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Grass Genome Evolution

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The grass family, which includes more than 10,000 species, is the single most important family in agriculture. Although relatively small compared with other flowering plant families, it surpasses all others in economic importance (maize, wheat, and rice alone account for a major portion of food calories consumed worldwide) and in ecological importance as well (grasses cover >20% of the earth's land surface and often dominate temperate and tropical habitats) (Gaut, 2002). The extent of genetic and genomic information available on several species, such as barley, wheat, maize, rice, and sorghum, which belong to different tribes in the grass family, has enabled some of the most comprehensive comparative genomics studies in plants. From an evolutionary standpoint, the grass family is fascinating because of the degree of variation found in overall size, ploidy level, and chromosome number. For example, bread wheat (Triticum aestivum) has a hexaploid genome (2n = 42) of 17 Gb and maize (Zea mays) a diploid genome (2n = 20) of 2.5 Gb, whereas diploid rice (Oryza sativa; 2n = 24) has a much smaller genome of 0.4 Gb (sizes refer to the haploid genome in each case). Unraveling the course of grass genome evolution from a common ancestor is a daunting task, but it is one that might also reveal common properties of eukaryotic genome evolution in general.

In this issue of The Plant Cell, Salse et al. (pages 11–24) provide a comprehensive analysis of intragenomic duplications and comparative synteny in rice and wheat. The authors propose that grass genomes have evolved from a common ancestor with a basic number of five chromosomes, which underwent a series of whole-genome and segmental duplications, chromosome fusions, and translocations to produce an intermediate ancestral cereal genome of 12 chromosomes.

Previous comparative genomic studies based on restriction fragment length polymorphism analyses showed that the rice genome could be divided into a series of genomic building blocks (linkage blocks) and that the chromosomes of other cereal grasses could be constructed from combinations of these same basic building blocks (reviewed in Devos 2005). This led to the conclusion that the rice genome likely is similar in structure to the ancestral grass genome. Various genomic analyses in rice, sorghum, and maize have suggested an ancestral whole-genome duplication predating the divergence of the different cereal genomes 77 million years ago (Paterson et al., 2004; Wang et al., 2005; Yu et al., 2005; Wei et al., 2007), but the structure and basic number of chromosomes of the ancestral genome has remained uncertain (Gaut, 2002).

Recently, Wei et al. (2007) investigated the origin of maize genomic structure and proposed a model for the evolution of the cereal genomes from an ancestor with a basic number of 12 chromosomes whose structure is similar to the rice genome. The work of Salse et al. provides additional support for this model of cereal evolution but further suggests that the 12 ancestral chromosomes themselves arose from duplications and rearrangements of a basic number of five chromosomes.

Salse et al. compared 42,654 rice gene sequences to 6426 mapped wheat ESTs using improved sequence alignment criteria and statistical analysis. This allowed the identification of duplications covering 70% of both the rice and wheat genomes. The authors then conducted a detailed analysis of the length, composition, and divergence time of these duplications and made comparisons with sorghum and maize. This led to a model of grass genome evolution from a common ancestor with a basic number of five chromosomes. The authors suggest that the common ancestor with n = 5 chromosomes underwent a whole-genome duplication that resulted in an n = 10 intermediate, followed by two interchromosomal translocations and fusions that led to the construction of two new chromosomes, resulting in the n = 12 intermediate ancestor that has been described previously (see figure ). As in the model proposed by Wei et al. (2007), rice has retained this intermediate ancestral chromosome number, whereas it has been reduced in the wheat, maize, and sorghum genomes, following a pattern that may be typical of plant chromosome evolution in general.

View larger version (20K): [in this window] [in a new window] [as a PowerPoint slide]   Model of Ancestral Grass Genome Evolution. A common ancestor with n = 5 chromosomes underwent a whole-genome duplication resulting in an n = 10 intermediate. This was followed by two interchromosomal translocations and fusions that led to the construction of two new chromosomes, resulting in an n = 12 intermediate ancestor. The five ancestral chromosomes are named according to rice nomenclature. The model presented by Salse et al. continues to propose how the genomes of rice, wheat, maize, and sorghum evolved from the n = 12 intermediate. (Adapted from Salse et al. [2008].)

The work of Salse et al. represents a substantial step forward in our understanding of cereal chromosome evolution because it reconciles previous observations and apparent inconsistencies that have been reported in individual grass genome studies. The authors note that additional genomic studies ultimately are needed in monocot species outside of the Poales to support conclusions about the ancestral species.

	Footnotes

 
www.plantcell.org/cgi/doi/10.1105/tpc.108.058586

	REFERENCES

TOP REFERENCES

 
Devos, K. (2005). Updating the ‘crop circle’. Curr. Opin. Plant Biol. 8: 155–162.[CrossRef][ISI][Medline]

Gaut, B.S. (2002). Evolutionary dynamics of grass genomes. New Phytol. 154: 15–28.[CrossRef][ISI]

Paterson, A.H., Bowers, J.E., and Chapman, B.A. (2004). Ancient polyploidization predating divergence of the cereals, and its consequences for comparative genomics. Proc. Natl. Acad. Sci. USA 101: 9903–9908.[Abstract/Free Full Text]

Salse, J., Bolot, S., Throude, M., Jouffe, V., Piegu, B., Quraishi, U.M., Calcagno, T., Cooke, R., Delseny, M., and Feuillet, C. (2008). Identification and characterization of shared duplications between rice and wheat provide new insight into grass genome evolution. Plant Cell 20: 11–24.[Abstract/Free Full Text]

Wang, X., Shi, X., Hao, B., Ge, S., and Luo, J. (2005). Duplication and DNA segmental loss in the rice genome: implications for diploidization. New Phytol. 165: 937–946.[CrossRef][ISI][Medline]

Wei, F., et al. (2007). Physical and genetic structure of the maize genome reflects its complex evolutionary history. PLoS Genet. 3: e123.[CrossRef][Medline]

Yu, J., et al. (2005). The genomes of Oryza sativa: A history of duplications. PLoS Biol. 3: 266–281.[CrossRef][ISI]

Related articles in Plant Cell:

Identification and Characterization of Shared Duplications between Rice and Wheat Provide New Insight into Grass Genome Evolution

Jérôme Salse, Stéphanie Bolot, Michaël Throude, Vincent Jouffe, Benoît Piegu, Umar Masood Quraishi, Thomas Calcagno, Richard Cooke, Michel Delseny, and Catherine Feuillet
Plant Cell 2008 20: 11-24. [Abstract] [Full Text]  

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