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Groen, S. C.

Publications and source records attributed to Groen, S. C..

16 recordsLinked to original sources

Co-transcriptomic network analysis of host-parasite interactions reveals genes underpinning parasite fitness

Interactions between parasites and their host organisms generate continuous variation in infection outcomes. Although dual transcriptome studies have demonstrated extensive molecular dialogues between interacting species, it is still unclear how natural variation in host and parasite gene regulatory networks and coordination between them contribute to diverse disease phenotypes. Here, we re-contextualized co-transcriptomes from recombinant inbred lines of the plant-parasitic root-knot nematode Meloidogyne hapla infecting Medicago truncatula host plants with relative measures of infection intensity as a proxy for parasite load. We used infection intensity to estimate interaction gradients on gene expression by calculating its covariance with transcript levels. Quantitative analyses of interaction gradients for host and parasite transcriptomes identified major differences in development-related transcriptional programs along the infection continuum. In addition, integrated network analyses connected host cell wall remodeling with parasite protein production and secretion. Silencing of candidate root-knot nematode genes reduced host galling and parasite reproductive fitness, providing experimental support for our network-derived predictions. Together, our findings present an integrated systems genetics framework connecting naturally occurring genetic variation to quantitative disease phenotypes.

systems biology↗

Epistasis between Na+/K+-ATPase Substitutions May Influence Salinity Tolerance in Steinernema Entomopathogenic Nematodes

Soil salinity varies widely across geographies both due to natural factors and human activities, including agriculture, road salt application, sea level rise, and desertification. Increases in soil salinity may affect organisms widely and particularly impact soil foodwebs. As parasites, entomopathogenic nematodes (EPNs) occupy crucial links in soil foodwebs and are important for agriculture as biological control agents of insect pests. Previous research found that the EPN Steinernema carpocapsae may exhibit higher salt tolerance than several of its congeners. We recently identified that S. carpocapsae uniquely evolved two amino acid substitutions in the first extracellular loop of the sodium pump (Na{square}/K{square}-ATPase). Here, we tested if these substitutions explain S. carpocapsaes reported lower sensitivity to salt. Our results confirm that S. carpocapsae exhibits higher salt tolerance and show it can more effectively locate and infect insect hosts than its congeners S. feltiae and S. hermaphroditum in highly saline environments. We then retraced the evolution of the two amino acid substitutions in S. carpocapsae by introducing them alone and in combination in Caenorhabditis elegans using CRISPR genome engineering. We found that C. elegans mutants with single substitutions showed improved salt tolerance. However, this improvement disappeared in the double mutant, whose sodium pump mimicked that of S. carpocapsae. This pattern of negative epistasis between the amino acid substitutions suggests they are not responsible for variation in salt tolerance between Steinernema species. Sodium pump evolution in S. carpocapsae might instead be driven by encounters with cardiac glycosides, which are released into soil by several clades of plants including milkweeds, sequestered by some of this EPNs herbivorous insect hosts, and known to target the first extracellular loop of the sodium pump. Our findings provide valuable insights into EPN adaptation to changes in environmental sodium levels and may have implications for their use in biological control.

ecology↗

Cardenolides May Affect Herbivory on Milkweeds (Asclepias spp.) by the Root-Knot Nematode Meloidogyne incognita

Root-knot nematodes (RKNs) of the genus Meloidogyne are important pests in agriculture. RKNs are generalist herbivores with a wide host range including crop and wild plants. The latter are an important source of defensive metabolites that may be helpful for RKN management. Milkweeds (Asclepias spp.) produce toxic cardenolides that protect them from herbivory. However, it is unclear if cardenolides may defend milkweeds against RKNs. Here, we tested this directly through herbivory assays with the RKN M. incognita on milkweed species that produce negligible and high levels of cardenolides, A. tuberosa and A. curassavica, respectively. We found that M. incognita induces fewer galls on A. curassavica than A. tuberosa and fails to reproduce after reaching maturity on the former but not the latter species. This suggests that the predominantly polar cardenolides in A. curassavica may engender long-term reproductive toxicity. Further toxicity assays with the polar cardenolide ouabain showed that cardenolides can also have more immediate toxic effects on M. incognita at higher concentrations. Ouabain caused a coiled, paralytic phenotype in juvenile RKNs, a sign of neurotoxicity, leading to lethality in a subset of RKNs. Some nematodes recovered upon ouabain removal, confirming that neurotoxic cardenolides have a nematostatic effect that results in death when exposure persists. Taken together, our results provide further evidence that cardenolides may function as anti-herbivore defenses against RKNs. The dead end host plant A. curassaviva appears to possess useful properties that may be leveraged for control of RKNs in agriculture.

plant biology↗

A Genetically Based Latitudinal Gradient in Aggressiveness of Root-Knot Nematode Populations on Tomato with the Mi-1 Resistance Gene

Tomato is a food crop of global importance, with a large proportion of processing tomatoes produced in California. One of the main problems plaguing tomato production is infection by populations of root-knot nematodes (RKNs; Meloidogyne spp.) that can evade or suppress ( break) resistance mediated by the Mi-1 gene, which has been introgressed into most processing tomato cultivars. In this study, we evaluate fourteen Meloidogyne spp. populations collected from fields across the state of California that can complete their life cycle on Mi-1 tomato cultivars. One of these populations was identified as M. javanica and the others as M. incognita. All RKN populations developed and reproduced on Mi-1 tomato cultivar Celebrity. Although we did not observe differences in gall index among populations when studied together in greenhouse conditions, significant quantitative variation in reproduction factor values was apparent among them. Several pathogens and parasites display geographical gradients in aggressiveness and we identified a negative correlation between populations latitudes-of-origin and reproduction factors. This suggests that populations of these thermophilic RKN species from lower latitudes tended to have evolved higher levels of aggressiveness on Mi-1 tomato, which may be linked to warmer temperatures throughout the year. Finally, populations with relatively low reproduction factor values still showed significant differences in the phenotypes of the galls they induced. Our results showed that Meloidogyne populations evolved genetic variation in aggressiveness along a latitudinal gradient in Californian processing tomato agroecosystems, which may have implications for managing these important crop pests.

evolutionary biology↗

Environment-dependent selection impacts heritable developmental stability and trait canalization in rice

Canalization, or the maintenance of trait values regardless of environmental or genetic variability, is fundamentally important for maintaining developmental stability. While this concept was described decades ago, we still know relatively little about how canalization is influenced by environmental stress, how it is shaped by natural selection, and the genetic underpinnings of canalization. In this study, we examined natural selection on microenvironmental canalization in rice (Oryza sativa) in wet and dry field conditions. We measured developmental stability in genetically identical replicates obtained from geographically widespread Indica and Japonica rice accessions, providing precise estimates of canalization in thousands of plants. We found that drought stress decreased canalization, showing that stress can increase instability. We also found evidence that canalization can evolve, given that canalization of several traits was heritable and under selection. We further uncovered specific genes underlying canalization, with genetic mapping and functional genetic experiments showing that the bZIP transcription factor-encoding gene OsTGA5/rTGA2.3, which is part of a module that balances stress response and plant growth, regulates canalization of several traits in an environment-dependent manner. At a genome-wide scale, canalization was associated with lower gene expression stochasticity at an earlier life stage, indicating that expression variation can reduce canalization and increase instability. Trait canalization was also positively correlated to temperature at accessions source environments, suggesting that selection on canalization can vary among environments. Overall, our study provides novel insights into the molecular genetic basis of environmental differences in developmental stability and how it might be shaped by selection. SignificanceMechanisms stabilizing organismal development in response to genetic mutations or environmental stressors (canalization) have been reported for numerous animals and plants, but their underlying genetic basis and whether they may be shaped by selection remain unclear. Here, we report patterns of drought-induced trait decanalization in populations of rice (Oryza sativa) grown in field environments. We determined that trait canalization is heritable and can evolve separately from trait means. We identified the gene OsTGA5, part of a regulatory module shaping trade-offs between growth and stress responses, as impacting trait canalization. Plants with less noisy gene expression and evolving in warmer environments display greater developmental stability, contributing to the notion that canalization in rice may be adaptive.

evolutionary biology↗

Alternative Splicing in TRPA1 Drives Sensory Adaptation to Electrophiles in Drosophilids

Behaviors are among the first traits to evolve as animals enter new niches, but their molecular bases are poorly understood. To address this gap, we used the mustard-feeding drosophilid fly Scaptomyza flava, which feeds on toxic Brassicales plants like wasabi that produce noxious, electrophilic isothiocyanates (ITCs or mustard oils). We found that S. flava exhibits dramatically reduced behavioral sensitivity to allyl isothiocyanate (AITC) compared to its microbe-feeding relatives Scaptomyza pallida and Drosophila melanogaster. We hypothesized that molecular evolution of the "wasabi receptor" TRPA1, known to detect ITCs in flies, could explain this loss of aversion. Our experiments revealed three interconnected evolutionary genetic changes consistent with this hypothesis. First, TRPA1 was expressed in labellar tissues of S. flava at the lowest levels among the three species, at a nearly four-fold lower level than in D. melanogaster. Second, S. flava expressed a higher proportion of TRPA1 splice variants previously reported to be less sensitive to chemical stimulus. Third, we identified amino acid substitutions in S. flava that could influence the structure of intracellular domains of TRPA1. To test the functional salience of these mechanisms in vitro and in vivo, we validated TRPA1 splicing isoforms using Xenopus oocyte electrophysiology and the GAL4/UAS system in D. melanogaster. Single TRPA1 isoform electrophysiology in vitro revealed evolution of the channel in the S. flava lineage towards reduced electrophile sensitivity. Ectopic expression of S. flava TRPA1 in D. melanogaster also consistently conferred weaker AITC sensitivity in vivo than expression of its orthologues, although this did not fully recapitulate differences in wild-type phenotypes between species, suggesting other molecular mechanisms were involved. To address this, we explored the consequences of isoform co-expression using oocyte electrophysiology. We found that enrichment of electrophile-insensitive TRPA1 splicing isoforms as observed in the salient S. flava sensory organs additively reduced cellular responses to AITC, which could further contribute to reduced electrophile aversion. Our findings illuminate how expression differences, protein structural changes, and especially alternative splicing, together can drive sensory evolution as animals behaviorally adapt to toxic new niches.

evolutionary biology↗

Amino Acid Substitutions in the Na+/K+-ATPase May Contribute to Salinity Tolerance in Insects

O_LIEnvironmental salinity levels vary naturally across terrestrial ecosystems but can be heightened locally by coastal proximity and desertification as well as human activities such as road salt application and agriculture. Since salt is essential for many physiological processes in insects, rising environmental sodium concentrations may drive behavioral changes, where insects select environments and food sources with suitable sodium levels, or evolutionary changes in constitutive or plastic physiological mechanisms to process salt, potentially altering ecological dynamics and species interactions. C_LIO_LINumerous hematophagous (blood feeding) insects such as the yellow-fever mosquito Aedes aeqypti are known to be able to breed in relatively saline environments. Among phytophagous (plant feeding) insects, grasshoppers can be important herbivores in arid and coastal salt-affected regions, whereas the monarch butterfly (Danaus plexippus) appears to perform relatively well on milkweed host plants growing in roadsides influenced by salt runoff. Several of these insects share a common trait: amino acid substitutions in the first extracellular loop of the Na+/K+-ATPase (NKA), a sodium pump crucial for maintaining ion balance. For the monarch these substitutions confer resistance to toxic cardenolides from milkweeds, but it is unclear whether NKA substitutions may influence salt tolerance. C_LIO_LIHere, we investigate whether the NKA substitutions found in these insects may contribute to salt tolerance using gene-edited Drosophila melanogaster mutant strains as models. We show that flies with substitution Q111L (found in Aedes mosquitoes) or a combination of Q111L and A119S (found in grasshoppers) exhibited greater salt tolerance, whereas flies carrying the combination of substitutions found in the monarch (Q111V, A119S, and N122H) did not. C_LIO_LIOur results suggest that the monarch may rely on alternate mechanisms for salt tolerance and that its NKA substitutions are important primarily for cardenolide resistance. However, substitution Q111L and the combination of Q111L and A119S may be relevant for salt tolerance in a variety of insects. Uncovering mechanisms of salt tolerance enhances our understanding of species distributions, ecological interactions, and evolutionary physiology in response to changing environmental salinity levels. C_LI

genetics↗

Network properties constrain natural selection on gene expression in Caenorhabditis elegans

Gene regulatory networks (GRNs) integrate genetic and environmental signals to coordinate complex phenotypes and evolve through a balance of selection and drift. Using publicly available datasets from Caenorhabditis elegans, we investigated the extent of natural selection on transcript abundance by linking population-scale variation in gene expression to fecundity, a key fitness component. While the expression of most genes covaried only weakly with fitness, which is typical for polygenic traits, we identified seven transcripts under significant directional selection. These included nhr-114 and feh-1, implicating variation in nutrient-sensing and metabolic pathways as impacting fitness. Stronger directional selection on tissue-specific and older genes highlighted the germline and nervous system as focal points of adaptive change. Network position further constrained selection on gene expression; high-connectivity genes faced stronger stabilizing and directional selection, highlighting GRN architecture as a key factor in microevolutionary dynamics. The activity of transcription factors such as zip-3, which regulates mitochondrial stress responses, emerged as targets of selection, revealing potential links between energy homeostasis and fitness. Our findings demonstrate how GRNs mediate the interplay between selection and drift, shaping microevolutionary trajectories of gene expression and phenotypic diversity.

systems biology↗

Evolutionary Systems Biology Identifies Genetic Trade-offs In Rice Defense Against Above- and Belowground Attackers

Like other plants, wild and domesticated rice species (Oryza nivara, O. rufipogon, and O. sativa) evolve in environments with various biotic and abiotic stresses that fluctuate in intensity through space and time. Microbial pathogens and invertebrate herbivores such as plant-parasitic nematodes and caterpillars show geographical and temporal variation in activity patterns and may respond differently to certain plant defensive mechanisms. As such, plant interactions with multiple community members may result in conflicting selection pressures on genetic polymorphisms. Here, through assays with different above- and belowground herbivores, the fall armyworm (Spodoptera frugiperda) and the southern root-knot nematode (Meloidogyne incognita), respectively, and comparison with rice responses to microbial pathogens, we identify potential genetic trade-offs at the KSL8 and MG1 loci on chromosome 11. KSL8 encodes the first committed step towards biosynthesis of either stemarane- or stemodane-type diterpenoids through the japonica (KSL8-jap) or indica (KSL8-ind) allele. Knocking out KSL8-jap and CPS4, encoding an enzyme that acts upstream in diterpenoid synthesis, in japonica rice cultivars increased resistance to S. frugiperda and decreased resistance to M. incognita. Furthermore, MG1 resides in a haplotype that provided resistance to M. incognita, while alternative haplotypes are involved in mediating resistance to the rice blast fungus Magnaporthe oryzae and other pests and pathogens. Finally, KSL8 and MG1 alleles are located within trans-species haplotypes and may be evolving under long-term balancing selection. Our data are consistent with a hypothesis that polymorphisms at KSL8 and MG1 may be maintained through complex and diffuse community interactions.

systems biology↗

Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genetic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families - genes directly mediating interactions with plant chemical defenses - underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many lineages are ancient (>150 million years ago [mya]), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several non-herbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza have among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on plants (bitter or electrophilic phytotoxins) or their ancestral diet (yeast and fruit volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight strong gene candidates that have also been linked to other dietary transitions in Drosophila.

evolutionary biology↗

Evolutionary systems biology reveals patterns of rice adaptation to drought-prone agro-ecosystems

Rice was domesticated around 10,000 years ago and has developed into a staple for half of humanity. The crop evolved and is currently grown in stably wet and intermittently dry agro-ecosystems, but patterns of adaptation to differences in water availability remain poorly understood. While previous field studies have evaluated plant developmental adaptations to water deficit, adaptive variation in functional and hydraulic components, particularly in relation to gene expression, has received less attention. Here, we take an evolutionary systems biology approach to characterize adaptive drought resistance traits across roots and shoots. We find that rice harbors heritable variation in molecular, physiological, and morphological traits that is linked to higher fitness under drought. We identify modules of co-expressed genes that are associated with adaptive drought avoidance and tolerance mechanisms. These expression modules showed evidence of polygenic adaptation in rice subgroups harboring accessions that evolved in drought-prone agro-ecosystems. Fitness-linked expression patterns had predictive value and allowed us to identify the drought-adaptive nature of optimizing photosynthesis and interactions with arbuscular mycorrhizal fungi. Taken together, our study provides an unprecedented, integrative view of rice adaptation to water-limited field conditions.

plant biology↗

Fitness costs and benefits of gene expression plasticity in rice under drought

Genome-wide gene expression changes in response to environmental variability have been widely documented, but we lack detailed and comprehensive understanding of the interplay between this form of phenotypic plasticity and natural selection. Selection on expression plasticity may be limited by environment-specific costs, and plasticity may in turn affect selection on baseline expression levels. Here, we address this fundamental issue by measuring selection on drought-induced plasticity of leaf transcripts in field-grown rice populations. Selection disfavored switching off housekeeping genes under drought. This stress-induced dysregulation did not constrain selection on baseline transcript levels, suggesting compensatory evolution may be possible. Selection rarely acted strongly on individual transcripts but worked polygenically on gradual (continuous) plasticity of co-expressed gene modules regulating photosynthesis via known drought-responsive transcription factors. Finally, selection was tied to inefficient gene architectural features and metabolic costs of expression. Our study provides a genome-wide view of costs and benefits of gene expression plasticity.

evolutionary biology↗

Evolution of herbivory remodels a Drosophila genome

One-quarter of extant Eukaryotic species are herbivorous insects, yet the genomic basis of this extraordinary adaptive radiation is unclear. Recently-derived herbivorous species hold promise for understanding how colonization of living plant tissues shaped the evolution of herbivore genomes. Here, we characterized exceptional patterns of evolution coupled with a recent (<15 mya) transition to herbivory of mustard plants (Brassicaceae, including Arabidopsis thaliana) in the fly genus Scaptomyza, nested within the paraphyletic genus Drosophila. We discovered a radiation of mustard-specialized Scaptomyza species, comparable in diversity to the Drosophila melanogaster species subgroup. Stable isotope, behavioral, and viability assays revealed these flies are obligate herbivores. Genome sequencing of one species, S. flava, revealed that the evolution of herbivory drove a contraction in gene families involved in chemosensation and xenobiotic metabolism. Against this backdrop of losses, highly targeted gains (\"blooms\") were found in Phase I and Phase II detoxification gene sub-families, including glutathione S-transferase (Gst) and cytochrome P450 (Cyp450) genes. S. flava has more validated paralogs of a single Cyp450 (N=6 for Cyp6g1) and Gst (N=5 for GstE5-8) than any other drosophilid. Functional studies of the Gst repertoire in S. flava showed that transcription of S. flava GstE5-8 paralogs was differentially regulated by dietary mustard oils, and of 22 heterologously expressed cytosolic S. flava GST enzymes, GSTE5-8 enzymes were exceptionally well-adapted to mustard oil detoxification in vitro. One, GSTE5-8a, was an order of magnitude more efficient at metabolizing mustard oils than GSTs from any other metazoan. The serendipitous intersection of two genetic model organisms, Drosophila and Arabidopsis, helped illuminate how an insect genome was remodeled during the evolutionary transformation to herbivory, identifying mechanisms that facilitated the evolution of the most diverse guild of animal life.\n\nSIGNIFICANCE STATEMENTThe origin of land plants >400 million years ago (mya) spurred the diversification of plant-feeding (herbivorous) insects and triggered an ongoing chemical co-evolutionary arms race. Because ancestors of most herbivorous insects first colonized plants >200 mya, the sands of time have buried evidence of how their genomes changed with their diet. We leveraged the serendipitous intersection of two genetic model systems: a close relative of yeast-feeding fruit fly (Drosophila melanogaster), the \"wasabi fly\" (Scaptomyza flava), that evolved to consume mustard plants including Arabidopsis thaliana. The yeast-to-mustard dietary transition remodeled the flys gene repertoire for sensing and detoxifying chemicals. Although many genes were lost, some underwent duplications that encode the most efficient detoxifying enzymes against mustard oils known from animals.

evolutionary biology↗

Genomic history and ecology of the geographic spread of rice

Rice (Oryza sativa) is one of the worlds most important food crops. We reconstruct the history of rice dispersal in Asia using whole-genome sequences of >1,400 landraces, coupled with geographic, environmental, archaeobotanical and paleoclimate data. We also identify extrinsic factors that impact genome diversity, with temperature a leading abiotic factor. Originating [~]9,000 years ago in the Yangtze Valley, rice diversified into temperate and tropical japonica during a global cooling event [~]4,200 years ago. Soon after, tropical rice reached Southeast Asia, where it rapidly diversified starting [~]2,500 yBP. The history of indica rice dispersal appears more complicated, moving into China [~]2,000 yBP. Reconstructing the dispersal history of rice and its climatic correlates may help identify genetic adaptation associated with the spread of a key domesticated species.\n\nOne sentence summaryWe reconstructed the ancient dispersal of rice in Asia and identified extrinsic factors that impact its genomic diversity.

evolutionary biology↗

The rice leaf microbiome has a conserved community structure controlled by complex host-microbe interactions

Understanding the factors that influence the outcome of crop interactions with microbes is key to managing crop diseases and improving yield. While the composition, structure and functional profile of crop microbial communities are shaped by complex interactions between the host, microbes and the environment, the relative contribution of each of these factors is mostly unknown. Here, we profiled the community composition of bacteria across leaves of 3,024 rice (Oryza sativa) accessions from field trials in China and the Philippines using metagenomics. Despite significant differences in diversity between environments, the structure and metabolic profiles of the microbiome appear to be conserved, suggesting that microbiomes converge onto core functions. Furthermore, co-occurrence analysis identified microbial hubs that regulate the network structure of the microbiome. We identified rice genomic regions controlling the abundance of these hubs, enriched for processes involved in stress responses and carbohydrate metabolism. We functionally validated the importance of these processes, finding that abundance of hub taxa was different in rice mutants with altered cellulose and salicylate accumulation, two major metabolites at the host-microbe interactions interface. By identifying key host genomic regions, host traits and hub microbes that govern microbiome composition, our study opens the door to designing future cropping systems.

microbiology↗

Genetic variants affecting plant size and chemical defenses jointly shape herbivory in Arabidopsis

Herbivorous insects exhibit strong feeding preferences when choosing among plant genotypes, yet experiments to map loci mediating plant susceptibility to herbivory rarely incorporate host choice. To address this gap, we applied genome-wide association (GWA) mapping to uncover genetic polymorphisms mediating damage from foraging insects (two populations of Scaptomyza flava) across a mixture of Arabidopsis thaliana genotypes in experimental enclosures. The effect of chemical defenses (glucosinolates) on herbivory depended on herbivore genotype. Unlike many studies that minimize the effects of host choice behavior, we also found a large effect of plant size on herbivory--likely through its effect on plant apparency--that was independent of herbivore genotype. These herbivory-associated loci are polymorphic at fine spatial scales, and thus have potential to shape variation in herbivory within natural populations. We also show that the polymorphism with the largest effect on herbivory underlies adaptive latitudinal variation in Arabidopsis plant size across Europe. Overall, our results provide genetic support for ecological observations that variation in both chemical defenses and non-canonical defense traits (e.g., plant size and phenology) jointly shapes plant-herbivore interactions.

plant biology↗