Colloquium

Brandon S. Gaut^*, Maud Le Thierry d'Ennequin, Andrew S. Peek, and Mark C. Sawkins

Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697-2525

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.

Genomic technologies have produced a wealth of data on the organization and structure of genomes. These data range from extensive marker-based genetic maps to “chromosome paintings” based on fluorescent in situ hybridization to complete genomic DNA sequences. Although genomic approaches have changed the amount and type of data, the challenges of interpreting genomic data in an evolutionary context have changed little from the challenges faced by Stebbins (1) and the coauthors of the evolutionary synthesis. The challenges are to infer the mechanisms of evolution and to construct a comprehensive picture of evolutionary change.

In this paper, we will focus on the processes that contribute to the evolution of plant nuclear genomes by using maize (Zea mays) as a model system. In some respects, it is premature to discuss the evolution of plant genomes, because the pending completion of the Arabidopsis (Arabidopsis thaliana) genome, with rice (Oryza sativa) following, is sure to unlock many mysteries about plant genome evolution. However, it must be remembered that Arabidopsis and rice are being sequenced, precisely because their genomes are atypically small and stream-lined. Even after these genomes are sequenced, it will still be a tremendous challenge to understand the evolution of plant nuclear genomes, like the maize genome, for which entire DNA sequences will not be readily available.

Maize is a member of the grass family (Poaceae). The grasses represent a range of genome size and structural complexity, with rice on one extreme. A diploid with 12 chromosomes (2n = 24), rice has one of the smallest plant genomes, with only 0.9 pg of DNA per 2C nucleus (Fig. 1). Other grass species exhibit far larger genomes. Wheat, for example, is a hexaploid with 21 chromosomes (2n = 42) and a haploid DNA content of 33.1 pg (2). Genera like Saccharum (sugarcane) and Festuca are even more complicated, displaying wide variation in ploidy level and over 100 chromosomes in some species. As a diploid with 10 chromosomes (2n = 20) and a 2C genome content roughly 6-fold larger than rice, maize lies somewhere in the middle of grass genome size and structural complexity (Fig. 1).

Fig. 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.51. The arrows represent the hypothesized timing of evolutionary events.

This paper focuses on the impact of chromosomal duplication, transposition, and nucleotide substitution on the evolution of the maize genome. We will discuss chromosomal duplication and transposition separately and will pay particular attention to their effects on DNA content. Nucleotide substitution will be discussed in the context of genetic diversity. Patterns of genetic diversity provide insight into the population genetic processes that act on different regions of the genome and thus uncover the evolutionary forces that act on genomes. We focus on maize throughout the paper but also generalize to other species when appropriate.

An Ancient Polyploid Origin. The first hints of the complex organization of the maize genome came from cytological studies.