Author Summary

Maize was domesticated from a wild grass, teosinte, that grows only in tropical environments in Mexico (1). Maize agriculture spread from its Meso-American center of origin to Canada and Chile before the arrival of Columbus. The transition to flowering in teosinte is highly sensitive to small changes in day lengths that occur in its native range, perhaps as a way to coordinate flowering with rainfall patterns. In contrast, reproductive fitness for maize of the higher latitudes depends on its capacity to flower under much longer summer day lengths (Fig. P1). Thus, the spread of maize from its tropical center of origin to the higher latitudes of the Americas required selection for adaptation to longer day lengths. Genetic analysis of the differences in photoperiod response among teosinte, tropical maize, and temperate maize revealed moderately complex inheritance involving more than 10 genes, one of which, ZmCCT, is similar to an important regulator of day-length response in rice.

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Fig. P1.

Reaction of temperate maize and teosinte to long day lengths. Under short day lengths, this teosinte population flowers earlier than temperate maize line B73, but under long day lengths shown here, it flowers much later or never. The figure shows temperate inbred B73, teosinte plants, and their F₁ hybrid growing in the field in Clayton, NC, under long day lengths. The temperate inbred line flowered several weeks before this photo was taken. The teosinte plant never flowered before the field was abandoned in September. ZmCCT and several other genes contribute to this differential response to photoperiod. (Photo taken July 14, 2008; courtesy of J.B. Holland.)

To understand the genetic basis of adaptations to different day lengths, we evaluated nearly 5,000 mapping lines derived from crosses of 27 diverse maize inbred lines that compose the maize nested association mapping (NAM) population. The parents of NAM are a geographically and genetically diverse sample of maize inbreds selected by plant breeders for adaptation to a range of latitudes. The photoperiod responses of the NAM lines and a set of 281 diverse inbreds (representing even more of the global diversity of maize) were measured by comparing their time to flowering in eight long-day length (>13 h) environments to three short (< 12 h)-day length environments after adjusting for temperature differences among environments.

Genetic linkage analysis of the NAM families revealed 14 quantitative trait loci (QTLs) associated with most of the observed variation for flowering time photoperiod response. These photoperiod response QTLs were mostly a subset of the more than twice as many QTLs detected for flowering time under long day lengths. The QTL with strongest effects mapped to a region on chromosome 10 previously identified as carrying a strong photoperiod response QTL in maize and teosinte mapping studies (2⇓–4). Surprisingly, only three tropical NAM founders carry variants (alleles) of this QTL that significantly increase the photoperiod response, and two tropical parent lines have QTL alleles with even less sensitivity to photoperiod than the standard temperate allele. In contrast, most tropical founders carry photoperiod-sensitive alleles at other important QTLs. Patterns of environment-dependent effects on flowering time varied substantially among the four key QTLs, demonstrating that each gene has a unique response to photoperiod.

We conducted a genome-wide association study of photoperiod response in the NAM population by using 26.5 M SNPs and 1 M copy-number variants identified in the maize HapMap version 2. We identified 118 SNPs and five CNVs associated with photoperiod response, which mapped within QTL support intervals much more frequently than expected by chance. Genome-wide association study associations were not enriched near 218 candidate genes identified a priori based on their effects on flowering time in maize or homology to flowering-time genes of Arabidopsis, sorghum, or rice, however. These results suggest that casting a wide net for candidate genes to test for associations with maize photoperiod response was largely unsuccessful.

We also performed a parallel whole-genome linkage mapping scan of flowering time under long days in a population of 866 lines derived from backcrosses of teosinte to a temperate maize line. We identified 23 QTLs controlling variation for flowering time under long day lengths, approximately half of which coincided with NAM flowering-time QTLs. The flowering-time QTL with the largest effect in the maize/teosinte population was syntenic to the major chromosome 10 photoperiod QTL identified in NAM. Briggs et al. (2) demonstrated that the teosinte allele at this QTL is highly responsive to photoperiod and is detected only under long day lengths.

Given the strong allelic effects observed at the QTL on chromosome 10, we targeted this region for high-resolution linkage mapping in maize and maize/teosinte mapping families. Results from all four fine-mapping populations were congruent in identifying a region on chromosome 10 that includes ZmCCT, a homologue of rice Ghd7. Highest resolution was obtained in the maize/teosinte mapping population, which identified ZmCCT as the only predicted gene within the QTL interval. Analysis of the sequences of ZmCCT and its upstream region in the maize 281 line global diversity panel revealed two SNPs in the promoter of this gene that were highly associated with photoperiod response in that panel after correction for population structure.

To determine if photoperiod-sensitive alleles at ZmCCT are frequent in teosinte, we measured the effects of ZmCCT QTL alleles from eight teosinte lines representing the genetic and geographic variability of the progenitor species in crosses with temperate maize. All teosinte alleles in this region have a strong effect on delaying flowering time. We also measured allele-specific ZmCCT transcript abundance in F₁ crosses between eight different teosintes and three temperate maize lines grown under long day lengths. The teosinte allele was expressed at higher levels than the maize allele in all cases. Thus, all teosintes tested carried cis-acting regulatory elements that increased the expression of ZmCCT relative to the maize allele. If ZmCCT functions in a manner homologous to its rice orthologue (5), higher expression of the teosinte allele under long day lengths is expected to repress expression of the maize florigen required to initiate flowering.

These results suggest that the mutation(s) that reduce the effect of ZmCCT on photoperiod response were rare or nonexistent in teosinte, but increased to high frequencies following the initial domestication of maize. The relatively common occurrence of photoperiod-insensitive ZmCCT alleles in tropical inbred lines could be a result of a selection sweep related to adaptation of maize to tropical environments outside of the range of teosinte. Alternatively, Ghd7 in rice is known to affect inflorescence architecture so ZmCCT may have first been selected in tropical maize for its effects on ear morphology, helping to move alleles that were preadapted to longer day lengths to higher frequency in tropical maize. Standing variation at photoperiod response loci provided early Americans the raw material with which they could select maize with adaptation to increasingly higher latitudes.