Maize as a model for the evolution of plant nuclear genomes

Abstract

The maize genome is replete with chromosomal duplications and repetitive DNA. The duplications resulted from an ancient polyploid event that occurred over 11 million years ago. Based on DNA sequence data, the polyploid event occurred after the divergence between sorghum and maize, and hence the polyploid event explains some of the difference in DNA content between these two species. Genomic rearrangement and diploidization followed the polyploid event. Most of the repetitive DNA in the maize genome is retrotransposable elements, and they comprise 50% of the genome. Retrotransposon multiplication has been relatively recent-within the last 5-6 million years-suggesting that the proliferation of retrotransposons has also contributed to differences in DNA content between sorghum and maize. There are still unanswered questions about repetitive DNA, including the distribution of repetitive DNA throughout the genome, the relative impacts of retrotransposons and chromosomal duplication in plant genome evolution, and the hypothesized correlation of duplication events with transposition. Population genetic processes also affect the evolution of genomes. We discuss how centromeric genes should, in theory, contain less genetic diversity than noncentromeric genes. In addition, studies of diversity in the wild relatives of maize indicate that different genes have different histories and also show that domestication and intensive breeding have had heterogeneous effects on genetic diversity across genes.

Figure 1

A phylogeny of diploid grass species. Numerical values next to species names represent the 2C genome content of the species, measured in picograms. The phylogeny and genome content information is taken from figure 1 of ref. . The arrows represent the hypothesized timing of evolutionary events.

Figure 2

A hypothesis for the origin of the maize genome (17). Under this hypothesis, Pennisetum and maize diverged ≈29 million years ago (mya), followed ≈9 million years later by the divergence of the two diploid progenitors of maize. Sorghum diverged from one of these progenitor lineages (≈16.5 mya) before the two diploid progenitors united to form allopolyploid maize. The polyploid event occurred sometime between 16.5 mya and 11.4 mya, with subsequent diploidization completed by 11.4 mya. Gray shading represents the period in which allotetraploidy and diploidization occurred.

Figure 3

The estimated insertion times of retrotransposons in the Adh1 region (49). Each gray box represents a retrotransposon. The horizontal line through the box is the estimate of insertion time, and the height of the box represents the standard deviation of the estimate. Arrows between boxes indicate the order of insertion. For example, Huck-2 inserted into Fourf ≈1 mya.

Figure 4

Genealogies of four genes, based on the neighbor-joining method (82) with Kimura 2-parameter distances (83). Taxa are abbreviated as follows: maize, domesticated maize; parv, ancestor of domesticated maize (Z. mays subsp. parviglumis); mex, Z. mays subsp. mexicana; lux, Zea luxurians; dip, Zea diploperennis; trip, Tripsacum dactyloides. Sequences from Z. luxurians are shown in bold. The data are from refs. and –. Scale bars indicate level of divergence among sequences; bootstrap values >80% are shown.