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.
There exists extraordinary morphological and genetic diversity among the maize landraces that have been developed by preColumbian 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.
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.
Association studies based on linkage disequilibrium (LD) can provide high resolution for identifying genes that may contribute to phenotypic variation. We report patterns of local and genomewide LD in 102 maize inbred lines representing much of the worldwide genetic diversity used in maize breeding, and address its implications for association studies in maize. In a survey of six genes, we found that intragenic LD generally declined rapidly with distance (r 2 < 0.1 within 1500 bp), but rates of decline were highly variable among genes. This rapid decline probably reflects large effective population sizes in maize during its evolution and high levels of recombination within genes. A set of 47 simple sequence repeat (SSR) loci showed stronger evidence of genome-wide LD than did single-nucleotide polymorphisms (SNPs) in candidate genes. LD was greatly reduced but not eliminated by grouping lines into three empirically determined subpopulations. SSR data also supplied evidence that divergent artificial selection on flowering time may have played a role in generating population structure. Provided the effects of population structure are effectively controlled, this research suggests that association studies show great promise for identifying the genetic basis of important traits in maize with very high resolution. In plant genetic studies, recombinant inbred lines have been very successful for mapping quantitative trait loci (QTLs) to 10-30 cM regions (1, 2), but association studies based on linkage disequilibrium (LD) may allow identification of the actual genes represented by QTLs. Only polymorphisms with extremely tight linkage to a locus with phenotypic effects are likely to be significantly associated with the trait in a randomly mating population, providing much finer resolution than genetic mapping. Association methods have been especially important for studying the genetic basis of human diseases, for which controlled genetic experiments are not feasible. However, these methods also have great potential for resolving individual genes responsible for QTLs (3-5).The resolution of association studies in a test sample depends on the structure of LD across the genome. LD, or the correlation between alleles at different sites, is generally dependent on the history of recombination between polymorphisms. However, factors such as genetic drift, selection within populations, and population admixture can also cause LD between markers and traits. [Following common practice (6, 7), we refer to gametic phase disequilibrium as LD whether or not it is caused by linkage.] Because many factors affect LD, its genomic structure in particular crop plants must be empirically determined before association studies can be applied. In maize, for example, divergent selection for adaptive traits such as time of maturation in different regions may have created LD among chromosomal regions containing major genes for these traits.Our goal in this study was to evaluate patterns of LD among 102 maize inbred lines representing the diversity ...
SummaryCrop 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.
Historically, association tests have been used extensively in medical genetics, but have had virtually no application in plant genetics. One obstacle to their application is the structured populations often found in crop plants, which may lead to nonfunctional, spurious associations. In this study, statistical methods to account for population structure were extended for use with quantitative variation and applied to our evaluation of maize flowering time. Mutagenesis and quantitative trait locus (QTL) studies suggested that the maize gene Dwarf8 might affect the quantitative variation of maize flowering time and plant height. The wheat orthologs of this gene contributed to the increased yields seen in the 'Green Revolution' varieties. We used association approaches to evaluate Dwarf8 sequence polymorphisms from 92 maize inbred lines. Population structure was estimated using a Bayesian analysis of 141 simple sequence repeat (SSR) loci. Our results indicate that a suite of polymorphisms associate with differences in flowering time, which include a deletion that may alter a key domain in the coding region. The distribution of nonsynonymous polymorphisms suggests that Dwarf8 has been a target of selection.
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.T he geography of origins and diversification of agricultural species has important implications for unraveling the ecological context of Neolithic societies and for understanding current patterns of diversity in domesticated plants and animals. Traditionally the realm of archeology and botany (1, 2), the study of plant domestication has seen important contributions from genetics during the last two decades (3). Genetic data often provide evidence that is hard to obtain by other means, making it an invaluable complement to other lines of inquiry.As a case in point, molecular markers were instrumental in establishing the single domestication of maize (Zea mays subspecies mays) from an extant wild relative (4, 5). Maize was shown to originate from annual teosinte (Zea mays subspecies parviglumis, hereafter parviglumis) around 9,000 y B.P., placing domestication in the mid-to lowland regions of southwest Mexico where parviglumis grows endemically. As predicted by this result (6), excavations in the heart of parviglumis' distribution have produced the earliest (8,700 y B.P.) phytolith evidence for maize cultivation (7). Other finds from Tabasco (7,300 y B.P.) (8) and Panama (7,400 y B.P.) (9) also support an early presence of maize throughout the Meso-American lowlands.Although different types of evidence seemingly concur, questions nonetheless remain about the interpretation of the genetic data. While unequivocal with respect to maize's wild ancestor, marker evidence suggests that maize from the Mexican highlands, rather than from the lowlands, is most closely related to parviglumis and appears to have given rise to all cultivars currently grown throug...
Among maize (Zea maize L.) breeders, there is a heightened awareness of the necessity for both maintaining genetic diversity for crop improvement and improving the quality of genetic resource management. Restriction fragment length polymorphisms (RFLPs) and isozymes can serve as genetic markers for estimating divergence or diversity; however, the limited number of polymorphic isozyme loci available and the labor intensive and time consuming nature of RFLPs make their use for this purpose prohibitive. Simple sequence repeats (SSRs), when resolved using agarose gels, may be a viable and costeffective alternative to RFLPs and isozymes. Ninety‐four elite maize inbred lines, representative of the genetic diversity among lines derived from the Corn Belt Dent and Southern Dent maize races, were assayed for polymorphism at 70 SSR marker loci using agarose gels. The 365 alleles identified served as raw data for estimating genetic similarities among these lines. The patterns of genetic divergence revealed by the SSR polymorphisms were consistent with known pedigrees. A cluster analysis placed the inbred lines in nine clusters that correspond to major heterotic groups or market classes for North American maize. A unique fingerprint for each inbred line could be obtained from as few as five SSR loci. The utility of polymerase chain reaction (PCR)‐based markers such as SSRs for measuring genetic diversity, for assigning lines to heterotic groups and for genetic fingerprinting equals or exceeds that of RFLP markers, a property that may prove a valuable asset for a maize breeding program.
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