An adaptive teosinte mexicana introgression modulates phosphatidylcholine levels and is associated with maize flowering time.

Native Americans domesticated maize (Zea mays ssp. mays) from lowland teosinte parviglumis (Zea mays ssp. parviglumis) in the warm Mexican southwest and brought it to the highlands of Mexico and South America where it was exposed to lower temperatures that imposed strong selection on flowering time. Phospholipids are important metabolites in plant responses to low-temperature and phosphorus availability and have been suggested to influence flowering time. Here, we combined linkage mapping with genome scans to identify High PhosphatidylCholine 1 (HPC1), a gene that encodes a phospholipase A1 enzyme, as a major driver of phospholipid variation in highland maize. Common garden experiments demonstrated strong genotype-by-environment interactions associated with variation at HPC1, with the highland HPC1 allele leading to higher fitness in highlands, possibly by hastening flowering. The highland maize HPC1 variant resulted in impaired function of the encoded protein due to a polymorphism in a highly conserved sequence. A meta-analysis across HPC1 orthologs indicated a strong association between the identity of the amino acid at this position and optimal growth in prokaryotes. Mutagenesis of HPC1 via genome editing validated its role in regulating phospholipid metabolism. Finally, we showed that the highland HPC1 allele entered cultivated maize by introgression from the wild highland teosinte Zea mays ssp. mexicana and has been maintained in maize breeding lines from the Northern United States, Canada, and Europe. Thus, HPC1 introgressed from teosinte mexicana underlies a large metabolic QTL that modulates phosphatidylcholine levels and has an adaptive effect at least in part via induction of early flowering time.

A B73×Palomero Toluqueño mapping population reveals local adaptation in Mexican highland maize.

Generations of farmer selection in the central Mexican highlands have produced unique maize varieties adapted to the challenges of the local environment. In addition to possessing great agronomic and cultural value, Mexican highland maize represents a good system for the study of local adaptation and acquisition of adaptive phenotypes under cultivation. In this study, we characterize a recombinant inbred line population derived from the B73 reference line and the Mexican highland maize variety Palomero Toluqueño. B73 and Palomero Toluqueño showed classic rank-changing differences in performance between lowland and highland field sites, indicative of local adaptation. Quantitative trait mapping identified genomic regions linked to effects on yield components that were conditionally expressed depending on the environment. For the principal genomic regions associated with ear weight and total kernel number, the Palomero Toluqueño allele conferred an advantage specifically in the highland site, consistent with local adaptation. We identified Palomero Toluqueño alleles associated with expression of characteristic highland traits, including reduced tassel branching, increased sheath pigmentation and the presence of sheath macrohairs. The oligogenic architecture of these three morphological traits supports their role in adaptation, suggesting they have arisen from consistent directional selection acting at distinct points across the genome. We discuss these results in the context of the origin of phenotypic novelty during selection, commenting on the role of de novo mutation and the acquisition of adaptive variation by gene flow from endemic wild relatives.

Characterization of introgression from the teosinte Zea mays ssp. mexicana to Mexican highland maize.

BACKGROUND: The spread of maize cultivation to the highlands of central Mexico was accompanied by substantial introgression from the endemic wild teosinte Zea mays ssp. mexicana, prompting the hypothesis that the transfer of beneficial variation facilitated local adaptation. METHODS: We used whole-genome sequence data to map regions of Zea mays ssp. mexicana introgression in three Mexican highland maize individuals. We generated a genetic linkage map and performed Quantitative Trait Locus mapping in an F2 population derived from a cross between lowland and highland maize individuals. RESULTS: Introgression regions ranged in size from several hundred base pairs to Megabase-scale events. Gene density within introgression regions was comparable to the genome as a whole, and over 1,000 annotated genes were located within introgression events. Quantitative Trait Locus mapping identified a small number of loci linked to traits characteristic of Mexican highland maize. DISCUSSION: Although there was no strong evidence to associate quantitative trait loci with regions of introgression, we nonetheless identified many Mexican highland alleles of introgressed origin that carry potentially functional sequence variants. The impact of introgression on stress tolerance and yield in the highland environment remains to be fully characterized.

The genomic signature of crop-wild introgression in maize.

The evolutionary significance of hybridization and subsequent introgression has long been appreciated, but evaluation of the genome-wide effects of these phenomena has only recently become possible. Crop-wild study systems represent ideal opportunities to examine evolution through hybridization. For example, maize and the conspecific wild teosinte Zea mays ssp. mexicana (hereafter, mexicana) are known to hybridize in the fields of highland Mexico. Despite widespread evidence of gene flow, maize and mexicana maintain distinct morphologies and have done so in sympatry for thousands of years. Neither the genomic extent nor the evolutionary importance of introgression between these taxa is understood. In this study we assessed patterns of genome-wide introgression based on 39,029 single nucleotide polymorphisms genotyped in 189 individuals from nine sympatric maize-mexicana populations and reference allopatric populations. While portions of the maize and mexicana genomes appeared resistant to introgression (notably near known cross-incompatibility and domestication loci), we detected widespread evidence for introgression in both directions of gene flow. Through further characterization of these genomic regions and preliminary growth chamber experiments, we found evidence suggestive of the incorporation of adaptive mexicana alleles into maize during its expansion to the highlands of central Mexico. In contrast, very little evidence was found for adaptive introgression from maize to mexicana. The methods we have applied here can be replicated widely, and such analyses have the potential to greatly inform our understanding of evolution through introgressive hybridization. Crop species, due to their exceptional genomic resources and frequent histories of spread into sympatry with relatives, should be particularly influential in these studies.

Teosinte as a model system for population and ecological genomics.

As the cost of next-generation sequencing diminishes and genomic resources improve, crop wild relatives are well positioned to make major contributions to the field of ecological genomics via full-genome resequencing and reference-assisted de novo assembly of genomes of plants from natural populations. The wild relatives of maize, collectively known as teosinte, are a more varied and representative study system than many other model flowering plants. In this review of the population and ecological genomics of the teosintes we highlight recent advances in the study of maize domestication, introgressive hybridization, and local adaptation, and discuss future prospects for applying the genomic resources of maize to this intriguing group of species. The maize/teosinte study system is an excellent example of how crops and their wild relatives can bridge the model/non-model gap.