Maize domestication and gene interaction

Abstract

Domestication is a tractable system for following evolutionary change. Under domestication, wild populations respond to shifting selective pressures, resulting in adaptation to the new ecological niche of cultivation. Due to the important role of domesticated crops in human nutrition and agriculture, the ancestry and selection pressures transforming a wild plant into a domesticate have been extensively studied. In Zea mays, morphological, genetic, and genomic studies have elucidated how a wild plant, the teosinte Zea mays subsp. parviglumis, was transformed into the domesticate Zea mays subsp. mays. Five major morphological differences distinguish these two subspecies, and careful genetic dissection has pinpointed the molecular changes responsible for several of these traits. But maize domestication was a consequence of more than just five genes, and regions throughout the genome contribute. The impacts of these additional regions are contingent on genetic background, both the interactions between alleles of a single gene and among alleles of the multiple genes that modulate phenotypes. Key genetic interactions include dominance relationships, epistatic interactions, and pleiotropic constraint, including how these variants are connected in gene networks. Here, we review the role of gene interactions in generating the dramatic phenotypic evolution seen in the transition from teosinte to maize. IntroductionThe advent of agriculture generated dramatic departures from the way humans had been interacting with their world. Ten to twelve thousand years ago, in independent locations around the world, cereal grains began to be consumed in larger quantities (Larson et al., 2014). Agriculture had drastic impacts on human culture, societal structure, and human health (Larsen, 2006). As a coevolutionary process, domestication also drastically altered the evolution of plants in novel agroenvironments. Although the temporal nature of this trajectory and transformation has been thoroughly investigated in the archaeological record (Smith, 2001), genetic and genomic approaches using extant crop and wild relative diversity have provided additional evidence about the process of domestication (Zeder et al., 2006), especially in those regions of the world where environmental conditions are not conducive to archaeological preservation. The initial stages of domestication are largely analogous to a plant encountering a new ecological niche. By growing plants and then planting their seeds in the next generation, selective breeding and seed saving allow for adaptation to agronomic environments. The domestication process may shift selection pressures from biotic interactions such as competition and colonization to traits of value for human consumption, including large non-dispersing seeds, reduced branching, and other nutritional and harvest-related phenotypes . Byproducts of cultivation can also alter biotic interactions, for example by allowing pests to specialize on a domesticate (Bernal et al., 2017;Gaillard et al., 2018), or alter ph...

Selective sorting of ancestral introgression in maize and teosinte along an elevational cline

“…Despite contemporary observations of hybrids in the field [109], there is little evidence of significant recent gene flow in either direction between sympatric maize- mexicana population pairs. Consistent with domestication loci acting as barriers to introgression, in both maize and mexicana an enriched subset of candidate domestication genes overlap ‘introgression deserts.’ More generally, we find introgressed mexicana alleles are on average deleterious in maize, but less evidence for a genomewide effect of selection against introgression into mexicana , possibly because epistasis masks the impact of maize alleles in a mexicana background [96]. Some loci show exceptional ancestry patterns consistent with selection favoring introgression in multiple populations, especially for mexicana ancestry in the highest elevation maize.…”

“…Despite evidence of introgression at many domestication loci, maize landraces retain all of the classic domestication traits, and mexicana populations maintain ‘wild’ forms. Epistasis for domestication traits [96] could help explain this discrepancy if compensatory effects from other loci contribute to maintaining domestication traits in admixed highland maize, or key domestication alleles segregate at moderate frequencies within mexicana (but do not have the same phenotypic effects in a teosinte background).…”

“…While some highland and locally-adapted alleles may be beneficial to maize, many introgressed mexicana alleles, especially those affecting domestication traits, should be selected against by farmers growing maize landraces. In addition, maize alleles introgressed into mexicana should be selected against because maize has accumulated genetic load from reduced population sizes during domestication [105] and because domestication traits generally reduce fitness in the wild [17,61,96], e.g. loss of disarticulation and effective seed dispersal [109].…”

Archaeogenomics of a ~2,100-year-old Egyptian leaf provides a new timestamp on date palm domestication

“…The widespread availability of high-throughput DNA sequencing has revolutionized the study of plant crop domestication history, leading to many unpreceded insights, such as the identification of crop progenitors (Ling et al, 2013; Gros-Balthazard et al, 2017, Chomicki et al 2020), hybridization and introgression events following the origin of crops (e.g. Cornille et al, 2012; Hufford et al, 2012; Baute et al, 2015; Muñoz-Rodrígez et al, 2018), refinement of the geographic origins of crops (Besnard et al, 2017; Cubry et al, 2018), the identification of genes controlling key domestication traits (Zhou et al, 2016; Stitzer and Ross-Ibarra, 2018) and more generally of convergent evolutionary processes that have challenged orthodoxies on domestication (reviewed by Purugganan, 2019). The application of genomic approaches to crop wild relatives is also bringing critical new resources for crop improvement (reviewed by Brozynska et al, 2016).…”

Conflict over fertilization underlies the transient evolution of reinforcement

“…mexicana grows as an agricultural weed. As described in the introduction, the biology of this system is favorable to the evolution of reinforcement — as gene flow occurs between sub-species and hybrids have reduced but non-zero fitness in either parental environment (Stitzer and Ross-Ibarra 2018). Stylar incompatibilities are common in Z. m. ssp.…”