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Stetter, M. G.

Publications and source records attributed to Stetter, M. G..

At least 19 recordsLinked to original sources

Standing genetic variation drives polygenic adaptation to different environmental shifts

Most organisms are well adapted to the environment they have been exposed to for many generations. However, changing environments pose existential threats to populations, unless they are able to adapt. Hence, a central challenge in evolutionary genetics is to understand the adaptation to complex environmental changes. As most traits are controlled by a large number of loci with varying effects on a trait, it is challenging to understand the explicit role of genetic changes during such polygenic adaptation. We use forward-in-time simulations to investigate the evolutionary dynamics of phenotypic and genetic adaptation in populations facing different environmental shifts. Specifically, we simulated sudden, gradual, and fluctuating environmental shifts for multiple trait architectures. Our results show distinct evolutionary paths across different types of environmental shifts and a higher extinction risk during sudden and fluctuating environmental shifts than during gradual shifts. Comparing the contribution of mutations from different sources highlights the critical role of standing genetic variation in driving phenotypic adaptation. We summarize allele frequency trajectories by clustering them by their temporal pattern and reveal how large- and small-effect mutations jointly shape the successful adaptation to changing environments. Additionally, we trained a convolutional neural network (CNN) on "genetic architecture matrices" of populations to jointly infer the type and magnitude of environmental changes and the mutational effect size distribution. The CNN was able to predict all three input parameters with very high accuracy, even on unseen parameter combinations. Our results demonstrate the impact of ecological change on the evolutionary outcome and the assorted mutational changes that enable successful adaptation.

evolutionary biology↗

Time series analysis in a maize landrace reveals rapid fixation of beneficial alleles

Identifying loci in the genome that allow a population to respond to selection pressure is essential to understand evolution and improve crops. Temporally consecutive generations under selection offer the opportunity to identify signatures of selection. Maize, as one of the most important crops worldwide is rich in genetic diversity and a model for breeding advances. Therefore, it is an ideal system to study genetic changes in response to selection. Here, we study the genetic changes in two replicates of a selection experiment in a European maize landrace, which showed rapid trait improvement over three cycles of selection. We identified an increase in genetic divergence across successive doubled-haploid populations derived from each selection cycle, consistent with the effect of strong directional selection. The genetic divergence observed between the replicates was greater than that between generations. In addition to the genome-wide signal, we identified multiple candidate loci under selection through temporal FST outlier analysis comparing the original landrace population to subsequent cycles. These loci showed a significant overlap with genomic regions, controlling intentionally selected traits and other traits. The significant overlap of selected loci between the two replicates shows the importance of major loci in response to directional selection, while the large number of non-overlapping loci demonstrates the polygenic response. Our work shows that the temporal dimension in plant breeding time-series enables the identification of candidate loci under selection and the genome-wide dynamics of change in response to selection.

evolutionary biology↗

Pleiotropy and repeated mutation drove convergent domestication of grain amaranth

Humans reshaped environments for domesticated plants, yet the extent of human agency in the domestication process remains unresolved. Color variation has been used as evidence for an intended process by humans, as the trait has been mainly linked to visual properties. In the ancient pseudocereal grain amaranth major domestication traits have not changed, but the seed color changed repeatedly from dark to white during multiple domestication processes. Here, we show that the transition to white seed color was of major ecological significance beyond human preference through mechanistic links to seed germination. We identify major metabolomic and transcriptomic changes in the proanthocyanidin pathway leading to loss of seed color and dormancy in domesticated amaranth. Despite the potentially large mutational target size of the proanthocyanidin pathway, the repeated mutation in a single gene led to the domestication phenotype. Multiple independent knock-out mutations in this gene reveal the repeated selection for the loss of seed dormancy in different parts of the Americas. Competition experiments show that the pleiotropic link between seed color and seed dormancy provides a competitive advantage to white seeds in agricultural environments. The reduction of proanthocyanidin content in the seed is observed in numerous crops, including rice and beans, suggesting a common ecological adaptation after early humans altered their environment through changing lifestyles. Our findings establish a direct mechanistic link between individual mutations, pathway-level biochemical reconfiguration, and ecological fitness, illustrating how plants adapted to human-modified environments largely without intentional human agency.

evolutionary biology↗

The grain amaranth pangenome reveals domestication-associated changes in diversity and function of structural variation

BackgroundGrain amaranth is a nutritious pseudocereal from the Americas that was independently domesticated three times from a common wild ancestor. The three domesticated grain amaranths, their wild progenitor, and a close wild relative form a species complex. Pangenomes enable the assessment of genetic variation beyond single nucleotide polymorphisms. ResultsWe have constructed a pangenome for the entire grain amaranth species complex, consisting of new, chromosome-scale genome assemblies for all five species, including the first reference genomes for A. caudatus and A. quitensis. Our high-quality assemblies reach near telomere-to-telomere contiguity. Comparative analyses within the grain amaranth pangenome revealed a high degree of collinearity and overall conserved chromosome structure across species. Genes are similarly conserved, with a [~]75% core gene set. We identify over 100,000 structural variants, distributed throughout the genomes. We quantify gene presence-absence and find that protein biosynthesis gene families were expanding during domestication, while gene loss reflects possible redundancies in other processes. We further map flowering time in a biparental population and find two QTL that together account for a 55-day difference in flowering time between homozygous genotypes. One QTL contains an ortholog of a known flowering-time regulator that may be disrupted by an insertion in the late flowering parent. ConclusionsOur work establishes high-quality genomic resources for the promising protein crop grain amaranth and sheds light on how structural variants shape genomic diversity and repeated evolutionary change in crops. The structural variants and flowering time loci identified can help to understand amaranth adaptation and provide breeding targets for crop improvement.

genomics↗

Domestication of the ancient grain Amaranthus cruentus L.

Grain amaranths are nutritious pseudocereals that have been domesticated in the Andes and North America mainly in Mexico. The repeated domestication of grain amaranths has recently been studied using genome-wide data. The results suggested independent processes of domestication from Amaranthus hybridus L. in different geographical regions. Although domestication process of the three grain amaranths has been partially elucidated, the detailed domestication centers remain unknown. Therefore, we study the geographic origin and center of domestication of A. cruentus within North America. We reveal a high genetic diversity and distinct history, using whole genome sequencing of 138 accessions belonging to A. cruentus and its closely related species (A. hypochondriacus L.) along with the wild relative A. hybridus mainly from South of Mexico and Guatemala. A. cruentus was most likely domesticated in central Mexico and then taken to Guatemala, where this species is most widely preferred and cultivated today. We identified three genomic groups of A. cruentus. Amaranthus cruentus group 1, representing the center of Mexico, A. cruentus group 2 mostly from Guatemala, and A. cruentus group 3 including individuals in Mexico, but distinct from group 1. Compared to A. hybridus, A. cruentus group 3 exhibited the lowest genetic differentiation and the highest genetic diversity among the A. cruentus groups. We find gene flow between A. cruentus group 1 and A. hybridus indicating the continuing interbreeding between wild and domesticated amaranth in its domestication center. Our results support the hypothesis of a Mexican origin of A. cruentus and a secondary center of domestication in Guatemala.

evolutionary biology↗

Adaptive Dynamics of Quantitative Traits in a SteadilyChanging Environment

Understanding the adaptation of quantitative traits to changing environments is a central challenge in evolutionary biology. However, the precise roles of the speed of environmental change and trait architecture in adaptive dynamics remain unclear. Here, we investigate their roles through an adaptive walk model and individual-based polygenic simulations within a moving-soptimum framework. We introduce a dimensionless parameter, the effective selection strength, to characterize quantitative traits in both models. We show that adapting populations attain a stationary state below a critical speed of environmental change. Properties of the stationary state are compared between the two approaches, and it is shown that the adaptive walk model provides a good approximation for long-term polygenic adaptation. Additionally, in the adaptive walk model, we derive an explicit formula for the logarithmic divergence of the stationary phenotypic gap upon approaching the critical speed. To elucidate population extinction in biologically realistic terms, we define a fitness-threshold-based critical speed and reveal its power-law dependence on the effective selection strength in both models. Finally, results of our polygenic simulations show how the genetic architecture in the stationary regime is shaped by a dynamic equilibrium between the influx of de novo mutations and their loss through fixation and extinction constrained by the rate of phenotypic change enforced by the optimum speed. Taken together, our study advances the understanding of polygenic adaptation and provides insights to simplify analytical work and computational simulations for future studies.

evolutionary biology↗

Domestication shaped the chromatin landscape of grain amaranth

Plant domestication has had profound impacts on the morphology and genetic diversity of crops. Beyond sequence diversity, changes in chromatin structure can play an important role in plant adaptation. However, the interplay between the chromatin landscape and plant domestication remains unclear. We present a high-quality genome assembly and chromatin landscape map of the ancient pseudo-cereal, amaranth. Using ATAC-sequencing of multiple accessions of three grain amaranth species and two wild relatives, we show that the overall amount of accessible chromatin is highly conserved, but about 2.5% of all chromatin switched states, with a higher fraction of the genome repeatedly opening during domestication processes. These differentially accessible chromatin regions, between the crops and their wild ancestor, were species-specific and significantly associated with selective sweeps - reflecting the repeated independent domestication of amaranth. Our findings reveal the dynamic interplay between domestication and the chromatin landscape, highlighting an additional layer of diversity in crops.

genomics↗

First Successful Targeted Mutagenesis Using CRISPR/Cas9 in Stably Transformed Grain Amaranth Tissue

Genome editing using CRISPR/Cas is a key technology for speeding up breeding for climate-resilient, high-yielding crops (Scheben et al., 2017). However, efficient targeted mutagenesis requires implementing stable transformation methods and establishing a CRISPR/Cas setup suitable for the species of interest (Shan et al., 2020). The availability of such methods is a significant bottleneck to advancing many promising, albeit under-researched, crops. Testing and establishing vectors for efficient application of CRISPR/Cas in non-model crops could boost research and breeding of new valuable crops (Ye and Fan, 2021). We edited key pathway genes in the betalain biosynthesis pathway of grain amaranth, i.e., A. hypochondriacus L., to prove how targeted mutagenesis can be implemented in an orphan crop using the CasCADE modular cloning system (Hoffie, 2022). Grain amaranth is a resilient C4 dicot orphan crop with excellent nutritional composition. These properties make amaranth a well-suited candidate to be bred as a climate-resilient crop (Joshi et al., 2018). However, no efficient and reproducible protocol for successful application of CRISPR/Cas9 or stable transformation and regeneration, has been demonstrated in A. hypochondriacus (Castellanos-Arevalo et al., 2020).

plant biology↗

Going New Places: Successful Adaptation and Genomic Integrity of Grain Amaranth in India

Global climate change will impact worldwide crop yields, requiring shifts and adaptation of crop varieties. The recent global spread of crops across different continents shows how plants successfully colonized new environments. One such spread is the introduction of the nutritious pseudocereal amaranth to India. Grain amaranth has been domesticated over 6,000 years ago in three different regions of the Americas and was introduced to India approximately 500 years ago. Nowadays numerous local landraces grow throughout the countrys wide climatic conditions. We investigate the introduction of grain amaranth to India to understand the factors allowing successful establishment of crops to novel environments, using whole genome sequencing of almost 200 accessions from India and more than 100 accessions from the crops native distribution. We find comparable levels of genetic diversity in the Americas and in India, despite the likely population bottleneck during the introduction to India. Surprisingly, the three grain amaranth species that were introduced do not show signs of gene-flow in India, while gene-flow in the Americas was high during the domestication of the crops. Correspondingly, the genetic differentiation between grain species was higher within India than in the native range, indicating a strong isolation between otherwise interbreeding populations. The reconstruction of the population history through demographic modelling of different scenarios suggested rapid expansion in the Indian population but a strong bottleneck in the native population, explaining the comparable diversity and isolation. We identified genomic loci under selection and associated with the climate in India that potentially enabled the adaptation to the new environment. These loci are predicted to provide an advantage under future climate scenarios, even in the native range. Our results suggest that introduced crops can act as reservoirs of genetic diversity, providing additional adaptive potential and resilience to future environmental change.

evolutionary biology↗

Local selection shaped the diversity of European maize landraces

The introduction of populations to novel environments can lead to a loss of genetic diversity and the accumulation of deleterious mutations due to selection and demographic changes. We investigate how the recent introduction of maize to Europe shaped the genetic diversity and differentiation of European traditional maize populations and quantify the impact of its recent range expansion and consecutive breeding on the accumulation of genetic load. We use genome-wide genetic markers of almost 2,000 individuals from 38 landraces, 155 elite breeding lines and a large set of doubled haploid lines derived from two landraces to find extensive population structure within European maize, with landraces being highly differentiated even over short geographic distances. Yet, diversity change does not follow the continuous pattern of range expansions. Landraces maintain high genetic diversity that is distinct between populations and does not decrease along the possible expansion routes. Signals of positive selection in European landraces that overlap with selection in Asian maize suggest convergent selection during maize introductions. At the same time, environmental factors partially explain genetic differences across Europe. Consistent with the maintenance of high diversity, we find no evidence of genetic load accumulating along the maize introduction route in European maize. However, modern breeding likely purged highly deleterious alleles but accumulated genetic load in elite germplasm. Our results reconstruct the history of maize in Europe and show that landraces have maintained high genetic diversity that could reduce genetic load in the European maize breeding pools.

evolutionary biology↗

Isoform-resolved genome annotation enables mapping of tissue-specific betalain regulation and anthocyanin regulator co-option in amaranth

* Betalains are coloring pigments produced in some families of the order Caryophyllales, where they replace anthocyanins as coloring pigments. While the betalain pathway itself is well studied, the tissue-specific regulation of the pathway remains mostly unknown. * We enhance the high-quality Amaranthus hypochondriacus reference genome and produce a substantially more complete genome annotation, incorporating isoform details. We annotate betalain and anthocyanin pathway genes along with their regulators in amaranth and map the genetic control and tissue-specific regulation of the betalain pathway. * Our improved genome annotation allowed us to identify causal mutations that lead to a knock-out of red betacyanins in natural accessions of amaranth. We reveal the tissue-specific regulation of flower color via a previously uncharacterized MYB transcription factor, AhMYB2. Downregulation of AhMYB2 in the flower leads to reduced expression of key betalain enzyme genes and loss of red flower color. * Our improved amaranth reference genome represents the most complete genome of amaranth to date and a valuable resource for betalain and amaranth research. High similarity of the flower betalain regulator AhMYB2 to anthocyanin regulators and a partially conserved interaction motif support the co-option of anthocyanin regulators for the betalain pathway as possible reason for mutual exclusiveness of the two pigments.

plant biology↗

Evolutionary rescue through gene flow despite genetic incompatibilities shaped diversity of the pseudo-cereal grain amaranth

Crop domestication and the subsequent expansion of crops have long been thought of as a linear process from a wild ancestor to a domesticate. However, evidence of gene flow from locally adapted wild relatives that provided adaptive alleles into crops has been identified in multiple species. Yet, little is known about the evolutionary consequences of gene flow during domestication and the interaction of gene flow and genetic load in crop populations. We study the pseudo-cereal grain amaranth that has been domesticated three times in different geographic regions of the Americas. We quantify the amount and distribution of gene flow and genetic load along the genome of the three grain amaranth species and their two wild relatives. Our results show ample gene flow between crop species and between crops and their wild relatives. Gene flow from wild relatives decreased genetic load in the three crop species. This suggests that wild relatives could provide evolutionary rescue by replacing deleterious alleles in crops. We assess experimental hybrids between the three crop species and found genetic incompatibilities between one Central American grain amaranth and the other two crop species. These incompatibilities might have created recent reproductive barriers and maintained species integrity today. Together, our results show that gene flow played an important role in the domestication and expansion of grain amaranth, despite genetic species barriers. The domestication of plants was likely not linear and created a genomic mosaic by multiple contributors with varying fitness effects for todays crops.

evolutionary biology↗

Domestication Reshaped the Genetic Basis of Inbreeding Depression in a Maize Landrace Compared to its Wild Relative, Teosinte

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.

evolutionary biology↗

PopAmaranth: A population genetic genome browser for grain amaranths and their wild relatives

The last decades of genomic, physiological, and population genetic research have accelerated the understanding and improvement of a numerous crops. The transfer of methods to minor crops could accelerate their improvement if knowledge is effectively shared between disciplines. Grain amaranth is an ancient nutritious pseudocereal from the Americas that is regaining importance due to its high protein content and favorable amino acid and micronutrient composition. To effectively combine genomic and population genetic information with molecular genetics, plant physiology, and use it for interdisciplinary research and crop improvement, an intuitive interaction for scientists across disciplines is essential. Here, we present PopAmaranth, a population genetic genome browser, which provides an accessible representation of the genetic variation of the three grain amaranth species (A. hypochondriacus, A. cruentus, and A. caudatus) and two wild relatives (A. hybridus and A. quitensis) along the A. hypochondriacus reference sequence. We performed population-scale diversity and selection analysis from whole-genome sequencing data of 88 curated genetically and taxonomically unambiguously classified accessions. We incorporate the domestication history of the three grain amaranths to make an evolutionary perspective for candidate genes and regions available. We employ the platform to show that genetic diversity in the water stress-related MIF1 gene declined during amaranth domestication and provide evidence for convergent saponin reduction between amaranth and quinoa. These examples show that our tool enables the detailed study of individual genes, provides target regions for breeding efforts and can enhance the interdisciplinary integration of population genomic findings across species. PopAmaranth is available through amaranthGDB at amaranthgdb.org/popamaranth.html SignificanceSharing population genetic results between disciplines can facilitate interdisciplinary research and accelerate the improvement of crops. Since the onset of genome sequencing online genome browser platforms have provide access to features of an organisms genetic information. Rarely this has been extended to population-wide summary statistics for evolutionary hypothesis testing. We implemented a population genetic genome browser PopAmaranth for three grain amaranth species and their two wild relatives. The intuitive and user-friendly interface of PopA-maranth makes the genetic diversity of the species complex available to broad audience of biologists across disciplines. We show how our tool can be used to study convergence across distant genera and find signals of past selection in domestication and stress related genes. Community platforms and genome browsers are an integrative element of numerous study systems. PopAmaranth can serve as template for other research communities to integrate and share their results.

genomics↗

Male linked genomic regions determine sex in dioecious Amaranthus palmeri

Dioecy, the separation of reproductive organs on different individuals, has evolved repeatedly in different plant families. Several evolutionary paths to dioecy have been suggested, but the mechanisms behind sex determination is not well understood. The diploid dioecious Amaranthus palmeri represents a well suited model system to study sex determination in plants. A. palmeri is one of the most troublesome weeds in the US, has successfully colonized other regions in the world and has evolved resistance to several herbicide classes. Despite the agricultural importance of the species, the genetic control and evolutionary state of dioecy in A. palmeri is currently unknown. Early cytogenetic experiments did not identify heteromorphic chromosomes. Here, we used whole genome sequencing of male and female pools from two independent populations to elucidate the genetic control of dioecy in A. palmeri. Read alignment to a close monoecious relative and allele frequency comparisons between male and female pools did not reveal significant sex linked genes. Consequently, we employed an alignment free k-mer comparison which enabled us to identify a large number of male specific k-mers. We assembled male specific contigs comprising a total of almost 2 Mb sequence, proposing a XY sex determination system in the species. Based on our findings we suggest an intermediate evolutionary state of dioecy in A. palmeri. Our findings give insight into the evolution of sex chromosomes in plants and may help to develop sustainable strategies for weed management.

plant biology↗

Loss of diversity and accumulation of genetic load in doubled-haploid lines from European maize landrace

Maize landraces are well adapted to their local environments and present valuable sources of genetic diversity for breeding and conservation. But the maintenance of open-pollinated landraces in ex-situ programs is challenging, as regeneration of seed can often lead to inbreeding depression and the loss of diversity due to genetic drift. Recent reports suggest that the production of doubled-haploid (DH) lines from landraces may serve as a convenient means to preserve genetic diversity in a homozygous form that is immediately useful for modern breeding. The production of doubled-haploid (DH) lines presents an extreme case of inbreeding which results in instantaneous homozygosity genome-wide. Here, we analyzed the effect of DH production on genetic diversity, using genome-wide SNP data from hundreds of individuals of five European landraces and their related DH lines. In contrast to previous findings, we observe a dramatic loss of diversity at both the haplotype level and that of individual SNPs. We identify thousands of SNPs that exhibit allele frequency differences larger than expected under models of neutral genetic drift and document losses of shared haplotypes. We find evidence consistent with selection at functional sites that are potentially involved in the diversity differences between landrace and DH populations. Although we were unable to uncover more details about the mode of selection, we conclude that landrace DH lines may be a valuable tool for the introduction of variation into maize breeding programs but come at the cost of decreased genetic diversity and increased genetic load.

evolutionary biology↗

The temporal dynamics of background selection in non-equilibrium populations

Neutral genetic diversity across the genome is determined by the complex interplay of mutation, demographic history, and natural selection. While the direct action of natural selection is limited to functional loci across the genome, its impact can have effects on nearby neutral loci due to genetic linkage. These effects of selection at linked sites, referred to as genetic hitchhiking and background selection (BGS), are pervasive across natural populations. However, only recently has there been a focus on the joint consequences of demography and selection at linked sites, and empirical studies have sometimes come to apparently contradictory conclusions as to their combined effects. In order to understand the relationship between demography and selection at linked sites, we conducted an extensive forward simulation study of BGS under a range of demographic models. We found that the relative levels of diversity in BGS and neutral regions vary over time and that the initial dynamics after a population size change are often in the opposite direction of the long-term expected trajectory. Our detailed observations of the temporal dynamics of neutral diversity in the context of selection at linked sites in non-equilibrium populations provides new intuition about why patterns of diversity under BGS vary through time in natural populations and help reconcile previously contradictory observations. Most notably, our results highlight that classical models of BGS are poorly suited for predicting diversity in non-equilibrium populations.

evolutionary biology↗

Convergent seed color adaptation during repeated domestication of an ancient new world grain

Out of the almost 2,000 plants that have been selected as crops, only few are fully domesticated, and many intermediates between wild plants and domesticates exist. Genetic constraints might be the reason why incompletely domesticated plants have few characteristic crop traits, and retained numerous wild plant features. Here, we investigate the incomplete domestication of an ancient grain from the Americas, amaranth. We sequenced 121 genomes of the crop and its wild ancestors to show that grain amaranth has been selected three times independently from a single wild ancestor, but has not been fully domesticated. Our analysis identified a MYB-like transcription factor gene as key regulator for seed color variation and shows that the trait was independently converted in Central and South America. We suggest a low effective population size at the time of domestication as potential cause for the lack of adaptation of complex domestication traits. Our results show how genetic constraints influenced domestication and might have set the fate of hundreds of crops.

evolutionary biology↗