This genome will influence not only future work in barley, but research and breeding of cereals in general.

Barley was domesticated from wild relatives around 10,000 years ago2, and was a major food source in the Near East. Today, it is perhaps best known for its role in the production of beer and whisky, and it is also a valuable animal feed. Although genetic research on barley has accelerated in the past decade3, a reference sequence of long, contiguous stretches of barley DNA has been lacking.

Mascher and colleagues took a hierarchical approach to assembling the genome, which comes from a malting barley variety called Morex that is planted in spring. The authors started by sequencing circular DNA constructs called bacterial artificial chromosomes (BACs), which each contained a tiny portion of the barley genome. They assembled these pieces into larger fragments using an existing physical map of the genome3 that provides some information about the order in which the pieces lie.

In addition, the researchers used a sophisticated technique for analysing the 3D structures of chromosomes, which enabled them to deduce sequence orders and to orient the assembly on the basis of the physical proximity of each sequence to others4. This approach was validated in work on the human genome5, and last year was used to construct a new genome6 for the frog Xenopus laevis.

In total, the researchers assembled 4.79 gigabases of the estimated 5.1-gigabase-long genome. Furthermore, 95% of the assembled fragments were linearly ordered, with half of all sequences belonging to DNA pieces of 1.9 megabases or longer, which is more than 1,000 times longer than the pieces used to assemble the earlier, lower-quality barley sequence3. This allowed Mascher et al. to produce seven chromosome-like sequences, matching the number of barley chromosomes. The authors identified and mapped the locations of about 39,000 genes. Notably, these genes accounted for only 1.4% of the genome, whereas more than 80% consisted of repetitive sequences called transposable elements.

An analysis of genome composition revealed a striking pattern. In each chromosome, there were three types of compartment — distal, interstitial and proximal — that had distinct organizational and structural properties. There was an exponential increase in the number of genes towards the distal compartment at each chromosome end, along with an increase in the rate of recombination (the process by which genetic material is exchanged during sexual reproduction).

The distal compartments were enriched in rapidly evolving defence genes, whereas the proximal compartment towards the centre of each chromosome contained more 'housekeeping' genes, which regulate everyday cellular activities such as respiration and photosynthesis (Fig. 1). The authors also found that the genome's repetitive sequences were highly unevenly distributed, with different types of repeat being located at different positions on the chromosome, and only certain types being found close to genes. The interstitial compartments contained repeats that, evolutionarily, had been inserted in the genome more recently than those in the proximal region.

Figure 1: Partitioning a barley chromosome.
Figure 1

Mascher and colleagues' sequence of the barley genome1 reveals that each of the seven barley chromosomes is compartmentalized into three sections: distal, interstitial and proximal. The distal regions are enriched in rapidly evolving genes, such as those involved in defence. By contrast, the proximal regions are enriched in housekeeping genes, which control everyday cell function. Recombination (exchange of genetic information during sexual reproduction) occurs readily in distal regions, but not in the proximal compartment. Genes are clustered most densely in the distal regions on both the long and short chromosome arms, with density decreasing proximally. The density of repetitive DNA sequences shows the opposite arrangement. The interstitial regions have intermediate gene and repeat density.

It has been known for some time3 that the proximal chromosomal regions do not recombine, unlike other regions of the chromosome. Therefore, the genes in these regions are locked into large blocks that are rarely broken up or reshuffled in the breeding process. Confirming the distinctive evolutionary history of this part of the chromosome, transposable elements in this compartment were more ancient than those in the other regions, and had been eroded by the accumulation of many mutations.

A potential consequence of a lack of proximal DNA recombination is exemplified by the HvCEN gene, which regulates both the time of flowering and adaptation to geographical latitude. Mascher and colleagues showed that this gene is located in a large, non-recombining block. Breeders select plants carrying a specific form of the HvCEN gene that is ideal for spring barley, and therefore unwittingly select for all the other genes in the non-recombining region, even though they might be unfavourable. The authors' genome sheds light on the gene complement in this block, which should enable improved breeding efforts, including gene editing to replace unwanted forms of genes, or induced recombination. Such efforts could produce highly desirable new gene combinations.

This reference sequence — the largest high-quality genome available from any plant sequenced so far — is a game-changer for barley genetics and breeding. However, it should be complemented by information from other barley plants that have different genetic make-ups (genotypes). It is estimated that a single genotype of a given plant species contains only about 85% of all the genes present in the species as a whole7,8. To optimize breeding potential, more genotypes must be sequenced at high quality. In addition to their reference sequence, Mascher et al. generated partial sequences of 96 high-yielding barley lines, which together demonstrate serious erosion of genetic diversity among modern barley varieties. This is essential new information for barley breeders, who should now redesign breeding strategies to increase diversity.

The barley reference genome will also boost basic research in cereals. Large collections of mutant barley plants exist, but have been mostly unstudied, because lack of access to the barley genome made it hard to identify the genes that cause trait changes. Such collections will now become accessible to rapid gene identification9,10. Furthermore, comparative analysis with species such as durum wheat, bread wheat and rye will open up exciting opportunities to better understand crop-specific biology and to study genome and chromosome evolution. Finally, an informed use of the barley genome, combined with the establishment of CRISPR–Cas9 gene-editing technology in barley11, will allow sophisticated breeding interventions that should help to improve traits such as grain quality and resistance to pests and diseases, giving a boost to this valuable crop.

Notes

References

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    The International Barley Genome Sequencing Consortium. Nature 491, 711–717 (2012).

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    et al. Sci. Data 4, 170044 (2017).

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    et al. Nature Biotechnol. 31, 1119–1125 (2013).

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    et al. Nature 538, 336–343 (2016).

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    et al. Plant Cell 26, 121–135 (2014).

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    The 1001 Genomes Consortium. Cell 166, 481–491 (2016).

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    et al. Plant Physiol. 155, 617–627 (2011).

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  1. Beat Keller and Simon G. Krattinger are in the Department of Plant and Microbial Biology, University of Zurich, CH-8008 Zurich, Switzerland.

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    •  & Simon G. Krattinger

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Correspondence to Beat Keller or Simon G. Krattinger.

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