Publications

2015
Miller M, Song Q, Shi X, Juenger TE, Chen JZ. Natural variation in timing of stress-responsive gene expression predicts heterosis in intraspecific hybrids of Arabidopsis. Nature Communications [Internet]. 2015. Publisher's VersionAbstract

The genetic distance between hybridizing parents affects heterosis; however, the mechanisms for this remain unclear. Here we report that this genetic distance correlates with natural variation and epigenetic regulation of circadian clock-mediated stress responses. In intraspecific hybrids of Arabidopsis thaliana, genome-wide expression of many biotic and abiotic stress-responsive genes is diurnally repressed and this correlates with biomass heterosis and biomass quantitative trait loci. Expression differences of selected stress-responsive genes among diverse ecotypes are predictive of heterosis in their hybrids. Stress-responsive genes are repressed in the hybrids under normal conditions but are induced to mid-parent or higher levels under stress at certain times of the day, potentially balancing the tradeoff between stress responses and growth. Consistent with this hypothesis, repression of two candidate stress-responsive genes increases growth vigour. Our findings may therefore provide new criteria for effectively selecting parents to produce high- or low-yield hybrids.

miller_et_al_2015.pdf
Lowry DB, Taylor SH, Bonnette J, Aspinwall MJ, Asmus AL, Keitt TH, Tobias CM, Juenger TE. QTLs for Biomass and Developmental Traits in Switchgrass (Panicum virgatum). Bioenerg. Res. [Internet]. 2015. Publisher's VersionAbstract

Genetic and genomic resources have recently been developed for the bioenergy crop switchgrass (Panicum virgatum). Despite these advances, little research has been focused on identifying genetic loci involved in natural variation of important bioenergy traits, including biomass. Quantitative trait locus (QTL) mapping is typically used to discover loci that contribute to trait variation. Once identified, QTLs can be used to improve agronomically important traits through marker-assisted selection. In this study, we conducted QTL mapping in Austin, TX, USA, with a full-sib mapping population derived from a cross between tetraploid clones of two major switchgrass cultivars (Alamo-A4 and Kanlow-K5). We observed significant among-genotype variation for the vast majority of growth, morphological, and phenological traits measured on the mapping population. Overall, we discovered 27 significant QTLs across 23 traits. QTLs for biomass production colocalized on linkage group 9b across years, as well as with a major biomass QTL discovered in another recent switchgrass QTL study. The experiment was conducted under a rainout shelter, which allowed us to examine the effects of differential irrigation on trait values. We found very minimal effects of the reduced watering treatment on traits, with no significant effect on biomass production. Overall, the results of our study set the stage for future crop improvement through marker-assisted selection breeding.

lowry.pdf
Behrman KD, Juenger TE, Kiniry JR, Keitt TH. Spatial land use trade-offs for maintenance of biodiversity, biofuel, and agriculture. Landscape Ecol [Internet]. 2015. Publisher's VersionAbstract

Context Expansion of bioenergy production is part of a global effort to reduce greenhouse gas emissions and mitigate climate change. Dedicated biomass crops will compete with other land uses as most high quality arable land is already used for agriculture, urban development, and biodiversity conservation. Objective First, we explore the trade-offs between converting land enrolled in the U.S. Conservation Reserve Program (CRP) to switchgrass for biofuel production or preserving it for biodiversity. Next, we examine the trade-offs between agriculture, biodiversity, and biofuel across the central and eastern U.S. Methods We compiled measures of biodiversity, agriculture, and biofuel from land cover classifications, species range maps, and mechanistic model output of switchgrass yield. We used a spatially explicit optimization algorithm to analyze the impacts of small-to-large scale biomass production by identifying locations that maximize biofuel produced from switchgrass and minimize negative impacts on biodiversity and agriculture. Results Using CRP land for switchgrass production increases the land area required to meet biomass goals and the species range area altered for birds, amphibians, mammals, and reptiles. When conversion is not limited to CRP, conversion scenarios including biodiversity and agriculture trade-offs require greater than 100 % more area for switchgrass to reach the same production goals. When land conversion scenarios do not include biodiversity, twice the range area for reptiles and amphibians could be altered. Conclusions Land-use trade-offs between biofuel production, agriculture, and biodiversity exist and alter optimum location of land conversion for low-to high
biofuel levels. This highlights the need for systematic land-use planning for the future.

kathrine_et_al_2015.pdf
Lasky JR, Upadhyaya HD, Ramu P, Deshpande S, Hash TC, Bonnette J, Juenger TE, Hyma K, Acharya C, Mitchell SE, et al. Genome-environment associations in sorghum landraces adaptive traits. Science Advances [Internet]. 2015;1 (6) :02-18. Publisher's VersionAbstract

Improving environmental adaptation in crops is essential for food security under global change, but phenotyping adaptive traits remains a major bottleneck. If associations between single-nucleotide polymorphism (SNP) alleles and environment of origin in crop landraces reflect adaptation, then these could be used to predict phenotypic variation for adaptive traits. We tested this proposition in the global food crop Sorghum bicolor, characterizing 1943 georeferenced landraces at 404,627 SNPs and quantifying allelic associations with bioclimatic and soil gradients. Environment explained a substantial portion of SNP variation, independent of geographical distance, and genic SNPs were enriched for environmental associations. Further, environment-associated SNPs predicted genotype-by-environment interactions under experimental drought stress and aluminum toxicity. Our results suggest that genomic signatures of environmental adaptation may be useful for crop improvement, enhancing germplasm identification and marker-assisted selection. Together, genome-environment associations and phenotypic analyses may reveal the basis of environmental adaptation.

lasky.pdf
Des Marais DL, Skillern WD, Juenger TE. Deeply Diverged Alleles in the Arabidopsis AREB1 Transcription Factor Drive Genome-Wide Differences in Transcriptional Response to the Environment. Mol Biol Evol. 2015;32 (4) :956-69.Abstract
Gene regulatory variation is an important driver of the evolution of physiological and developmental responses to the environment. The abscisic acid (ABA) signaling pathway has long been studied as a key component of the cellular response to abiotic stresses in plants. We identify two haplotypes in an Arabidopsis thaliana transcription factor, AREB1, which plays a central role in ABA-mediated response to osmotic stress. These two haplotypes show the sequence signature of long-term maintenance of genetic diversity, suggesting a role for a diversifying selection process such as balancing selection. We find that the two haplotypes, distinguished by a large number of single nucleotide polymorphisms and the presence or absence of four small insertion/deletions in AREB1 intron 1 and exon 2, are at roughly equal frequencies in Arabidopsis, and show high linkage disequilibrium and deep sequence divergence. We use a transgenic approach, along with mRNA Sequencing-based assay of genome-wide expression levels, and find considerable functional divergence between alleles representing the two haplotype groups. Specifically, we find that, under benign soil-water conditions, transgenic lines containing different AREB1 alleles differ in the expression of a large number of genes associated with pathogen response. There are relatively modest gene expression differences between the two transgenic lines under restricted soil water content. Our finding of pathogen-related activity expands the known roles of AREB1 in A. thaliana and reveals the molecular basis of gene-by-environment interaction in a putatively adaptive plant regulatory protein.
Malcom JW, Hernandez KM, Likos R, Wayne T, Leibold MA, Juenger TE. Extensive cross-environment fitness variation lies along few axes of genetic variation in the model alga, Chlamydomonas reinhardtii. New Phytol. 2015;205 (2) :841-51.Abstract
Variation is essential to ecological and evolutionary dynamics, but genetic variation of quantitative traits may be concentrated in a limited number of dimensions, constraining ecoevolutionary dynamics. We describe high-dimension variation in natural accessions of the model alga, Chlamydomonas reinhardtii, and test the hypothesis that extensive fitness variation across 30 environments is constrained to a small number of axes. We used high-throughput phenotyping to investigate morphological, fitness, and genotype × environment (G × E) variation in 18 natural C. reinhardtii accessions in 30 environments. The organismal phenotypes of cell cycle, cell size, and phototactic behavior exhibited substantial genetic variation between lines, and we found up to 74-fold fitness variation across accessions and environments. Approximately 47% of the extensive G × E variation is accounted for by the first two principal components (PCs) of the G-matrix corresponding to covariation in metals response, nitrogen availability, or salt and nutrient response. The natural variation of C. reinhardtii accessions supports the hypothesis that, despite abundant genetic variation across single environments, the species' adaptive response should be constrained along few major axes of selection. These results highlight the utility of natural accessions for integrating ecoevolutionary and genetic research.
Lowry DB, Hernandez K, Taylor SH, Meyer E, Logan TL, Barry KW, Chapman JA, Rokhsar DS, Schmutz J, Juenger TE. The genetics of divergence and reproductive isolation between ecotypes of Panicum hallii. New Phytol. 2015;205 (1) :402-14.Abstract
The process of plant speciation often involves the evolution of divergent ecotypes in response to differences in soil water availability between habitats. While the same set of traits is frequently associated with xeric/mesic ecotype divergence, it is unknown whether those traits evolve independently or if they evolve in tandem as a result of genetic colocalization either by pleiotropy or genetic linkage. The self-fertilizing C4 grass species Panicum hallii includes two major ecotypes found in xeric (var. hallii) or mesic (var. filipes) habitats. We constructed the first linkage map for P. hallii by genotyping a reduced representation genomic library of an F2 population derived from an intercross of var. hallii and filipes. We then evaluated the genetic architecture of divergence between these ecotypes through quantitative trait locus (QTL) mapping. Overall, we mapped QTLs for nine morphological traits that are involved in the divergence between the ecotypes. QTLs for five key ecotype-differentiating traits all colocalized to the same region of linkage group five. Leaf physiological traits were less divergent between ecotypes, but we still mapped five physiological QTLs. We also discovered a two-locus Dobzhansky-Muller hybrid incompatibility. Our study suggests that ecotype-differentiating traits may evolve in tandem as a result of genetic colocalization.
2014
Lowry DB, Behrman KD, Grabowski P, Morris GP, Kiniry JR, Juenger TE. Adaptations between Ecotypes and along Environmental Gradients in Panicum virgatum. American Society of Naturalists [Internet]. 2014;183 (5) :682-692. Publisher's VersionAbstract

Determining the patterns and mechanisms of natural selection in the wild is of fundamental importance to understanding the differentiation of populations and the evolution of new species. However, it is often unknown the extent to which adaptive genetic variation is distributed among ecotypes between distinct habitats versus along large-scale geographic environmental gradients, such as those that track latitude. Classic studies of selection in the wild in switchgrass, Panicum virgatum, tested for adaptation at both of these levels of natural variation. Here we review what these field experiments and modern agronomic field trials have taught us about natural variation and selection at both the ecotype and environmental gradient levels in P. virgatum. With recent genome sequencing efforts in P. virgatum, it is poised to become an excellent system for understanding the adaptation of grassland species across the eastern half of North America. The identification of genetic loci involved in different types of adaptations will help to understand the evolutionary mechanisms of diversification within P. virgatum and provide useful information for the breeding of highyielding cultivars for different ecoregions.

lowry_adaptationsbetweenecotypes-2014.pdf
Kenney AM, McKay JK, Richards JH, Juenger TE. Direct and indirect selection on flowering time, water-use efficiency (WUE, delta13C), and WUE plasticity to drought in Arabidopsis thaliana. Ecology and Evolution [Internet]. 2014;4 (23) :4505-4521. Publisher's VersionAbstract

Flowering time and water-use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time, WUE, and WUE plasticity to drought in Arabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) Is WUE plasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions of A. thaliana grown in well-watered and season-ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment. WUE and flowering time were consistently positively genetically correlated. WUE was correlated with WUE plasticity, but the direction changed between treatments. Selection generally favored early flowering and low WUE, with drought favoring earlier flowering significantly more than well-watered conditions. Selection for lower WUE was marginally stronger under drought. There were no net fitness costs of WUE plasticity. WUE plasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation between WUE and flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions of A. thaliana. WUE plasticity may be favored over completely fixed development in environments with periodic drought.

kenney_et_al-2014-ecology_and_evolution.pdf
Gordon SP, Priest H, Des Marais DL, Schackwitz W, Figueroa M, Martin J, Bragg JN, Tyler L, Lee C-R, Bryant D, et al. Genome diversity in Brachypodium distachyon: deep sequencing of highly diverse inbred lines. The Plant Journal [Internet]. 2014;(79) :361-374. Publisher's VersionAbstract

Brachypodium distachyon is small annual grass that has been adopted as a model for the grasses. Its small genome, high-quality reference genome, large germplasm collection, and selfing nature make it an excellent subject for studies of natural variation. We sequenced six divergent lines to identify a comprehensive set of polymorphisms and analyze their distribution and concordance with gene expression. Multiple methods and controls were utilized to identify polymorphisms and validate their quality. mRNA-Seq experiments under control and simulated drought-stress conditions, identified 300 genes with a genotype-dependent treatment response. We showed that large-scale sequence variants had extremely high concordance with altered expression of hundreds of genes, including many with genotype-dependent treatment responses. We generated a deep mRNA-Seq dataset for the most divergent line and created a de novo transcriptome assembly. This led to the discovery of >2400 previously unannotated transcripts and hundreds of genes not present in the reference genome. We built a public database for visualization and investigation of sequence variants among these widely used inbred lines.

gordon_et_al-2014-the_plant_journal.pdf
Meyer E, Aspinwall MJ, Lowry DB, Palacio-Mejía JD, Logan TL, Fay PA, Juenger TE. Integrating transcriptional, metabolomic, and physiological responses to drought stress and recovery in switchgrass (Panicum virgatum L.). BMC Genomics [Internet]. 2014;(15) :527. Publisher's VersionAbstract

Background: In light of the changes in precipitation and soil water availability expected with climate change, understanding the mechanisms underlying plant responses to water deficit is essential. Toward that end we have conducted an integrative analysis of responses to drought stress in the perennial C4 grass and biofuel crop, Panicum virgatum (switchgrass). Responses to soil drying and re-watering were measured at transcriptional, physiological, and metabolomic levels. To assess the interaction of soil moisture with diel light: dark cycles, we profiled gene expression in drought and control treatments under pre-dawn and mid-day conditions.


Results: Soil drying resulted in reduced leaf water potential, gas exchange, and chlorophyll fluorescence along with differential expression of a large fraction of the transcriptome (37%). Many transcripts responded differently depending on time of day (e.g. up-regulation pre-dawn and down-regulation mid-day). Genes associated with C4 photosynthesis were down-regulated during drought, while C4 metabolic intermediates accumulated. Rapid changes in gene expression were observed during recovery from drought, along with increased water use efficiency and chlorophyll fluorescence.

Conclusions: Our findings demonstrate that drought responsive gene expression depends strongly on time of day and that gene expression is extensively modified during the first few hours of drought recovery. Analysis of covariation in gene expression, metabolite abundance, and physiology among plants revealed non-linear relationships that suggest critical thresholds in drought stress responses. Future studies may benefit from evaluating these thresholds among diverse accessions of switchgrass and other C4 grasses.

meyer_etal2014.pdf
Des Marais DL, Auchincloss LC, Sukamtoh E, McKay JK, Logan T, Richards JH, Juenger TE. Variation in MPK12 affects water use efficiency in Arabidopsis and reveals a pleiotropic link between guard cell size and ABA response. PNAS [Internet]. 2014;111 (7) :2836-2841. Publisher's VersionAbstract

Plant water relations are critical for determining the distribution, persistence, and fitness of plant species. Studying the genetic basis of ecologically relevant traits, however, can be complicated by their complex genetic, physiological, and developmental basis and their interaction with the environment. Water use efficiency (WUE), the ratio of photosynthetic carbon assimilation to stomatal conductance to water, is a dynamic trait with tremendous ecological and agricultural importance whose genetic control is poorly understood. In the present study, we use a quantitative trait locus-mapping approach to locate, fine-map, clone, confirm, and characterize an allelic substitution that drives differences in WUE among natural accessions of Arabidopsis thaliana. We show that a single amino acid substitution in an abscisic acid-responsive kinase, AtMPK12, causes reduction in WUE, and we confirm its functional role using transgenics. We further demonstrate that natural alleles at AtMPK12 differ in their response to cellular and environmental cues, with the allele from the Cape Verde Islands (CVI) being less responsive to hormonal inhibition of stomatal opening and more responsive to short-term changes in vapor pressure deficit. We also show that the CVI allele results in constitutively larger stomata. Together, these differences cause higher stomatal conductance and lower WUE compared with the common allele. These physiological changes resulted in reduced whole-plant transpiration efficiency and reduced fitness under water-limited compared with well-watered conditions. Our work demonstrates how detailed analysis of naturally segregating functional variation can uncover the molecular and physiological basis of a key trait associated with plant performance in ecological and agricultural settings.

pnas-2014-des_marais-2836-41.pdf
Verslues PE, Lasky JR, Juenger TE, Liu T-W, Kumar NM. Genome-wide association mapping combined with reverse genetics identifies new effectors of low water potential-induced proline accumulation in Arabidopsis. Plant Physiol. 2014;164 (1) :144-59.Abstract
Arabidopsis (Arabidopsis thaliana) exhibits natural genetic variation in drought response, including varying levels of proline (Pro) accumulation under low water potential. As Pro accumulation is potentially important for stress tolerance and cellular redox control, we conducted a genome-wide association (GWAS) study of low water potential-induced Pro accumulation using a panel of natural accessions and publicly available single-nucleotide polymorphism (SNP) data sets. Candidate genomic regions were prioritized for subsequent study using metrics considering both the strength and spatial clustering of the association signal. These analyses found many candidate regions likely containing gene(s) influencing Pro accumulation. Reverse genetic analysis of several candidates identified new Pro effector genes, including thioredoxins and several genes encoding Universal Stress Protein A domain proteins. These new Pro effector genes further link Pro accumulation to cellular redox and energy status. Additional new Pro effector genes found include the mitochondrial protease LON1, ribosomal protein RPL24A, protein phosphatase 2A subunit A3, a MADS box protein, and a nucleoside triphosphate hydrolase. Several of these new Pro effector genes were from regions with multiple SNPs, each having moderate association with Pro accumulation. This pattern supports the use of summary approaches that incorporate clusters of SNP associations in addition to consideration of individual SNP probability values. Further GWAS-guided reverse genetics promises to find additional effectors of Pro accumulation. The combination of GWAS and reverse genetics to efficiently identify new effector genes may be especially applicable for traits difficult to analyze by other genetic screening methods.
Lowry DB, Behrman KD, Grabowski P, Morris GP, Kiniry JR, Juenger TE. Adaptations between ecotypes and along environmental gradients in Panicum virgatum. Am Nat. 2014;183 (5) :682-92.Abstract
Determining the patterns and mechanisms of natural selection in the wild is of fundamental importance to understanding the differentiation of populations and the evolution of new species. However, it is often unknown the extent to which adaptive genetic variation is distributed among ecotypes between distinct habitats versus along large-scale geographic environmental gradients, such as those that track latitude. Classic studies of selection in the wild in switchgrass, Panicum virgatum, tested for adaptation at both of these levels of natural variation. Here we review what these field experiments and modern agronomic field trials have taught us about natural variation and selection at both the ecotype and environmental gradient levels in P. virgatum. With recent genome sequencing efforts in P. virgatum, it is poised to become an excellent system for understanding the adaptation of grassland species across the eastern half of North America. The identification of genetic loci involved in different types of adaptations will help to understand the evolutionary mechanisms of diversification within P. virgatum and provide useful information for the breeding of high-yielding cultivars for different ecoregions.
Kenney AM, McKay JK, Richards JH, Juenger TE. Direct and indirect selection on flowering time, water-use efficiency (WUE, δ (13)C), and WUE plasticity to drought in Arabidopsis thaliana. Ecol Evol. 2014;4 (23) :4505-21.Abstract
Flowering time and water-use efficiency (WUE) are two ecological traits that are important for plant drought response. To understand the evolutionary significance of natural genetic variation in flowering time, WUE, and WUE plasticity to drought in Arabidopsis thaliana, we addressed the following questions: (1) How are ecophysiological traits genetically correlated within and between different soil moisture environments? (2) Does terminal drought select for early flowering and drought escape? (3) Is WUE plasticity to drought adaptive and/or costly? We measured a suite of ecophysiological and reproductive traits on 234 spring flowering accessions of A. thaliana grown in well-watered and season-ending soil drying treatments, and quantified patterns of genetic variation, correlation, and selection within each treatment. WUE and flowering time were consistently positively genetically correlated. WUE was correlated with WUE plasticity, but the direction changed between treatments. Selection generally favored early flowering and low WUE, with drought favoring earlier flowering significantly more than well-watered conditions. Selection for lower WUE was marginally stronger under drought. There were no net fitness costs of WUE plasticity. WUE plasticity (per se) was globally neutral, but locally favored under drought. Strong genetic correlation between WUE and flowering time may facilitate the evolution of drought escape, or constrain independent evolution of these traits. Terminal drought favored drought escape in these spring flowering accessions of A. thaliana. WUE plasticity may be favored over completely fixed development in environments with periodic drought.
Gordon SP, Priest H, Des Marais DL, Schackwitz W, Figueroa M, Martin J, Bragg JN, Tyler L, Lee C-R, Bryant D, et al. Genome diversity in Brachypodium distachyon: deep sequencing of highly diverse inbred lines. Plant J. 2014;79 (3) :361-74.Abstract
Brachypodium distachyon is small annual grass that has been adopted as a model for the grasses. Its small genome, high-quality reference genome, large germplasm collection, and selfing nature make it an excellent subject for studies of natural variation. We sequenced six divergent lines to identify a comprehensive set of polymorphisms and analyze their distribution and concordance with gene expression. Multiple methods and controls were utilized to identify polymorphisms and validate their quality. mRNA-Seq experiments under control and simulated drought-stress conditions, identified 300 genes with a genotype-dependent treatment response. We showed that large-scale sequence variants had extremely high concordance with altered expression of hundreds of genes, including many with genotype-dependent treatment responses. We generated a deep mRNA-Seq dataset for the most divergent line and created a de novo transcriptome assembly. This led to the discovery of >2400 previously unannotated transcripts and hundreds of genes not present in the reference genome. We built a public database for visualization and investigation of sequence variants among these widely used inbred lines.
Meyer E, Aspinwall MJ, Lowry DB, Palacio-Mejía JD, Logan TL, Fay PA, Juenger TE. Integrating transcriptional, metabolomic, and physiological responses to drought stress and recovery in switchgrass (Panicum virgatum L.). BMC Genomics. 2014;15 :527.Abstract
BACKGROUND: In light of the changes in precipitation and soil water availability expected with climate change, understanding the mechanisms underlying plant responses to water deficit is essential. Toward that end we have conducted an integrative analysis of responses to drought stress in the perennial C4 grass and biofuel crop, Panicum virgatum (switchgrass). Responses to soil drying and re-watering were measured at transcriptional, physiological, and metabolomic levels. To assess the interaction of soil moisture with diel light: dark cycles, we profiled gene expression in drought and control treatments under pre-dawn and mid-day conditions. RESULTS: Soil drying resulted in reduced leaf water potential, gas exchange, and chlorophyll fluorescence along with differential expression of a large fraction of the transcriptome (37%). Many transcripts responded differently depending on time of day (e.g. up-regulation pre-dawn and down-regulation mid-day). Genes associated with C4 photosynthesis were down-regulated during drought, while C4 metabolic intermediates accumulated. Rapid changes in gene expression were observed during recovery from drought, along with increased water use efficiency and chlorophyll fluorescence. CONCLUSIONS: Our findings demonstrate that drought responsive gene expression depends strongly on time of day and that gene expression is extensively modified during the first few hours of drought recovery. Analysis of covariation in gene expression, metabolite abundance, and physiology among plants revealed non-linear relationships that suggest critical thresholds in drought stress responses. Future studies may benefit from evaluating these thresholds among diverse accessions of switchgrass and other C4 grasses.
Lasky JR, Des Marais DL, Lowry DB, Povolotskaya I, McKay JK, Richards JH, Keitt TH, Juenger TE. Natural variation in abiotic stress responsive gene expression and local adaptation to climate in Arabidopsis thaliana. Mol Biol Evol. 2014;31 (9) :2283-96.Abstract
Gene expression varies widely in natural populations, yet the proximate and ultimate causes of this variation are poorly known. Understanding how variation in gene expression affects abiotic stress tolerance, fitness, and adaptation is central to the field of evolutionary genetics. We tested the hypothesis that genes with natural genetic variation in their expression responses to abiotic stress are likely to be involved in local adaptation to climate in Arabidopsis thaliana. Specifically, we compared genes with consistent expression responses to environmental stress (expression stress responsive, "eSR") to genes with genetically variable responses to abiotic stress (expression genotype-by-environment interaction, "eGEI"). We found that on average genes that exhibited eGEI in response to drought or cold had greater polymorphism in promoter regions and stronger associations with climate than those of eSR genes or genomic controls. We also found that transcription factor binding sites known to respond to environmental stressors, especially abscisic acid responsive elements, showed significantly higher polymorphism in drought eGEI genes in comparison to eSR genes. By contrast, eSR genes tended to exhibit relatively greater pairwise haplotype sharing, lower promoter diversity, and fewer nonsynonymous polymorphisms, suggesting purifying selection or selective sweeps. Our results indicate that cis-regulatory evolution and genetic variation in stress responsive gene expression may be important mechanisms of local adaptation to climatic selective gradients.
Easlon HM, Nemali KS, Richards JH, Hanson DT, Juenger TE, McKay JK. The physiological basis for genetic variation in water use efficiency and carbon isotope composition in Arabidopsis thaliana. Photosynth Res. 2014;119 (1-2) :119-29.Abstract
Ecologists and physiologists have documented extensive variation in water use efficiency (WUE) in Arabidopsis thaliana, as well as association of WUE with climatic variation. Here, we demonstrate correlations of whole-plant transpiration efficiency and carbon isotope composition (δ(13)C) among life history classes of A. thaliana. We also use a whole-plant cuvette to examine patterns of co-variation in component traits of WUE and δ(13)C. We find that stomatal conductance (g s) explains more variation in WUE than does A. Overall, there was a strong genetic correlation between A and g s, consistent with selection acting on the ratio of these traits. At a more detailed level, genetic variation in A was due to underlying variation in both maximal rate of carboxylation (V cmax) and maximum electron transport rate (Jmax). We also found strong effects of leaf anatomy, where lines with lower WUE had higher leaf water content (LWC) and specific leaf area (SLA), suggesting a role for mesophyll conductance (g m) in variation of WUE. We hypothesize that this is due to an effect through g m, and test this hypothesis using the abi4 mutant. We show that mutants of ABI4 have higher SLA, LWC, and g m than wild-type, consistent with variation in leaf anatomy causing variation in g m and δ(13)C. These functional data also add further support to the central, integrative role of ABI4 in simultaneously altering ABA sensitivity, sugar signaling, and CO2 assimilation. Together our results highlight the need for a more holistic approach in functional studies, both for more accurate annotation of gene function and to understand co-limitations to plant growth and productivity.
Des Marais DL, Auchincloss LC, Sukamtoh E, McKay JK, Logan T, Richards JH, Juenger TE. Variation in MPK12 affects water use efficiency in Arabidopsis and reveals a pleiotropic link between guard cell size and ABA response. Proc Natl Acad Sci U S A. 2014;111 (7) :2836-41.Abstract
Plant water relations are critical for determining the distribution, persistence, and fitness of plant species. Studying the genetic basis of ecologically relevant traits, however, can be complicated by their complex genetic, physiological, and developmental basis and their interaction with the environment. Water use efficiency (WUE), the ratio of photosynthetic carbon assimilation to stomatal conductance to water, is a dynamic trait with tremendous ecological and agricultural importance whose genetic control is poorly understood. In the present study, we use a quantitative trait locus-mapping approach to locate, fine-map, clone, confirm, and characterize an allelic substitution that drives differences in WUE among natural accessions of Arabidopsis thaliana. We show that a single amino acid substitution in an abscisic acid-responsive kinase, AtMPK12, causes reduction in WUE, and we confirm its functional role using transgenics. We further demonstrate that natural alleles at AtMPK12 differ in their response to cellular and environmental cues, with the allele from the Cape Verde Islands (CVI) being less responsive to hormonal inhibition of stomatal opening and more responsive to short-term changes in vapor pressure deficit. We also show that the CVI allele results in constitutively larger stomata. Together, these differences cause higher stomatal conductance and lower WUE compared with the common allele. These physiological changes resulted in reduced whole-plant transpiration efficiency and reduced fitness under water-limited compared with well-watered conditions. Our work demonstrates how detailed analysis of naturally segregating functional variation can uncover the molecular and physiological basis of a key trait associated with plant performance in ecological and agricultural settings.

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