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Plomion, C.

Publications and source records attributed to Plomion, C..

17 recordsLinked to original sources

A higher load of deleterious mutations has a detrimental effect on tree growth in maritime pine

A high proportion of deleterious mutations in the genome is predicted to cause a reduction in fitness known as genetic load. In plants, most studies focus on how detrimental mutations increase as a consequence of population bottlenecks, for instance in cultivated species as a negative outcome of domestication or at the margin of species ranges. However, the actual adverse effect of genetic load on individual phenotypes remains little characterised, especially in wild plant species with large populations and long lifespans. We estimated genetic load based on genomic data in populations of the conifer maritime pine (Pinus pinaster, Ait.), and examined its association with phenotypic traits related to growth, phenology, and water-use efficiency measured under common garden conditions. Our results revealed a strong negative correlation between genetic load and tree height on the Mediterranean island of Corsica, thus suggesting a negative cumulative effect of deleterious mutations on tree growth at the regional scale. Our study is one of the first to experimentally demonstrate adverse phenotypic effects (reduced tree growth) of genetic load in a long-lived plant.

evolutionary biology↗

Estimation of contemporary effective population size in plant populations: limitations of genomic datasets

Effective population size (Ne) is a pivotal evolutionary parameter with crucial implications in conservation practice and policy. Genetic methods to estimate Ne have been preferred over demographic methods because they rely on genetic data rather than time-consuming ecological monitoring. Methods based on linkage disequilibrium, in particular, have become popular in conservation as they require a single sampling and provide estimates that refer to recent generations. A software programme based on the linkage disequilibrium method, GONE, looks particularly promising to estimate contemporary and recent-historical Ne (up to 200 generations in the past). Genomic datasets from non-model species, especially plants, may present some constraints to the use of GONE, as linkage maps and reference genomes are seldom available, and SNP genotyping is usually based on reduced-representation methods. In this study, we use empirical datasets from four plant species to explore the limitations of plant genomic datasets when estimating Ne using the algorithm implemented in GONE, in addition to exploring some typical biological limitations that may affect Ne estimation using the linkage disequilibrium method, such as the occurrence of population structure. We show how accuracy and precision of Ne estimates potentially change with the following factors: occurrence of missing data, limited number of SNPs/individuals sampled, and lack of information about the location of SNPs on chromosomes, with the latter producing a significant bias, previously unexplored with empirical data. We finally compare the Ne estimates obtained in GONE for the last generations with the contemporary Ne estimates obtained in the programmes currentNe and NeEstimator.

evolutionary biology↗

Plant mutations: slaying beautiful hypotheses by surprising evidence

Somatic mutations potentially play a role in plant evolution, but common expectations pertaining to plant somatic mutations remain insufficiently tested. Unlike in most animals, the plant germline is assumed to be set aside late in development, leading to the expectation that plants accumulate somatic mutations along growth. Therefore, several predictions were made on the fate of somatic mutations: mutations have generally low frequency in plant tissues; mutations at high frequency have a higher chance of intergenerational transmission; branching topology of the tree dictates mutation distribution; and, exposure to UV radiation increases mutagenesis. To provide new insights into mutation accumulation and transmission in plants, we produced two high-quality reference genomes and a unique dataset of 60 high-coverage whole-genome sequences of two tropical tree species, Dicorynia guianensis (Fabaceae) and Sextonia rubra (Lauraceae). We identified 15,066 de novo somatic mutations in D. guianensis and 3,208 in S. rubra, surprisingly almost all found at low frequency. We demonstrate that: 1) low-frequency mutations can be transmitted to the next generation; 2) mutation phylogenies deviate from the branching topology of the tree; and 3) mutation rates and mutation spectra are not demonstrably affected by differences in UV exposure. Altogether, our results suggest far more complex links between plant growth, ageing, UV exposure, and mutation rates than commonly thought. Significance StatementThe origin and fate of new mutations have received less attention in plants than in animals. Similarly to animals, plant mutations are expected to accumulate with growth and time, and under exposure to UV light. However, contrary to animals, plant reproductive organs form late in an individuals development, allowing the transmission to the progeny of mutations accumulated along growth. Here, we resequenced DNA from different branches differentially exposed to sunlight of two tropical tree species. We showed that new mutations are generally rare in plant tissues and do not mimic branching patterns but can nevertheless be transmitted to the progeny. Our findings provide a new perspective on heritable plant mutation and its pivotal role as the engine of evolution.

genomics↗

Extensive variation of leaf specialized metabolite production in sessile oak (Quercus petraea) populations is to a large extent genetically determined but not locally adaptive.

Specialized or secondary metabolites play a key role in plant resistance against abiotic stresses and defences against bioaggressors. For example, in sessile oaks Quercus petraea, phenolics contribute to reduce herbivore damage and improve drought resistance. Here, we explored the natural variation of specialized metabolites in nine European provenances of sessile oaks and aimed to detect its underlying genetic bases. We sampled mature leaves from high and low branches on 225 sessile oak trees located in a common garden and used untargeted metabolomics to characterise the variation of 217 specialized metabolites. In addition, we used whole genome low-depth sequencing to genotype individuals for 1.4M genetic markers. We found that leaf specialized metabolites displayed extensive within-provenance variation, but very little differentiation between provenances. In addition, a genome-wide association study allowed detecting significant associations for 42% of these metabolites. Hence, our results suggest that genetic variation for most leaf specialized metabolites is unlikely to be locally adaptive, however lack of differentiation among populations suggests selection acts locally to maintain diversity at loci associated with leaf specialized metabolites variation.

evolutionary biology↗

Synchronous effective population size changes and genetic stability of forest trees through glacial cycles

The effect of past environmental changes on the demography and genetic diversity of natural populations remains a contentious issue and has rarely been investigated across multiple, phylogenetically distant species. Here, we performed comparative population genomic analyses and demographic inferences for seven widely distributed and ecologically contrasted European forest tree species based on concerted sampling of 164 populations across their natural ranges. For all seven species, the effective population size, Ne, increased or remained stable over many glacial cycles and up to 15 million years in the most extreme cases. Hence, surprisingly, the drastic environmental changes associated with the Pleistocene glacial cycles have had little impact on the level of genetic diversity of dominant forest tree species, despite major shifts in their geographic ranges. Based on their trajectories of Ne over time, the seven tree species can be divided into three major groups, highlighting the importance of life history and range size in determining synchronous variation in genetic diversity, over time. Altogether, our results indicate that forest trees were able to retain their evolutionary potential over very long periods of time despite strong environmental changes. One-Sentence SummaryPopulation genomic analyses reveal that forest trees retained their evolutionary potential over the Quaternary.

evolutionary biology↗

Locally adapted oak populations along an elevation gradient display different molecular strategies to regulate bud phenology.

Research conductedWith the ongoing global warming, there are serious concerns about the persistence of locally adapted populations. Indeed, with the raising of temperature, the phenological cycle of tree species may be strongly affected since higher winter temperatures may have a negative impact on endodormancy release if chilling requirements are not fulfilled during winter and late frost in spring may expose trees if buds flush too early. Thus, Environmental gradients (showing continuous variations of environmental conditions) constitute a design of choice to analyze the effect of winter dormancy in locally adapted population. MethodsIn the present study, we used an elevation gradient in the Pyrenees to explore the gene expression network involved in dormancy regulation in natural populations of sessile oak locally adapted to temperature. Terminal buds were harvested during dormancy induction and release at different elevations. Then, gene expression was quantified using RNAseq and we used a likelihood ratio test to identify genes displaying significant dormancy, elevation or dormancy-by-elevation interaction effects. Key resultsOur results highlight molecular processes in locally adapted populations along this elevation cline, and made it possible to identify key dormancy-by-elevation responsive genes revealing that locally adapted populations have evolved distinct molecular strategies to adapt their bud phenology in response to environmental variation (i.e. temperature).

plant biology↗

Water stress-associated isolation barriers between two sympatric oak species

Drought and waterlogging impede tree growth and may even lead to tree death. With climate change, these environmental factors are a growing source of concern, particularly for temperate forests. Oaks, an emblematic group of tree species, have evolved a range of adaptations to cope with these constraints. The two most widely distributed European species -- pedunculate oak (PO) and sessile oaks (SO) -- have overlapping ranges, but are highly constrained locally by soil water content variation. These differences in local ecological requirements provide a powerful biological model for studying the role of ecological barriers in speciation. We used an experimental set-up mimicking the ecological preferences of these species, in which seedlings were subjected to waterlogging and drought. We studied gene expression in roots by RNA-seq and identified genes differentially expressed between treatments with different outcomes depending on species. These "species x environment"-responsive genes revealed adaptive molecular strategies involving adventitious and lateral root formation, aerenchyma formation in PO, and osmoregulation and ABA regulation in SO. With this experimental design, we also identified genes with expression profiles presenting a "species" effect regardless of imposed constraints with important roles in intrinsic reproductive barriers. Finally, we compared our findings with those for a genome scan of species divergence and found that the candidate genes were enriched in highly differentiated SNPs. This suggests that many of the genes involved in the contrasting transcriptomic responses are subject to natural selection and that gene regulation helps to maintain these two different oak species in sympatry.

plant biology↗

Molecular plasticity to soil water deficit differs between sessile oak (Quercus Petraea (Matt.) Liebl.) high and low water use efficiency genotypes

BackgroundWater use efficiency (WUE) is an important adaptive trait for soil water deficit. The molecular and physiological bases of WUE regulation in crops have been studied in detail in the context of plant breeding. Knowledge for most forest tree species lags behind, despite the need to identify populations or genotypes able to cope with the longer, more intense drought periods likely to result from climate warming. ResultsWe aimed to bridge this gap in knowledge for sessile oak (Quercus Petraeae Matt. L.), one of the most ecologically and economically important tree species in Europe, using a factorial design including two genotypes (low and high WUE) and two watering regimes (control and drought). By monitoring the ecophysiological response, we were able to identify groups of genotypes with high and low WUE. We then performed RNA-seq to quantify gene expression for the most extreme genotypes exposed to two watering regimes. By analyzing the interaction term, we were able to capture the molecular strategy of each group of plants for coping with drought. Regardless of water availability, the high WUE genotypes overexpressed genes associated with drought responses, and the control of stomatal density and distribution, and displayed a downregulation of genes associated with early stomatal closure and high transpiration rate. High-WUE genotypes, thus, coped with drought by fine-tuning the expression of genes with known functions in the regulation of stomatal size, density, movement or aperture and transpiration rate. ConclusionFine physiological screening of sessile oaks with contrasting WUE, and their molecular characterization i) highlighted subtle differences in transcription between low and high WUE genotypes, identifying key molecular players in the genetic control of this trait, and ii) revealed the genes underlying the molecular strategy that had evolved in each group to cope with water deficit, providing new insight into the value of WUE for adaptation to drought.

plant biology↗

Genome-wide evolutionary response of European oakssince the Little Ice Age

The pace of tree microevolution during Anthropocene warming is largely unknown. We used a retrospective approach to monitor genomic changes in oak trees since the Little Ice Age (LIA). Allelic frequency changes were assessed from whole-genome pooled sequences for four age-structured cohorts of sessile oak (Quercus petraea) dating back to 1680, in each of three different oak forests in France. The genetic covariances of allelic frequency changes increased between successive time periods, highlighting genome-wide effects of linked selection. We found imprints of convergent linked selection in the three forests during the late LIA, and a shift of selection during more recent time periods. The changes in allelic covariances within and between forests mirrored the documented changes in the occurrence of extreme events (droughts and frosts) over the last three hundred years. The genomic regions with the highest covariances were enriched in genes involved in plant responses to pathogens and abiotic stresses (temperature and drought). These responses are consistent with the reported sequence of frost (or drought) and disease damage ultimately leading to the oak dieback after extreme events. Our results therefore provide evidence of selection operating on long-lived species during recent climatic changes.

evolutionary biology↗

Combining climatic and genomic data improves range-wide tree height growth prediction in a forest tree

Population response functions based on climatic and phenotypic data from common gardens have long been the gold standard for predicting quantitative trait variation in new environments. However, prediction accuracy might be enhanced by incorporating genomic information that captures the neutral and adaptive processes behind intra-population genetic variation. We used five clonal common gardens containing 34 provenances (523 genotypes) of maritime pine (Pinus pinaster Aiton) to determine whether models combining climatic and genomic data capture the underlying drivers of height-growth variation, and thus improve predictions at large geographical scales. The plastic component explained most of the height-growth variation, probably resulting from population responses to multiple environmental factors. The genetic component stemmed mainly from climate adaptation, and the distinct demographic and selective histories of the different maritime pine gene pools. Models combining climate-of-origin and gene pool of the provenances, and positive-effect height-associated alleles (PEAs) captured most of the genetic component of height-growth and better predicted new provenances compared to the climate-based population response functions. Regionally-selected PEAs were better predictors than globally-selected PEAs, showing high predictive ability in some environments, even when included alone in the models. These results are therefore promising for the future use of genome-based prediction of quantitative traits.

genetics↗

Polygenic adaptation and negative selection across traits, years and environments in a long-lived plant species (Pinus pinaster Ait.)

A decade of association studies in multiple organisms suggests that most complex traits are polygenic; that is, they have a genetic architecture determined by numerous loci distributed across the genome, each with small effect-size. Thus, determining the degree of polygenicity and its variation across traits, environments and years is useful to understand the genetic basis of phenotypic variation. In this study, we applied multilocus approaches to estimate the degree of polygenicity of fitness-related traits in a long-lived plant (Pinus pinaster Ait., maritime pine) and to analyze how polygenicity changes across environments and years. To do so, we evaluated five categories of fitness-related traits (survival, height, phenology-related, functional, and biotic-stress response traits) in a clonal common garden network, planted in contrasted environments (over 12,500 trees). First, most of the analyzed traits showed evidence of local adaptation based on QST-FST comparisons. Second, we observed a remarkably stable degree of polygenicity, averaging 6% (range of 0-27%), across traits, environments and years. As previously suggested for humans, some of these traits showed also evidence of negative selection, which could explain, at least partially, the high degree of polygenicity. The observed genetic architecture of fitness-related traits in maritime pine supports the polygenic adaptation model. Because polygenic adaptation can occur rapidly, our study suggests that current predictions on the capacity of natural forest tree populations to adapt to new environments should be revised, which is of special relevance in the current context of climate change.

genetics↗

Growth and mortality of the oak processionary moth, Thaumetopoea processionea L., on two oak species: direct and trait-mediated effects of host and neighbour species identity

The presence of heterospecific neighbours can affect damage caused by pest insects on focal plants. However, how plant neighbours influence herbivore performance is poorly understood. We tested the independent and interactive effects of tree species identity and tree neighbour type (conspecific vs. heterospecific) on the performance of a major oak pest, the oak processionary moth larvae (OPM, Thaumetopoea processionea) fed on Quercus robur and Q. petraea. We performed a factorial greenhouse experiment in which we grew two oak saplings per pot, either from the same species or from both species. We quantified growth and mortality of OPM larvae, leaf phenolic compounds, C:N ratio and bud phenology. OPM larvae performed significantly better on Q. petraea than on Q. robur, regardless of plant neighbour type. Phenolic compounds and C:N, but not phenology, differed between oak species and neighbour species identity. Only bud phenology had a significant effect on OPM performance, which was better when young larvae had access to recently unfolded leaves, regardless of oak species and neighbour identity. Although oak neighbour identity altered the expression of leaf traits, this effect had no measurable consequences on OPM performance. However, further studies should consider the effect of oak species neighbour on OPM preferences for either Q. robur or Q. petraea, in pure and mixed stands, before translating current results into recommendations for forest management. Author ContributionTD and BC conceived the study and acquired the data. TD performed experiment and analysed the data. EV, TD and XM performed the chemical analyses. TD and BC drafted the first version of the manuscript and all authors wrote the final version of the manuscript. TD, BC conceived and designed research. TD performed experiment and analysed data. EV, TD, XM performed the chemical analyses. TD, BC wrote the manuscript. All authors read and approved the manuscript. AM and DB conceived and designed research. AM and BB conducted experiments. GR contributed new reagents or analytical tools. AM, BB and GR analysed data. AM wrote the manuscript. All authors read and approved the manuscript.

ecology↗

Genetic basis of susceptibility to Diplodia sapinea and Armillaria ostoyae in maritime pine

Forest ecosystems are increasingly challenged by extreme events, e.g. drought, storms, pest and pathogenic fungi outbreaks, causing severe ecological and economical losses. Understanding the genetic basis of adaptive traits in tree species is of key importance to preserve forest ecosystems, as genetic variation in a trait (i.e. heritability) determines its potential for human-mediated or evolutionary change. Maritime pine (Pinus pinaster Aiton), a conifer widely distributed in southwestern Europe and northwestern Africa, grows under contrasted environmental conditions promoting local adaptation. Genetic variation at adaptive phenotypes, including height, growth phenology and susceptibility to two fungal pathogens (Diplodia sapinea and Armillaria ostoyae) and an insect pest (Thaumetopoea pityocampa), were assessed in a range-wide clonal common garden of maritime pine. Broad-sense heritability was significant for height (0.219), growth phenology (0.165-0.310) and pathogen susceptibility (necrosis length caused by D. sapinea, 0.152; and by A. ostoyae, 0.021) measured after inoculation under controlled conditions, but not for pine processionary moth incidence in the common garden. The correlations of trait variation among populations revealed contrasting trends for pathogen susceptibility to D. sapinea and A. ostoyae with respect to height. Taller trees showed longer necrosis length caused by D. sapinea while shorter trees were more affected by A. ostoyae. Moreover, maritime pine populations from areas with high summer temperatures and frequent droughts were less susceptible to D. sapinea but more susceptible to A. ostoyae. Finally, an association study using 4,227 genome-wide SNPs revealed several loci significantly associated to each trait (range of 3-26), including a possibly disease-induced translation initiation factor, eIF-5. This study provides important insights to develop genetic conservation and breeding strategies integrating species responses to biotic stressors.

genetics↗

Genomic landscape of the global oak phylogeny

O_LIThe tree of life is highly reticulate, with the history of population divergence buried amongst phylogenies deriving from introgression and lineage sorting. In this study, we test the hypothesis that there are regions of the oak (Quercus, Fagaceae) genome that are broadly informative about phylogeny and investigate global patterns of oak diversity.\nC_LIO_LIWe utilize fossil data and restriction-site associated DNA sequencing (RAD-seq) for 632 individuals representing ca. 250 oak species to infer a time-calibrated phylogeny of the worlds oaks. We use reversible-jump MCMC to reconstruct shifts in lineage diversification rates, accounting for among-clade sampling biases. We then map the > 20,000 RAD-seq loci back to a recently published oak genome and investigate genomic distribution of introgression and phylogenetic support across the phylogeny.\nC_LIO_LIOak lineages have diversified among geographic regions, followed by ecological divergence within regions, in the Americas and Eurasia. Roughly 60% of oak diversity traces back to four clades that experienced increases in net diversification due to climatic transitions or ecological opportunity.\nC_LIO_LIThe support we find for the phylogeny contrasts with high genomic heterogeneity in phylogenetic signal and introgression. Oaks are phylogenomic mosaics, and their diversity may in fact depend on the gene flow that shapes the oak genome.\nC_LI

evolutionary biology↗

Adaptive introgression as a driver of local adaptation to climate in European white oaks

Latitudinal and elevational gradients provide valuable experimental settings for studies of the potential impact of global warming on forest tree species. The availability of long-term phenological surveys in common garden experiments for traits associated with climate, such as bud flushing, for sessile oaks (Quercus petraea), provides an ideal opportunity to investigate this impact.\n\nWe sequenced 18 sessile oak populations, and used available sequencing data for three other closely related European white oak species (Q. pyrenaica, Q. pubescens, Q. robur), to explore the evolutionary processes responsible for shaping the genetic variation across latitudinal and elevational gradients in extant sessile oaks. We used phenotypic surveys in common garden experiments and climatic data for the population of origin, to perform genome-wide scans for population differentiation, genotype-environment (GEA) and genotype-phenotype associations (GPA).\n\nThe inferred historical relationships between Q. petraea populations suggest that interspecific gene flow occurred between Q. robur and Q. petraea populations from cooler or wetter areas. A genome-wide scan of differentiation between Q. petraea populations identified SNPs displaying strong interspecific relative divergence between these two species. These SNPs followed genetic clines along climatic or phenotypic gradients, providing further support for the likely contribution of introgression to the adaptive divergence of Q. petraea populations.\n\nOverall, the results of this study indicate that adaptive introgression of Q. robur alleles has occurred. We discuss the results of this study in the framework of the post-glacial colonization scenario, in which introgression and diversifying selection have been proposed as essential drivers of Q. petraea microevolution.

evolutionary biology↗

High-quality SNPs from genic regions highlight introgression patterns among European white oaks (Quercus petraea and Q. robur).

The Src homology-2 domain containing phosphatase SHP2 is a critical regulator of signal transduction, being implicated in cell growth and differentiation. Activating mutations cause developmental disorders and act as oncogenic drivers in hematologic cancers. SHP2 is activated by phosphopeptide binding to the N-SH2 domain, triggering the release of N-SH2 from the catalytic PTP domain. Based on early crystallographic data, it has been widely accepted that opening of the binding cleft of N-SH2 serves as the key "allosteric switch" driving SHP2 activation. To test the putative coupling between binding cleft opening and SHP2 activation as assumed by the "allosteric switch" model, we critically reviewed structural data of SHP2 and we used extensive molecular dynamics (MD) simulation and free energy calculations of isolated N-SH2 in solution, SHP2 in solution, and SHP2 in a crystal environment. Our results demonstrate that the binding cleft in N-SH2 is constitutively flexible and open in solution, and that a closed cleft found in certain structures is a consequence of crystal contacts. The degree of opening of the binding cleft has only a negligible effect on the free energy of SHP2 activation. Instead, SHP2 activation is greatly favored by the opening of the central {beta}- sheet of N-SH2. We conclude that opening of the N-SH2 binding cleft is not the key allosteric switch triggering SHP2 activation. Significance StatementSHP2 is a multi-domain protein, playing an important role in up-regulating cellular processes such as cell survival, proliferation, and programmed cell death. SHP2 mutations cause developmental disorders and were found in many cancer types, including neuroblastoma, breast cancer, and leukemia. In healthy cells, SHP2 mainly takes an autoinhibited, inactive form, and SHP2 is activated upon binding of phosphopeptides to the N-SH2 domain. For the past two decades, the widening of the binding cleft upon peptide binding has been considered as the key event driving SHP2 activation. Here, by analyzing crystallographic data and molecular simulations, we demonstrate that the binding cleft in N-SH2 is, instead, already open and accessible in solution, and its degree of opening does not influence SHP2 activation.

evolutionary biology↗

Secondary contacts between European white oaks reveal genes underlying reproductive isolation

AO_SCPLOWBSTRACTC_SCPLOWOaks are dominant forest tree species widely distributed across the Northern Hemisphere, where they constitute natural resources of economic, ecological, social and historical value. Hybridization and adaptive introgression have long been thought to be major drivers of their ecological success. Thus, the maintenance of species barriers remains a key question, given the extent of interspecific gene flow. In this study, we scanned the genomes of four European white oak species for reproductive barriers. We identified the ecological and phylogenic relationships of these species and inferred a long-term strict isolation followed by a recent and extensive postglacial contact. Then, we made use of the tremendous genetic variation among these species (31 million SNPs) to identify genomic regions for reproductive isolation. A literature-based functional annotation of the underlying genes highlighted important functions driving the reproductive isolation between these sister species. These functions were consistent with their ecological preferences and included tolerance to biotic and abiotic constraints. This study holds important implications for the renewal of European forests under global warming.

evolutionary biology↗