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  • Review Article
  • Published:

Leafing through the genomes of our major crop plants: strategies for capturing unique information

Nature Reviews Genetics volume 7, pages 174–184 (2006)Cite this article

Key Points

  • Crop domestication ranks among the greatest of human achievements, and is closely correlated with human population growth and social evolution. Intensive directional selection that is applied during crop domestication and breeding has led to the rapid evolution of many extraordinary models for particular aspects of morphology and development.

  • The sequencing of the Arabidopsis thaliana genome and that of two Oryza subspecies foreshadowed new opportunities that could result from obtaining the complete genetic blueprints of our main crops.

  • Combining comprehensive sequence information with knowledge of the morphological and physiological diversity of angiosperms, and their well-understood phylogeny, will answer many questions about angiosperm genome evolution and function.

  • Because plant genome sizes vary over a range of at least 1,000-fold, the decision to sequence one is a complex equation that balances genome size with scientific, economic and social impact, phylogenetic distance from previously sequenced plants, the amount of relevant information that is available from previous studies and the persuasiveness of individual (or groups of) investigators.

  • Features of genome organization that differentiate plants from animals and/or microbes, such as autopolyploidy and an abundance of repetitive DNA, further complicate the sequencing equation.

  • With transcriptome coverage in many angiosperms above the ∼50% of genes beyond which the EST approach loses efficiency in revealing new genes, two new representational approaches — methyl filtration and Cot-based cloning and sequencing — show promise to further advance transcriptome coverage. They will also access information about introns and regulatory sequences from genomes for which complete sequencing is not yet justifiable.

  • In terms of the full sequencing of crop genomes, comparison of whole-genome shotgun and clone-based rice sequencing efforts highlights the controversy over the merits of these respective strategies. Both approaches are incorporated to varying degrees into the sequencing of at least eight other crop genomes that are in progress or have been scheduled for public sequencing efforts.

  • Many benefits of crop genome sequencing might be quickly realized by the use of 'phylogenetic shadowing' approaches. A 2× coverage of the high-complexity regions of 16 angiosperm genomes might provide the resolution that is required to detect conserved elements of as small as 8 nucleotides in most lineages, at a level of sequencing which is within the current annual capacity of some individual sequencing centres.

Abstract

Crop plants not only have economic significance, but also comprise important botanical models for evolution and development. This is reflected by the recent increase in the percentage of publicly available sequence data that are derived from angiosperms. Further genome sequencing of the major crop plants will offer new learning opportunities, but their large, repetitive, and often polyploid genomes present challenges. Reduced-representation approaches — such as EST sequencing, methyl filtration and Cot-based cloning and sequencing — provide increased efficiency in extracting key information from crop genomes without full-genome sequencing. Combining these methods with phylogenetically stratified sampling to allow comparative genomic approaches has the potential to further accelerate progress in angiosperm genomics.

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Figure 1: Long-term trends in angiosperm DNA-sequence generation.
Figure 2: Whole-genome shotgun versus clone-by-clone sequencing strategies.
Figure 3: A phylogenetic view of angiosperm sequencing projects.

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Acknowledgements

Thanks to J. Bowers, P. Brown, C. dePamphilis, J. Estill, J. Giovannoni, S. Kresovich, R. Mauricio, J. McNeal, C. Peterson, D. Peterson, J. Shaw, P. Soltis, H. Tang, S. Tanksley, N. Young and others for helpful data and discussions, and the US National Science Foundation, US Department of Agriculture, International Consortium for Sugarcane Biotechnology and US Golf Association for financial support.

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  1. Plant Genome Mapping Laboratory, University of Georgia, Athens, 30602, Georgia, USA

    Andrew H. Paterson

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  1. Andrew H. Paterson
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FURTHER INFORMATION

Consultative Group on International Agricultural Research

GenBank

Joint Genome Institute Community Sequencing Program — Sequencing Plans for 2006

Joint Genome Institute Populus trichocarpa sequencing project

Medicago truncatula sequencing resources

Multinational Brassica Genome Project

The International Tomato Sequencing Project

The Potato Genome Sequencing Consortium

The US Department of Agriculture Germplasm Resources Information Network

Glossary

Germplasm

The hereditary materials within a species.

Subfunctionalization

Division of ancestral functions of a gene between duplicated copies of the original gene.

Neofunctionalization

Evolution of new function(s) for a gene, which are thought to be made possible by duplication of the gene, with one copy retaining the ancestral function.

Epistasis

Nonlinear interactions between independent genes that affect their impact on a phenotype.

Ramet

An individual plant that is part of a clump of plants that are genetically identical to a single parent.

Genet

A set of individuals that are produced by asexual reproduction from a single zygote.

Sequence-tagged site

A genetic locus that is defined by unique sequence information.

Gene conversion

A meiotic process of directed change in which one allele directs the conversion of a partner allele to its own form, probably by repair of heteroduplex DNA.

Haplotype

The genetic constitution of an individual chromosome; this can refer to one locus or to an entire genome. A genome-wide haplotype would comprise half a diploid genome, including one allele from each allelic gene pair.

Minimum tiling path

A set of (usually large-insert) clones that collectively cover a genome, chromosome or target region, with a minimum of redundancy.

Radiation hybrid

A cell line that contains one or more chromosome segments from another species, which is generated by irradiation of cells from a target species, followed by fusion with normal cultured cells from a 'host' species. This allows the mapping of genes or other DNA sequences on the basis of similarities and differences in the ability of different cell lines to bind DNA probes from the target organism.

Chromosome-specific cell lines

Similar to radiation hybrids, these are generated by irradiation of cells from a target species, followed by fusion with normal cultured cells from a 'host' species. However, unlike radiation hybrids, they contain only one chromosome from the target organism. This allows mapping of genes or other DNA sequences on the basis of the binding of DNA probes from the target organism.

Optical mapping

Use of light microscopy to directly image individual DNA molecules, which are bound to specially derivatized surfaces and then cleaved by restriction enzymes.

Foldback DNA

When denatured, this DNA reassociates at a high rate that cannot be explained by bimolecular association. This is probably due to the presence on the same strand of palindromic elements that can self-anneal.

Parsimony

In systematics, parsimony refers to choosing the simplest explanation of the observed data. For example, which phylogenetic tree requires the fewest possible mutations to explain the data.

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Paterson, A. Leafing through the genomes of our major crop plants: strategies for capturing unique information. Nat Rev Genet 7, 174–184 (2006). https://doi.org/10.1038/nrg1806

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