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Tenaillon, M. I.

Publications and source records attributed to Tenaillon, M. I..

13 recordsLinked to original sources

Dissecting the phenotypic and genetic determinants of maize-bean interactions in intercropping

O_LICereal-legume intercropping is a cornerstone of agroecological systems because interactions between species can enhance agroecosystem resilience. Yet, the mechanisms underlying these interactions remain poorly understood. To address this gap, we investigated the maize-bean association under low-input conditions. C_LIO_LIWe conducted a two-year intercropping experiment with 200 climbing bean lines grown alongside three maize landraces in France and Romania. We evaluated bean phenotypic responses above- and below-ground to 3 maize landraces, treated as distinct biotic environments (E). Direct and indirect genetic effects were assessed by mapping bean and maize phenotypic traits onto the bean genome (G), with G x E interactions tested using contrasts among maize landraces. C_LIO_LICompetitive interactions dominated, maize acting as the stronger competitor. Maize landraces created distinct biotic environments affecting bean traits. Best-performing partners varied across experimental fields, with no evidence of bean local adaptation. The most productive and balanced mixtures were obtained with the traditionally intercropped maize landrace. Genome-wide association analyses identified loci underlying direct and indirect genetic effects, including candidate genes associated with neighbor perception. C_LIO_LIThese findings reveal the genetic complexity of maize-bean interactions and highlight competitive tolerance in bean and reduced aggressiveness in maize as key traits for improving cereal-legume intercrop performance. C_LI

genetics↗

How to be dispensable: genomic and transcriptomic determinants in maize genes

BackgroundPlant genomes harbour a substantial proportion of dispensable genes - present only in a subset of individuals - that differ from ubiquitously shared core genes in multiple genomic and expression features. While these differences have been repeatedly documented, the factors shaping gene dispensability remain poorly understood. ResultsWe assembled a pan-gene set from eight maize inbred lines from American and European germplasms, together with their transcriptomic profile across 22 tissues/conditions, revealing the genomic and transcriptomic determinants of maize gene dispensability. Multivariate analysis demonstrates that gene expression level and purifying selection - rather than gene size - are the primary factors distinguishing core from dispensable genes. Dispensable genes overlap Helitrons at 4.6 times the rate of core genes, implicating Helitron-mediated gene capture as a major mechanism of dispensable gene formation. Classifying genes into stably expressed, variably expressed, and on-off categories shows that all three classes contain dispensable genes, though in different proportions than for core genes. Contrary to previous assumptions, we show that dispensable genes can participate in basal biological functions just as core genes, and that gene duplication likely provides only a partial mechanism for functional complementation of accessory genes absence. ConclusionsOur results provide novel insights into the molecular and evolutionary factors distinguishing core from dispensable genes and into the biological mechanisms shaping gene dispensability in maize, and demonstrate that classifying genes by transcriptional patterns provides a powerful framework for understanding the biological functions and evolutionary dynamics of both core and dispensable genes.

plant biology↗

Evolution of crop phenotypic spaces through domestication

O_LIWe used domestication as an in vivo replicated experiment to investigate how divergent selection has shaped the evolution of multivariate phenotypic spaces. C_LIO_LIWe measured 11 to 57 qualitative and quantitative traits in 13 species, either unique or shared between species, and established a framework for cross-species comparisons. C_LIO_LIOur results revealed significant convergence that translated into a cross-species domestication syndrome. Most species exhibited a reduction of the multivariate phenotypic space during domestication. We brought evidence that Near Infrared spectra measured on leaves reflect phenotypic evolution unrelated with domestication, enabling its use as a control for sampling effects across species. Building on this, we developed a multivariate Phenotypic Divergence Index (mPDI) to rank species by the extent of phenotypic divergence under domestication. We found a high disjunction of wild and domestic phenotypic spaces in all species. Neither the mPDI nor the relative size of wild versus domestic multivariate phenotypic spaces was influenced by the domestication timing or mating system. Lastly, we observed a progressive decoupling of trait correlations with increasing time since domestication. C_LIO_LIIn addition to introducing a new index that can be applied for cross-species comparisons, our study uncovers recurring patterns shared among species, pointing to general principles underlying plant domestication. C_LI

evolutionary biology↗

A multidisciplinary on-farm survey of maize-bean intercropping shows that revival of traditionalagricultural systems requires careful consideration of partner varieties and agronomic practices.

O_LICereal-legume intercropping is a promising strategy for sustainable agroecosystems. The traditional intercropping of maize and bean is experiencing a revival in some modern agricultural settings, such as in southwestern France, where maize hybrids are intercropped with the commercialized Tarbais bean. We conducted on-farm surveys and a field assay to address the following questions: How does the cropping system impact yield, nutrient uptake, and rhizosphere bacterial assemblages? Do positive or negative interactions between maize and beans dominate in intercropping? What is the effect of intercropping on plant transcriptomics? C_LIO_LIWe recorded farming practices, conducted yield and nutrient measurements, and characterized soil bacterial assemblages to compare sole-cropped maize and beans with intercropped plants. A controlled field assay was also established to extend this comparison to plant gene expression differences. C_LIO_LIIntercropping was associated with a trend towards increased bacterial diversity. The cropping system significantly influenced agronomic traits, with frequent farm-by-cropping system interactions underscoring the critical role of farming practices. Competition dominated maize-bean intercropping, with 34 negative correlations among the 47 significant ones between maize and bean traits. This competition affected yield and nutrition, but primarily impacted beans, which produced fewer but bigger/heavier seeds. Transcriptomic results concurred with these findings, revealing no differentially expressed genes in maize but 5,070 in beans under competition. C_LIO_LIOverall, our findings suggest that beneficial interactions between the two crops are hindered under current field conditions, underscoring the importance of carefully considering partner varieties and farming practices to revive traditional agricultural systems. C_LI Societal Impact StatementCereal-legume intercropping is a promising strategy for sustainable agroecosystems that leverages the biological complementarities between plant species, reducing the need for chemical inputs while enhancing field biodiversity. Here, we focused on maize-bean intercropping, which is experiencing a revival in modern conventional agricultural settings. We found a trend towards an increased soil bacterial diversity in intercropping. However, competition between the two crops dominated and primarily impacted yield and gene expression in beans. Despite lower yield, bean seeds exhibited greater size. Our study indicates that implementing variety selection of both species and adapting farming practices is essential to fully harness the potential of intercropping.

plant biology↗

RIDGE, a tool tailored to detect gene flow barriers across species pairs

Characterizing the processes underlying reproductive isolation between diverging lineages is central to understanding speciation. Here, we present RIDGE - Reproductive Isolation Detection using Genomic polymorphisms - a tool tailored for quantifying gene flow barrier proportions and identifying the corresponding genomic regions. RIDGE relies on an Approximate Bayesian Computation with a model-averaging approach to accommodate diverse scenarios of lineage divergence. It captures heterogeneity in effective migration rate along the genome while accounting for variation in linked selection and recombination. The barrier detection test relies on numerous summary statistics to compute a Bayes factor, offering a robust statistical framework that facilitates cross-species comparisons. Simulations revealed that RIDGE is particularly efficient both at capturing signals of ongoing migration and at identifying barrier loci, including for recent divergence times (~0.1 2Ne generations). Applying RIDGE to four published crow datasets, we validated our tool by identifying a well-known large genomic region associated with mate choice patterns. We identified additional barrier loci between species pairs, which have shown, on the one hand, that depending on the biological, demographic, and selection contexts, different combinations of summary statistics are informative for the detection of signals. On the other hand, these analyses also highlight the value of our newly developed outlier statistics in challenging detection conditions.

evolutionary biology↗

The coupling between mutations effects and environment guides the exploration of the phenotypic space as evidenced in artificial selection experiments

Quantitative genetics models have shown that long-term selection responses depend on initial variance and mutational influx. Understanding limits of selection requires quantifying the role of mutational variance. However, correlative responses to selection on non-focal traits can perturb the selection response on the focal trait; and generations are often confounded with selection environments so that genotype by environment (GxE) interactions are ignored. The Saclay Divergent Selection Experiments (DSE) on maize flowering time were used to track the fate of individual mutations combining genotyping data and phenotyping data from yearly measurements (DSEYM) and common garden experiments (DSECG) with four objectives (1) to quantify the relative contribution of standing and mutational variance to the selection response, (2) to estimate genotypic mutation effects, (3) to study the impact of GxE interactions in the selection response, (4) to analyze how trait correlations modulate the exploration of the phenotypic space. We validated experimentally the expected enrichment of fixed beneficial mutations with an average effect of +0.278 and +0.299 days to flowering, depending on the genetic background. Fixation of unfavorable mutations reached up to 25% of incoming mutations, a genetic load possibly due to antagonistic pleiotropy, whereby mutations fixed in the selection environment (DSEYM) turned to be unfavorable in the evaluation environment (DSECG). Global patterns of trait correlations were conserved across genetic backgrounds but exhibited temporal patterns. Traits weakly or uncorrelated with flowering time triggered stochastic exploration of the phenotypic space, owing to microenvironment-specific fixation of standing variants and pleiotropic mutational input.

evolutionary biology↗

Not so local: the population genetics of convergent adaptation in maize and teosinte.

What is the genetic architecture of local adaptation and what is the geographic scale over which it operates? We investigated patterns of local and convergent adaptation in five sympatric population pairs of traditionally cultivated maize and its wild relative teosinte (Zea mays subsp. parviglumis). We found that signatures of local adaptation based on the inference of adaptive fixations and selective sweeps are frequently exclusive to individual populations, more so in teosinte compared to maize. However, for both maize and teosinte, selective sweeps are also frequently shared by several populations, and often between subspecies. We were further able to infer that selective sweeps were shared among populations most often via migration, though sharing via standing variation was also common. Our analyses suggest that teosinte has been a continued source of beneficial alleles for maize, even after domestication, and that maize populations have facilitated adaptation in teosinte by moving beneficial alleles across the landscape. Taken together, our results suggest local adaptation in maize and teosinte has an intermediate geographic scale, one that is larger than individual populations but smaller than the species range.

evolutionary biology↗

Gene network simulations provide testable predictions for the molecular domestication syndrome

The domestication of plant species lead to repeatable morphological evolution, often referred to as the phenotypic domestication syndrome. Domestication is also associated with important genomic changes, such as the loss of genetic diversity compared to adequately large wild populations, and modifications of gene expression patterns. Here, we explored theoretically the effect of a domestication-like scenario on the evolution of gene regulatory networks. We ran population genetics simulations in which individuals were featured by their genotype (an interaction matrix encoding a gene regulatory network) and their gene expressions, representing the phenotypic level. Our domestication scenario included a population bottleneck and a selection switch mimicking human-mediated directional and canalizing selection, i.e., change in the optimal gene expression level and selection towards more stable expression across environments. We showed that domestication profoundly alters genetic architectures. Based on four examples of plant domestication scenarios, our simulations predict (i) a drop in neutral allelic diversity, (ii) a change in gene expression variance that depends upon the domestication scenario, (iii) transient maladaptive plasticity, (iv) a deep rewiring of the gene regulatory networks, with a trend towards gain of regulatory interactions, and (v) a global increase in the genetic correlations among gene expressions, with a loss of modularity in the resulting coexpression patterns and in the underlying networks. We provide empirically testable predictions on the differences of genetic architectures between wild and domesticated forms. The characterization of such systematic evolutionary changes in the genetic architecture of traits contributes to define a molecular domestication syndrome.

evolutionary biology↗

Interplay between high drift-high selection limits the genetic load in small selfing maize populations

Population and quantitative genetic models provide useful approximations to predict long-term selection responses sustaining phenotypic shifts, and underlying multilocus adaptive dynamics. Valid across a broad range of parameters, their use for understanding the adaptive dynamics of small selfing populations undergoing strong selection intensity (thereafter High Drift-High selection regime, HDHS) remains to be explored. Saclay Divergent Selection Experiments (DSEs) on maize flowering time provide an interesting example of populations evolving under HDHS, with significant selection responses over 20 generations in two directions. We combined experimental data from Saclay DSEs, forward individual-based simulations, and theoretical predictions to dissect the evolutionary mechanisms at play in the observed selection responses. We asked two main questions: How do mutations arise, spread, and reach fixation in populations evolving under HDHS ? How does the interplay between drift and selection influence observed phenotypic shifts ? We showed that the long-lasting response to selection in small populations is due to the rapid fixation of mutations occurring during the generations of selection. Among fixed mutations, we also found a clear signal of enrichment for beneficial mutations revealing a limited cost of selection. Both environmental stochasticity and variation in selection coefficients likely contributed to exacerbate mutational effects, thereby facilitating selection grasp and fixation of small-effect mutations. Together our results highlight that despite a small number of polymorphic loci expected under HDHS, adaptive variation is continuously fueled by a vast mutational target. We discuss our results in the context of breeding and long-term survival of small selfing populations.

evolutionary biology↗

A wild Cucurbita genome reveals the role of structural variants and introgression in domestication

Despite their economic importance and well-characterized domestication syndrome, the genomic impact of domestication and the identification of variants underlying the domestication traits in Cucurbita species (pumpkins and squashes) is currently lacking. Cucurbita argyrosperma, also known as cushaw pumpkin or silver-seed gourd, is a Mexican crop consumed primarily for its seeds rather than fruit flesh. This makes it a good model to study Cucurbita domestication, as seeds were an essential component of early Mesoamerican diet and likely the first targets of human-guided selection in pumpkins and squashes. We obtained population-level data using tunable Genotype by Sequencing libraries for 192 individuals of the wild and domesticated subspecies of C. argyrosperma across Mexico. We also assembled the first wild Cucurbita genome at a chromosome level. Comparative genomic analyses revealed several structural variants and presence/absence of genes related to domestication. Our results indicate a monophyletic origin of this domesticated crop in the lowlands of Jalisco. We uncovered candidate domestication genes that are involved in the synthesis and regulation of growth hormones, plant defense mechanisms, flowering time and seed development. The presence of shared selected alleles with the closely related species Cucurbita moschata suggests domestication-related introgression between both taxa.

evolutionary biology↗

Genomic footprints of local adaptation along elevation gradients associate with present phenotypic variation in teosintes

Local adaptation across species range is widespread. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Because elevation gradients display continuous environmental changes at a short geographical scale, they provide an exceptional opportunity to investigate these questions. Here, we used two common gardens to phenotype 1664 plants from 11 populations of annual teosintes. These populations were sampled across two elevation gradients in Mexico. Our results point to a syndrome of adaptation to altitude with the production of offspring that flowered earlier, produced less tillers, and larger, longer and heavier grains with increasing elevation. We genotyped these plants for 178 outlier single nucleotide polymorphisms (SNPs), which had been chosen because they displayed excess of allele differentiation and/or correlation with environmental variables in six populations with contrasted altitudes. A high proportion of outlier SNPs associated with the phenotypic variation of at least one trait. We tested phenotypic pairwise correlations between traits, and found that the higher the correlation, the greater the number of common associated SNPs. In addition, allele frequencies at 87 of the outlier SNPs correlated with an environmental component best summarized by altitudinal variation on a broad sample of 28 populations. Chromosomal inversions were enriched for both phenotypically-associated and environmentally-correlated SNPs. Altogether, our results are consistent with the set-up of an altitudinal syndrome promoted by local adaptation of teosinte populations in the face of gene flow. We showed that pleiotropy is pervasive and potentially has constrained the evolution of traits. Finally, we recovered variants underlying phenotypic variation at adaptive traits. Because elevation mimics climate change through space, these variants may be relevant for future maize breeding. Author summaryAcross their native range, species encounter a diversity of habitats promoting local adaptation of geographically distributed populations. While local adaptation is widespread, much has yet to be discovered about the conditions of its emergence, the targeted traits, their molecular determinants and the underlying ecological drivers. Here we employed a reverse ecology approach, combining phenotypes and genotypes, to mine the determinants of local adaptation of teosinte populations distributed along two steep altitudinal gradients in Mexico. Evaluation of 11 populations in two common gardens located at mid-elevation pointed to the set-up of an altitudinal syndrome, in spite of gene flow. We scanned genomes to identify loci with allele frequencies shifts along elevation. Interestingly, variation at these loci was commonly associated to variation of phenotypes. Because elevation mimics climate change through space, these variants may be relevant for future maize breeding.

evolutionary biology↗

Transcriptomic response to divergent selection for flowering time in maize reveals convergence and key players of the underlying gene regulatory network

Artificial selection experiments are designed to investigate phenotypic evolution of complex traits and its genetic bases. Here we focused on flowering time, a trait of key importance for plant adaptation and life-cycle shifts. We undertook divergent selection experiments (Saclay DSEs) from two maize inbred lines. After 13 generations of selection, we obtained we obtained a time-lag of roughly two weeks between Early- and Late-populations. We used this material to characterize the genome-wide transcriptomic response to selection in the shoot apical meristem (SAM) before, during and after floral transition in realistic field conditions during two consecutive years. We validated the reliability of performing RNA-sequencing in uncontrolled conditions. We found that roughly half of maize genes were expressed in the SAM, 59.3% of which were differentially expressed. We detected a majority of genes with differential expression between inbreds and across meristem status, and retrieved a subset of 2,451 genes involved in the response to selection. Among these, we found a significant enrichment for genes with known function in maize flowering time. Furthermore, they were more often shared between inbreds than expected by chance, suggesting convergence of gene expression. We discuss new insights into the expression pattern of key players of the underlying gene regulatory network including ZCN8, RAP2.7, ZMM4, KN1, GA2ox1, as well as alternative scenarios for genetic convergence.

plant biology↗

Was maize domesticated in the Balsas Basin? Complex patterns of genetic divergence, gene flow and ancestral introgressions among Zea subspecies suggest an alternative scenario

The study of maize domestication has overlooked the genetic structure within maizes wild relative teosinte. Prior to investigating the domestication history of maize (Zea mays subspecies mays), one should first understand the population history of teosintes and how they relate to maize. To achieve this, we used 32,739 SNPs obtained from a broad sampling of teosinte populations and 46 maize landraces and a) inferred current and past gene flow among teosinte populations and maize, b) analyzed the degree of introgression among Zea mays subspecies, and c) explored the putative domestication location of maize. We found geographic structure and introgression between Zea mays taxa. Teosinte subspecies have diverged significantly from maize, which indicates that current teosinte populations have evolved mainly independently from maize since the domestication. Our results further suggest that the likely ancestor of maize may maybe have come from Jalisco or the Pacific coast.\n\nOne Sentence SummaryShared polymorphism in teosinte suggests a Jalisco origin of maize domestication.

evolutionary biology↗