ZmCCT9 enhances maize adaptation to higher latitudes
Contributed by John F. Doebley, December 3, 2017 (sent for review October 16, 2017; reviewed by Nathan M. Springer and Jonathan F. Wendel)
Significance
Flowering time is a critical determinant of crop adaptation to local environments. As a result of natural and artificial selection, maize has evolved a reduced photoperiod sensitivity to adapt to regions over 90° of latitude in the Americas. Here we show that a distant Harbinger-like transposon acts as a cis-regulatory element to repress ZmCCT9 expression to promote flowering under the long days of higher latitudes. The transposon at ZmCCT9 and another functional transposon at a second flowering-time gene, ZmCCT10, arose sequentially following domestication and were targeted by selection as maize spread from the tropics to higher latitudes. Our results demonstrate that new functional variation created by transposon insertions helped maize to spread over a broad range of latitudes rapidly.
Abstract
From its tropical origin in southwestern Mexico, maize spread over a wide latitudinal cline in the Americas. This feat defies the rule that crops are inhibited from spreading easily across latitudes. How the widespread latitudinal adaptation of maize was accomplished is largely unknown. Through positional cloning and association mapping, we resolved a flowering-time quantitative trait locus to a Harbinger-like transposable element positioned 57 kb upstream of a CCT transcription factor (ZmCCT9). The Harbinger-like element acts in cis to repress ZmCCT9 expression to promote flowering under long days. Knockout of ZmCCT9 by CRISPR/Cas9 causes early flowering under long days. ZmCCT9 is diurnally regulated and negatively regulates the expression of the florigen ZCN8, thereby resulting in late flowering under long days. Population genetics analyses revealed that the Harbinger-like transposon insertion at ZmCCT9 and the CACTA-like transposon insertion at another CCT paralog, ZmCCT10, arose sequentially following domestication and were targeted by selection for maize adaptation to higher latitudes. Our findings help explain how the dynamic maize genome with abundant transposon activity enabled maize to adapt over 90° of latitude during the pre-Columbian era.
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Flowering time is a major determinant of the local adaptation of crops (1–10). Maize (Zea mays ssp. mays) was domesticated in southwestern Mexico ∼9,000 y ago from its wild progenitor, teosinte (Zea mays ssp. parviglumis), a tropical species that exhibits substantial photoperiod sensitivity and requires short-day (SD) conditions to flower (6, 11). As a result of natural and artificial selection, maize has evolved a reduced photoperiod sensitivity to adapt to long-day (LD) environments from latitude 58° north in Canada to 40° south in Chile (12–14). This widespread expansion over 90° of latitude across the North–South axis of the Americas was a remarkable achievement in the pre-Columbian era compared with the spread of other New World crops (i.e., potato and cotton), which remained in narrower latitudinal ranges before the era of modern breeding (15, 16). Understanding how this feat was achieved specifically with maize is an important question in the history of crop domestication.
Transposable elements were first discovered in maize by Barbara McClintock (17) and have since been shown to play important roles in shaping genome evolution and gene regulatory networks of many species (18). Compared with other crops, maize is exceptionally abundant in transposon activity, and nearly 85% of the maize genome consists of transposable elements (19, 20). This abundant transposon activity helps generate substantial genetic diversity upon which selection can act during evolution, as inferred by Barbara McClintock decades ago (21). Although many loci affecting natural variation in flowering time have been detected in maize using various types of mapping populations (6, 13, 22), only two of them, Vgt1 (23–25) and ZmCCT (6, 7, 26), have been well characterized and found to contribute to flowering-time adaptation. Interestingly, both loci are associated with the regulatory roles of transposable elements. Despite this progress, whether transposable elements play a prevalent role in driving maize flowering-time adaptation remains to be further tested and elucidated.
In this study, we report the cloning and characterization of a flowering-time QTL (qDTA9) that was previously mapped in a maize-teosinte experimental population (27). We show that qDTA9 is underlain by a Harbinger-like transposable element located 57 kb upstream of a CCT domain-containing gene, ZmCCT9. The Harbinger-like transposable element functions as a repressor of ZmCCT9 to promote flowering under LD conditions. ZmCCT9 confers LD-dependent flowering repression by negatively regulating the expression of florigen ZCN8. We finally show that the Harbinger-like transposable element arose more recently compared with the CACTA-like transposon insertion at another CCT paralog, ZmCCT10 (6, 7, 26). Both transposon insertions were targeted by selection and have played crucial roles as maize spread geographically from its tropical origin to higher latitudes.
Results and Discussion
Positional Cloning of qDTA9.
Using a large population of 866 maize-teosinte BC2S3 recombinant inbred lines (RILs), we previously performed quantitative trait locus (QTL) mapping for days to anthesis (DTA) under LD conditions (27) and detected a QTL (qDTA9) between markers M114923 and M123776 on chromosome 9 (Fig. 1A). To fine-map qDTA9, we selected a heterogeneous inbred family (HIF) that was heterozygous only at qDTA9 (SI Appendix, Fig. S1) and used it to generate a large near-isogenic line (NIL) population (n = 5,394). Following a recombinant-derived progeny testing strategy (6, 27, 28), qDTA9 was delimited to a 2.4-kb noncoding region between markers M115705 and M115707 (Fig. 1 B and C).
Fig. 1.
At the same time, a pair of NILs that is homozygous for the maize and teosinte alleles across the qDTA9 region, designated NIL(maize) and NIL(teosinte), was developed from the HIF for subsequent analysis. Field examination under natural LD conditions showed that NIL(maize) flowered approximately 4 d earlier than NIL(teosinte) (Fig. 1 D–F), along with reduced plant height and leaf number (SI Appendix, Fig. S2). However, no significant differences in flowering time were observed when NIL(maize) and NIL(teosinte) were grown under natural SD conditions (SI Appendix, Fig. S3). These results suggest that qDTA9 is regulated by photoperiod.
Association Mapping for qDTA9.
To further identify potential causative variants responsible for qDTA9, we performed an association analysis by resequencing the 2.4-kb causative region in an association panel containing 513 diverse maize inbred lines that was scored for DTA under LD conditions in Beijing (39.9°N, 116.4°E) (7). In total, 41 variants (SNPs and insertions and deletions) with minor allele frequencies ≥0.05 were identified and tested for association with DTA using a mixed linear model (29). Overall, 13 variants exhibited significant association with DTA after Bonferroni multiple test correction (P ≤ 2.44 × 10−4) (Fig. 1G). Interestingly, a 360-bp Harbinger-like transposable element that is present in 41.3% of maize inbred lines showed the strongest association with DTA (P = 5.26 × 10−7), with the Harbinger-like element promoting flowering (Fig. 1G). As expected, the maize parent of the BC2S3 population carried the Harbinger-like element, whereas the teosinte parent lacked the Harbinger-like element (SI Appendix, Fig. S4 A and B). The Harbinger-like element is in strong linkage disequilibrium (r2 > 0.5) with all other significant variants, creating a linkage disequilibrium block flanking the Harbinger-like element (Fig. 1H). We also tested the association of the Harbinger-like element with flowering time scored in five other locations at diverse latitudes (7). To account for the effect of temperature differences among environments on the observed flowering times, DTA were converted to growing degree days (30). Interestingly, the Harbinger-like element exhibited significant associations with flowering time only at higher latitudes (Fig. 1I), potentially indicating a role for the Harbinger-like element in latitudinal adaptation.
According to the B73 reference genome (AGPv2), the Harbinger-like transposable element is located 57 kb upstream of GRMZM2G004483 (SI Appendix, Fig. S4A), which encodes a CCT domain protein homologous to the rice photoperiod response regulator Ghd7 (SI Appendix, Fig. S5) (3). GRMZM2G004483 shows 36% protein sequence identity to ZmCCT (SI Appendix, Fig. S6), a CCT paralog residing on chromosome 10 that was recently shown to play an important role in the regulation of maize photoperiod flowering (6, 7, 26). To distinguish these two CCT genes, we hereafter refer to them as ZmCCT9 and ZmCCT10 based on the chromosomes on which they reside. We speculate that ZmCCT9 is most likely the target gene regulated by qDTA9 and that the Harbinger-like element in the 2.4-kb causative region for qDTA9 is a distant cis-regulatory variant of ZmCCT9 that alters ZmCCT9 expression to control flowering time.
Knockout of ZmCCT9 Causes Early Flowering Under Long Days.
To validate the function of ZmCCT9, we knocked out the endogenous ZmCCT9 gene in maize inbred line ZC01 using CRISPR/Cas9 technology (31, 32). Two 20-bp sequences in the first and second exons of ZmCCT9 were selected as target sites for Cas9 cleavage (Fig. 2A). PCR and sequencing analysis of 20 independent first-generation (T0) transgenic lines identified three homozygous mutations with deletions in the target sites that truncated the ZmCCT9 ORF; these are referred to as KO#1, KO#2, and KO#3 (Fig. 2B and SI Appendix, Fig. S7). These three null mutants were self-pollinated, and the resulting T1 progenies were planted in natural LD conditions to investigate their flowering times. Notably, all three null mutants (KO#1, KO#2, and KO#3) flowered significantly earlier than wild-type plants under LD conditions (Fig. 2 C–E), strongly indicating that ZmCCT9 is involved in the regulation of flowering time in maize.
Fig. 2.
ZmCCT9 Is Diurnally Regulated and Exhibits Differential Expression Between the Maize Allele and the Teosinte Allele.
To elucidate the cellular localization of ZmCCT9, we introduced the ZmCCT9-GFP and ZmCCT9-EGFP fusion genes under the control of the CaMV35S promoter into onion epidermal cells and maize protoplasts, respectively. The results showed that the GFP signal is localized to the nucleus (Fig. 3A), supporting a role for ZmCCT9 as a nuclear transcription factor. To determine whether the upstream Harbinger-like element altered ZmCCT9 expression, we investigated the spatiotemporal expression patterns of ZmCCT9 in NIL(maize) and NIL(teosinte) under LD conditions. ZmCCT9 was expressed mainly in mature leaves (Fig. 3B) and showed higher expression in NIL(teosinte) than in NIL(maize) at all examined growth stages, with a maximum difference in expression at the V4 stage (Fig. 3C). RNA in situ hybridization analysis showed that ZmCCT9 primarily accumulates in leaf vascular bundles and sclerenchyma fiber cells (Fig. 3D).
Fig. 3.
Genes involved in photoperiod flowering are diurnally regulated (2–4, 7, 33–37). We therefore examined the diurnal expression patterns of ZmCCT9 in mature leaves of NIL(maize) and NIL(teosinte) under artificial LD and SD conditions. Under LD conditions, ZmCCT9 transcript levels in NIL(teosinte) showed strong diurnal oscillation, with the highest expression 3 h after dawn; in contrast, the amplitude of ZmCCT9 expression in NIL(maize) was significantly attenuated (Fig. 3E). Under SD conditions, ZmCCT9 in NIL(maize) and NIL(teosinte) showed similar weak diurnal expression patterns (Fig. 3E). These results suggest that ZmCCT9 is diurnally regulated and that the maize allele exhibits a much reduced photoperiod sensitivity relative to the teosinte allele, likely due to the repressive effect of the Harbinger-like element in the 2.4-kb causative region for qDTA9.
The Harbinger-Like Element Acts in Cis to Repress ZmCCT9 Expression to Promote Flowering Under Long Days.
To test the effect of the Harbinger-like element on gene expression, we cloned the maize and teosinte sequences that differed only at the Harbinger-like element (SI Appendix, Fig. S8) into reporter constructs upstream of the minimal promoter of the cauliflower mosaic virus (mpCaMV), the firefly luciferase (LUC) ORF, and the nopaline synthase terminator (Fig. 4A) and compared their effect on gene expression in maize leaf protoplasts (Fig. 4B). The results showed that the maize construct containing the Harbinger-like element significantly repressed luciferase activity relative to the teosinte construct without the Harbinger-like element and the empty construct (Fig. 4B). However, no significant differences between the teosinte construct and the empty construct were detected (Fig. 4B). These results suggest that the Harbinger-like element represses LUC expression and, by inference, ZmCCT9 expression in vivo.
Fig. 4.
The importance of qDTA9 has been observed consistently in previous flowering-time mapping studies (13, 22, 27, 30, 38). qDTA9 was one of the largest-effect flowering-time QTLs detected under LD conditions in a maize nested association mapping (NAM) population consisting of 5,000 RILs derived from crossing 25 diverse inbred lines to a common parent, B73 (13). We found that the Harbinger-like genotypes across the 26 NAM founders were highly consistent with the QTL segregation patterns across the NAM population (Fig. 4C). The effect of qDTA9 was detected mainly in tropical NAM founders that lack the Harbinger-like element, and these lines consistently exhibited delayed flowering relative to the reference temperate line B73 harboring the Harbinger-like element (Fig. 4C). Conversely, NAM founders carrying the Harbinger-like element tended to have no effect at qDTA9 (Fig. 4C).
Cis-acting variants typically affect the transcription of their target genes in an allele-specific manner (6, 23, 39, 40). We measured allele-specific ZmCCT9 transcript abundance in mature leaves of F1 crosses between the 25 NAM founders and the reference B73. The results showed that the NAM founders lacking the Harbinger-like element, which are mostly tropical lines, consistently exhibited higher expression of ZmCCT9 than the B73 allele under LD conditions (Fig. 4C), which highly corresponds with the QTL segregation patterns across the NAM founders. Taken together, these data further demonstrate that the Harbinger-like element acts in cis to repress ZmCCT9 expression to promote flowering under LD conditions.
ZmCCT9 Functions Upstream of ZCN8 to Regulate Flowering Time.
To determine the regulatory relationship of ZmCCT9 in the maize photoperiod pathway, we examined the expression patterns of several known photoperiod genes (Gigz1a, ZCN8, ZmCCT10, and CONZ1) (6, 7, 26, 37, 41, 42) in mature leaves of NIL(maize) and NIL(teosinte) under LD conditions. Interestingly, of these genes, only ZCN8, which encodes the maize florigen and functions as a floral activator (37, 42), exhibited significant difference in expression in the two NILs; NIL(maize) showed higher expression of ZCN8 than NIL(teosinte), indicating that ZCN8 is negatively regulated by ZmCCT9 under LD conditions (SI Appendix, Fig. S9). Consistent with this result, ZCN8 expression was significantly elevated in CRISPR/Cas9-engineered null mutants compared with wild-type plants under LD conditions (SI Appendix, Fig. S10). Analysis of diurnal expression of these photoperiod-related genes further showed that only ZCN8 exhibited differential diurnal expression in NIL(maize) and NIL(teosinte) under LD conditions (SI Appendix, Fig. S11A). However, ZCN8 showed similar diurnal expression patterns in NIL(maize) and NIL(teosinte) under SD conditions (SI Appendix, Fig. S11B). Taken together, these results suggest that ZmCCT9 functions as a critical LD suppressor connecting ZCN8 expression and the circadian network.
The Harbinger-Like Element Arose After Initial Domestication and Was Targeted by Selection.
To examine the evolutionary origin of the Harbinger-like element, we genotyped the Harbinger-like locus in 73 diverse teosinte accessions (Z. mays ssp. parviglumis) (SI Appendix, Table S1). Interestingly, none of the investigated teosintes carried the Harbinger-like element, indicating that the Harbinger-like transposon insertion is most likely a de novo mutation that occurred after initial domestication. To determine whether selection has acted on the Harbinger-like element, we analyzed the nucleotide diversity across the 2.4-kb region in a panel of 27 diverse maize inbred lines and 19 teosinte (Z. mays ssp. parviglumis) accessions (Fig. 5A and SI Appendix, Table S2). Interestingly, in the A region flanking the Harbinger-like element, maize lines carrying the Harbinger-like element retained only 7.8% of the nucleotide diversity of teosinte (Fig. 5B). A coalescence simulation incorporating the maize domestication bottleneck (43–45) showed that this severe loss of genetic diversity cannot be explained by the maize domestication bottleneck alone, indicating a strong past selection near the Harbinger-like element. No significant selection signals were detected at regions B and C (Fig. 5B). Phylogenetic analysis of the A region clearly separated lines carrying the Harbinger-like element from lines lacking it, such that all teosintes cluster together with maize lines lacking the Harbinger-like element (SI Appendix, Fig. S12).
Fig. 5.
The Two Transposon Insertions at ZmCCT9 and ZmCCT10 Arose Sequentially Following Domestication and Exhibited Strong Latitudinal Adaptation.
We previously cloned ZmCCT10, which controls the largest-effect flowering-time QTL, qDTA10, in the same maize-teosinte BC2S3 population and the maize NAM population (6). A CACTA-like transposon insertion at the promoter of ZmCCT10 was found to be the causative variant (7). Interestingly, both the Harbinger-like transposon insertion at ZmCCT9 and the CACTA-like transposon insertion at ZmCCT10 are de novo mutations that occurred after initial domestication and show evidence of selection. To reveal how these two transposable elements contributed to maize flowering-time adaptation, we analyzed their allele distribution in the 513 modern maize inbred lines that were used in the association mapping. We found that 51.4% of tropical inbred lines carried the CACTA-like transposon at ZmCCT10 and that this percentage further increased to 85.4% in temperate inbred lines (Fig. 5C). However, the Harbinger-like transposon insertion at ZmCCT9 remained at a low frequency (10.3%) in tropical inbred lines but increased to 79% in temperate inbred lines (Fig. 5C). These contrasting frequency distributions suggest that these two transposons might be associated with distinct patterns of geographic dispersal. To test this hypothesis, we investigated the distribution of these two transposons among 1,008 maize landrace accessions (SI Appendix, Table S3) representing the entire pre-Columbian range of maize races native to the Americas (46, 47). As expected, both transposons showed strong associations with latitude, with both predominantly accumulating at higher latitudes (Fig. 5 D–H). However, closer inspection showed that the two transposons exhibit different frequency distributions along latitudes (Fig. 5H). Compared with the Harbinger-like transposon insertion at ZmCCT9, which occurs at low frequency at low latitudes, the CACTA-like transposon insertion at ZmCCT10 occurs at a relatively higher frequency at low latitudes (Fig. 5H), suggesting that the CACTA-like transposon insertion at ZmCCT10 arose earlier than the Harbinger-like transposon insertion at ZmCCT9. To verify this, we performed molecular dating using previously described methods (48). The results showed that the CACTA-like transposon insertion and the Harbinger-like transposon insertion arose ∼7,269 and ∼4,645 y B.P., respectively. These estimates suggest that both transposon insertions arose postdomestication and that the Harbinger-like transposon insertion at ZmCCT9 arose ∼2,624 y later than the CACTA-like transposon insertion at ZmCCT10, thereby leading to the differences in the geographic range.
Conclusions
In summary, this work uncovered a distant Harbinger-like transposon acting in cis to alter ZmCCT9 expression to regulate maize flowering time. ZmCCT9 confers LD-dependent flowering repression by negatively regulating the expression of the florigen ZCN8. The two transposon insertions at ZmCCT10 and ZmCCT9 arose sequentially after the initial domestication of maize and were targeted by selection as maize spread from its tropical origin to higher latitudes. Additionally, a transposable element insertion at Vgt1, a third locus involved in maize adaption to higher latitudes, has also been identified as a candidate causal variant (23–25). These findings further demonstrate the important roles of transposable elements in creating functional variation and driving species evolution (7, 23, 48–53), as inferred by Barbara McClintock decades ago (21). Moreover, our results help explain how the dynamic maize genome with abundant transposon activity enabled maize to “break the rule” that latitude constrains crop diffusion and was spread by its Native American inventors over 90° of latitude from Chile to Canada during the pre-Columbian era. The selection of natural regulatory variation at paralogs with similar biological functions might represent an efficient and prevalent strategy for local adaptation of crops.
Materials and Methods
Plant materials are described in SI Appendix, SI Materials and Methods. Details of the methods and experimental procedures are provided in SI Appendix, SI Materials and Methods, including fine mapping, association mapping, transgenic analysis, RNA extraction, quantitative real-time PCR analysis, RACE, subcellular localization, RNA in situ hybridization, protoplast transient expression assay, allele-specific expression assay, nucleotide diversity analysis, selection test, molecular dating analysis, and phylogenetic analysis.
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. MG233400–MG233921).
Acknowledgments
We thank Jigang Li (State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University) and Lubin Tan (Department of Plant Genetics and Breeding, China Agricultural University) for helpful discussions and advice on molecular experiments. This work was supported by grants from the National Key Research and Development Program of China (2016YFD0100404 and 2016YFD0100303); the National Natural Science Foundation of China (31771806 and 91535108); and the Recruitment Program of Global Experts and the Fundamental Research Funds for the Central Universities.
Supporting Information
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Copyright © 2018 the Author(s). Published by PNAS. This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).
Data Availability
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession nos. MG233400–MG233921).
Submission history
Published online: December 26, 2017
Published in issue: January 9, 2018
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Acknowledgments
We thank Jigang Li (State Key Laboratory of Plant Physiology and Biochemistry, China Agricultural University) and Lubin Tan (Department of Plant Genetics and Breeding, China Agricultural University) for helpful discussions and advice on molecular experiments. This work was supported by grants from the National Key Research and Development Program of China (2016YFD0100404 and 2016YFD0100303); the National Natural Science Foundation of China (31771806 and 91535108); and the Recruitment Program of Global Experts and the Fundamental Research Funds for the Central Universities.
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The authors declare no conflict of interest.
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