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.
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.
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Raven, P., Evert, R. & Eichhorn, S. Biology of Plants (Worth Publishers Inc., New York, 1992).
Paterson, A. et al. Convergent domestication of cereal crops by independent mutations at corresponding genetic loci. Science 269, 1714–1718 (1995).
Lin, Y., Schertz, K. & Paterson, A. Comparative analysis of QTLs affecting plant height and maturity across the Poaceae, in reference to an interspecific sorghum population. Genetics 141, 391–411 (1995).
Hu, F. Y. et al. Convergent evolution of perenniality in rice and sorghum. Proc. Natl Acad. Sci. USA 100, 4050–4054 (2003).
Clement, C. R. 1492 and the loss of Amazonian crop genetic resources. I. The relation between domestication and human population decline. Econ. Bot. 53, 188–202 (1999).
Kim, J. K. & Triplett, B. A. Cotton fiber growth in planta and in vitro. Models for plant cell elongation and cell wall biogenesis. Plant Physiol. 127, 1361–1366 (2001).
Vavilov, N. The law of homologous series in variation. J. Genet. 12, 1 (1922).
Tocchini-Valentini, G. D., Fruscoloni, P. & Tocchini-Valentini, G. P. Structure, function, and evolution of the tRNA endonucleases of Archaea: An example of subfunctionalization. Proc. Natl Acad. Sci. USA 102, 8933–8938 (2005).
Li, Z. K., Pinson, S. R. M., Park, W. D., Paterson, A. H. & Stansel, J. W. Epistasis for three grain yield components in rice (Oryza sativa L). Genetics 145, 453–465 (1997).
Li, Z. K. et al. Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics 158, 1737–1753 (2001).
Younghusband, F. The Epic of Mount Everest (E. P. Publishing, London, 1926).
Mitton, J. B. & Grant, M. C. Genetic variation and the natural history of quaking aspen. Bioscience 46, 25–31 (1996).
Lynch, A. J. J. & Balmer, J. The Ecology, phytosociology and stand structure of an ancient endemic plant, Lomatia tasmanica (Proteaceae), approaching extinction. Aust. J. Bot. 52, 619–627 (2004).
Blanc, G. & Wolfe, K. H. Widespread paleopolyploidy in model plant species inferred from age distributions of duplicate genes. Plant Cell 16, 1667–1678 (2004).
Lagercrantz, U. & Lydiate, D. J. Comparative genome mapping in Brassica. Genetics 144, 1903–1910 (1996).
Stankiewicz, P. & Lupski, J. R. Genome architecture, rearrangements and genomic disorders. Trends Genet. 18, 74–82 (2002).
Rong, J. et al. Comparative genomics of Gossypium and Arabidopsis: unraveling the consequences of both ancient and recent polyploidy. Genome Res. 15, 1198–1210 (2005).
Bowers, J. E. et al. Comparative physical mapping links retention of microsynteny to chromosome structure and recombination in grasses. Proc. Natl Acad. Sci. USA 102, 13206–13211 (2005).
Brown, A. H. D. Enzyme polymorphism in plant-populations. Theor. Popul. Biol. 15, 1–42 (1979).
Dehal, P. et al. The draft genome of Ciona intestinalis: insights into chordate and vertebrate origins. Science 298, 2157–2167 (2002).
Bennett, M. & Smith, J. Nuclear DNA amounts in angiosperms. Philos. Trans. R. Soc. Lond. B 334, 309–345 (1991).
Peterson, D. G., Wessler, S. R. & Paterson, A. H. Efficient capture of unique sequences from eukaryotic genomes. Trends Genet. 18, 547–550 (2002).
SanMiguel, P., Gaut, B. S., Tikhonov, A., Nakajima, Y. & Bennetzen, J. L. The paleontology of intergene retrotransposons of maize. Nature Genet. 20, 43–45 (1998).
Ming, R. et al. Detailed alignment of saccharum and sorghum chromosomes: comparative organization of closely related diploid and polyploid genomes. Genetics 150, 1663–1682 (1998).
Pfeiffer, T., Schrader, L. E. & Bingham, E. T. Physiological comparisons of isogenic diploid–tetraploid, tetraploid–octoploid alfalfa populations. Crop Sci. 20, 299–303 (1980).
Ming, R., Liu, S. C., Moore, P. H., Irvine, J. E. & Paterson, A. H. QTL analysis in a complex autopolyploid: genetic control of sugar content in sugarcane. Genome Res. 11, 2075–2084 (2001).
Bowers, J. E., Chapman, B. A., Rong, J. K. & Paterson, A. H. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events. Nature 422, 433–438 (2003). A synthesis of divergent approaches to the study of genome organization that clarified the evolutionary history of angiosperm chromosomes.
Haas B. J. et al. Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol. 3, research0029.1–research0029.12 (2002).
Kikuchi, S. et al. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science 301, 376–379 (2003).
Soares, M. B. et al. Construction and characterization of a normalized cDNA library. Proc. Natl Acad. Sci. USA 91, 9228–9232 (1994).
Rabinowicz, P. D. et al. Differential methylation of genes and retrotransposons facilitates shotgun sequencing of the maize genome. Nature Genet. 23, 305–308 (1999). An elegant primary demonstration of the merits of the methylation filtration approach.
Rabinowicz, P. D., McCombie, W. R. & Martienssen, R. A. Gene enrichment in plant genomic shotgun libraries. Curr. Opin. Plant Biol. 6, 150–156 (2003).
Peterson, D. G. et al. Integration of Cot analysis, DNA cloning, and high-throughput sequencing facilitates genome characterization and gene discovery. Genome Res. 12, 795–807 (2002). An elegant primary demonstration of the merits of the Cot-based cloning and sequencing approach.
Britten, R. J. & Kohne, D. E. Repeated Sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science 161, 529–540 (1968).
Goldberg, R. B. From Cot curves to genomics. How gene cloning established new concepts in plant biology. Plant Physiol. 125, 4–8 (2001).
Whitelaw, C. A. et al. Enrichment of gene-coding sequences in maize by genome filtration. Science 302, 2118–2120 (2003).
Kovalchuk, O. et al. Genome hypermethylation in Pinus silvestris of Chernobyl — a mechanism for radiation adaptation? Mutat. Res. 529, 13–20 (2003).
Meng, L., Bregitzer, P., Zhang, S. B. & Lemaux, P. G. Methylation of the exon/intron region in the Ubi1 promoter complex correlates with transgene silencing in barley. Plant Mol. Biol. 53, 327–340 (2003).
Baurens, F. C., Nicolleau, J., Legavre, T., Verdeil, J. L. & Monteuuis, O. Genomic DNA methylation of juvenile and mature Acacia mangium micropropagated in vitro with reference to leaf morphology as a phase change marker. Tree Physiol. 24, 401–407 (2004).
Yuan, Y. N., SanMiguel, P. J. & Bennetzen, J. L. High-Cot sequence analysis of the maize genome. Plant J. 34, 249–255 (2003).
Springer, N. M. & Barbazuk, W. B. Utility of different gene enrichment approaches toward identifying and sequencing the maize gene space. Plant Physiol. 136, 3023–3033 (2004). A particularly balanced comparison of methylation filtration and Cot-based cloning and sequencing in maize.
Lamoureux, D., Peterson, D. G., Li, W., Fellers, J. P. & Gill, B. S. The efficacy of Cot-based gene enrichment in wheat (Triticum aestivum L.). Genome 48, 1120–1126 (2005).
Fu, Y., Hsia, A. P., Guo, L. & Schnable, P. S. Types and frequencies of sequencing errors in methyl-filtered and high C(0)t maize genome survey sequences. Plant Physiol. 135, 2040–2045 (2004).
Wicker, T. et al. The repetitive landscape of the chicken genome. Genome Res. 15, 126–136 (2005).
Nelson, D. L. et al. Alu polymerase chain-reaction — a method for rapid isolation of human-specific sequences from complex DNA sources. Proc. Natl Acad. Sci. USA 86, 6686–6690 (1989).
Batzer, M. A. & Deininger, P. L. Alu repeats and human genomic diversity. Nature Rev. Genet. 3, 370–379 (2002).
Green, E. D. Strategies for the systematic sequencing of complex genomes. Nature Rev. Genet. 2, 573–583 (2001).
Collins, F. S., Lander, E. S., Rogers, J. & Waterston, R. H. Finishing the euchromatic sequence of the human genome. Nature 431, 931–945 (2004).
Marra, M. et al. High-throughput fingerprint analysis of large-insert clones. Genome Res. 7, 1072–1084 (1997).
Soderlund, C., Humphrey, S., Dunham, A. & French, L. Contigs built with fingerprints, markers and FPC V4.7. Genome Res. 10, 1772–1787 (2000).
Weiler, K. S. & Wakimoto, B. T. Heterochromatin and gene expression in Drosophila. Annu. Rev. Genet. 29, 577–605 (1995).
Copenhaver, G. P. et al. Genetic definition and sequence analysis of Arabidopsis centromeres. Science 286, 2468–2474 (1999).
Nagaki, K. et al. Sequencing of a rice centromere uncovers active genes. Nature Genetics 36, 138–145 (2004).
Zhang, Y. et al. Structural features of the rice chromosome 4 centromere. Nucleic Acids Res. 32, 2023–2030 (2004).
Jiang, N., Bao, Z. R., Zhang, X. Y., Eddy, S. R. & Wessler, S. R. Pack-MULE transposable elements mediate gene evolution in plants. Nature 431, 569–573 (2004).
Juretic, N., Hoen, D. R., Huynh, M. L., Harrison, P. M. & Bureau, T. E. The evolutionary fate of MULE-mediated duplications of host gene fragments in rice. Genome Res. 15, 1292–1297 (2005).
D'Ennequin, M. L. T., Toupance, B., Robert, T., Godelle, B. & Gouyon, P. Plant domestication: a model for studying the selection of linkage. J. Evol. Biol. 12, 1138–1147 (1999).
Paterson, A. H. What has QTL mapping taught us about plant domestication? New Phytologist 154, 591–608 (2002).
Johnson, M. E. et al. Positive selection of a gene family during the emergence of humans and African apes. Nature 413, 514–519 (2001).
Initiative, T. A. G. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408, 796–815 (2000).
Matsumoto, T. et al. The map-based sequence of the rice genome. Nature 436, 793–800 (2005).
Goff, S. A. et al. A draft sequence of the rice genome (Oryza sativa L. ssp japonica). Science 296, 92–100 (2002).
Yu, J. et al. A draft sequence of the rice genome (Oryza sativa L. ssp indica). Science 296, 79–92 (2002).
Yu, J. et al. The genomes of Oryza sativa: a history of duplications. PLoS Biol. 3, 266–281 (2005).
Gao, W. X. et al. Wide-cross whole-genome radiation hybrid mapping of cotton (Gossypium hirsutum L.). Genetics 167, 1317–1329 (2004).
Kynast, R. G. et al. Dissecting the maize genome by using chromosome addition and radiation hybrid lines. Proc. Natl Acad. Sci. USA 101, 9921–9926 (2004).
Aston, C., Mishra, B. & Schwartz, D. C. Optical mapping and its potential for large-scale sequencing projects. Trends Biotechnol. 17, 297–302 (1999).
Boffelli, D., Nobrega, M. A. & Rubin, E. M. Comparative genomics at the vertebrate extremes. Nature Rev. Genet. 5, 456–465 (2004).
Margulies, E. H. et al. An initial strategy for the systematic identification of functional elements in the human genome by low-redundancy comparative sequencing. Proc. Natl Acad. Sci. USA 102, 4795–4800 (2005). A detailed consideration of the phylogenetic shadowing approach.
Ohta, T. Slightly deleterious mutant substitutions in evolution. Nature 246, 96–98 (1973).
Bejerano, G. et al. Ultraconserved elements in the human genome. Science 304, 1321–1325 (2004).
Eddy, S. R. A model of the statistical power of comparative genome sequence analysis. PLoS Biol. 3, 95–102 (2005). Describes the theoretical underpinnings of the phylogenetic shadowing approach.
Soltis, D. E. et al. Missing links: the genetic architecture of flower and floral diversification. Trends Plant Sci. 7, 22–31 (2002).
Pryer, K. M., Schneider, H., Zimmer, E. A. & Banks, J. A. Deciding among green plants for whole genome studies. Trends Plant Sci. 7, 550–554 (2002).
Sanderson, M. J., Thorne, J. L., Wikstrom, N. & Bremer, K. Molecular evidence on plant divergence times. Am. J. Bot. 91, 1656–1665 (2004).
Bell, C. D., Soltis, D. E. & Soltis, P. S. The age of the angiosperms: a molecular timescale without a clock. Evolution 59, 1245–1258 (2005).
Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).
Lin, Y. et al. A Sorghum propinquum BAC library, suitable for cloning genes associated with loss-of-function mutations during crop domestication. Mol. Breed. 5, 511–520 (1999).
Sachidanandam, R. et al. A map of human genome sequence variation containing 1.42 million single nucleotide polymorphisms. Nature 409, 928–933 (2001).
Reich, D. E. et al. Human genome sequence variation and the influence of gene history, mutation and recombination. Nature Genet. 32, 135–142 (2002).
Hinds, D. A. et al. Whole-genome patterns of common DNA variation in three human populations. Science 307, 1072–1079 (2005).
Gabriel, S. B. et al. The structure of haplotype blocks in the human genome. Science 296, 2225–2229 (2002).
Ahmadi, K. R. et al. A single-nucleotide polymorphism tagging set for human drug metabolism and transport. Nature Genet. 37, 84–89 (2005).
Wright, S. I. et al. The effects of artificial selection of the maize genome. Science 308, 1310–1314 (2005).
Wang, R. L., Stec, A., Hey, J., Lukens, L. & Doebley, J. The limits of selection during maize domestication. Nature 398, 236–239 (1999).
Thornsberry, J. M. et al. Dwarf8 polymorphisms associate with variation in flowering time. Nature Genet. 28, 286–289 (2001). The seminal application of association genetics to the characterization of plant (maize) germplasm.
Gallavotti, A. et al. The role of barren stalk1 in the architecture of maize. Nature 432, 630–635 (2004).
Wang, H. et al. The origin of the naked grains of maize. Nature 436, 714–719 (2005).
Brown, A. H. D. Core collections — a practical approach to genetic-resources management. Genome 31, 818–824 (1989).
Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376–380 (2005).
Shendure, J. et al. Accurate multiplex polony sequencing of an evolved bacterial genome. Science 309, 1728–1732 (2005). References 90 and 91 describe next-generation DNA-sequencing technologies that promise further acceleration of sequence acquisition.
Gunderson, K. L., Steemers, F. J., Lee, G., Mendoza, L. G. & Chee, M. S. A genome-wide scalable SNP genotyping assay using microarray technology. Nature Genet. 37, 549–554 (2005). A particularly promising genotyping assay that seems to be scalable to transcriptome- or even genome-wide applications.
Koo, B., Pardey, P. & Wright, B. The price of conserving agricultural biodiversity. Nature Biotechnol. 21, 126–128 (2003).
Britten, R. J. & Davidson, E. H. Studies on nucleic-acid reassociation kinetics — empirical equations describing DNA reassociation. Proc. Natl Acad. Sci. USA 73, 415–419 (1976).
Pearson, W. R., Davidson, E. H. & Britten, R. J. Program for least-squares analysis of reassociation and hybridization data. Nucleic Acids Res. 4, 1727–1737 (1977).
Cech, T. R., Rosenfel. A & Hearst, J. E. Characterization of most rapidly renaturing sequences in mouse main-band DNA. J. Mol. Biol. 81, 299–325 (1973).
Klein, H. L. & Welch, S. K. Inverted repeated sequences in yeast nuclear-DNA. Nucleic Acids Res. 8, 4651–4669 (1980).
Paterson, A., Bowers, J., Peterson, D., Estill, J. & Chapman, B. Structure and evolution of cereal genomes. Curr. Opin. Genet. Devel. 13, 644–650 (2003).
Paterson, A. H., Bowers, J. E. & Chapman, B. A. Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl Acad. Sci. USA 101, 9903–9908 (2004).
Guyot, R. & Keller, B. Ancestral genome duplication in rice. Genome 47, 610–614 (2004).
Wang, X., Shi, X., Hao, B. L., Ge, S. & Luo, J. Duplication and DNA segmental loss in rice genome and their implications for diploidization. New Phytologist 165, 937–946 (2005).
Paterson, A. H., Bowers, J. E., Vandepoele, K. & Van de Peer, Y. Ancient duplication of cereal genomes. New Phytologist 165, 658–661 (2005).
Vandepoele, K., Simillion, C. & Van de Peer, Y. Evidence that rice and other cereals are ancient aneuploids. Plant Cell 15, 2192–2202 (2003).
Bedell, J. A. et al. Sorghum genome sequencing by methylation filtration. PLoS Biol. 3, 103–115 (2005).
Bowers, J. E. et al. A high-density genetic recombination map of sequence-tagged sites for sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses. Genetics 165, 367–386 (2003).
Messing, J. et al. Sequence composition and genome organization of maize. Proc. Natl Acad. Sci. USA 101, 14349–14354 (2004).
Bremer, K. et al. An ordinal classification for the families of flowering plants. Ann. Mo. Bot. Gard. 85, 531–553 (1998).
Soltis, D. E., Soltis, P. S., Endress, P. K. & Chase, M. W. Phylogeny and Evolution of Angiosperms (Sinauer Associates, Sunderland, Massachusetts, 2005).
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.
The author declares no competing financial interests.
The hereditary materials within a species.
Division of ancestral functions of a gene between duplicated copies of the original gene.
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.
Nonlinear interactions between independent genes that affect their impact on a phenotype.
An individual plant that is part of a clump of plants that are genetically identical to a single parent.
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.
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.
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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