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Des Marais, D. L.

Publications and source records attributed to Des Marais, D. L..

13 recordsLinked to original sources

From tiny to massive: exploring genome evolution in the model 1 grass genus Brachypodium

Brachypodium is a powerful model system for investigating grass genome evolution, yet genomic resources remain concentrated in the three annual species, whereas perennial species are less sampled. Here, we present chromosome-level assemblies for two perennial species, Brachypodium mexicanum and B. arbuscula, which represent the earliest-diverging lineages of the genus and the earliest-diverging lineage of the core perennial clade, respectively. Synteny-based phylogenomics indicate that B. mexicanum is a meso-allotetraploid composed of two closely related but temporally distinct x=10 subgenomes, here designed as P and U, each carrying subgenome-specific chromosome rearrangements. We further show that the unusually large B. mexicanum genome, in contrast to the reduced genomes of most other Brachypodium species, is primarily due to transposable elements distributed across all chromosomal regions. By contrast, the diploid genome of the earliest-diverging core perennial, B. arbuscula, contains few transposable elements, whereas the most recent diverged diploid perennial B. sylvaticum shows evidence of a secondary TEs proliferation. Comparisons of lineage-specific and functionally enriched orthogroups among B. mexicanum, core perennial species and annual species suggest that ancestral hybridization between annual and perennial lineages may have contributed to the origin of allotetraploid B. mexicanum. These assemblies provide a framework for testing how polyploidy, descending dysploidy, transposable-element turnover, and life-history evolution jointly shaped genome architecture in Brachypodium.

evolutionary biology↗

Breeding of microbiomes conferring salt tolerance to plants

Microbiome breeding by host-mediated selection is a technique to artificially select for microbiomes conferring benefits to plants. Here, we describe leaf ionomics, microbial community composition, and network analyses of a microbiome-breeding experiment to generate microbiomes conferring salt tolerance to Brachypodium distachyon, a model for cereal crops. Plants receiving microbiomes selected to confer tolerance to either sodium- or aluminium-stress produced 69-198% higher total seed weight than plants receiving control microbiomes. Sodium-selected microbiomes reduced leaf-sodium concentration by 50%, whereas aluminium-selected microbiomes had no effect on leaf-tissue nutrient concentration, suggesting different mechanisms underlying microbiome-mediated salt tolerance. By testing these selected microbiomes in a cross-fostering experiment, we show that artificially-selected microbiomes attain (a) ecological robustness contributing to transplantability (inheritance) of microbiome-encoded effects between plants; and (b) network features identifying key bacteria promoting stress tolerance. Combined, these findings elucidate critical mechanisms underlying host-mediated selection as a tool to breed beneficial microbiomes in an agricultural context.

evolutionary biology↗

Plant nutritional and metabolic responses to drought and elevated CO2 revealed by machine learning-enabled non-targeted metabolomics

Projected atmospheric CO2 rise, coupled with intensification of drought in many regions, impacts the physiology of C3 plants beyond photosynthesis and carbon metabolism. The interaction between CO2 and drought affects the concentrations of many nutrients in crops, often resulting in excessive agrochemical use and less nutritious food production. To address these challenges, we investigated nutrient dynamics in Brachypodium distachyon, a model crop plant, under ambient and elevated CO2, factorially combined with well-watered or drought treatments. Integrative analyses of plant physiology, transcriptomics, and machine learning-enabled non-targeted metabolomics revealed that plant elemental composition and metabolomic responses to elevated CO2 strongly depend on water availability and differ between shoots and roots. Elevated CO2 and drought significantly impaired nitrogen status, with root nitrate uptake being more negatively affected than ammonium uptake. However, elevated CO2 increased iron partitioning in shoots under drought, potentially driven by enhanced carbon availability facilitating chelator synthesis for iron translocation. The high accumulation of sphingolipids in roots under combined stresses suggests a protective role against ionome imbalances. These findings highlight how climate stressors interact to shape plant nutrient dynamics, providing insights that can guide agricultural practices and breeding strategies to optimize nutrient management and foster sustainable agriculture under changing climate.

plant biology↗

Does domestication trade-off stress tolerance for leaf growth? A search for evidence across eight Pooideae grass species

Plant domestication is thought to create trade-offs between high yield and stress tolerance, raising concerns about yield stability in future climates. Previous studies have found limited direct evidence for such trade-offs, often focusing on weakened defenses associated with higher growth rates. However, trade-offs can also occur when traits (such as yield in agriculture) optimized for favorable conditions perform less efficiently in stressful conditions. Deciphering the mechanisms driving these trade-offs is crucial for maintaining yield in changing environments. We examine leaf growth, a key trait influencing carbon assimilation, in eight species of grasses. We use a machine learning pipeline to automatically extract cell dimensions and positions from leaf microscope images to study cell kinematics, finding that domesticated plants generally have longer leaves, larger division zones and higher cell production rates. We found no clear evidence of trade-off between domestication and drought response in final leaf length. However, a trade-off is observed in development as wild species exhibited a smaller decrease in elongation zone size under drought than their domesticated counterparts. These nuanced trade-offs associated with domestication highlight the importance of examining physiological traits and mechanisms in greater detail, possibly informing breeding strategies to enhance crop resilience in the face of climate change. HighlightThis study uses a high throughput pipeline to characterize leaf elongation responding to drought stress across eight species including barley, wheat, oat and wild relatives.

plant biology↗

Expression variability following gene duplication facilitates gene retention

Genome analyses reveal that gene duplication in eukaryotes is pervasive, providing a primary source for the emergence of new genes. However, the mechanisms dictating early duplicate retention and the emergence of functional biases--such as the enrichment of tandem duplicates in environmental responses--remain unclear. Here, to better understand the mechanisms and factors determining gene retention, we study a frequently overlooked molecular feature--expression variability--as measured by within-line expression variation, termed variability. We demonstrate that, on average, genes with duplicates exhibit higher expression variability than singletons. Furthermore, small-scale duplications (SSDs) and whole-genome duplications (WGDs) display contrasting functional outcomes and time-dependent profiles in expression variability. These findings suggest a potential overarching mechanism that facilitates gene expression divergence, functional gains of environmental responses, and duplicate retention following SSDs.

evolutionary biology↗

Genetic variation in phenology of wild Arabidopsis thaliana plants

Phenology and the timing of development are often under selection. However, the relative contributions of genotype, environment, and prior developmental transitions to variance in the phenology of wild plants is largely unknown. Individual components of phenology (e.g., germination) might be loosely related with the timing of maturation due to variation in prior developmental transitions. Given widespread evidence that genetic variation in life history is adaptive, we investigated to what degree experimentally measured genetic variation in Arabidopsis phenology predicts phenology of plants in the wild. As a proxy of phenology, we obtained collection dates from nature of 227 naturally inbred Arabidopsis thaliana accessions from across Eurasia. We compared this phenology in nature with experimental data on the descendant inbred lines that we synthesized from two new and 155 published controlled experiments. We tested whether the genetic variation in flowering and germination timing from experiments predicted the phenology of the same lines in nature. We found that genetic variation in phenology from controlled experiments significantly predicts day of collection from wild individuals, as a proxy for date of flowering, across Eurasia. However, local variation in collection dates within a region was not explained by genetic variance in phenology in experiments, suggesting high plasticity across small-scale environmental gradients or complex interactions between the timing of different developmental transitions. While experiments have shown phenology is under selection, understanding the subtle environmental and stochastic effects on phenology may help to clarify the heritability and evolution of phenological traits in nature.

evolutionary biology↗

Genetic diversity in gene regulatory interactions underlies the response to soil drying in the model grass Brachypodium distachyon

Gene expression is a quantitative trait under the control of genetic and environmental factors and their interaction, so-called GxE. Understanding the mechanisms driving GxE is fundamental for ensuring stable crop performance across environments and for predicting the response of natural populations to climate change. Gene expression is regulated through complex molecular networks, yet the interactions between genotype and environment on genome-wide regulatory networks are rarely considered. In this study, we model genome-scale gene expression variation between two natural accessions of the model grass Brachypodium distachyon and their response to soil drying. We identified genotypic, environmental, and GxE responses in physiological, metabolic, and gene expression traits. We then identified gene regulation conservation and variation among conditions and genotypes, simplified as co-expression clusters in each combination of genotype and environmental treatment. Putative gene regulatory interactions are inferred as network edges with a graphical modelling approach, resulting in hypotheses about gene-gene interactions specific to -- or with higher affinity in -- one genotype, one treatment, or in one genotype under treatment. We further find that some gene-gene interactions are conserved across conditions such that differential expression of one gene is apparently transmitted to a target gene. These variably detected edges cluster together in co-expression modules, suggestive of different constraints or selection strength acting on specific pathways. These variable features of gene regulatory networks may represent candidates modulate environmental response via genome editing, and suggest possible targets of evolutionary change in gene regulatory networks associated with phenotypic plasticity.

plant biology↗

Dissecting genetic correlation through recombinantperturbations: the role of developmental bias

Genetic correlation represents an important class of evolutionary constraint, which is itself evolvable. Empirical studies have found mixed results on whether genetic correlations change rapidly or slowly. This uncertainty challenges our ability to predict the outcome of selection. Despite the tremendous diversity and complexity of life forms, there are certain forms of life that are never observed. This might be because of developmental biases that restrict how organisms can evolve, or because they have low fitness in any environment yet available on Earth. Given that both developmental bias and selection can generate similar phenotypes, it is difficult to distinguish between the two causes of evolutionary stasis among related taxa. For example, remarkably invariant traits are observed spanning million years, such as wing shape in Drosophila wherein qualitative differences are rare within genera. Here, we ask whether the absence of certain combinations of traits, as indicated by genetic correlation, reflects developmental bias. However, much confusion and controversy remain over definitions of developmental bias, and probing it is challenging. We thus present a novel approach aiming to dissect genetic correlations and estimate the relative contribution of developmental bias in maintaining genetic correlations. We do so by leveraging a common but under-utilized type of data: genetic crosses. Through empirical analyses, we find that our approach can distinguish whether genetically correlated traits are developmentally constrained to covary. We also find that our developmental bias metric is an indicator of genetic correlation stability across conditions. Our framework presents a feasible way to dissect the mechanisms underlying genetic correlation and pleiotropy.

evolutionary biology↗

Genomics highlight an underestimation of the urban heat island effect on red oak phenology

The phenological timing of leaf-out in temperate forests is a critical transition point each year, altering the global climate system via changes to carbon and hydrologic cycles and land-surface albedo. In turn, climate is impacting phenology by advancing leaf-out an average of 2.8 +/-0.35 days per decade as the planet warms. Thus, understanding the relationship between warming and leaf-out is critical for understanding future global change. Rural-to-urban gradients in temperature, which result in clines over which urban areas are up to 4{degrees}C warmer than their surrounding countryside (dubbed the urban heat island - UHI - effect), may be used as a space-for-time substitution in studies of response to climate change. However, studies have recently highlighted that using the UHI effect over space rather than measurements at the same site through time results in consistently weaker relationships between temperature and leaf-out date in spring (i.e., urban-to-rural gradients underpredict the impact of warming on leaf-out). While such studies suggest many potential environmental explanations, the effect of genetic diversity is often neglected. While sensitive to environmental warming, leaf-out phenology is also highly heritable. Given that rural areas are largely natural sites, they likely have higher intraspecific genetic diversity than urban sites, where plants are selected by land managers for a narrow set of resilience traits. Here we measured the environment, genomic background, and phenological timing of northern red oak (Q. rubra) over several years between an urban and rural site to demonstrate how genetic background explains why the UHI effect leads to an underprediction of plant response to warming. Using a space-for-time substitution, we found that the date of leaf-out at our sites is predicted to advance approximately 20 days over the next 80 years. However, if we further account for the genomic background at the two sites, leaf-out, phenology is predicted to advance 22 days; a 10% difference between the two models. We demonstrate that this stronger relationship is because urban trees are largely a monoculture and, moreover, are most closely related to individuals at the rural site that leaf out latest. We highlight the critical need to consider genetic background, particularly in studies examining highly heritable traits, because both environment and genetics are changing across rural-to-urban gradients.

plant biology↗

Patterns of gene co-expression under water-deficit treatments and pan-genome occupancy in Brachypodium distachyon.

Natural populations are characterized by abundant genetic diversity driven by a range of different types of mutation. The tractability of sequencing complete genomes has allowed new insights into the variable composition of genomes, summarized as a species pan-genome. These analyses demonstrate that many genes are absent from the first reference genomes, whose analysis dominated the initial years of the genomic era. Our field now turns towards understanding the functional consequence of these highly variable genomes. Here, we analyzed weighted gene co-expression networks from leaf transcriptome data for drought response in the purple false brome Brachypodium distachyon and the differential expression of genes putatively involved in adaptation to this stressor. We specifically asked whether genes with variable "occupancy" in the pan-genome - genes which are either present in all studied genotypes or missing in some genotypes - show different distributions among co-expression modules. Co-expression analysis united genes expressed in drought-stressed plants into nine modules covering 72 hub genes (87 hub isoforms), and genes expressed under controlled water conditions into 13 modules, covering 190 hub genes (251 hub isoforms). We find that low occupancy pan-genes are under-represented among several modules, while other modules are over-enriched for low-occupancy pan-genes. We also provide new insight into the regulation of drought response in B. distachyon, specifically identifying one module with an apparent role in primary metabolism that is strongly responsive to drought. Our work shows the power of integrating pan-genomic analysis with transcriptomic data using factorial experiments to understand the functional genomics of environmental response.

plant biology↗

Tracking the Ancestry of Known and 'Ghost' Homeologous Subgenomes in Model Grass Brachypodium Polyploids

Unraveling the evolution of plant polyploids is a challenge when their diploid progenitor species are extinct or unknown or when their progenitor genome sequences are unavailable. The subgenome identification methods cannot adequately retrieve the homeologous genomes that are present in the allopolyploids if they do not take into account the potential existence of unknown progenitors. We addressed this challenge in the widely distributed dysploid grass genus Brachypodium, which is a model genus for temperate cereals and biofuel grasses. We used a transcriptome-based phylogeny and newly designed subgenome detection algorithms coupled with a comparative chromosome barcoding analysis. Our phylogenomic subgenome detection pipeline was validated in Triticum allopolyploids, which have known progenitor genomes, and was used to infer the identities of three extant and four ghost subgenomes in six Brachypodium polyploids (B. mexicanum, B. boissieri, B. retusum, B. phoenicoides, B. rupestre and B. hybridum), of which five contain undescribed homeologous subgenomes. The existence of the seven Brachypodium progenitor genomes in the polyploids was confirmed by their karyotypic barcode profiles. Our results demonstrate that our subgenome detection method is able to uncover the ancestral genomic components of both allo- and autopolyploids.

plant biology↗

Trait plasticity and covariance along a continuous soil moisture gradient

Water availability is perhaps the greatest environmental determinant of plant yield and fitness. However, our understanding of plant-water relations is limited because it is primarily informed by experiments considering soil moisture variability at two discrete levels - wet and dry - rather than as a continuously varying environmental gradient. Here we used experimental and statistical methods based on function-valued traits to explore responses to a continuous soil moisture gradient in physiological and morphological traits in two species and five genotypes each of the model grass Brachypodium. We find that most traits exhibit non-linear responses to soil moisture variability. We also observe differences in the shape of these non-linear responses between traits, species, and genotypes. Emergent phenomena arise from this variation including changes in trait correlations and evolutionary constraints as a function of soil moisture. These results point to the importance of considering non-linearity in plant-water relations to understand plastic and evolutionary responses to changing climates.

plant biology↗

Topological features of gene regulatory networks predict patterns of natural diversity in environmental response

Molecular interactions affect the evolution of complex traits. For instance, adaptation may be constrained by pleiotropic or epistatic effects, both of which will be reflected in the structure of molecular interaction networks. To date, empirical studies investigating the role of molecular interactions in phenotypic evolution have been idiosyncratic, offering no clear patterns. Here, we investigated the network topology of genes putatively involved in local adaptation to two abiotic stressors--drought and cold--in Arabidopsis thaliana. Our findings suggest that the gene-interaction topologies for both cold and drought stress response are non-random, with genes that show genetic variation in drought response (GxE) being significantly more peripheral and cold response genes being significantly more central than genes not involved in either response. We suggest that the observed topologies reflect different constraints on the genetic pathways involved in the assayed phenotypes. The approach presented here may inform predictive models linking genetic variation in molecular signaling networks with phenotypic variation, specifically traits involved in environmental response.\n\nSignificance StatementOur study focuses on genes whose transcriptional activity exhibits genetic variation in response to the environment, or \"GxE.\" GxE is a widely observed phenomenon of critical importance to understanding the genotype-to-phenotype map, the evolution of natural populations, medical genetics, population response to climate change, and agricultural improvement. We investigated expression GxE in plant responses to two abiotic cues: cold and drought. We found that genes showing genetically variable response to cold stress are centrally located in regulatory networks whereas genes showing genetically variable response to drought stress are peripherally located in regulatory networks. This result suggests that selection is presented with vastly different mutational landscapes for shaping evolutionary or breeding response to these two important climatic factors

evolutionary biology↗