By 4000 years ago, people had introduced maize to the southwestern United States; full agriculture was established quickly in the lowland deserts but delayed in the temperate highlands for 2000 years. We test if the earliest upland maize was adapted for early flowering, a characteristic of modern temperate maize. We sequenced fifteen 1900-year-old maize cobs from Turkey Pen Shelter in the temperate Southwest. Indirectly validated genomic models predicted that Turkey Pen maize was marginally adapted with respect to flowering, as well as short, tillering, and segregating for yellow kernel color. Temperate adaptation drove modern population differentiation and was selected in situ from ancient standing variation. Validated prediction of polygenic traits improves our understanding of ancient phenotypes and the dynamics of environmental adaptation.
The process of evolution under domestication has been studied using phylogenetics, population genetics–genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance–covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.
In plants, many major regulatory genes that control plant growth and development have been identified and characterized. Despite a detailed knowledge of the function of these genes little is known about how they contribute to the natural variation for complex traits. To determine whether major regulatory genes of maize contribute to standing variation in Balsas teosinte we conducted association mapping in 584 Balsas teosinte individuals. We tested 48 markers from nine candidate regulatory genes against 13 traits for plant and inflorescence architecture. We identified significant associations using a mixed linear model that controls for multiple levels of relatedness. Ten associations involving five candidate genes were significant after correction for multiple testing, and two survive the conservative Bonferroni correction. zf l2, the maize homolog of FLORICAULA of Antirrhinum, was associated with plant height. zap1, the maize homolog of APETALA1 of Arabidopsis, was associated with inflorescence branching. Five SNPs in the maize domestication gene, teosinte branched1, were significantly associated with either plant or inflorescence architecture. Our data suggest that major regulatory genes in maize do play a role in the natural variation for complex traits in teosinte and that some of the minor variants we identified may have been targets of selection during domestication.
Previous association analyses showed that variation at major regulatory genes contributes to standing variation for complex traits in Balsas teosinte, the progenitor of maize. This study expands our previous association mapping effort in teosinte by testing 123 markers in 52 candidate genes for association with 31 traits in a population of 817 individuals. Thirty-three significant associations for markers from 15 candidate genes and 10 traits survive correction for multiple testing. Our analyses suggest several new putative causative relationships between specific genes and trait variation in teosinte. For example, two ramosa genes (ra1 and ra2) associate with ear structure, and the MADS-box gene, zagl1, associates with ear shattering. Since zagl1 was previously shown to be a target of selection during maize domestication, we suggest that this gene was under selection for its effect on the loss of ear shattering, a key domestication trait. All observed effects were relatively small in terms of the percentage of phenotypic variation explained (,10%). We also detected several epistatic interactions between markers in the same gene that associate with the same trait. Candidategene-based association mapping appears to be a promising method for investigating the inheritance of complex traits in teosinte.T HROUGH the characterization of major loss-offunction mutants, geneticists have determined the function of a vast number of genes. Despite a general knowledge of how these genes control developmental and physiological processes, very little is known about how (or if) they contribute to natural variation for complex traits. Association mapping with its high mapping resolution, its potential to sample multiple alleles, and its use of preexisting populations provides a powerful tool to investigate the role of these genes in the genetic architecture of complex traits ( Previously, we detected significant associations between polymorphisms in nine candidate genes and phenotypic variation in the maize ancestor, Balsas teosinte (Zea mays ssp. parviglumis) (Weber et al. 2007). Our study builds upon our prior analyses in several ways, including an increase in the numbers of individuals, candidate genes, and traits. We also selected our association mapping panel to decrease the amount of population structure as compared to our prior study. With this strategy, we detected 33 associations between complex traits in teosinte and our candidate genes that survive a correction for multiple testing. These include associations between indeterminate spikelet1 and inflorescence branching, ramosa1 and ramosa2 and ear structure, sugary1 and seed oil content, and terminal ear1 and ear length. We also observed an association between zea agamous-like1 (zagl1) and ear shattering. Since zagl1 was a target of selection during domestication, we propose that it was selected for its role in ear disarticulation. Several epistatic 1
Gene flow between maize [Zea mays (L.)] and its wild relatives does occur, but at very low frequencies. Experiments were undertaken in Tapachula, Nayarit, Mexico to investigate gene flow between a hybrid maize, landraces of maize and teosinte (Z. mays ssp. mexicana, races Chalco and Central Plateau). Hybridization, flowering synchrony, pollen size and longevity, silk elongation rates, silk and trichome lengths and tassel diameter and morphology were measured. Hybrid and open-pollinated maize ears produced a mean of 8 and 11 seeds per ear, respectively, when hand-pollinated with teosinte pollen, which is approximately 1-2% of the ovules normally produced on a hybrid maize ear. Teosinte ears produced a mean of 0.2-0.3 seeds per ear when pollinated with maize pollen, which is more than one-fold fewer seeds than produced on a maize ear pollinated with teosinte pollen. The pollination rate on a per plant basis was similar in the context of a maize plant with 400-500 seeds and a teosinte plant with 30-40 inflorescences and 9-12 fruitcases per inflorescence. A number of other factors also influenced gene-flow direction: (1) between 90% and 95% of the fruitcases produced on teosinte that was fertilized by maize pollen were sterile; (2) teosinte collections were made in an area where incompatibility systems that limit fertilization are present; (3) silk longevity was much shorter for teosinte than for maize (approx. 4 days vs. approx. 11 days); (4) teosinte produced more pollen on a per plant basis than the landraces and commercial hybrid maize; (5) teosinte frequently produced lateral branches with silks close to a terminal tassel producing pollen. Collectively these factors tend to favor crossing in the direction of teosinte to maize. Our results support the hypothesis that gene flow and the subsequent introgression of maize genes into teosinte populations most probably results from crosses where teosinte first pollinates maize. The resultant hybrids then backcross with teosinte to introgress the maize genes into the teosinte genome. This approach would slow introgression and may help explain why teosinte continues to co-exist as a separate entity even though it normally grows in the vicinity of much larger populations of maize.
Conservation of crop wild relatives (CWR) has always been predicated on the promise of new and useful traits, and thus modern genetics and genomics tools must help fulfill the promise and continue to secure the conservation of these resources. However, the vast genetic potential present in CWR is often difficult to tap, as identification of superior alleles can be hampered by the effects of the environment on expression of these alleles and masked in different genetic backgrounds; transfer of superior alleles into breeding pools to create new crop varieties can be slow and expensive. Some crop species have been more amenable to introgression of traits from wild relatives than others. In some cases, these species may be less diverged from their wild ancestors, which become a good source of mono‐ to oligogenic traits, many of which are more qualitative in nature, and sometimes of quantitative traits. Sunflower (Helianthus annuus L.) is an introgression success story, and many traits, including cytoplasmic male sterility, herbicide tolerance, drought and biotic stress resistance, and modified fatty acid profiles, have been introgressed into the cultivated gene pool from wild relatives without depression of oil yield and quality. Others, including maize (Zea mays L.), have shown little progress in widening the cultivated gene pool using exotic sources due to temporary yield depression, potential for loss of quality, and disturbance of current logistical habits. Here, we review the breeding history of sunflower and maize and explore variables that have limited the use of CWR in some species and allowed success in others. Surprisingly, in both sunflower and maize, biological limitations are similar and smaller than expected and appear to be surmountable with sufficient determination. Possible new technologies and policies to allow a deeper mining of these genetic resources in all crop species are discussed.
What is the genetic architecture of local adaptation and what is the geographic scale that it operates over? We investigated patterns of local and convergent adaptation in five sympatric population pairs of traditionally cultivated maize and its wild relative teosinte (Zea mays subsp. parviglumis). We found that signatures of local adaptation based on the inference of adaptive fixations and selective sweeps are frequently exclusive to individual populations, more so in teosinte compared to maize. However, for both maize and teosinte, selective sweeps are frequently shared by several populations, and often between the subspecies. We were further able to infer that selective sweeps were shared among populations most often via migration, though sharing via standing variation was also common. Our analyses suggest that teosinte has been a continued source of beneficial alleles for maize, post domestication, and that maize populations have facilitated adaptation in teosinte by moving beneficial alleles across the landscape. Taken together, out results suggest local adaptation in maize and teosinte has an intermediate geographic scale, one that is larger than individual populations, but smaller than the species range.
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