Genetic signals of origin, spread, and introgression in a large sample of maize landraces.

The last two decades have seen important advances in our knowledge of maize domestication, thanks in part to the contributions of genetic data. Genetic studies have provided firm evidence that maize was domesticated from Balsas teosinte (Zea mays subspecies parviglumis), a wild relative that is endemic to the mid- to lowland regions of southwestern Mexico. An interesting paradox remains, however: Maize cultivars that are most closely related to Balsas teosinte are found mainly in the Mexican highlands where subspecies parviglumis does not grow. Genetic data thus point to primary diffusion of domesticated maize from the highlands rather than from the region of initial domestication. Recent archeological evidence for early lowland cultivation has been consistent with the genetics of domestication, leaving the issue of the ancestral position of highland maize unresolved. We used a new SNP dataset scored in a large number of accessions of both teosinte and maize to take a second look at the geography of the earliest cultivated maize. We found that gene flow between maize and its wild relatives meaningfully impacts our inference of geographic origins. By analyzing differentiation from inferred ancestral gene frequencies, we obtained results that are fully consistent with current ecological, archeological, and genetic data concerning the geography of early maize cultivation.

The genetic architecture of maize flowering time.

Flowering time is a complex trait that controls adaptation of plants to their local environment in the outcrossing species Zea mays (maize). We dissected variation for flowering time with a set of 5000 recombinant inbred lines (maize Nested Association Mapping population, NAM). Nearly a million plants were assayed in eight environments but showed no evidence for any single large-effect quantitative trait loci (QTLs). Instead, we identified evidence for numerous small-effect QTLs shared among families; however, allelic effects differ across founder lines. We identified no individual QTLs at which allelic effects are determined by geographic origin or large effects for epistasis or environmental interactions. Thus, a simple additive model accurately predicts flowering time for maize, in contrast to the genetic architecture observed in the selfing plant species rice and Arabidopsis.

Genetic properties of the maize nested association mapping population.

Maize genetic diversity has been used to understand the molecular basis of phenotypic variation and to improve agricultural efficiency and sustainability. We crossed 25 diverse inbred maize lines to the B73 reference line, capturing a total of 136,000 recombination events. Variation for recombination frequencies was observed among families, influenced by local (cis) genetic variation. We identified evidence for numerous minor single-locus effects but little two-locus linkage disequilibrium or segregation distortion, which indicated a limited role for genes with large effects and epistatic interactions on fitness. We observed excess residual heterozygosity in pericentromeric regions, which suggested that selection in inbred lines has been less efficient in these regions because of reduced recombination frequency. This implies that pericentromeric regions may contribute disproportionally to heterosis.

Use of selection with recurrent backcrossing and QTL mapping to identify loci contributing to southern leaf blight resistance in a highly resistant maize line.

B73 is a historically important maize line with excellent yield potential but high susceptibility to the foliar disease southern leaf blight (SLB). NC292 and NC330 are B73 near-isogenic lines (NILs) that are highly resistant to SLB. They were derived by repeated backcrossing of an elite source of SLB resistance (NC250P) to B73, with selection for SLB resistance among and within backcross families. The goal of this paper was to characterize the loci responsible for the increased SLB resistance of NC292 and NC330 and to determine how many of the SLB disease resistance quantitative trait loci (dQTL) were selected for in the development of NC292 and NC330. Genomic regions that differentiated NC292 and NC330 from B73 and which may contribute to NC292 and NC330s enhanced SLB resistance were identified. Ten NC250P-derived introgressions were identified in both the NC292 and NC330 genomes of which eight were shared between genomes. dQTL were mapped in two F(2:3) populations derived from lines very closely related to the original parents of NC292 and NC330--(B73rhm1 x NC250A and NC250A x B73). Nine SLB dQTL were mapped in the combined populations using combined SLB disease data over all locations (SLB AllLocs). Of these, four dQTL precisely colocalized with NC250P introgressions in bins 2.05-2.06, 3.03, 6.01, and 9.02 and three were identified near NC250P introgressions in bins 1.09, 5.05-5.06, and 10.03. Therefore the breeding program used to develop NC292 and NC330 was highly effective in selecting for multiple SLB resistance alleles.

Population structure and genetic diversity of New World maize races assessed by DNA microsatellites.

Because of the economic importance of maize and its scientific importance as a model system for studies of domestication, its evolutionary history is of general interest. We analyzed the population genetic structure of maize races by genotyping 964 individual plants, representing almost the entire set of ∼350 races native to the Americas, with 96 microsatellites. Using Bayesian clustering, we detected four main clusters consisting of highland Mexican, northern United States (US), tropical lowland, and Andean races. Phylogenetic analysis indicated that the southwestern US was an intermediary stepping stone between Mexico and the northern US. Furthermore, southeastern US races appear to be of mixed northern flint and tropical lowland ancestry, while lowland middle South American races are of mixed Andean and tropical lowland ancestry. Several cases of post-Columbian movement of races were detected, most notably from the US to South America. Of the four main clusters, the highest genetic diversity occurs in highland Mexican races, while diversity is lowest in the Andes and northern US. Isolation by distance appears to be the main factor underlying the historical diversification of maize. We identify highland Mexico and the Andes as potential sources of genetic diversity underrepresented among elite lines used in maize breeding programs.

Panzea: a database and resource for molecular and functional diversity in the maize genome.

Serving as a community resource, Panzea (http://www.panzea.org) is the bioinformatics arm of the Molecular and Functional Diversity in the Maize Genome project. Maize, a classical model for genetic studies, is an important crop species and also the most diverse crop species known. On average, two randomly chosen maize lines have one single-nucleotide polymorphism every approximately 100 bp; this divergence is roughly equivalent to the differences between humans and chimpanzees. This exceptional genotypic diversity underlies the phenotypic diversity maize needs to be cultivated in a wide range of environments. The Molecular and Functional Diversity in the Maize Genome project aims to understand how selection has shaped molecular diversity in maize and then relate molecular diversity to functional phenotypic variation. The project will screen 4000 loci for the signature of selection and create a wide range of maize and maize-teosinte mapping populations. These populations will be genotyped and phenotyped, permitting high-power and high-resolution dissection of the traits and relating the molecular diversity to functional variation. Panzea provides access to the genotype, phenotype and polymorphism data produced by the project through user-friendly web-based database searches and data retrieval/visualization tools, as well as a wide variety of information and services related to maize diversity.

Maize association population: a high-resolution platform for quantitative trait locus dissection.

Crop improvement and the dissection of complex genetic traits require germplasm diversity. Although this necessary phenotypic variability exists in diverse maize, most research is conducted using a small subset of inbred lines. An association population of 302 lines is now available--a valuable research tool that captures a large proportion of the alleles in cultivated maize. Provided that appropriate statistical models correcting for population structure are included, this tool can be used in association analyses to provide high-resolution evaluation of multiple alleles. This study describes the population structure of the 302 lines, and investigates the relationship between population structure and various measures of phenotypic and breeding value. On average, our estimates of population structure account for 9.3% of phenotypic variation, roughly equivalent to a major quantitative trait locus (QTL), with a high of 35%. Inclusion of population structure in association models is critical to meaningful analyses. This new association population has the potential to identify QTL with small effects, which will aid in dissecting complex traits and in planning future projects to exploit the rich diversity present in maize.

Dissection of maize kernel composition and starch production by candidate gene association.

Cereal starch production forms the basis of subsistence for much of the world's human and domesticated animal populations. Starch concentration and composition in the maize (Zea mays ssp mays) kernel are complex traits controlled by many genes. In this study, an association approach was used to evaluate six maize candidate genes involved in kernel starch biosynthesis: amylose extender1 (ae1), brittle endosperm2 (bt2), shrunken1 (sh1), sh2, sugary1, and waxy1. Major kernel composition traits, such as protein, oil, and starch concentration, were assessed as well as important starch composition quality traits, including pasting properties and amylose levels. Overall, bt2, sh1, and sh2 showed significant associations for kernel composition traits, whereas ae1 and sh2 showed significant associations for starch pasting properties. ae1 and sh1 both associated with amylose levels. Additionally, haplotype analysis of sh2 suggested this gene is involved in starch viscosity properties and amylose content. Despite starch concentration being only moderately heritable for this particular panel of diverse maize inbreds, high resolution was achieved when evaluating these starch candidate genes, and diverse alleles for breeding and further molecular analysis were identified.

Genetic structure and diversity among maize inbred lines as inferred from DNA microsatellites.

Two hundred and sixty maize inbred lines, representative of the genetic diversity among essentially all public lines of importance to temperate breeding and many important tropical and subtropical lines, were assayed for polymorphism at 94 microsatellite loci. The 2039 alleles identified served as raw data for estimating genetic structure and diversity. A model-based clustering analysis placed the inbred lines in five clusters that correspond to major breeding groups plus a set of lines showing evidence of mixed origins. A "phylogenetic" tree was constructed to further assess the genetic structure of maize inbreds, showing good agreement with the pedigree information and the cluster analysis. Tropical and subtropical inbreds possess a greater number of alleles and greater gene diversity than their temperate counterparts. The temperate Stiff Stalk lines are on average the most divergent from all other inbred groups. Comparison of diversity in equivalent samples of inbreds and open-pollinated landraces revealed that maize inbreds capture <80% of the alleles in the landraces, suggesting that landraces can provide additional genetic diversity for maize breeding. The contributions of four different segments of the landrace gene pool to each inbred group's gene pool were estimated using a novel likelihood-based model. The estimates are largely consistent with known histories of the inbreds and indicate that tropical highland germplasm is poorly represented in maize inbreds. Core sets of inbreds that capture maximal allelic richness were defined. These or similar core sets can be used for a variety of genetic applications in maize.

A single domestication for maize shown by multilocus microsatellite genotyping.

There exists extraordinary morphological and genetic diversity among the maize landraces that have been developed by pre-Columbian cultivators. To explain this high level of diversity in maize, several authors have proposed that maize landraces were the products of multiple independent domestications from their wild relative (teosinte). We present phylogenetic analyses based on 264 individual plants, each genotyped at 99 microsatellites, that challenge the multiple-origins hypothesis. Instead, our results indicate that all maize arose from a single domestication in southern Mexico about 9,000 years ago. Our analyses also indicate that the oldest surviving maize types are those of the Mexican highlands with maize spreading from this region over the Americas along two major paths. Our phylogenetic work is consistent with a model based on the archaeological record suggesting that maize diversified in the highlands of Mexico before spreading to the lowlands. We also found only modest evidence for postdomestication gene flow from teosinte into maize.