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Key Message Modeling of the distribution of allele frequency over year of variety release identifies major loci involved in historical breeding of winter wheat. Abstract Winter wheat is a major crop with a rich selection history in the modern era of crop breeding. Genetic gains across economically important traits like yield have been well characterized and are the major force driving its production. Winter wheat is also an excellent model for analyzing historical genetic selection. As a proof of concept, we analyze two major collections of winter wheat varieties that were bred in Western Europe from 1916 to 2010, namely the Triticeae Genome (TG) and WAGTAIL panels, which include 333 and 403 varieties, respectively. We develop and apply a selection mapping approach, Regression of Alleles on Years (RALLY), in these panels, as well as in simulated populations. RALLY maps loci under sustained historical selection by using a simple logistic model to regress allele counts on years of variety release. To control for drift-induced allele frequency change, we develop a hybrid approach of genomic control and delta control. Within the TG panel, we identify 22 significant RALLY quantitative selection loci (QSLs) and estimate the local heritabilities for 12 traits across these QSLs. By correlating predicted marker effects with RALLY regression estimates, we show that alleles whose frequencies have increased over time are heavily biased toward conferring positive yield effect, but negative effects in flowering time, lodging, plant height and grain protein content. Altogether, our results (1) demonstrate the use of RALLY to identify selected genomic regions while controlling for drift, and (2) reveal key patterns in the historical selection in winter wheat and guide its future breeding.

Modern crop breeding is in constant demand for new genetic diversity as part of the arms race with genetic gain. The elite gene pool has limited genetic variation and breeders are trying to introduce novelty from unadapted germplasm, landraces and wild relatives. For polygenic traits, currently available approaches to introgression are not ideal, as there is a demonstrable bias against exotic alleles during selection. Here, we propose a partitioned form of genomic selection, called Origin Specific Genomic Selection (OSGS), where we identify and target selection on favorable exotic alleles. Briefly, within a population derived from a bi-parental cross, we isolate alleles originating from the elite and exotic parents, which then allows us to separate out the predicted marker effects based on the allele origins. We validated the usefulness of OSGS using two nested association mapping (NAM) datasets: barley NAM (elite-exotic) and maize NAM (elite-elite), as well as by computer simulation. Our results suggest that OSGS works well in its goal to increase the contribution of favorable exotic alleles in bi-parental crosses, and it is possible to extend the approach to broader multi-parental populations.

Significance We investigated the genetic architecture of maize domestication using a quantitative genetics approach. With multiple populations of teosinte and maize, we also compared the genetic architecture among populations within maize and teosinte. We showed that genetic architecture among populations within teosinte or maize is generally conserved, in contrast to the radical differences between teosinte and maize. Our results suggest that while selection drove changes in essentially all traits between teosinte and maize, selection is far less important for explaining domestication trait differences among populations within teosinte or maize., Very little is known about how domestication was constrained by the quantitative genetic architecture of crop progenitors and how quantitative genetic architecture was altered by domestication. Yang et al. [C. J. Yang et al., Proc. Natl. Acad. Sci. U.S.A. 116, 5643–5652 (2019)] drew multiple conclusions about how genetic architecture influenced and was altered by maize domestication based on one sympatric pair of teosinte and maize populations. To test the generality of their conclusions, we assayed the structure of genetic variances, genetic correlations among traits, strength of selection during domestication, and diversity in genetic architecture within teosinte and maize. Our results confirm that additive genetic variance is decreased, while dominance genetic variance is increased, during maize domestication. The genetic correlations are moderately conserved among traits between teosinte and maize, while the genetic variance–covariance matrices (G-matrices) of teosinte and maize are quite different, primarily due to changes in the submatrix for reproductive traits. The inferred long-term selection intensities during domestication were weak, and the neutral hypothesis was rejected for reproductive and environmental response traits, suggesting that they were targets of selection during domestication. The G-matrix of teosinte imposed considerable constraint on selection during the early domestication process, and constraint increased further along the domestication trajectory. Finally, we assayed variation among populations and observed that genetic architecture is generally conserved among populations within teosinte and maize but is radically different between teosinte and maize. While selection drove changes in essentially all traits between teosinte and maize, selection explains little of the difference in domestication traits among populations within teosinte or maize.

Inbreeding depression is the reduction in fitness and vigor resulting from mating of close relatives observed in many plant and animal species. The extent to which the genetic load of mutations contributing to inbreeding depression is due to rare large-effect variation versus potentially more common variants with very small individual effects is unknown and may be affected by population history. We compared the effects of outcrossing and self-fertilization on 18 traits in a landrace population of maize, which underwent a population bottleneck during domestication, and a neighboring population of its wild relative teosinte. Inbreeding depression was greater in maize than teosinte for 15 of 18 traits, congruent with the greater segregating genetic load predicted from sequence data in the maize population. For many traits - and more commonly in maize - genetic variation among selffertilized families was less than expected based on additive and dominance variance estimated in outcrossed families, suggesting that a negative covariance between additive and homozygous dominance effects limits the variation available to selection under partial inbreeding. We identified quantitative trait loci (QTL) representing large-effect rare variants carried by only a single parent, which were more important in teosinte than maize. Teosinte also carried more putative juvenile-acting lethal variants identified by segregation distortion. These results suggest a mixture of mostly polygenic, smalleffect recessive variation underlying inbreeding depression, with an additional contribution from rare larger-effect variants that was more important in teosinte but depleted in maize following to the domestication bottleneck. Purging associated with the maize domestication bottleneck may have selected against large effect variants, but polygenic load is harder to purge and segregating mutational burden increased in maize compared to teosinte.

Multiparental Advanced Generation Inter-Cross (MAGIC) populations are valuable crop resources with a wide array of research uses including genetic mapping of complex traits, management of genetic resources and breeding of new varieties. Multiple founders are crossed to create a rich mosaic of highly recombined founder genomes in the MAGIC recombinant inbred lines (RILs). Many variations of MAGIC population designs exist; however, a large proportion of the currently available populations have been created empirically and based on similar designs. In our evaluations of five MAGIC populations, we found that the choice of designs has a large impact on the recombination landscape in the RILs. The most popular design used in many MAGIC populations has been shown to have a bias in recombinant haplotypes and low level of unique recombinant haplotypes, and therefore is not recommended. To address this problem and provide a remedy for the future, we have developed the “magicdesign” R package for creating and testing any MAGIC population design via simulation. A Shiny app version of the package is available as well. Our “magicdesign” package provides a unifying tool and a framework for creativity and innovation in MAGIC population designs. For example, using this package, we demonstrate that MAGIC population designs can be found which are very effective in creating haplotype diversity without the requirement for very large crossing programs. Furthermore, we show that interspersing cycles of crossing with cycles of selfing is effective in increasing haplotype diversity. These approaches are applicable in species that are hard to cross or in which resources are limited.

Recombinant inbred lines (RILs) are an important resource for mapping genes controlling complex traits in many species. While RIL populations have been developed for maize, a maize RIL population with multiple teosinte inbred lines as parents has been lacking. Here, we report a teosinte nested association mapping population (TeoNAM), derived from crossing five teosinte inbreds to the maize inbred line W22. The resulting 1257 BC1S4RILs were genotyped with 51,544 SNPs, providing a high-density genetic map with a length of 1540 cM. On average, each RIL is 15% homozygous teosinte and 8% heterozygous. We performed joint linkage mapping (JLM) and genome-wide association study (GWAS) for 22 domestication and agronomic traits. A total of 255 QTLs from JLM were identified with many of these mapping to known genes or novel candidate genes. TeoNAM is a useful resource for QTL mapping for the discovery of novel allelic variation from teosinte. TeoNAM provides the first report thatPROSTRATE GROWTH1, a rice domestication gene, is also a QTL associated with tillering in teosinte and maize. We detected multiple QTLs for flowering time and other traits for which the teosinte allele contributes to a more maize-like phenotype. Such QTL could be valuable in maize improvement.

Significance Crop domestication is a well-established system for understanding evolution. We interrogated the genetic architecture of maize domestication from a quantitative genetics perspective. We analyzed domestication-related traits in a maize landrace and a population of its ancestor, teosinte. We observed strong divergence in the underlying genetic architecture including change in the genetic correlations among traits. Despite striking divergence, selection intensities were low for all traits, indicating that selection under domestication can be weaker than natural selection. Analyses suggest total grain weight per plant was not improved and that genetic correlations placed considerable constraint on selection. We hope our results will motivate crop evolutionists to perform similar work in other crops., 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.

Distinctness, Uniformity and Stability (DUS) is an intellectual property system introduced in 1961 by the International Union for the Protection of New Varieties of Plants (UPOV) for safeguarding the investment and rewarding innovation in developing new plant varieties. Despite the rapid advancement in our understanding of crop biology over the past 60 years, the DUS system has changed little and is still largely dependent upon a set of morphological traits for testing candidate varieties. As the demand for more plant varieties increases, the barriers to registration of new varieties become more acute and thus require urgent review to the system. To highlight the challenges and remedies in the current system, we evaluated a comprehensive panel of 805 UK barley varieties that span the entire history of DUS testing. Our findings reveal the system deficiencies such as inconsistencies in DUS traits across environments, limitations in DUS trait combinatorial space, and inadequacies in currently available DUS markers. We advocate the concept of genomic DUS and provide evidence for a shift towards a robust genomics-enabled registration system for new crop varieties., Yang et al. use a genomic approach to evaluate a panel of 805 UK barley varieties and the value of the DUS system for plant registration. Their findings suggest that morphological traits are not appropriate for registering new barley varieties, and suggest that a genomic system should be developed for future use.

Distinctness, Uniformity and Stability (DUS) is an intellectual property system introduced in 1961 by the International Union for the Protection of New Varieties of Plants (UPOV) for safeguarding the investment and rewarding innovation in developing new plant varieties. Despite the rapid advancement in our understanding of crop biology over the past 60 years, the DUS system has not changed and is still dependent upon a set of morphological traits for testing candidate varieties. As the demand for more plant varieties increases, the barriers to registration of new varieties become more acute and thus require urgent review to the system. To highlight the challenges and remedies in the current system, we evaluated a comprehensive panel of 805 UK barley varieties that span the entire history of DUS testing. Our findings reveal the system deficiencies and provide evidence for a shift towards a robust genomics enabled registration system for new crop varieties.

The genetics of domestication has been extensively studied ever since the rediscovery of Mendel’s law of inheritance and much has been learned about the genetic control of trait differences between crops and their ancestors. Here, we ask how domestication has altered genetic architecture by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. We observed a strongly reduced number of QTL for domestication traits in maize relative to teosinte, which is consistent with the previously reported depletion of additive variance by selection during domestication. We also observed more dominance in maize than teosinte, likely a consequence of selective removal of additive variants. We observed that large effect QTL have low minor allele frequency (MAF) in both maize and teosinte. Regions of the genome that are strongly differentiated between teosinte and maize (high FST) explain less quantitative variation in maize than teosinte, suggesting that, in these regions, allelic variants were brought to (or near) fixation during domestication. We also observed that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of the additive variance in both teosinte and maize is “missing” in the sense that it cannot be ascribed to detectable QTL and only 25% of variance maps to specific QTL. This latter result suggests that morphological evolution during domestication is largely attributable to very large numbers of QTL of very small effect., Author summary Although the genetics of trait differences between crops and their progenitors has been extensively studied, far less is known about the genetic architecture of trait variation in crop progenitors and how this architecture was altered during domestication. Here, we address this issue by comparing the genetic architecture of 18 domestication traits in maize and its ancestor teosinte using matched populations. Our results show that genetic architecture was reshaped during domestication in multiple ways. Maize has a greatly reduced number of QTL for domestication traits relative to teosinte and alleles at these QTL show greater dominance in maize. QTL alleles of large effect are present in both maize and teosinte, but more common in maize. We observed that regions of the genome that are strongly differentiated between teosinte and maize (high FST) explain less additive variation in maize than teosinte and that genomic regions of high recombination explain a disproportionately large proportion of heritable variance both before and after domestication. Finally, we observed that about 75% of heritability is “missing” in the sense that it not associated with detectable QTL, which suggests that the raw material for domestication was largely composed of vast numbers of QTL of diminishingly small effects.

Teosinte, the ancestor of maize, possesses multiple ears at each node along its main stalk, whereas maize has only a single ear at each node. With its greater ear number, teosinte is referred to as being more prolific. The grassy tillers 1 (gt1) gene has been identified as a large-effect quantitative trait locus underlying this prolificacy difference between maize and teosinte, and the causal polymorphism for the difference was mapped to a 2.7kb control region 5' of the gt1 ORF. The most common maize haplotype (M1) at the gt1 control region confers low prolificacy. A prior study reported that 29% of maize varieties possess the teosinte haplotype (T) for the control region, although these varieties are nonprolific. This observation suggested that these maize lines might possess an additional factor, other than gt1, suppressing prolificacy in maize. We discovered that the factor suppressing prolificacy in maize varieties with the gt1 T haplotype mapped to a 3.20 cM interval, which includes gt1 Subsequent DNA sequence analysis revealed that the maize varieties with the apparent T haplotype actually possess a distinct maize haplotype (M2) that is similar, but not identical, to the T haplotype in sequence but is associated with a nonprolific phenotype similar to the M1 haplotype. Our data indicate that the M2 haplotype or a closely linked factor confers a nonprolific phenotype. Our data suggest that 2 different alleles or haplotypes (M1 and M2) of gt1 were selected during domestication, and that nonprolificacy in all maize varieties is likely a result of allele substitutions at gt1.

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 center of origin, maize experienced a rapid range expansion and spread over 90° of latitude in the Americas [ 2 , 3 , 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 (QTL) (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 SNP (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.

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.

The effects of an allelic substitution at a gene often depend critically on genetic background, the genotype at other genes in the genome. During the domestication of maize from its wild ancestor (teosinte), an allelic substitution atteosinte branched(tb1) caused changes in both plant and ear architecture. The effects oftb1on phenotype were shown to depend on multiple background loci including one called enhancer oftb1.2 (etb1.2).We mappedetb1.2to a YABBY class transcription factor (ZmYAB2.1) and showed that the maize alleles ofZmYAB2.1are either expressed at a lower level than teosinte alleles or disrupted by insertions in the sequences.tb1andetb1.2interact 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 withtb1acting as a repressor ofZmYAB2.1expression. Curiously,ZmYAB2.1was previously identified as a candidate gene for another domestication trait in maize, non-shattering ears. Consistent with this proposed role,ZmYAB2.1is 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 ofZmYAB2.1as a background factor interacting withtb1is a first step toward a gene-level understanding of howtb1and the background within which it works evolved in concert during maize domestication.