SignificanceFlowering 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.
SUMMARY Maize (Zea mays ssp. mays) was domesticated in southwestern Mexico ~9,000 years ago from its wild ancestor, teosinte (Zea mays ssp. parviglumis) [1]. From its centre of origin, maize experienced a rapid range expansion and spread over 90°of latitude in the Americas [2–4] which required a novel flowering time adaptation. ZEA CENTRORADIALIS 8 (ZCN8) is the maize florigen gene and has a central role in mediating flowering [5, 6]. Here, we show that ZCN8 underlies a major quantitative trait locus (qDTA8) for flowering time that was consistently detected in multiple maize-teosinte experimental populations. Through association analysis in a large diverse panel of maize inbred lines, we identified a single nucleotide polymorphism (SNP-1245) in the ZCN8 promoter that showed the strongest association with flowering time. SNP-1245 co-segregated with qDTA8 in maize-teosinte mapping populations. We demonstrate that SNP-1245 is associated with differential binding by the flowering activator ZmMADS1. SNP-1245 was a target of selection during early domestication which drove the pre-existing early-flowering allele to near fixation in maize. Interestingly, we detected an independent association block upstream of SNP-1245, wherein the early-flowering allele that most likely originated from Zea mays ssp. mexicana introgressed into the early-flowering haplotype of SNP-1245 and contributed to maize adaptation to northern high latitudes. Our study demonstrates how independent cis-regulatory variants at a gene can be selected at different evolutionary times for local adaptation, highlighting how complex cis-regulatory control mechanisms evolve. Finally, we propose a polygenic map for the pre-Columbian spread of maize throughout the Americas.
Gene expression regulation plays an important role in controlling plant phenotypes and adaptation. Here, we report a comprehensive assessment of gene expression variation through the transcriptome analyses of a large maize-teosinte experimental population. Genome-wide mapping identified 25 660 expression quantitative trait loci (eQTL) for 17 311 genes, capturing an unprecedented range of expression variation. We found that local eQTL were more frequently mapped to adjacent genes, displaying a mode of expression piggybacking, which consequently created co-regulated gene clusters. Genes within the co-regulated gene clusters tend to have relevant functions and shared chromatin modifications. Distant eQTL formed 125 significant distant eQTL hotspots with their targets significantly enriched in specific functional categories. By integrating different sources of information, we identified putative trans- regulators for a variety of metabolic pathways. We demonstrated that the bHLH transcription factor R1 and hexokinase HEX9 might act as crucial regulators for flavonoid biosynthesis and glycolysis, respectively. Moreover, we showed that domestication or improvement has significantly affected global gene expression, with many genes targeted by selection. Of particular interest, the Bx genes for benzoxazinoid biosynthesis may have undergone coordinated cis-regulatory divergence between maize and teosinte, and a transposon insertion that inactivates Bx12 was under strong selection as maize spread into temperate environments with a distinct herbivore community.
Summary The number of leaves and their distributions on plants are critical factors determining plant architecture in maize (Zea mays), and leaf number is frequently used as a measure of flowering time, a trait that is key to local environmental adaptation.Here, using a large set of 866 maize‐teosinte BC 2S3 recombinant inbred lines genotyped by using 19 838 single nucleotide polymorphism markers, we conducted a comprehensive genetic dissection to assess the genetic architecture of leaf number and its genetic relationship to flowering time.We demonstrated that the two components of total leaf number, the number of leaves above (LA) and below (LB) the primary ear, were under relatively independent genetic control and might be subject to differential directional selection during maize domestication and improvement. Furthermore, we revealed that flowering time and leaf number are commonly regulated at a moderate level. The pleiotropy of the genes ZCN8, dlf1 and ZmCCT on leaf number and flowering time were validated by near‐isogenic line analysis. Through fine mapping, qLA1‐1, a major‐effect locus that specifically affects LA, was delimited to a region with severe recombination suppression derived from teosinte.This study provides important insights into the genetic basis of traits affecting plant architecture and adaptation. The genetic independence of LA from LB enables the optimization of leaf number for ideal plant architecture breeding in maize.
Summary Maize (Zea mays) tassels underwent profound morphological changes during maize domestication and improvement. Although a number of genes affecting maize inflorescence development have been identified, the genetic basis of the morphological changes in maize tassels since domestication is not well understood.Here, using a large population of 866 maize‐teosinte BC 2S3 recombinant inbred lines genotyped using 19 838 single nucleotide polymorphism (SNP) markers, we performed high‐resolution quantitative trait locus (QTL) mapping for five tassel morphological traits.We showed that the five tassel traits were associated with different genetic architecture features. Known genes for maize inflorescence development identified by mutagenesis were significantly enriched in the tassel trait QTLs, and many of these genes, including ramosa1 (ra1), barren inflorescence2 (bif2), unbranched2 (ub2), zea floricaula leafy2 (zfl2) and barren stalk fastigiate1 (baf1), showed evidence of selection. An in‐depth nucleotide diversity analysis at the bif2 locus identified strong selection signatures in the 5′‐regulatory region. We also found that several known flowering time genes co‐localized with tassel trait QTLs. A further association analysis indicated that the maize photoperiod gene ZmCCT was significantly associated with tassel size variation. Using near‐isogenic lines, we narrowed down a major‐effect QTL for tassel length, qTL9‐1, to a 513‐kb physical region.These results provide important insights into the genetic architecture that controls maize tassel evolution.
Summary Flowering time is a major determinant of the local adaptation of plants. Although numerous loci affecting flowering time have been mapped in maize, their underlying molecular mechanisms and roles in adaptation remain largely unknown. Here, we report the identification and characterization of MADS‐box transcription factor ZmMADS69 that functions as a flowering activator through the ZmRap2.7‐ZCN8 regulatory module and contributes to adaptation. We show that ZmMADS69 underlies a quantitative trait locus controlling the difference in flowering time between maize and its wild ancestor, teosinte. Maize ZmMADS69 allele is expressed at a higher level at floral transition and confers earlier flowering than the teosinte allele under long days and short days. Overexpression of ZmMADS69 causes early flowering, while a transposon insertion mutant of ZmMADS69 exhibits delayed flowering. ZmMADS69 shows pleiotropic effects for multiple traits of agronomic importance. ZmMADS69 functions upstream of the flowering repressor ZmRap2.7 to downregulate its expression, thereby relieving the repression of the florigen gene ZCN8 and causing early flowering. Population genetic analyses showed that ZmMADS69 was a target of selection and may have played an important role as maize spread from the tropics to temperate zones. Our findings provide important insights into the regulation and adaptation of flowering time.
Crops feed the world's population and shape human civilization. The improvement of crop productivity has been ongoing for almost 10,000 years and has evolved from an experience-based to a knowledge-driven practice over the past three decades. Natural alleles and their reshuffling are long-standing genetic changes that affect how crops respond to various environmental conditions and agricultural practices. Decoding the genetic basis of natural variation is central to understanding crop evolution and, in turn, improving crop breeding. Here, we review current advances in the approaches used to map the causal alleles of natural variation, provide refined insights into the genetics and evolution of natural variation, and outline how this knowledge promises to drive the development of sustainable agriculture under the dome of emerging technologies. Expected final online publication date for the Annual Review of Plant Biology, Volume 72 is May 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.
Alternative splicing (AS) enhances transcriptome diversity and plays important roles in regulating plant processes. Although widespread natural variation in AS has been observed in plants, how AS is regulated and contribute to phenotypic variation is poorly understood. Here, we report a population-level transcriptome assembly and genome-wide association study to identify splicing quantitative trait loci (sQTLs) in developing maize () kernels from 368 inbred lines. We detected 19,554 unique sQTLs for 6570 genes. Most sQTLs showed small isoform usage changes without involving major isoform switching between genotypes. The sQTL-affected isoforms tend to display distinct protein functions. We demonstrate that nonsense-mediated mRNA decay, microRNA-mediated regulation, and small interfering peptide-mediated peptide interference are frequently involved in sQTL regulation. The natural variation in AS and overall mRNA level appears to be independently regulated with different -sequences preferentially used. We identified 214 putative-acting splicing regulators, among which , encoding an hnRNP-like glycine-rich RNA binding protein, regulates the largest-cluster. Knockout of by CRISPR/Cas9 altered splicing of numerous downstream genes. We found that 739 sQTLs colocalized with previous marker-trait associations, most of which occurred without changes in overall mRNA level. Our findings uncover the importance of AS in diversifying gene function and regulating phenotypic variation.
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