Entering the second century of maize quantitative genetics

Abstract

Maize is the most widely grown cereal in the world. In addition to its role in global agriculture, it has also long served as a model organism for genetic research. Maize stands at a genetic crossroads, as it has access to all the tools available for plant genetics but exhibits a genetic architecture more similar to other outcrossing organisms than to self-pollinating crops and model plants. In this review, we summarize recent advances in maize genetics, including the development of powerful populations for genetic mapping and genome-wide association studies (GWAS), and the insights these studies yield on the mechanisms underlying complex maize traits. Most maize traits are controlled by a large number of genes, and linkage analysis of several traits implicates a 'common gene, rare allele' model of genetic variation where some genes have many individually rare alleles contributing. Most natural alleles exhibit small effect sizes with little-to-no detectable pleiotropy or epistasis. Additionally, many of these genes are locked away in low-recombination regions that encourage the formation of multi-gene blocks that may underlie maize's strong heterotic effect. Domestication left strong marks on the maize genome, and some of the differences in trait architectures may be due to different selective pressures over time. Overall, maize's advantages as a model system make it highly desirable for studying the genetics of outcrossing species, and results from it can provide insight into other such species, including humans.

Figure 1

Nested association mapping (NAM) design. (a) The maize NAM population was created by crossing 25 diverse founder lines by the reference line B73. Single-seed descent and self-pollination for five generations were then used to generate 200 recombinant inbred lines (RILs) for each subfamily. Figure based on Yu et al. (2008). (b, c) Identifying significant associations in NAM proceeds through two routes. Joint linkage mapping (b) across the subfamilies can identify quantitative trait loci (QTL) for specific traits at moderate resolution by taking advantage of the shared B73 line in all the subfamilies (Li et al., 2011). Genome-wide association (c) instead uses the information of which chromosomal segments were inherited from which parent (top) to project dense genotyping from the founder lines onto the progeny for improved resolution (bottom). Colored bars show which parent the chromosomal segment originated from. Single-nucleotide polymorphisms (SNPs) in panel c are shown as either matching the allele present in B73 (white) or as the alternative allele (black).

Figure 2

Maize dispersion and diversity. Maize originated in the Balsas river basin of southwestern Mexico approximately 9000 years ago (Matsuoka et al., 2002). Over the next several thousand years, it spread through the Americas, crossing (and adapting to) deserts, mountains, tropics and almost every other environment present across both continents before contact with European explorers spread it throughout the world. Arrows show probable routes of pre-Columbian dispersion based on phylogenetic reconstruction (Matsuoka et al., 2002); biome data are from the USDA National Resource Conservation Service (http://www.nrcs.usda.gov).

Figure 3

Maize population dynamics and trait architecture. The genetic pool leading to modern maize has fluctuated greatly over its history, both in terms of absolute (census) population and effective population size, and also the selective pressures operating on it. Major divisions in maize history are indicated, with approximate durations noted. As many of the population values are unknown, the indicated population sizes are a range of likely estimates, with relative differences more important than absolute ones. Differences in the genetic architectures of certain traits may be due to the different lengths of time and population regimes that the traits have evolved under. (Note that although heterosis is not truly a trait, breeding for distinct heterotic groups can be seen as diversifying selection with heterosis as the final goal (Duvick, 2005)).