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Juenger, T. E.

Publications and source records attributed to Juenger, T. E..

15 recordsLinked to original sources

Rapid adaptation and extinction across climates in synchronized outdoor evolution experiments of Arabidopsis thaliana

Climate change is threatening species with extinction, and rapid evolutionary adaptation may be their only option for population rescue over short ecological timescales. However, direct observations of rapid genetic adaptation and population dynamics across climates are rare across species. To fill this gap, we conducted a replicated, globally synchronized evolution experiment with the plant Arabidopsis thaliana for 5 years in over 30 outdoor experimental gardens with distinct climates across Europe, the Levant, and North America. We performed whole-genome sequencing on [~]70,000 surviving reproductive individuals and directly observed rapid and repeatable adaptation across climates. Allele frequency changes over time were parallel in experimental evolution replicates within the same climates, while they diverged across contrasting climates--with some allele frequency shifts best explained by strong selection between -46% to +60%. Screening the genome for signals of rapid climate adaptation identified a polygenic architecture with both known and novel adaptive genetic variants connected to important ecological phenotypes including environmental stress responses, CAM5 and HEAT SHOCK FACTORs, and germination and spring flowering timing, CYTOCHROME P450s and TSF. We found evolutionary adaptation trends were often predictable, but variable across environments. In warm climates, high evolutionary predictability was associated with population survival up to 5 years, while erratic trends were an early warning for population extinction. Together, these results show rapid climate adaptation may be possible, but understanding its limits across species will be key for biodiversity forecasting.

evolutionary biology↗

Measuring the Strength of Spatial Sorting

Empirical work suggests that spatial sorting--a mechanism of evolutionary change fueled by spatial assortment of phenotypes--may lead to phenotypic shifts on ecological timescales. However, we currently lack theoretical tools to measure the strength of spatial sorting, as we do to measure the strength of natural selection. To address this gap, we present a quantitative genetics model and identify an evolutionary parameter in the model to measure the strength of spatial sorting. This parameter, the standardized sorting gradient, is structurally akin to the standardized selection gradient, commonly used to measure the strength of natural selection. To show the utility of our approach, we analyzed wing-morphology data of soapberry bugs (Jadera haematoloma) recolonizing flooded habitats extirpated by a hurricane. We found that the estimated strength of spatial sorting ranked in the top ten percentile of standardized selection gradients documented in the scientific literature. Our results underscore that, like natural selection, spatial sorting, too, can yield rapid evolution after extreme events.

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↗

The shared genetic basis of leaf morphology and tensile resistance underlies the effect of growing season length in a widespread perennial grass

PremiseLeaf tensile resistance, a leafs ability to withstand pulling forces, is an important determinant of plant ecological strategies. One potential driver of leaf tensile resistance is growing season length. When growing seasons are long, strong leaves--which often require more time and resources to construct than weak leaves--may be more advantageous than when growing seasons are short. Growing season length and other ecological conditions may also impact the morphological traits that underlie leaf tensile resistance. MethodsTo understand variation in leaf tensile resistance, we measured size-dependent leaf strength and size-independent leaf toughness in diverse genotypes of the widespread perennial grass Panicum virgatum (switchgrass) in a common garden. We then used quantitative genetic approaches to estimate the heritability of leaf tensile resistance and whether there were genetic correlations between leaf tensile resistance and other morphological traits. Key ResultsLeaf tensile resistance was positively associated with aboveground biomass (a proxy for fitness). Moreover, both measures of leaf tensile resistance exhibited high heritability and were positively genetically correlated with leaf lamina thickness and leaf mass per area (LMA). Leaf tensile resistance also increased with habitat-of-origin growing season length and this effect was mediated by both LMA and leaf thickness. ConclusionsDifferences in growing season length may promote selection for different leaf lifespans and may explain existing variation in leaf tensile resistance in P. virgatum. In addition, the high heritability of leaf tensile resistance suggests that P. virgatum will be able to respond to climate change as growing seasons lengthen.

plant biology↗

Heritability and host genomic determinants of switchgrass root-associated microbiota in field sites spanning its natural range.

A fundamental goal in plant microbiome research is to determine the relative impacts of host and environmental effects on root microbiota composition, particularly how host genotype impacts bacterial community composition. Most studies characterizing the effect of plant genotype on root microbiota undersample host genetic diversity and grow plants outside of their native ranges, making the associations between host and microbes difficult to interpret. Here we characterized the root microbiota of a large population of switchgrass, a North American native C4 bioenergy crop, in three field locations spanning its native range. Our data, composed of >2000 samples, suggest field location is the primary determinant of microbiome composition; however, substantial heritable variation is widespread across bacterial taxa, especially those in the Sphingomonadaceae family. Despite diverse compositions, we find that relatively few highly prevalent bacterial taxa make up the majority of the switchgrass root microbiota, a large fraction of which is shared across sites. Local genotypes preferentially recruit / filter for local microbes, supporting the idea of affinity between local plants and their microbiota. Using genome-wide association, we identified loci impacting the abundance of >400 microbial strains and found an enrichment of genes involved in immune responses, signaling pathways, and secondary metabolism. We found loci associated with over half of the core microbiota (i.e. microbes in >80% of samples) regardless of field location. Finally, we show a genetic relationship between a basal plant immunity pathway and relative abundances of root microbiota. This study brings us closer to harnessing and manipulating beneficial microbial associations via host genetics.

plant biology↗

Natural variation identifies new effectors of water use efficiency in Arabidopsis.

Water use efficiency (WUE) is the ratio of biomass gained per unit of water consumed; thus, it can be altered by genetic factors that affect either side of the ratio. In the present study, we exploited natural variation for WUE as an unbiased approach to discover loci affecting either biomass accumulation or water use as factors affecting WUE. Genome-wide association (GWAS) analysis using integrated WUE measured through carbon isotope discrimination ({delta}13C) of Arabidopsis thaliana accessions identified genomic regions associated with WUE. Reverse genetic analysis of 70 candidate genes selected based on the GWAS results and transcriptome data identified 25 genes affecting WUE as measured by gravimetric and {delta}13C analyses. Mutants of four genes had higher WUE than wild type, while mutants of the other 21 genes had lower WUE. The differences in WUE were caused by either altered biomass or water consumption (or both). Stomatal density was not a primary cause of altered WUE in these mutants. Leaf surface temperatures indicated that transpiration differed for mutants of 16 genes, but generally biomass accumulation had greater effect on WUE. The genes we identified are involved in diverse cellular processes including hormone and calcium signaling, meristematic activity, photosynthesis, flowering time, leaf/vasculature development, and cell wall composition; however, none of them had been previously linked to WUE or traits related to plant water relations. Thus, our study successfully identified new effectors of WUE that can be used to understand the genetic basis of WUE and improve crop productivity.

plant biology↗

Transcriptome and DNA methylome dynamics reveal differential characteristics of inflorescence development between two ecotypes in Panicum hallii

The morphological diversity of the inflorescence determines flower and seed production, which is critical for plant adaptation and fitness. Cytosine methylation is an epigenetic mark that contributes to gene expression regulation during inflorescence development. Panicum hallii is a wild perennial grass in the subfamily Panicoideae that has been developed as a model to study perennial grass biology and adaptive evolution. Highly divergent inflorescences have evolved between the two major ecotypes in P. hallii, the upland ecotype with compact inflorescence and large seed and the lowland ecotype with an open inflorescence and small seed. Here we performed a comparative transcriptome and DNA methylome analysis across different stages of inflorescence between these two divergent ecotypes of P. hallii. Global transcriptome analysis identified differentially expressed genes (DEGs) involved in panicle divergence, stage-specific expression, and co-expression modules underlying inflorescence development. Comparing DNA methylome profiles revealed a remarkable level of differential DNA methylation associated with the evolution of the P. hallii inflorescence. We found that most differentially methylated regions (DMRs) occurred within the flanking regulatory regions of genes, especially the promoter. Integrative analysis of DEGs and DMRs characterized the global features of DMR-associated DEGs in the divergence of P. hallii inflorescence, which includes homologs of important inflorescence and seed developmental genes that have been previously identified in domesticated crops. Evolutionary analysis measured by Ka/Ks ratio suggested that most DMR-associated DEGs are under relatively strong purifying selection. This study provides insights into the transcriptome and epigenetic landscape of inflorescence divergence in P. hallii and a novel genomic resource for perennial grass biology. One sentence summaryA comparative transcriptome and DNA methylome analysis of inflorescence between upland and lowland ecotypes reveal gene expression and DNA methylation variation underlying inflorescence divergence in Panicum hallii.

evolutionary biology↗

A pleiotropic flowering time QTL exhibits gene-by-environmental interaction for fitness in a perennial grass

Flowering time is crucial for wild plant populations to adapt to their local environments. Although the genetic basis of flowering variation has been studied in many plant species, its mechanisms in non-model organisms and its adaptive value in the field are still poorly understood. Here, we report new insights into the genetic basis of flowering time and its effect on fitness in Panicum hallii, a native perennial grass. We conducted genetic mapping in populations derived from representative inland and coastal ecotypes to identify flowering time QTL and loci exhibited extensive QTL-by-environment interactions. Patterns of segregation within recombinant hybrids provide strong support for directional selection driving ecotypic divergence in flowering time. A major QTL on chromosome 5 (q-FT5) was detected in all experiments and is a key locus controlling flowering variation. Fine-mapping and expression studies identified a FLOWERING LOCUS T orthologue, FT-like 9 (PhFTL9), as the candidate underlying q-FT5. We used reciprocal transplant experiment to test for global local adaptation and the specific impact of q-FT5 on performance. We did not observe local adaptation in terms of fitness tradeoffs when contrasting ecotypes in home versus away habitats. However, we observed that the coastal allele of q-FT5 conferred a fitness advantage only in its local habitat but not at the inland site. Sequence analysis of the PhFTL9 promoter identified ecotypic specific cis-element variation associated with environmental responsiveness. Together, our findings demonstrate the genetic basis of flowering variation in a perennial grass and provide evidence for conditional neutrality underlying flowering divergence.

evolutionary biology↗

Correlational selection and genetic architecture promote the leaf economics spectrum in a perennial grass

The leaf economics spectrum (LES) is hypothesized to result from a trade-off between resource acquisition and conservation. Yet few studies have examined the evolutionary mechanisms behind the LES, perhaps because most species exhibit relatively specialized leaf economics strategies. In a genetic mapping population of the phenotypically diverse grass Panicum virgatum, we evaluate two interacting mechanisms that may drive LES evolution: 1) genetic architecture, where multiple traits are coded by the same gene (pleiotropy) or by genes in close physical proximity (linkage), and 2) correlational selection, where selection acts non-additively on combinations of multiple traits. We found evidence suggesting that shared genetic architecture (pleiotropy) controls covariation between two pairs of leaf economics traits. Additionally, at five common gardens spanning 17 degrees of latitude, correlational selection favored particular combinations of leaf economics traits. Together, these results demonstrate how the LES can evolve within species.

ecology↗

Mapping of genotype-by-environment interactions in phenology identifies two cues for flowering in switchgrass (Panicum virgatum)

The timing of vegetative and reproductive growth in plants ("phenological timings") depend on genetic effects (G), environmental (e.g., weather) cues, and their interaction. Here, we measure phenological timings in two highly divergent switchgrass (Panicum virgatum) subpopulations using repeated plantings of cloned individuals at eight sites across the central United States. The timing of vegetative growth for the two subpopulations reversed between their two natural ranges and had strong negative correlations between these regions; in contrast, the timing of flowering was positively correlated between gardens. We expect that these phenotypic correlations consist of polygenic effects on phenology which have distinct patterns of GxE segregating at different mapped loci. Thus, we infer the mixture of ways genetic effects impact phenological timings, such as across common gardens (GxE) or with weather cues (GxWeather). We demonstrate that we can identify genetic variation with GxWeather and assign genetic loci to specific weather-based cues or other patterns. For example, in the Gulf subpopulation, 65% of genetic effects on the timing of vegetative growth covary with daylength 14 days prior to green-up date, and 33% of genetic effects on the timing of flowering covary with cumulative rainfall in the week prior to flowering. However, most variation in genetic effects cannot be attributed to variation in weather variables. Selective breeding for particular alleles at GxWeather loci could alter flowering responsiveness in a photoperiod or rainfall-specific way. More broadly, our approach refines the characterization of genotype-by-environment interactions and can be implemented in any species phenotyped in multiple environments.

genetics↗

Host genetic control of succession in the switchgrass leaf fungal microbiome

Leaf fungal microbiomes can be fundamental drivers of host plant success, as they contain pathogens that devastate crop plants and taxa that enhance nutrient uptake, discourage herbivory, and antagonize pathogens. We measured leaf fungal diversity with amplicon sequencing across an entire growing season in a diversity panel of switchgrass (Panicum virgatum). We also sampled a replicated subset of genotypes across three additional sites to compare the importance of time, space, ecology, and genetics. We found a strong successional pattern in the microbiome shaped both by host genetics and environmental factors. Further, we used genome-wide association mapping and RNA-sequencing to show that three cysteine-rich receptor-like kinases were linked to a genetic locus associated with microbiome structure. These genes were more highly expressed in genotypes susceptible to fungal pathogens, which were central to microbial covariance networks, suggesting that host immune genes are a principal means of controlling the entire leaf microbiome.

ecology↗

Genomics of sorghum local adaptation to a parasitic plant

Host-parasite coevolution can maintain high levels of genetic diversity in traits involved in species interactions. In many systems, host traits exploited by parasites are constrained by use in other functions, leading to complex selective pressures across space and time. Here, we study genome-wide variation in the staple crop Sorghum bicolor (L.) Moench and its association with the parasitic weed Striga hermonthica (Delile) Benth., a major constraint to food security in Africa. We hypothesize that geographic selection mosaics across gradients of parasite occurrence maintain genetic diversity in sorghum landrace resistance. Suggesting a role in local adaptation to parasite pressure, multiple independent loss-of-function alleles at sorghum LOW GERMINATION STIMULANT 1 (LGS1) are broadly distributed among African landraces and geographically associated with S. hermonthica occurrence. However, low frequency of these alleles within S. hermonthica-prone regions and their absence elsewhere implicate potential tradeoffs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and belowground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with tradeoffs, we find signatures of balancing selection surrounding LGS1 and other candidates from analysis of genome-wide associations with parasite distribution. Experiments with CRISPR-Cas9 edited sorghum further indicate the benefit of LGS1-mediated resistance strongly depends on parasite genotype and abiotic environment and comes at the cost of reduced photosystem gene expression. Our study demonstrates long-term maintenance of diversity in host resistance genes across smallholder agroecosystems, providing a valuable comparison to both industrial farming systems and natural communities. SIGNIFICANCE STATEMENTUnderstanding co-evolution in crop-parasite systems is critical to management of myriad pests and pathogens confronting modern agriculture. In contrast to wild plant communities, parasites in agricultural ecosystems are usually expected to gain the upper hand in co-evolutionary arms races due to limited genetic diversity of host crops in cultivation. Here, we develop a framework to characterize associations between genome variants in global landraces (traditional varieties) of the staple crop sorghum with the distribution of the devastating parasitic weed Striga hermonthica. We find long-term maintenance of diversity in genes related to parasite resistance, highlighting an important role of host adaptation for co-evolutionary dynamics in smallholder agroecosystems.

evolutionary biology↗

Geographic variation in the genetic basis of resistance to leaf rust in locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum)

O_LILocal adaptation is an important process in plant evolution, which can be impacted by differential pathogen pressures along environmental gradients. However, the degree to which pathogen resistance loci vary in effect across space and time is incompletely described. C_LIO_LITo understand how the genetic architecture of resistance varies across time and geographic space, we quantified rust (Puccinia spp.) severity in switchgrass (Panicum virgatum) plantings at eight locations across the central United States for three years and conducted quantitative trait locus (QTL) mapping for rust progression. C_LIO_LIWe mapped several variable QTLs, but two large-effect QTLs which we have named Prr1 and Prr2 were consistently associated with rust severity in multiple sites and years, particularly in northern sites. In contrast, there were numerous small-effect QTLs at southern sites, indicating a genotype-by-environment interaction in rust resistance loci. Interestingly, Prr1 and Prr2 had a strong epistatic interaction, which also varied in strength and direction of effect across space. C_LIO_LIOur results suggest that abiotic factors covarying with latitude interact with the genetic loci underlying plant resistance to control rust infection severity. Further, our results indicate that segregating genetic variation in epistatically interacting loci may play a key role in determining response to infection across geographic space. C_LI

genomics↗

Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana

Intraspecific trait variation is caused by genetic and plastic responses to environment. This intraspecific diversity is captured in immense natural history collections, giving us a window into trait variation across continents and through centuries of environmental shifts. Here we tested if hypotheses based on life history and the leaf economics spectrum explain intraspecific trait changes across global spatiotemporal environmental gradients. We measured phenotypes on a 216-year time series of Arabidopsis thaliana accessions from across the native range and applied spatially varying coefficient models to quantify region-specific trends in trait coordination and trait responses to climate gradients. All traits exhibited significant change across space and/or through time. For example, {delta}15N decreased over time across much of the range and leaf C:N increased, consistent with predictions based on anthropogenic changes in land use and atmosphere. Plants were collected later in the growing season in more recent years in many regions, possibly because populations shifted toward more spring germination and summer flowering as opposed to fall germination and spring flowering. When climate variables were considered, collection dates were earlier in warmer years, while summer rainfall had opposing associations with collection date depending on regions. There was only a modest correlation among traits, indicating a lack of a single life history/physiology axis. Nevertheless, leaf C:N was low for summer- versus spring-collected plants, consistent with a life history-physiology axis from slow-growing winter annuals to fast-growing spring/summer annuals. Regional heterogeneity in phenotype trends indicates complex responses to spatiotemporal environmental gradients potentially due to geographic genetic variation and climate interactions with other aspects of environment. Our study demonstrates how natural history collections can be used to broadly characterize trait responses to environment, revealing heterogeneity in response to anthropogenic change.

ecology↗

The genetic architecture of shoot and root trait divergence between upland and lowland ecotypes of a perennial grass.

Introduction Introduction Materials and Methods Results Discussion Conclusion Author Contributions: References Adaptation to abiotic stress is an important driver of contemporary evolution in plant populations. Abiotic stressors have been implicated as driving factors in ecological speciation (Stebbins, 1952;Lexer & Fay, 2005), where populations have diverged across a number of traits, exhibit different niche characteristics, and eventually become reproductively isolated (Clausen, 1951; Lowry, 2012; Yardeni et al., 2016). Local adaptation to soil water availability is an especially important driver of plant evolution (Stebbins, 1952; Rajakaruna, 2004; ...

plant biology↗