ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize

Abstract

Teosinte, the progenitor of maize, is restricted to tropical environments in Mexico and Central America. The pre-Columbian spread of maize from its center of origin in tropical Southern Mexico to the higher latitudes of the Americas required postdomestication selection for adaptation to longer day lengths. Flowering time of teosinte and tropical maize is delayed under long day lengths, whereas temperate maize evolved a reduced sensitivity to photoperiod. We measured flowering time of the maize nested association and diverse association mapping panels in the field under both short and long day lengths, and of a maize-teosinte mapping population under long day lengths. Flowering time in maize is a complex trait affected by many genes and the environment. Photoperiod response is one component of flowering time involving a subset of flowering time genes whose effects are strongly influenced by day length. Genome-wide association and targeted high-resolution linkage mapping identified ZmCCT, a homologue of the rice photoperiod response regulator Ghd7, as the most important gene affecting photoperiod response in maize. Under long day lengths ZmCCT alleles from diverse teosintes are consistently expressed at higher levels and confer later flowering than temperate maize alleles. Many maize inbred lines, including some adapted to tropical regions, carry ZmCCT alleles with no sensitivity to day length. Indigenous farmers of the Americas were remarkably successful at selecting on genetic variation at key genes affecting the photoperiod response to create maize varieties adapted to vastly diverse environments despite the hindrance of the geographic axis of the Americas and the complex genetic control of flowering time.genetic diversity | quantitative trait locus T he rapid spread of agriculture from the Fertile Crescent was enabled in part by the East-West axis of Eurasia, permitting crop cultivation to spread across large geographic regions at a common latitude (1). The relatively simple genetic control of flowering time of the key crops domesticated in the Fertile Crescent, wheat and barley (2), coupled with a predominantly selffertilizing mating system, also facilitated colonization of new environments by rare mutants with large effects on flowering time responses to day length and temperature.In contrast, the spread of maize from its origin in Southern Mexico 6 to 10,000 y ago was relatively slow (1), hindered by the North-South axis of the Americas. Maize (Zea mays L. subsp. mays) was domesticated from the Mexican native teosinte Zea mays L. subsp. parviglumis (3), a species adapted to day lengths less than 13 h. Under the longer day lengths of higher latitudes, teosinte flowers very late or not at all (4). From its Meso-American origin, maize was spread by early humans to geographically and ecologically diverse environments from Canada to Chile well before the arrival of Columbus to the Americas (5, 6), requiring its adaptation to long day lengths. Thus, although the spread of maize occurred later than that of wheat, ...

Hallauer’s Tusón: a decade of selection for tropical-to-temperate phenological adaptation in maize

“…Relative to other characteristics of maize, variation in photoperiodism is conditioned by a smaller number of loci, with one quantitative trait locus explaining nearly 10% of the variation in photoperiodism (Hung et al, 2012b). This architecture might explain the concomitant, relatively rapid change in the generational mean and variance that initially occurred as the population transitioned toward photoperiod insensitivity (Figure 2; Table 2).…”

“…In maize, a polygenic architecture of mostly small-effect alleles has been described to underlie flowering time per se (Chardon et al, 2004;Buckler et al, 2009), whereas a smaller number of loci appear to underlie photoperiodism (Hung et al, 2012b). Understanding how the genetic variation associated with flowering time interacts with the environment and responds to selection for adaptation is of basic interest and can help breeders address challenges of food security (Godfray et al, 2010;Tester and Langridge, 2010).…”

Interaction of Photoperiod and Vernalization Determines Flowering Time of Brachypodium distachyon

“…In the tropical cereals rice (Oryza sativa) and Zea mays, GHD7 represses flowering in long days and transcripts of GHD7 are correspondingly higher in long days versus short days (Xue et al, 2008;Hung et al, 2012). We measured VRN2L expression in Brachypodium spp.…”

Beyond the single gene: How epistasis and gene-by-environment effects influence crop domestication

“…Such phenotypic stability would facilitate selection, enabling the spread of domesticated crops away from their native environments into other climates and latitudes (24).…”

“…For example, teosinte is a tropical short-day plant and will not flower in the longer days of higher latitudes. The major gene affecting photoperiod response in Z. mays, ZmCCT, has teosinte alleles highly sensitive to day length but less sensitive or insensitive maize alleles (24). The reduction in sensitivity allows many temperate maize varieties to flower in longerday photoperiod regimes than can tropical maize or teosinte.…”