A revisited history of cacao domestication in pre-Columbian times revealed by archaeogenomic approaches.

Humans have a long history of transporting and trading plants, contributing to the evolution of domesticated plants. Theobroma cacao originated in the Neotropics from South America. However, little is known about its domestication and use in these regions. In this study, ceramic residues from a large sample of pre-Columbian cultures from South and Central America were analyzed using archaeogenomic and biochemical approaches. Here we show, for the first time, the widespread use of cacao in South America out of its native Amazonian area of origin, extending back 5000 years, likely supported by cultural interactions between the Amazon and the Pacific coast. We observed that strong genetic mixing between geographically distant cacao populations occurred as early as the middle Holocene, in South America, driven by humans, favoring the adaptation of T. cacao to new environments. This complex history of cacao domestication is the basis of today's cacao tree populations and its knowledge can help us better manage their genetic resources.

A Quantitative Theory for Genomic Offset Statistics.

Genomic offset statistics predict the maladaptation of populations to rapid habitat alteration based on association of genotypes with environmental variation. Despite substantial evidence for empirical validity, genomic offset statistics have well-identified limitations, and lack a theory that would facilitate interpretations of predicted values. Here, we clarified the theoretical relationships between genomic offset statistics and unobserved fitness traits controlled by environmentally selected loci and proposed a geometric measure to predict fitness after rapid change in local environment. The predictions of our theory were verified in computer simulations and in empirical data on African pearl millet (Cenchrus americanus) obtained from a common garden experiment. Our results proposed a unified perspective on genomic offset statistics and provided a theoretical foundation necessary when considering their potential application in conservation management in the face of environmental change.

Genomic footprints of selection in early-and late-flowering pearl millet landraces.

Pearl millet is among the top three-cereal production in one of the most climate vulnerable regions, sub-Saharan Africa. Its Sahelian origin makes it adapted to grow in poor sandy soils under low soil water regimes. Pearl millet is thus considered today as one of the most interesting crops to face the global warming. Flowering time, a trait highly correlated with latitude, is one of the key traits that could be modulated to face future global changes. West African pearl millet landraces, can be grouped into early- (EF) and late-flowering (LF) varieties, each flowering group playing a specific role in the functioning and resilience of Sahelian smallholders. The aim of this study was thus to detect genes linked to flowering but also linked to relevant traits within each flowering group. We thus investigated genomic and phenotypic diversity in 109 pearl millet landrace accessions, i.e., 66 early-flowering and 43 late-flowering, grown in the groundnut basin, the first area of rainfed agriculture in Senegal dominated by dry cereals (millet, maize, and sorghum) and legumes (groundnuts, cowpeas). We were able to confirm the role of PhyC gene in pearl millet flowering and identify several other genes that appear to be as much as important, such as FSR12 and HAC1. HAC1 and two other genes appear to be part of QTLs previously identified and deserve further investigation. At the same time, we were able to highlight a several genes and variants that could contribute to the improvement of pearl millet yield, especially since their impact was demonstrated across flowering cycles.

Diversity and determinants of bitterness, astringency, and fat content in cultivated Nacional and native Amazonian cocoa accessions from Ecuador.

Cocoa (Theobroma cacao L.) is the only tree that can produce cocoa. Cocoa beans are highly sought after by chocolate makers to produce chocolate. Cocoa can be fine aromatic, characterized by floral and fruity notes, or it can be described as standard cocoa with a more pronounced cocoa aroma and bitterness. In this study, the genetic and biochemical determinants of sensorial notes and nonvolatile compounds related to bitterness, astringency, fat content, and protein content will be investigated in two populations: a cultivated modern Nacional population and a population of cocoa accessions collected recently in the Ecuadorian South Amazonia area of origin of the Nacional ancestral variety. For this purpose, a genome-wide association study (GWAS) was carried out on both populations, with results of biochemical compounds evaluated by near-infrared spectroscopy (NIRS) assays and with sensory evaluations. Twenty areas of associations were detected for sensorial data especially bitterness and astringency. Fifty-three areas of associations were detected linked to nonvolatile compounds. A total of 81 candidate genes could be identified in the areas of the association.

Pearl millet genomic vulnerability to climate change in West Africa highlights the need for regional collaboration.

Climate change is already affecting agro-ecosystems and threatening food security by reducing crop productivity and increasing harvest uncertainty. Mobilizing crop diversity could be an efficient way to mitigate its impact. We test this hypothesis in pearl millet, a nutritious staple cereal cultivated in arid and low-fertility soils in sub-Saharan Africa. We analyze the genomic diversity of 173 landraces collected in West Africa together with an extensive climate dataset composed of metrics of agronomic importance. Mapping the pearl millet genomic vulnerability at the 2050 horizon based on the current genomic-climate relationships, we identify the northern edge of the current areas of cultivation of both early and late flowering varieties as being the most vulnerable to climate change. We predict that the most vulnerable areas will benefit from using landraces that already grow in equivalent climate conditions today. However, such seed-exchange scenarios will require long distance and trans-frontier assisted migrations. Leveraging genetic diversity as a climate mitigation strategy in West Africa will thus require regional collaboration.

Evidence for Dosage Compensation in Coccinia grandis, a Plant with a Highly Heteromorphic XY System.

About 15,000 angiosperms are dioecious, but the mechanisms of sex determination in plants remain poorly understood. In particular, how Y chromosomes evolve and degenerate, and whether dosage compensation evolves as a response, are matters of debate. Here, we focus on Coccinia grandis, a dioecious cucurbit with the highest level of X/Y heteromorphy recorded so far. We identified sex-linked genes using RNA sequences from a cross and a model-based method termed SEX-DETector. Parents and F1 individuals were genotyped, and the transmission patterns of SNPs were then analyzed. In the >1300 sex-linked genes studied, maximum X-Y divergence was 0.13-0.17, and substantial Y degeneration is implied by an average Y/X expression ratio of 0.63 and an inferred gene loss on the Y of ~40%. We also found reduced Y gene expression being compensated by elevated expression of corresponding genes on the X and an excess of sex-biased genes on the sex chromosomes. Molecular evolution of sex-linked genes in C. grandis is thus comparable to that in Silene latifolia, another dioecious plant with a strongly heteromorphic XY system, and cucurbits are the fourth plant family in which dosage compensation is described, suggesting it might be common in plants.

An efficient RNA-seq-based segregation analysis identifies the sex chromosomes of Cannabis sativa.

Cannabis sativa-derived tetrahydrocannabinol (THC) production is increasing very fast worldwide. C. sativa is a dioecious plant with XY Chromosomes, and only females (XX) are useful for THC production. Identifying the sex chromosome sequence would improve early sexing and better management of this crop; however, the C. sativa genome projects have failed to do so. Moreover, as dioecy in the Cannabaceae family is ancestral, C. sativa sex chromosomes are potentially old and thus very interesting to study, as little is known about old plant sex chromosomes. Here, we RNA-sequenced a C. sativa family (two parents and 10 male and female offspring, 576 million reads) and performed a segregation analysis for all C. sativa genes using the probabilistic method SEX-DETector. We identified >500 sex-linked genes. Mapping of these sex-linked genes to a C. sativa genome assembly identified the largest chromosome pair being the sex chromosomes. We found that the X-specific region (not recombining between X and Y) is large compared to other plant systems. Further analysis of the sex-linked genes revealed that C. sativa has a strongly degenerated Y Chromosome and may represent the oldest plant sex chromosome system documented so far. Our study revealed that old plant sex chromosomes can have large, highly divergent nonrecombining regions, yet still be roughly homomorphic.

A western Sahara centre of domestication inferred from pearl millet genomes.

There have been intense debates over the geographic origin of African crops and agriculture. Here, we used whole-genome sequencing data to infer the domestication origin of pearl millet (Cenchrus americanus). Our results supported an origin in western Sahara, and we dated the onset of cultivated pearl millet expansion in Africa to 4,900 years ago. We provided evidence that wild-to-crop gene flow increased cultivated genetic diversity leading to diversity hotspots in western and eastern Sahel and adaptive introgression of 15 genomic regions. Our study reconciled genetic and archaeological data for one of the oldest African crops.

The Rise and Fall of African Rice Cultivation Revealed by Analysis of 246 New Genomes.

African rice (Oryza glaberrima) was domesticated independently from Asian rice. The geographical origin of its domestication remains elusive. Using 246 new whole-genome sequences, we inferred the cradle of its domestication to be in the Inner Niger Delta. Domestication was preceded by a sharp decline of most wild populations that started more than 10,000 years ago. The wild population collapse occurred during the drying of the Sahara. This finding supports the hypothesis that depletion of wild resources in the Sahara triggered African rice domestication. African rice cultivation strongly expanded 2,000 years ago. During the last 5 centuries, a sharp decline of its cultivation coincided with the introduction of Asian rice in Africa. A gene, PROG1, associated with an erect plant architecture phenotype, showed convergent selection in two rice cultivated species, Oryza glaberrima from Africa and Oryza sativa from Asia. In contrast, a shattering gene, SH5, showed selection signature during African rice domestication, but not during Asian rice domestication. Overall, our genomic data revealed a complex history of African rice domestication influenced by important climatic changes in the Saharan area, by the expansion of African agricultural society, and by recent replacement by another domesticated species.

Molecular basis of African yam domestication: analyses of selection point to root development, starch biosynthesis, and photosynthesis related genes.

BACKGROUND: After cereals, root and tuber crops are the main source of starch in the human diet. Starch biosynthesis was certainly a significant target for selection during the domestication of these crops. But domestication of these root and tubers crops is also associated with gigantism of storage organs and changes of habitat. RESULTS: We studied here, the molecular basis of domestication in African yam, Dioscorea rotundata. The genomic diversity in the cultivated species is roughly 30% less important than its wild relatives. Two percent of all the genes studied showed evidences of selection. Two genes associated with the earliest stages of starch biosynthesis and storage, the sucrose synthase 4 and the sucrose-phosphate synthase 1 showed evidence of selection. An adventitious root development gene, a SCARECROW-LIKE gene was also selected during yam domestication. Significant selection for genes associated with photosynthesis and phototropism were associated with wild to cultivated change of habitat. If the wild species grow as vines in the shade of their tree tutors, cultivated yam grows in full light in open fields. CONCLUSIONS: Major rewiring of aerial development and adaptation for efficient photosynthesis in full light characterized yam domestication.

Pearl millet genome sequence provides a resource to improve agronomic traits in arid environments.

Pearl millet [Cenchrus americanus (L.) Morrone] is a staple food for more than 90 million farmers in arid and semi-arid regions of sub-Saharan Africa, India and South Asia. We report the ∼1.79 Gb draft whole genome sequence of reference genotype Tift 23D2B1-P1-P5, which contains an estimated 38,579 genes. We highlight the substantial enrichment for wax biosynthesis genes, which may contribute to heat and drought tolerance in this crop. We resequenced and analyzed 994 pearl millet lines, enabling insights into population structure, genetic diversity and domestication. We use these resequencing data to establish marker trait associations for genomic selection, to define heterotic pools, and to predict hybrid performance. We believe that these resources should empower researchers and breeders to improve this important staple crop.

No Excess of Cis-Regulatory Variation Associated with Intraspecific Selection in Wild Pearl Millet (Cenchrus americanus).

Several studies suggest that cis-regulatory mutations are the favorite target of evolutionary changes, one reason being that cis-regulatory mutations might have fewer deleterious pleiotropic effects than protein-coding mutations. A review of the process also suggests that this bias towards adaptive cis-regulatory variation might be less pronounced at the intraspecific level compared with the interspecific level. In this study, we assessed the contribution of cis-regulatory variation to adaptation at the intraspecific level using populations of wild pearl millet (Cenchrus americanus ssp. monodii) sampled along an environmental gradient in Niger. From RNA sequencing of hybrids to assess allele-specific expression, we identified genes with cis-regulatory divergence between two parental accessions collected in contrasted environmental conditions. This revealed that ∼15% of transcribed genes showed cis-regulatory variation. Intersecting the gene set exhibiting cis-regulatory variation with the gene set identified as targets of selection revealed no excess of cis-acting mutations among the selected genes. We additionally found no excess of cis-regulatory variation among genes associated with adaptive traits. As our approach relied on methods identifying mainly genes submitted to strong selection pressure or with high phenotypic effect, the contribution of cis-regulatory changes to soft selection or polygenic adaptive traits remains to be tested. However our results favor the hypothesis that enrichment of adaptive cis-regulatory divergence builds up over time. For short evolutionary time-scales, cis-acting mutations are not predominantly involved in adaptive evolution associated with strong selective signal.

Genome scan reveals selection acting on genes linked to stress response in wild pearl millet.

Uncovering genomic regions involved in adaption is a major goal in evolutionary biology. High-throughput sequencing now makes it possible to tackle this challenge in nonmodel species. Yet, despite the increasing number of methods targeted to specifically detect genomic footprints of selection, the complex demography of natural populations often causes high rates of false positive in gene discoveries. The aim of this study was to identify climate adaptations in wild pearl millet populations, Cenchrus americanus ssp. monodii. We focused on two climate gradients, one in Mali and one in Niger. We used a two-step strategy to limit false-positive outliers. First, we considered gradients as biological replicates and performed RNA sequencing of four populations at the extremities. We combined four methods-three based on differentiation among populations and one based on diversity patterns within populations-to identify outlier SNPs from a set of 87 218 high-quality SNPs. Among 11 155 contigs of pearl millet reference transcriptome, 540 exhibited selection signals as evidenced by at least one of the four methods. In a second step, we genotyped 762 samples in 11 additional populations distributed along the gradients using SNPs from the detected contigs and random SNPs as control. We further assessed selection on this large data set using a differentiation-based method and a method based on correlations with environmental variables based. Four contigs displayed consistent signatures between the four extreme and 11 additional populations, two of which were linked to abiotic and biotic stress responses.

Deciphering the genetics of flowering time by an association study on candidate genes in bread wheat (Triticum aestivum L.).

Earliness is very important for the adaptation of wheat to environmental conditions and the achievement of high grain yield. A detailed knowledge of key genetic components of the life cycle would enable an easier control by the breeders. The objective of the study was to investigate the effect of candidate genes on flowering time. Using a collection of hexaploid wheat composed of 235 lines from diverse geographical origins, we conducted an association study for six candidate genes for flowering time and its components (vernalization sensitivity and earliness per se). The effect on the variation of earliness components of polymorphisms within the copies of each gene was tested in ANOVA models accounting for the underlying genetic structure. The collection was structured in five groups that minimized the residual covariance. Vernalization requirement and lateness tend to increase according to the mean latitude of each group. Heading date for an autumnal sowing was mainly determined by the earliness per se. Except for the Constans (CO) gene orthologous of the barley HvCO3, all gene polymorphisms had a significant impact on earliness components. The three traits used to quantify vernalization requirement were primarily associated with polymorphisms at Vrn-1 and then at Vrn-3 and Luminidependens (LD) genes. We found a good correspondence between spring/winter types and genotypes at the three homeologous copies of Vrn-1. Earliness per se was mainly explained by polymorphisms at Vrn-3 and to a lesser extent at Vrn-1, Hd-1 and Gigantea (GI) genes. Vernalization requirement and earliness as a function of geographical origin, as well as the possible role of the breeding practices in the geographical distribution of the alleles and the hypothetical adaptive value of the candidate genes, are discussed.

Dynamic management of crop diversity: From an experimental approach to on-farm conservation.

In agricultural systems, biodiversity includes diversity within species and among species and provides many benefits for production, resilience and conservation. This article addresses the effects of a strategy of in situ conservation called dynamic management (DM) on population evolution, adaptation and diversity. Two French DM initiatives are considered, the first one corresponding to an experimental context, the second to an on-farm management. Results from a study over 26 years of experimental DM of bread wheat (Triticum aestivum L.) are first presented, including the evolution of agronomic traits and genetic diversity at neutral and fitness related loci. While this experiment greatly increased scientific knowledge of the effects of natural selection on cultivated populations, it also showed that population conservation cannot rely only on a network of experimental stations. In collaboration with a farmers' network in France, researchers have begun studying the effects of on-farm DM (conservation and selection) on diversity and adaptation. Results from these studies show that on-farm DM is a key element for the long-term conservation and use of agricultural biodiversity. This method of in situ conservation deserves more attention in industrialised countries.

Evolution of flowering time in experimental wheat populations: a comprehensive approach to detect genetic signatures of natural selection.

In annual plant species, flowering time is a major adaptive trait that synchronizes the initiation of reproduction with favorable environmental conditions. Here, we aimed at studying the evolution of flowering time in three experimental populations of bread wheat, grown in contrasting environments (Northern to Southern France) for 12 generations. By comparing the distribution of phenotypic and presumably neutral variation, we first showed that flowering time responded to selection during the 12 generations of the experiment. To get insight into the genetic architecture of that trait, we then tested whether the distribution of genetic polymorphisms at six candidate genes, presumably involved in the trait expression, departed from neutral expectation. To that end, we focused on the temporal variation during the course of the experiment, and on the spatial differentiation at the end of the experiment, using previously published methods adapted to our experimental design. Only those genes that were strongly associated with flowering time variation were detected as responding to selection. For genes that had low-to-moderate phenotypic effects, or when there was interaction across different genes, we did not find evidence of selection using methods based on the distribution of temporal or spatial variation. In such cases, it might be more informative to consider multilocus and multiallelic combinations across genes, which could be the targets of selection.

Insight into the genetic bases of climatic adaptation in experimentally evolving wheat populations.

Experimental populations evolving under natural selection represent an interesting tool to study genetic bases of adaptation. Evolution of genes possibly involved in adaptive response can be followed together with the corresponding phenotypic traits. Using experimental populations of hexaploid wheat, we studied the evolution of flowering time, a major adaptive trait that synchronizes the initiation of reproduction and the occurrence of favourable environmental conditions. During 12 generations, three populations were grown in contrasted environments (Vervins North France, Le Moulon near Paris, Toulouse South France) under the influence of natural selection, drift, mutation and recombination. Evolution of diversity at the major gene VRN-1 involved in wheat vernalization response has been analysed jointly with earliness estimated in controlled conditions. Whatever the population, rapid phenotypic changes as well as parallel genotypic variations were observed in the first seven generations, probably as the result of selection acting on this major gene which explains 80% of the trait variation overall. Different allelic combinations at physically unlinked copies of VRN-1 located on distinct genomes (A, B and D) were selected between populations. As theoretically expected, due to population differentiation, a high level of genetic diversity was maintained overall in generation 12. Surprisingly, in two populations out of three, the emergence of new alleles by mutation or migration, coupled with temporal variable selection or frequency-dependent selection, allowed to maintain within-population diversity despite local genetic drift and natural selection. This result may plead for an evolutionary approach of wheat genetic resource conservation.

Strong linkage disequilibrium near the selected Yr17 resistance gene in a wheat experimental population.

Dynamic management (DM) is a method of genetic resources conservation that aims at maintaining evolutionary process in subdivided populations cultivated in contrasted environments. Such populations are often submitted to strong natural selection as it was the case for experimental wheat populations maintained under DM. Understanding impacts of selection on genetic diversity around selected genes is necessary for the middle-term maintenance of genetic variability in DM populations. Evolution of diversity at six neutral markers located near the yellow rust resistance gene Yr17 has been studied for the parental lines and for generations 1, 5, 10 and 17 in one of the DM populations. Yr17 provided complete resistance to yellow rust in France until 1997 and thus was suspected to be under strong selection. The gene is located on a fragment introgressed in winter wheat from a wild species. The presence of the gene was estimated using a marker closely related to the gene. We showed that the Yr17 gene has been selected between generations 5 and 10. Generally, selection tends to reduce diversity around selected genes, generating linkage disequilibrium (LD) between a gene and adjacent markers. Here, the major effect of the Yr17 gene selection was a reduction of multilocus diversity and the maintenance of strong pre-existing LD in the zone surrounding the gene for a distance of 20 cM. As expected, the presence of the exogenous introgression was responsible for restrictions to recombination which contributed to the maintenance of strong correlations between loci. However, we found a noticeable number of recombinations around the gene indicating a progressive incorporation of the fragment into the wheat genome.