From many, one: genetic control of prolificacy during maize domestication.
ABSTRACT: A reduction in number and an increase in size of inflorescences is a common aspect of plant domestication. When maize was domesticated from teosinte, the number and arrangement of ears changed dramatically. Teosinte has long lateral branches that bear multiple small ears at their nodes and tassels at their tips. Maize has much shorter lateral branches that are tipped by a single large ear with no additional ears at the branch nodes. To investigate the genetic basis of this difference in prolificacy (the number of ears on a plant), we performed a genome-wide QTL scan. A large effect QTL for prolificacy (prol1.1) was detected on the short arm of chromosome 1 in a location that has previously been shown to influence multiple domestication traits. We fine-mapped prol1.1 to a 2.7 kb "causative region" upstream of the grassy tillers1 (gt1) gene, which encodes a homeodomain leucine zipper transcription factor. Tissue in situ hybridizations reveal that the maize allele of prol1.1 is associated with up-regulation of gt1 expression in the nodal plexus. Given that maize does not initiate secondary ear buds, the expression of gt1 in the nodal plexus in maize may suppress their initiation. Population genetic analyses indicate positive selection on the maize allele of prol1.1, causing a partial sweep that fixed the maize allele throughout most of domesticated maize. This work shows how a subtle cis-regulatory change in tissue specific gene expression altered plant architecture in a way that improved the harvestability of maize.
Project description:Genomic scans for genes that show the signature of past selection have been widely applied to a number of species and have identified a large number of selection candidate genes. In cultivated maize (Zea mays ssp. mays) selection scans have identified several hundred candidate domestication genes by comparing nucleotide diversity and differentiation between maize and its progenitor, teosinte (Z. mays ssp. parviglumis). One of these is a gene called zea agamous-like1 (zagl1), a MADS-box transcription factor, that is known for its function in the control of flowering time. To determine the trait(s) controlled by zagl1 that was (were) the target(s) of selection during maize domestication, we created a set of recombinant chromosome isogenic lines that differ for the maize versus teosinte alleles of zagl1 and which carry cross-overs between zagl1 and its neighbor genes. These lines were grown in a randomized trial and scored for flowering time and domestication related traits. The results indicated that the maize versus teosinte alleles of zagl1 affect flowering time as expected, as well as multiple traits related to ear size with the maize allele conferring larger ears with more kernels. Our results suggest that zagl1 may have been under selection during domestication to increase the size of the maize ear.
Project description:Many domesticated crop plants have been bred for increased apical dominance, displaying greatly reduced axillary branching compared to their wild ancestors. In maize, this was achieved through selection for a gain-of-function allele of the TCP transcription factor teosinte branched1 (tb1). The mechanism for how a dominant Tb1 allele increased apical dominance, is unknown. Through ChIP seq, RNA seq, hormone and sugar measurements on 1?mm axillary bud tissue, we identify the genetic pathways putatively regulated by TB1. These include pathways regulating phytohormones such as gibberellins, abscisic acid and jasmonic acid, but surprisingly, not auxin. In addition, metabolites involved in sugar sensing such as trehalose 6-phosphate were increased. This suggests that TB1 induces bud suppression through the production of inhibitory phytohormones and by reducing sugar levels and energy balance. Interestingly, TB1 also putatively targets several other domestication loci, including teosinte glume architecture1, prol1.1/grassy tillers1, as well as itself. This places tb1 on top of the domestication hierarchy, demonstrating its critical importance during the domestication of maize from teosinte.
Project description:We examined pollen grains and starch granules from a large number of modern populations of teosinte (wild Zea spp.), maize (Zea mays L.), and closely related grasses in the genus Tripsacum to assess their strengths and weaknesses in studying the origins and early dispersals of maize in its Mesoamerican cradle of origin. We report new diagnostic criteria and question the accuracy of others used previously by investigators to identify ancient maize where its wild ancestor, teosinte, is native. Pollen grains from teosinte overlap in size with those of maize to a much greater degree than previously reported, making the differentiation of wild and domesticated maize in palynological studies difficult. There is presently no valid method for separating maize and teosinte pollen on a morphological basis. Starch grain analysis, a recently developed tool of archaeobotany, appears to be of significant utility in distinguishing the seeds of teosinte from maize. We propose that the differences in starch grain morphology and size between wild and domesticated maize defined in this study may be associated with domestication genes in Zea that have been documented in the starch biosynthesis pathway. As previously reported, phytoliths effectively discriminate the female reproductive structures of Tripsacum, teosinte, and maize. Multiproxy microfossil studies of archaeological and paleoecological contexts appear to be effective tools for investigating the earliest stages of maize domestication and dispersals.
Project description:The shape of a plant is largely determined by regulation of lateral branching. Branching architecture can vary widely in response to both genotype and environment, suggesting regulation by a complex interaction of autonomous genetic factors and external signals. Tillers, branches initiated at the base of grass plants, are suppressed in response to shade conditions. This suppression of tiller and lateral branch growth is an important trait selected by early agriculturalists during maize domestication and crop improvement. To understand how plants integrate external environmental cues with endogenous signals to control their architecture, we have begun a functional characterization of the maize mutant grassy tillers1 (gt1). We isolated the gt1 gene using positional cloning and found that it encodes a class I homeodomain leucine zipper gene that promotes lateral bud dormancy and suppresses elongation of lateral ear branches. The gt1 expression is induced by shading and is dependent on the activity of teosinte branched1 (tb1), a major domestication locus controlling tillering and lateral branching. Interestingly, like tb1, gt1 maps to a quantitative trait locus that regulates tillering and lateral branching in maize and shows evidence of selection during maize domestication. Branching and shade avoidance are both of critical agronomic importance, but little is known about how these processes are integrated. Our results indicate that gt1 mediates the reduced branching associated with the shade avoidance response in the grasses. Furthermore, selection at the gt1 locus suggests that it was involved in improving plant architecture during the domestication of maize.
Project description:Domestication research has largely focused on identification of morphological and genetic differences between extant populations of crops and their wild relatives. Little attention has been paid to the potential effects of environment despite substantial known changes in climate from the time of domestication to modern day. In recent research, the exposure of teosinte (i.e., wild maize) to environments similar to the time of domestication, resulted in a plastic induction of domesticated phenotypes in teosinte. These results suggest that early agriculturalists may have selected for genetic mechanisms that cemented domestication phenotypes initially induced by a plastic response of teosinte to environment, a process known as genetic assimilation. To better understand this phenomenon and the potential role of environment in maize domestication, we examined differential gene expression in maize (Zea mays ssp. mays) and teosinte (Zea mays ssp. parviglumis) between past and present conditions. We identified a gene set of over 2000 loci showing a change in expression across environmental conditions in teosinte and invariance in maize. In fact, overall we observed both greater plasticity in gene expression and more substantial changes in co-expressionnal networks in teosinte across environments when compared to maize. While these results suggest genetic assimilation played at least some role in domestication, genes showing expression patterns consistent with assimilation are not significantly enriched for previously identified domestication candidates, indicating assimilation did not have a genome-wide effect.
Project description:The last two decades have seen important advances in our knowledge of maize domestication, thanks in part to the contributions of genetic data. Genetic studies have provided firm evidence that maize was domesticated from Balsas teosinte (Zea mays subspecies parviglumis), a wild relative that is endemic to the mid- to lowland regions of southwestern Mexico. An interesting paradox remains, however: Maize cultivars that are most closely related to Balsas teosinte are found mainly in the Mexican highlands where subspecies parviglumis does not grow. Genetic data thus point to primary diffusion of domesticated maize from the highlands rather than from the region of initial domestication. Recent archeological evidence for early lowland cultivation has been consistent with the genetics of domestication, leaving the issue of the ancestral position of highland maize unresolved. We used a new SNP dataset scored in a large number of accessions of both teosinte and maize to take a second look at the geography of the earliest cultivated maize. We found that gene flow between maize and its wild relatives meaningfully impacts our inference of geographic origins. By analyzing differentiation from inferred ancestral gene frequencies, we obtained results that are fully consistent with current ecological, archeological, and genetic data concerning the geography of early maize cultivation.
Project description:The prolamin-box binding factor1 (pbf1) gene encodes a transcription factor that controls the expression of seed storage protein (zein) genes in maize. Prior studies show that pbf1 underwent selection during maize domestication although how it affected trait change during domestication is unknown. To assay how pbf1 affects phenotypic differences between maize and teosinte, we compared nearly isogenic lines (NILs) that differ for a maize versus teosinte allele of pbf1 Kernel weight for the teosinte NIL (162mg) is slightly but significantly greater than that for the maize NIL (156mg). RNAseq data for developing kernels show that the teosinte allele of pbf1 is expressed at about twice the level of the maize allele. However, RNA and protein assays showed no difference in zein profile between the two NILs. The lower expression for the maize pbf1 allele suggests that selection may have favored this change; however, how reduced pbf1 expression alters phenotype remains unknown. One possibility is that pbf1 regulates genes other than zeins and thereby is a domestication trait. The observed drop in seed weight associated with the maize allele of pbf1 is counterintuitive but could represent a negative pleiotropic effect of selection on some other aspect of kernel composition.
Project description:Gene expression differences between divergent lineages caused by modification of cis regulatory elements are thought to be important in evolution. We assayed genome-wide cis and trans regulatory differences between maize and its wild progenitor, teosinte, using deep RNA sequencing in F1 hybrid and parent inbred lines for three tissue types (ear, leaf and stem). Pervasive regulatory variation was observed with approximately 70% of ?17,000 genes showing evidence of regulatory divergence between maize and teosinte. However, many fewer genes (1,079 genes) show consistent cis differences with all sampled maize and teosinte lines. For ?70% of these 1,079 genes, the cis differences are specific to a single tissue. The number of genes with cis regulatory differences is greatest for ear tissue, which underwent a drastic transformation in form during domestication. As expected from the domestication bottleneck, maize possesses less cis regulatory variation than teosinte with this deficit greatest for genes showing maize-teosinte cis regulatory divergence, suggesting selection on cis regulatory differences during domestication. Consistent with selection on cis regulatory elements, genes with cis effects correlated strongly with genes under positive selection during maize domestication and improvement, while genes with trans regulatory effects did not. We observed a directional bias such that genes with cis differences showed higher expression of the maize allele more often than the teosinte allele, suggesting domestication favored up-regulation of gene expression. Finally, this work documents the cis and trans regulatory changes between maize and teosinte in over 17,000 genes for three tissues.
Project description:The process of evolution under domestication has been studied using phylogenetics, population genetics-genomics, quantitative trait locus (QTL) mapping, gene expression assays, and archaeology. Here, we apply an evolutionary quantitative genetic approach to understand the constraints imposed by the genetic architecture of trait variation in teosinte, the wild ancestor of maize, and the consequences of domestication on genetic architecture. Using modern teosinte and maize landrace populations as proxies for the ancestor and domesticate, respectively, we estimated heritabilities, additive and dominance genetic variances, genetic-by-environment variances, genetic correlations, and genetic covariances for 18 domestication-related traits using realized genomic relationships estimated from genome-wide markers. We found a reduction in heritabilities across most traits, and the reduction is stronger in reproductive traits (size and numbers of grains and ears) than vegetative traits. We observed larger depletion in additive genetic variance than dominance genetic variance. Selection intensities during domestication were weak for all traits, with reproductive traits showing the highest values. For 17 of 18 traits, neutral divergence is rejected, suggesting they were targets of selection during domestication. Yield (total grain weight) per plant is the sole trait that selection does not appear to have improved in maize relative to teosinte. From a multivariate evolution perspective, we identified a strong, nonneutral divergence between teosinte and maize landrace genetic variance-covariance matrices (G-matrices). While the structure of G-matrix in teosinte posed considerable genetic constraint on early domestication, the maize landrace G-matrix indicates that the degree of constraint is more unfavorable for further evolution along the same trajectory.
Project description:The effects of an allelic substitution at a gene often depend critically on genetic background, i.e., the genotypes at other genes in the genome. During the domestication of maize from its wild ancestor (teosinte), an allelic substitution at teosinte branched (tb1) caused changes in both plant and ear architecture. The effects of tb1 on phenotype were shown to depend on multiple background loci, including one called enhancer of tb1.2 (etb1.2). We mapped etb1.2 to a YABBY class transcription factor (ZmYAB2.1) and showed that the maize alleles of ZmYAB2.1 are either expressed at a lower level than teosinte alleles or disrupted by insertions in the sequences. tb1 and etb1.2 interact epistatically to control the length of internodes within the maize ear, which affects how densely the kernels are packed on the ear. The interaction effect is also observed at the level of gene expression, with tb1 acting as a repressor of ZmYAB2.1 expression. Curiously, ZmYAB2.1 was previously identified as a candidate gene for another domestication trait in maize, nonshattering ears. Consistent with this proposed role, ZmYAB2.1 is expressed in a narrow band of cells in immature ears that appears to represent a vestigial abscission (shattering) zone. Expression in this band of cells may also underlie the effect on internode elongation. The identification of ZmYAB2.1 as a background factor interacting with tb1 is a first step toward a gene-level understanding of how tb1 and the background within which it works evolved in concert during maize domestication.