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Title: The genomic basis for short-term evolution of environmental adaptation in maize

Author
item WISSER, RANDALL - University Of Delaware
item FANG, ZHOU - North Carolina State University
item Holland, Jim - Jim
item TEIXEIRA, JULIANA - University Of Delaware
item DOUGHERTY, JOHN - University Of Delaware
item WELDEKIDAN, TECLEMARIAM - University Of Delaware
item DE LEON, NATALIA - University Of Wisconsin
item Flint-Garcia, Sherry
item Lauter, Nicholas
item MURRAY, SETH - Texas A&M University
item XU, WENWEI - Texas A&M Agrilife
item HALLAUER, ARNEL - Iowa State University

Submitted to: Genetics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/4/2019
Publication Date: 12/1/2019
Citation: Wisser, R.J., Fang, Z., Holland, J.B., Teixeira, J.E., Dougherty, J., Weldekidan, T., De Leon, N., Flint-Garcia, S.A., Lauter, N.C., Murray, S.C., Xu, W., Hallauer, A. 2019. The genomic basis for short-term evolution of environmental adaptation in maize. Genetics. 213(4):1479-1494. https://doi.org/10.1534/genetics.119.302780.
DOI: https://doi.org/10.1534/genetics.119.302780

Interpretive Summary: Crop species are capable of adapting to a wide range of growing environments if there is sufficient variation in a population and if selection pressure is applied to the population for adaptive characteristics. In corn (maize), populations from tropical environments are generally maladapted to the U.S. Corn Belt due to late flowering and other associated characteristics. We studied changes in the genome of a tropical, late flowering population that was gradually adapted to central Iowa over ten generations of selection for earlier flowering. This identified changes in genes scattered across the whole genome and certain gene regions that may have been involved in environmental adaptation. Some gene regions were important in the earlier generations of selection for faster flowering, while other regions were important in the later generations of adaptation. This study demonstrates the genetic complexity of adapting tropical corn to temperate environments, but that adaptation can be accomplished in just a few generations of selection. This information will be useful to corn breeders and geneticists as they work to broaden the genetic diversity of the U.S. corn crop by incorporating useful variation from tropical sources.

Technical Abstract: Understanding the evolutionary capacity of populations to adapt to novel environments is one of the major pursuits in genetics. Moreover, for plant breeding, maladaptation is the foremost barrier to capitalizing on intraspecific variation in order to develop new breeds for future climate scenarios in agriculture. Using a unique study design, we simultaneously dissected the population and quantitative genomic basis of short-term evolution in a tropical landrace of maize that was translocated to a temperate environment and phenotypically selected for adaptation in flowering time phenology. Underlying 10 generations of directional selection, which resulted in a 26-day mean decrease in female-flowering time, Embedded Image of the heritable variation mapped to Embedded Image of the genome, where, overall, alleles shifted in frequency beyond the boundaries of genetic drift in the expected direction given their flowering time effects. However, clustering these non-neutral alleles based on their profiles of frequency change revealed transient shifts underpinning a transition in genotype–phenotype relationships across generations. This was distinguished by initial reductions in the frequencies of few relatively large positive effect alleles and subsequent enrichment of many rare negative effect alleles, some of which appear to represent allelic series. With these genomic shifts, the population reached an adapted state while retaining Embedded Image of the standing molecular marker variation in the founding population. Robust selection and association mapping tests highlighted several key genes driving the phenotypic response to selection. Our results reveal the evolutionary dynamics of a finite polygenic architecture conditioning a capacity for rapid environmental adaptation in maize.