Population genomics of Zea species identifies selection signatures during maize domestication and adaptation

Authors: XU, GEN - China Agricultural University; ZHANG, XUAN - China Agricultural University; CHEN, WENKANG - China Agricultural University; ZHANG, RENYU - China Agricultural University; LI, ZHI - China Agricultural University; WEN, WEIWEI - Huazhong Agricultural University; Warburton, Marilyn; LI, JIANSHENG - China Agricultural University; LI, HUIHUI - Chinese Academy Of Agricultural Sciences; YANG, XIAOHONG - China Agricultural University

Submitted to: Genome Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/5/2022
Publication Date: 2/18/2022
Citation: Xu, G., Zhang, X., Chen, W., Zhang, R., Li, Z., Wen, W., Warburton, M.L., Li, J., Li, H., Yang, X. 2022. Population genomics of Zea species identifies selection signatures during maize domestication and adaptation. Genome Biology. 22:72. https://doi.org/10.1186/s12870-022-03427-w.
DOI: https://doi.org/10.1186/s12870-022-03427-w

Interpretive Summary: The domestication of maize (Zea mays L. ssp. mays) from its wild progenitor, teosinte, was done over a long time by people who changed it in the process. The changes can be found at the DNA sequence level, in many different genes, which were the ones that people needed to create a plant that yielded a nutritious grain but also would grow in new places that the wild ancestor could not. In this study, we looked at a large group of maize and its wild ancestors at the level of the DNA. The wild ancestors are a group of seven related species, which are called Zea mays ssp. parviglumis, which we noted was the direct progenitor of maize, in agreement with previous studies; Zea mays ssp. mexicana, most closely related to Z. parviglumis; and followed in order by Zea huehuetenangsis, Zea perennis and Zea diploperennis, Zea luxurians, and Zea nicaraguensis. We determined that Z. parviglumis and Z. mexicana contributed many useful traits to the first domesticated maize. That early maize was further modified by farmers over another long period of time, as they selected the best seeds to plant for their needs and local conditions. These changes can also be found at the DNA sequence level. This paper documents the changes in maize due to domestication, gene flow from teosintes after domestication, and due to selection for local adaptation. This information will be useful to breeders looking for new traits in modern maize.

Technical Abstract: Modern cultivated maize (Zea mays L. ssp. mays) has undergone intensive selection during domestication and adaptation. To better understand these processes, we conducted a genome-wide survey of 982 maize inbred lines and 190 teosinte accessions using over 40,000 single-nucleotide polymorphism markers. Population structure, principal component analysis, and phylogenetic trees all confirmed the evolutionary relationship between maize and teosinte. We also determined the evolutionary lineage of all species within teosinte, and that Zea mays ssp. parviglumis was closest to Zea mays ssp. mexicana, followed in order by Zea huehuetenangsis, Zea perennis and Zea diploperennis, Zea luxurians, and Zea nicaraguensis. Shared haplotype analysis showed similar and high levels of gene flow from Zea mays ssp. parviglumis and Zea mays ssp. mexicana to maize, confirming the critical contribution of Zea mays ssp. mexicana to the maize gene pool. Scans for selection signatures identified 1,152 domestication sweeps by comparing wild and cultivated maize and 1,084 adaptation sweeps by comparing tropical and temperate maize, including a set of known domestication and adaptation genes, i.e. TB1 and ZmCCT9. Among these selective sweeps, 596 (51.7%) of the domestication-related selective sweeps and 589 (54.3%) of the adaptation-related selective sweeps were co-located with quantitative trait loci for flowering time related traits. Genome-wide association study identified 125 loci significantly associated with flowering-time related traits, 32 of which identified candidate genes, (i.e. ZmRR1, a gene with putative function in red-light signaling), that had undergone selection during maize adaptation. This study provides valuable insights into maize evolutionary history, and abundant genetic resources that will greatly bene't basic research and genetic improvement of maize.