In plants, local adaptation across species range is frequent. Yet, much has to be discovered on its environmental drivers, the underlying functional traits and their molecular determinants. Genome scans are popular to uncover outlier loci potentially involved in the genetic architecture of local adaptation, however links between outliers and phenotypic variation are rarely addressed. Here we focused on adaptation of teosinte populations along two elevation gradients in Mexico that display continuous environmental changes at a short geographical scale. We used two common gardens, and phenotyped 18 traits in 1664 plants from 11 populations of annual teosintes. In parallel, we genotyped these plants for 38 microsatellite markers as well as for 171 outlier single nucleotide polymorphisms (SNPs) that displayed excess of allele differentiation between pairs of lowland and highland populations and/or correlation with environmental variables. Our results revealed that phenotypic differentiation at 10 out of the 18 traits was driven by local selection. Trait covariation along the elevation gradient indicated that adaptation to altitude results from the assembly of multiple co-adapted traits into a complex syndrome: as elevation increases, plants flower earlier, produce less tillers, display lower stomata density and carry larger, longer and heavier grains. The proportion of outlier SNPs associating with phenotypic variation, however, largely depended on whether we considered a neutral structure with 5 genetic groups (73.7%) or 11 populations (13.5%), indicating that population stratification greatly affected our results. Finally, chromosomal inversions were enriched for both SNPs whose allele
Hybrid seed inviability (HSI) is an important mechanism of reproductive isolation and speciation. HSI varies in strength among populations of diploid species but it remains to be tested whether similar processes affect natural variation in HSI within ploidy-variable species (triploid block).Here we used extensive endosperm, seed and F 1 -hybrid phenotyping to explore HSI variation within a diploid-autotetraploid species. By leveraging 12 population pairs from three ploidy contact zones, we tested for the effect of interploidy crossing direction (parent of origin), ploidy divergence and spatial arrangement in shaping reproductive barriers in a naturally relevant context.We detected strong parent-of-origin effects on endosperm development, F 1 germination and survival, which was also reflected in the rates of triploid formation in the field. Endosperm cellularization failure was least severe and F 1 -hybrid performance was slightly better in the primary contact zone, with genetically closest diploid and tetraploid lineages.We demonstrated overall strong parent-of-origin effects on HSI in a ploidy variable species, which translate to fitness effects and contribute to interploidy reproductive isolation in a natural context. Subtle intraspecific variation in these traits suggests the fitness consequences of HSI are predominantly a constitutive property of the species regardless of the evolutionary background of its populations.
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Enhancers are key players in the spatio-temporal coordination of gene expression during numerous crucial processes, including tissue differentiation across development. Characterizing the transcription factors (TFs) and genes they connect, and the molecular functions underpinned is important to better characterize developmental processes. In plants, the recent molecular characterization of enhancers revealed their capacity to activate the expression of several target genes. Nevertheless, identifying these target genes at a genome-wide level is challenging, particularly for large-genome species, where enhancers and target genes can be hundreds of kilobases away. Therefore, the contribution of enhancers to plant regulatory networks remains poorly understood. Here, we investigate the enhancer-driven regulatory network of two maize tissues at different stages: leaves at seedling stage (V2-IST) and husks (bracts) at flowering. Using systems biology, we integrate genomic, epigenomic, and transcriptomic data to model the regulatory relationships between TFs and their potential target genes, and identify regulatory modules specific to husk and V2-IST. We show that leaves at the V2-IST stage are characterized by the response to hormones and macromolecules biogenesis and assembly, which are regulated by the BBR/BPC and AP2/ERF TF families, respectively. In contrast, husks are characterized by cell wall modification and response to abiotic stresses, which are, respectively, orchestrated by the C2C2/DOF and AP2/EREB families. Analysis of the corresponding enhancer sequences reveals that two different transposable element families (TIR transposon Mutator and MITE Pif/Harbinger) have shaped part of the regulatory network in each tissue, and that MITEs have provided potential new TF binding sites involved in husk tissue-specificity.
Enhancers are important regulators of gene expression during numerous crucial processes including tissue differentiation across development. In plants, their recent molecular characterization revealed their capacity to activate the expression of several target genes through the binding of transcription factors. Nevertheless, identifying these target genes at a genome-wide level remains a challenge, in particular in species with large genomes, where enhancers and target genes can be hundreds of kilobases away. Therefore, the contribution of enhancers to regulatory network is still poorly understood in plants. In this study, we investigate the enhancer-driven regulatory network of two maize tissues at different stages: leaves at seedling stage and husks (bracts) at flowering. Using a systems biology approach, we integrate genomic, epigenomic and transcriptomic data to model the regulatory relationship between transcription factors and their potential target genes. We identify regulatory modules specific to husk and V2-IST, and show that they are involved in distinct functions related to the biology of each tissue. We evidence enhancers exhibiting binding sites for two distinct transcription factor families (DOF and AP2/ERF) that drive the tissue-specificity of gene expression in seedling immature leaf and husk. Analysis of the corresponding enhancer sequences reveals that two different transposable element families (TIR transposon Mutator and MITE Pif/Harbinger ) have shaped the regulatory network in each tissue, and that MITEs have provided new transcription factor binding sites that are involved in husk tissue-specificity.
Anthropogenic and natural divergence processes in crop-wild fruit tree complexes are less studied than in annual crops, especially in the Caucasus, a pivotal region for plant domestication. We investigated anthropogenic and natural divergence processes in apples in the Caucasus from using 26 microsatellite markers amplified on 508 wild and cultivated samples. We found two specific Iranian cultivated populations that were differentiated from Malus domestica, the standard cultivated apple worldwide, suggesting a specific local domestication process in Iran. Some Iranian apple cultivars belonged to the Caucasian wild apple gene pools, indicating that farmers also use local wild apple for cultivation. Substantial wild-crop and crop-crop gene flow were also inferred. We identified seven genetically differentiated populations of wild apples (Malus orientalis) in the Caucasus. Niche modeling indicated that these populations likely resulted from range changes linked to the last glaciation. This study pinpoints Iran as a key region in the evolution and domestication of apple and further demonstrates the role of gene flow during fruit tree domestication as well as the impact of climate change on the natural divergence of a wild fruit tree. The results also provide a practical base for apple conservation and breeding programs in the Caucasus.
SummaryWith frequent host shifts involving the colonization of new hosts across large geographical ranges, crop pests are good models for examining the mechanisms of rapid colonization. The microbial partners of pest insects may be involved or affected by colonization, which has been little studied so far. We investigated the demographic history of the rosy apple aphid, Dysaphis plantaginea, a major pest of the cultivated apple (Malus domestica) in Europe, North Africa and North America, as well as the diversity of its endosymbiotic bacterial community. We genotyped a comprehensive sample of 714 colonies from Europe, Morocco and the US using mitochondrial (CytB and CO1), bacterial (16s rRNA and TrnpB), and 30 microsatellite markers. We detected five populations spread across the US, Morocco, Western and Eastern Europe, and Spain. Populations showed weak genetic differentiation and high genetic diversity, except the Moroccan and the North American that are likely the result of recent colonization events. Coalescent-based inferences releaved high levels of gene flow among populations during the colonization, but did not allow determining the sequence of colonization of Europe, America and Morroco by D. plantaginea, likely because of the weak genetic differentiation and the occurrence of gene flow among populations. Finally, we found that D. plantaginea rarely hosts any other endosymbiotic bacteria than its obligate nutritional symbiont Buchnera aphidicola. This suggests that secondary endosymbionts did not play any role in the rapid spread of the rosy apple aphid. These findings have fundamental importance for understanding pest colonization processes and implications for sustainable pest control programs.
2In plants, local adaptation across species range is frequent. Yet, much has to 3 be discovered on its environmental drivers, the underlying functional traits and their 4 molecular determinants. Genome scans are popular to uncover outlier loci potentially 5 involved in the genetic architecture of local adaptation, however links between 6 outliers and phenotypic variation are rarely addressed. Here we focused on adaptation 7 of teosinte populations along two elevation gradients in Mexico that display 8 continuous environmental changes at a short geographical scale. We used two 9 common gardens, and phenotyped 18 traits in 1664 plants from 11 populations of 10 annual teosintes. In parallel, we genotyped these plants for 38 microsatellite markers 11 as well as for 171 outlier single nucleotide polymorphisms (SNPs) that displayed 12 excess of allele differentiation between pairs of lowland and highland populations 13 and/or correlation with environmental variables. Our results revealed that phenotypic 14 differentiation at 10 out of the 18 traits was driven by local selection. Trait covariation 15 along the elevation gradient indicated that adaptation to altitude results from the 16 assembly of multiple co-adapted traits into a complex syndrome: as elevation 17 increases, plants flower earlier, produce less tillers, display lower stomata density and 18 carry larger, longer and heavier grains. The proportion of outlier SNPs associating 19 with phenotypic variation, however, largely depended on whether we considered a 20 neutral structure with 5 genetic groups (73.7%) or 11 populations (13.5%), indicating 21 that population stratification greatly affected our results. Finally, chromosomal 22 inversions were enriched for both SNPs whose allele frequencies shifted along 23 elevation as well as phenotypically-associated SNPs. Altogether, our results are 24 consistent with the establishment of an altitudinal syndrome promoted by local 25 selective forces in teosinte populations in spite of detectable gene flow. Because 26 elevation mimics climate change through space, SNPs that we found underlying 27 phenotypic variation at adaptive traits may be relevant for future maize breeding. 28 29 Author summary 33 Across their native range species encounter a diversity of habitats promoting local 34 adaptation of geographically distributed populations. While local adaptation is 35widespread, much has yet to be discovered about the conditions of its emergence, the 36 targeted traits, their molecular determinants and the underlying ecological drivers. 37Here we employed a reverse ecology approach, combining phenotypes and genotypes, 38 to mine the determinants of local adaptation of teosinte populations distributed along 39 two steep altitudinal gradients in Mexico. Evaluation of 11 populations in two 40 common gardens located at mid-elevation pointed to adaptation via an altitudinal 41 multivariate syndrome, in spite of gene flow. We scanned genomes to identify loci 42 with allele frequencies shifts along elevation, a subset of whic...
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