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Joint analysis of days to flowering reveals independent temperate adaptations in maize

Abstract

Domesticates are an excellent model for understanding biological consequences of rapid climate change. Maize (Zea mays ssp. mays) was domesticated from a tropical grass yet is widespread across temperate regions today. We investigate the biological basis of temperate adaptation in diverse structured nested association mapping (NAM) populations from China, Europe (Dent and Flint) and the United States as well as in the Ames inbred diversity panel, using days to flowering as a proxy. Using cross-population prediction, where high prediction accuracy derives from overall genomic relatedness, shared genetic architecture, and sufficient diversity in the training population, we identify patterns in predictive ability across the five populations. To identify the source of temperate adapted alleles in these populations, we predict top associated genome-wide association study (GWAS) identified loci in a Random Forest Classifier using independent temperate–tropical North American populations based on lines selected from Hapmap3 as predictors. We find that North American populations are well predicted (AUC equals 0.89 and 0.85 for Ames and USNAM, respectively), European populations somewhat well predicted (AUC equals 0.59 and 0.67 for the Dent and Flint panels, respectively) and that the Chinese population is not predicted well at all (AUC is 0.47), suggesting an independent adaptation process for early flowering in China. Multiple adaptations for the complex trait days to flowering in maize provide hope for similar natural systems under climate change.

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Fig. 1: Relatedness between the five study populations.
Fig. 2: MDS of GBS genotypes of American landraces from Takuno et al. (Takuno et al. 2015), replicated 10X each to drive the first two coordinates, and NAM population parents.
Fig. 3: Distribution of reported spatially corrected phenotypes for days to anthesis.
Fig. 4: GBLUP cross-population predictive abilities for DTA using all 70 million segregating SNPs in Hapmap 3.21.
Fig. 5: Pairwise population differentiation, FST and cross-population predictive ability (r) for DTA.
Fig. 6: Average area under the curve (AUC, in bold)—the false positive rate (FPR) to true positive rate (TPR) ratio—and predictor rankings across all chromosomes from Random Forest Classifier for GWAS results between populations to evaluate overlap in GWAS results between populations.
Fig. 7: Average area under the curve (AUC, in bold)—the false positive rate (FPR) to true positive rate (TPR) ratio—and predictor rankings across all chromosomes from Random Forest Classifier with GWAS additive p values as the response, and N.

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Acknowledgements

The authors thank Robert Bukowski from BRC Bioinformatics Facility, Institute of Biotechnology at Cornell University for early access to the KNNi imputed HapMap 3 dataset, and Jeffrey Ross-Ibarra and Matt Hufford for early access to the American landraces. We also thank Laura Morales for discussions and reviewing earlier drafts of the manuscript. This work was supported by National Science Foundation Grants IOS-0922493 and IOS-1238014 and the US Department of Agriculture–Agricultural Research Service.

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Swarts, K., Bauer, E., Glaubitz, J.C. et al. Joint analysis of days to flowering reveals independent temperate adaptations in maize. Heredity 126, 929–941 (2021). https://doi.org/10.1038/s41437-021-00422-z

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