Publications

2021
John T Lovell, Alice H MacQueen SMJBJND, Adam Session, Shengqiang Shu KBSB, Aren Ewing, Paul P Grabowski THMH, Anna Lipzen, Thomas H Pendergast CPPQESV, Rita Sharma, Ada Stewart VSYTR, Melissa Williams, Guohong Albert Wu YY, Kathrine D Behrman, Arvid R Boe PFFFAB, Juan Manuel Martínez-Reyna, Roser Matamala RMB, Michael Udvardi, Rod A Wing YWLBE, Daniel S Rokhsar, Jane Grimwood TJJSE. Genomic mechanisms of climate adaptation in polyploid bioenergy switchgrass. Nature [Internet]. 2021. Publisher's VersionAbstract
Long-term climate change and periodic environmental extremes threaten food and fuel security1 and global crop productivity2,3,4. Although molecular and adaptive breeding strategies can buffer the effects of climatic stress and improve crop resilience5, these approaches require sufficient knowledge of the genes that underlie productivity and adaptation6—knowledge that has been limited to a small number of well-studied model systems. Here we present the assembly and annotation of the large and complex genome of the polyploid bioenergy crop switchgrass (Panicum virgatum). Analysis of biomass and survival among 732 resequenced genotypes, which were grown across 10 common gardens that span 1,800 km of latitude, jointly revealed extensive genomic evidence of climate adaptation. Climate–gene–biomass associations were abundant but varied considerably among deeply diverged gene pools. Furthermore, we found that gene flow accelerated climate adaptation during the postglacial colonization of northern habitats through introgression of alleles from a pre-adapted northern gene pool. The polyploid nature of switchgrass also enhanced adaptive potential through the fractionation of gene function, as there was an increased level of heritable genetic diversity on the nondominant subgenome. In addition to investigating patterns of climate adaptation, the genome resources and gene–trait associations developed here provide breeders with the necessary tools to increase switchgrass yield for the sustainable production of bioenergy.
Jae Young Choi, Liliia R Abdulkina JYICJLIAPYBTAG, Samsad Razzaque, Dorothy E Shippen TJESMPEVD. Natural variation in plant telomere length is associated with flowering time. The Plant Cell [Internet]. 2021. Publisher's VersionAbstract
Telomeres are highly repetitive DNA sequences found at the ends of chromosomes that protect the chromosomes from deterioration duringcell division. Here, using whole-genome re-sequencing and terminal restriction fragment assays, we found substantial natural intraspecific variation in telomere length in Arabidopsis thaliana, rice (Oryza sativa), and maize (Zea mays). Genome-wide association study (GWAS) mapping in A. thaliana identified 13 regions with GWAS-significant associations underlying telomere length variation, including a region that harbors the telomerase reverse transcriptase (TERT) gene. Population genomic analysis provided evidence for a selective sweep at the TERT region associated with longer telomeres. We found that telomere length is negatively correlated with flowering time variation not only in A. thaliana, but also in maize and rice, indicating a link between life-history traits and chromosome integrity. Our results point to several possible reasons for this correlation, including the possibility that longer telomeres may be more adaptive in plants that have faster developmental rates (and therefore flower earlier). Our work suggests that chromosomal structure itself might be an adaptive trait associated with plant life-history strategies.
Esther Singer JVP, Trent Northen CMJ, Juenger TE. Novel and Emerging Capabilities that Can Provide a Holistic Understanding of the Plant Root Microbiome. Phytobiomes Journal [Internet]. 2021. Publisher's VersionAbstract
In recent years, the root microbiome (i.e., microorganisms growing inside, on, or in close proximity to plant roots) has been shown to play an important role in plant health and productivity. Despite its importance, the root microbiome is challenging to study because of its complexity, heterogeneity, and subterranean location. Fortunately, root microbiome research has seen a tremendous influx of novel technologies (e.g., imaging tools, robotics, and molecular analyses), experimental platforms (e.g., micro- and mesocosms), and data integration, modeling, and prediction tools in the past decade that have greatly increased our ability to dissect the complex network of interactions between above- and belowground environmental parameters, plants, bacteria, and fungi that dictate soil and broader ecosystem health. Herein, we discuss methods that are currently used in root microbiome research and that can be expanded to phytobiome research in general ranging from laboratory studies to mesocosm-scale studies and, finally, to field studies; evaluate their relevance to ecosystem studies; and discuss future root microbiome research directions.
Palacio-Mejía JD, Grabowski PP, Ortiz EM, Silva-Arias GA, Haque T, Marais DDL, Bonnette J, Lowry DB, Juenger TE. Geographic patterns of genomic diversity and structure in the C4 grass Panicum hallii across its natural distribution. AoB Plants [Internet]. 2021. Publisher's VersionAbstract
Geographic patterns of within-species genomic diversity are shaped by evolutionary processes, life history and historical and contemporary factors. New genomic approaches can be used to infer the influence of such factors on the current distribution of infraspecific lineages. In this study, we evaluated the genomic and morphological diversity as well as the genetic structure of the C4 grass Panicum hallii across its complex natural distribution in North America. We sampled extensively across the natural range of P. hallii in Mexico and the USA to generate double-digestion restriction-associated DNA (ddRAD) sequence data for 423 individuals from 118 localities. We used these individuals to study the divergence between the two varieties of P. halliiP. hallii var. filipes and P. hallii var. hallii as well as the genetic diversity and structure within these groups. We also examined the possibility of admixture in the geographically sympatric zone shared by both varieties, and assessed distribution shifts related with past climatic fluctuations. There is strong genetic and morphological divergence between the varieties and consistent genetic structure defining seven genetic clusters that follow major ecoregions across the range. South Texas constitutes a hotspot of genetic diversity with the co-occurrence of all genetic clusters and admixture between the two varieties. It is likely a recolonization and convergence point of populations that previously diverged in isolation during fragmentation events following glaciation periods.
2020
Chieppa J, Brown T, Giresi P, Juenger TE, de Dios VR, Tissue DT, Aspinwall MJ. Climate and stomatal traits drive covariation in nighttime stomatal conductance and daytime gas exchange rates in a widespread C4 grass. New Phytologist [Internet]. 2020. Publisher's VersionAbstract
  • Nighttime stomatal conductance (gsn) varies among plant functional types and species, but factors shaping the evolution of gsn remain unclear. Examinations of intraspecific variation in gsn as a function of climate and co‐varying leaf traits may provide new insight into the evolution of gsn and its adaptive significance.
  • We grew 11 genotypes of Panicum virgatum (switchgrass) representing differing home‐climates in a common garden experiment and measured nighttime and daytime leaf gas exchange, as well as stomatal density (SD) and size during early‐, mid‐, and late‐summer. We used piecewise structural equation modelling to determine direct and indirect relationships between home‐climate, gas exchange, and stomatal traits.
  • We found no direct relationship between home‐climate and gsn. However, genotypes from hotter climates possessed higher SD, which resulted in higher gsn. Across genotypes, higher gsn was associated with higher daytime stomatal conductance and net photosynthesis.
  • Our results indicate that higher gsn may arise in genotypes from hotter climates via increased SD. High SD may provide benefits to genotypes from hotter climates through enhanced daytime transpirational cooling or by permitting maximal gas exchange when conditions are suitable. These results highlight the role of climate and trait coordination in shaping genetic differentiation in gsn.
Jennifer Bragg PT, Li Zhang, Tina Williams DW, John T. Lovell, Adam Healey JSJEBPCLC, Juenger T, Tobias CM. Environmentally responsive QTL controlling surface wax load in switchgrass. Theoretical and Applied Genetics [Internet]. 2020. Publisher's VersionAbstract
The C4 perennial grass Panicum virgatum (switchgrass) is a native species of the North American tallgrass prairie. This adaptable plant can be grown on marginal lands and is useful for soil and water conservation, biomass production, and as a forage. Two major switchgrass ecotypes, lowland and upland, differ in a range of desirable traits, and the responsible underlying loci can be localized efficiently in a pseudotestcross design. An outbred four-way cross (4WCR) mapping population of 750 F 2 lines was used to examine the genetic basis of differences in leaf surface wax load between two lowland (AP13 and WBC) and two upland (DAC and VS16) tetraploid cultivars. The objective of our experiments was to identify wax compositional variation among the population founders and to map underlying loci responsible for surface wax variation across environments. GCMS analyses of surface wax extracted from …
Xua W, Yua G, Zarea A, Zurwellerb B, Rowlandc DL, Reyes-Cabrerad J, Fritschi FB, Matamalae R, Juenger TE. Overcoming small minirhizotron datasets using transfer learning. Computers and Electronics in Agriculture [Internet]. 2020;175. Publisher's VersionAbstract
Minirhizotron technology is widely used to study root growth and development. Yet, standard approaches for tracing roots in minirhiztron imagery is extremely tedious and time consuming. Machine learning approaches can help to automate this task. However, lack of enough annotated training data is a major limitation for the application of machine learning methods. Transfer learning is a useful technique to help with training when available datasets are limited. In this paper, we investigated the effect of pre-trained features from the massive-scale, irrelevant ImageNet dataset and a relatively moderate-scale, but relevant peanut root dataset on switchgrass root imagery segmentation applications. We compiled two minirhizotron image datasets to accomplish this study: one with 17,550 peanut root images and another with 28 switchgrass root images. Both datasets were paired with manually labeled ground truth masks. Deep neural networks based on the U-net architecture were used with different pre-trained features as initialization for automated, precise pixel-wise root segmentation in minirhizotron imagery. We observed that features pre-trained on a closely related but relatively moderate size dataset like our peanut dataset were more effective than features pre-trained on the large but unrelated ImageNet dataset. We achieved high quality segmentation on peanut root dataset with 99.04% accuracy at the pixel-level and overcame errors in human-labeled ground truth masks. By applying transfer learning technique on limited switchgrass dataset with features pre-trained on peanut dataset, we obtained 99% segmentation accuracy in switchgrass imagery using only 21 images for training (fine tuning). Furthermore, the peanut pre-trained features can help the model converge faster and have much more stable performance. We presented a demo of plant root segmentation for all models under https://github.com/GatorSense/PlantRootSeg.
Yu G, Zare A, Sheng H, Matamala R, Reyes-Cabrera J, Fritschi FB, Juenger TE. Root identification in minirhizotron imagery with multiple instance learning. Machine Vision and Applications [Internet]. 2020. Publisher's VersionAbstract
In this paper, multiple instance learning (MIL) algorithms to automatically perform root detection and segmentation in minirhizotron imagery using only image-level labels are proposed. Root and soil characteristics vary from location to location, and thus, supervised machine learning approaches that are trained with local data provide the best ability to identify and segment roots in minirhizotron imagery. However, labeling roots for training data (or otherwise) is an extremely tedious and time-consuming task. This paper aims to address this problem by labeling data at the image level (rather than the individual root or root pixel level) and train algorithms to perform individual root pixel level segmentation using MIL strategies. Three MIL methods (multiple instance adaptive cosine coherence estimator, multiple instance support vector machine, multiple instance learning with randomized trees) were applied to root detection and compared to non-MIL approaches. The results show that MIL methods improve root segmentation in challenging minirhizotron imagery and reduce the labeling burden. In our results, multiple instance support vector machine outperformed other methods. The multiple instance adaptive cosine coherence estimator algorithm was a close second with an added advantage that it learned an interpretable root signature which identified the traits used to distinguish roots from soil and did not require parameter selection.
VanWallendael A, Bonnette J, Juenger TE, Felix B Fritschi, Philip A Fay RMJL‐RFRJGBDLBMC. Geographic variation in the genetic basis of resistance to leaf rust between locally adapted ecotypes of the biofuel crop switchgrass (Panicum virgatum). New Phytologist [Internet]. 2020. Publisher's VersionAbstract

Summary

 

  • Local 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.
  • To 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 USA for 3 yr and conducted quantitative trait locus (QTL) mapping for rust progression.
  • We 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. By 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 the strength and direction of effect across space.
  • Our results suggest that abiotic factors covarying with latitude interact with the genetic loci underlying plant resistance to control rust infection severity. Furthermore, our results indicate that segregating genetic variation in epistatically interacting loci may play a key role in determining response to infection across geographic space.
Heckman RW, Khasanova AR, Johnson NS, Weber S, Bonnette JE, Aspinwall MJ, Reichmann LG, Juenger TE, Fay PA, Hawkes CV. Plant biomass, not plant economics traits, determines responses of soil CO2 efflux to precipitation in the C4 grass Panicum virgatum. Journal of Ecology [Internet]. 2020. Publisher's VersionAbstract
  • Plant responses to major environmental drivers like precipitation can influence important aspects of carbon (C) cycling like soil CO2 efflux ( jec13382-math-0001 ). These responses may be predicted by two independent classes of drivers: plant size—larger plants respire more and produce a larger quantity of labile C, and plant economics—plants possessing more acquisitive plant economics strategies (i.e. high metabolic rate and tissue nutrient content) produce higher‐quality tissue that respires rapidly and decomposes quickly.
  • At two sites in central Texas, USA with similar climates and differing soil characteristics, we examined the response of eight Panicum virgatum genotypes to three annual precipitation levels defined by the driest, average and wettest years from each site's precipitation history. We evaluated the individual and joint influence of plant genotypes and precipitation on jec13382-math-0002 and traits related to plant economics and plant size. We then used confirmatory path analysis to evaluate whether effects of precipitation on jec13382-math-0003 were in part related to effects of precipitation on plant economics traits or size (‘mediated’ effects).
  • These genotypes exhibited variation in plant economics traits and above‐ground net primary productivity (ANPP), an above‐ground measure of plant size. Increasing precipitation increased jec13382-math-0004 and ANPP more than plant economics traits. At both sites, ANPP was the best predictor of jec13382-math-0005 . Moreover, the sites differed in the ways that plant size and plant economics traits combined with precipitation to influence jec13382-math-0006 . At the Austin site, the positive effect of precipitation on jec13382-math-0007 was mediated primarily by ANPP, offset by a smaller effect of leaf nitrogen content; no direct precipitation effect was detected. At the Temple site, increasing precipitation had positive direct and ANPP‐mediated effects on jec13382-math-0008 . This suggests that greater water limitation at Austin may strengthen the links between plant size and jec13382-math-0009 .
  • Synthesis. Estimates of C cycling can be improved by accounting for mediation of precipitation effects on jec13382-math-0010 by plant economics traits and plant size in resource‐limited environments.
MacQueen AH, White JW, Lee R, Osorno JM, Schmutz J, Miklas PN, Myers J, McClean PE, Juenger TE. Genetic Associations in Four Decades of Multi-Environment Trials Reveal Agronomic Trait Evolution in Common Bean. Genetics [Internet]. 2020. Publisher's VersionAbstract
Multi-environment trials (METs) are widely used to assess the performance of promising crop germplasm. Though seldom designed to elucidate genetic mechanisms, MET datasets are often much larger than could be duplicated for genetic research and, given proper interpretation, may offer valuable insights into the genetics of adaptation across time and space. The Cooperative Dry Bean Nursery (CDBN) is a MET for common bean (Phaseolus vulgaris) grown for over 70 years in the United States and Canada, consisting of 20 to 50 entries each year at 10 to 20 locations. The CBDN provides a rich source of phenotypic data across entries, years, and locations that is amenable to genetic analysis. To study stable genetic effects segregating in this MET, we conducted genome-wide association (GWAS) using best linear unbiased predictions (BLUPs) derived across years and locations for 21 CDBN phenotypes and genotypic data (1.2M SNPs) for 327 CDBN genotypes. The value of this approach was confirmed by the discovery of three candidate genes and genomic regions previously identified in balanced GWAS. Multivariate adaptive shrinkage (mash) analysis, which increased our power to detect significant correlated effects, found significant effects for all phenotypes. Mash found two large genomic regions with effects on multiple phenotypes, supporting a hypothesis of pleiotropic or linked effects that were likely selected on in pursuit of a crop ideotype. Overall, our results demonstrate that statistical genomics approaches can be used on MET phenotypic data to discover significant genetic effects and to define genomic regions associated with crop improvement.
DeLeo VL, Menge DNL, Hanks EM, Juenger TE, Lasky JR. Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana. Global Change Biology [Internet]. 2020;26 (2) :523-538. Publisher's VersionAbstract
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 its 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 or through time. For example, δ15N 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.
Bellis ES, Bhaskara GB, Juenger TE, Lasky JR. Genomics of sorghum local adaptation to a parasitic plant. PNAS [Internet]. 2020. Publisher's VersionAbstract
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 trade-offs restricting their fixation. LGS1 is thought to cause resistance by changing stereochemistry of strigolactones, hormones that control plant architecture and below-ground signaling to mycorrhizae and are required to stimulate parasite germination. Consistent with trade-offs, 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 that 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.
2019
DeLeo VL, Menge DNL, Hanks EM, Juenger TE, Lasky JR. Effects of two centuries of global environmental variation on phenology and physiology of Arabidopsis thaliana. Global Change Biology [Internet]. 2019. Publisher's VersionAbstract
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 its 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 or through time. For example, δ15N 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.
Liliia R. Abdulkina, Callie Kobayashi JTL, ...., Juenger TE, Shakirov EV. Components of the ribosome biogenesis pathway underlie establishment of telomere length set point in Arabidopsis. Nature Communications [Internet]. 2019;10 (5479). Publisher's VersionAbstract
Telomeres cap the physical ends of eukaryotic chromosomes to ensure complete DNA replication and genome stability. Heritable natural variation in telomere length exists in yeast, mice, plants and humans at birth; however, major effect loci underlying such polymorphism remain elusive. Here, we employ quantitative trait locus (QTL) mapping and transgenic manipulations to identify genes controlling telomere length set point in a multi-parent Arabidopsis thaliana mapping population. We detect several QTL explaining 63.7% of the total telomere length variation in the Arabidopsis MAGIC population. Loss-of-function mutants of the NOP2A candidate gene located inside the largest effect QTL and of two other ribosomal genes RPL5A and RPL5B establish a shorter telomere length set point than wild type. These findings indicate that evolutionarily conserved components of ribosome biogenesis and cell proliferation pathways promote telomere elongation.
Esther Singer, Jason Bonnette, Bonnette J, Woyke T, Juenger TE. Conservation of Endophyte Bacterial Community Structure Across Two Panicum Grass Species. Frontiers in Microbiology [Internet]. 2019. Publisher's VersionAbstract
Panicum represents a large genus of many North American prairie grass species. These include switchgrass (Panicum virgatum), a biofuel crop candidate with wide geographic range, as well as Panicum hallii, a close relative to switchgrass, which serves as a model system for the study of Panicum genetics due to its diploid genome and short growth cycles. For the advancement of switchgrass as a biofuel crop, it is essential to understand host microbiome interactions, which can be impacted by plant genetics and environmental factors inducing ecotype-specific phenotypic traits. We here compared rhizosphere and root endosphere bacterial communities of upland and lowland P. virgatum and P. hallii genotypes planted at two sites in Texas. Our analysis shows that sampling site predominantly contributed to bacterial community variance in the rhizosphere, however, impacted root endosphere bacterial communities much less. Instead we observed a relatively large core endophytic microbiome dominated by ubiquitously root-colonizing bacterial genera StreptomycesPseudomonas, and Bradyrhizobium. Endosphere communities displayed comparable diversity and conserved community structures across genotypes of both Panicum species. Functional insights into interactions between P. hallii and its root endophyte microbiome could hence inform testable hypotheses that are relevant for the improvement of switchgrass as a biofuel crop.
Lowry D, Lovell J, Zhang L, Bonnette J, Fay PA, Mitchell RB, Lloyd-Reilley J, Boe AR, Wu Y, Francis M. Rouquette Jr. RLW, et al. QTL × environment interactions underlie adaptive divergence in switchgrass across a large latitudinal gradient. PNAS [Internet]. 2019. Publisher's VersionAbstract
Local adaptation is the process by which natural selection drives adaptive phenotypic divergence across environmental gradients. Theory suggests that local adaptation results from genetic tradeoffs at individual genetic loci, where adaptation to one set of environmental conditions results in a cost to fitness in alternative environments. However, the degree to which there are costs associated with local adaptation is poorly understood because most of these experiments rely on two-site reciprocal transplant experiments. Here, we quantify the benefits and costs of locally adaptive loci across 17° of latitude in a four-grandparent outbred mapping population in outcrossing switchgrass (Panicum virgatum L.), an emerging biofuel crop and dominant tallgrass species. We conducted quantitative trait locus (QTL) mapping across 10 sites, ranging from Texas to South Dakota. This analysis revealed that beneficial biomass (fitness) QTL generally incur minimal costs when transplanted to other field sites distributed over a large climatic gradient over the 2 y of our study. Therefore, locally advantageous alleles could potentially be combined across multiple loci through breeding to create high-yielding regionally adapted cultivars.
Razzaque S, Elias S, Haque T, Biswas S, Jewel GMNA, Rahman S, Weng X, Ismail AM, Walia H, Juenger TE, et al. Gene Expression analysis associated with salt stress in a reciprocally crossed rice population. Scientific Reports [Internet]. 2019;9 (Article number: 8249 ). Publisher's VersionAbstract
The rice landrace Horkuch, endemic to the southern saline coast of Bangladesh, is known to have salt tolerance traits and can therefore contribute to a high yielding recipient for breeding purposes. In this study, we reciprocally crossed Horkuch with high yielding but salt sensitive IR29 to detect the complement of genes that were responsible for conferring salt tolerance versus sensitivity at the seedling developmental stage. We looked at tolerant and sensitive F3 families from individual F2 segregating plants and analyzed them for differential gene expressions using RNAseq. In general, we observed higher numbers of genes differentially expressed in leaves compared to root tissues. This included both upregulation and downregulation of gene expression across our experimental factors. Gene expression decreased in sensitive leaf after stress exposure where tolerant plants showed the opposite trend. In root, tolerant plants expression decreased at higher time points of stress exposure. We also observed a strong maternal cytoplasmic effect on gene expression and this was most evident in roots where there was upregulation in functional enrichments related to phosphorylation, electron carriers, transporter and cation transmembrane activities. Stress groups (tolerant and sensitive) response in F3 families were distinctive in both cytoplasmic backgrounds and involved uniquely upregulated genes in tolerant progenies including membrane sensor proteins, enzymes involved with signaling pathways, such as those producing trehalose and G-protein coupled receptor proteins, photosynthesis-related enzymes and golgi body recycling as well as prolamin precursor proteins involved in refolding of proteins. On the other hand, sensitivity was found to be associated with differential upregulation of only a few redox proteins and higher number of apoptosis related genes compared to the tolerant response. Overall, our highly replicated experimental design was powerful and allowed the detection of relatively subtle differential expression. Our future goal is to correlate these expression differences with QTLs in this population, which would help identify the relative importance of specific genetic loci and provide a direct avenue for combining higher levels of salt tolerance with better agronomic traits in rice.
Duszynska D, Vilhjalmsson B, Bravo RC, Swamidatta S, Juenger TE, Donoghue MTA, Comte A, Nordborg M, Sharbel TF, Brychkova G, et al. Transgenerational efects of inter‑ploidy cross direction on reproduction and F2 seed development of Arabidopsis thaliana F1 hybrid triploids. Plant Reproduction [Internet]. 2019. Publisher's VersionAbstract
The success or failure of reproductive outcomes from intra-species crosses between plants of diferent ploidy levels is an important factor in fowering plant evolution and crop breeding. However, the efects of inter-ploidy cross directions on F1 hybrid ofspring ftness are poorly understood. In Arabidopsis thaliana, hybridization between diploid and tetraploid plants can produce viable F1 triploid plants. When selfed, such F1 triploid plants act as aneuploid gamete production “machines” where the vast majority of gametes generated are aneuploid which, following sexual reproduction, can generate aneuploid swarms of F2 progeny (Henry et al. 2009). There is potential for some aneuploids to cause gametophyte abortion and/or F2 seed abortion (Henry et al. 2009). In this study, we analyse the reproductive success of 178 self-fertilized inter-accession F1 hybrid triploids and demonstrate that the proportions of aborted or normally developed F2 seeds from the selfed F1 triploids depend upon a combination of natural variation and cross direction, with strong interaction between these factors. Singleseed ploidy analysis indicates that the embryonic DNA content of phenotypically normal F2 seeds is highly variable and that these DNA content distributions are also afected by genotype and cross direction. Notably, genetically identical reciprocal F1 hybrid triploids display grandparent-of-origin efects on F2 seed set, and hence on the ability to tolerate aneuploidy in F2 seed. There are diferences between reciprocal F1 hybrid triploids regarding the proportions of normal and aborted F2 seeds generated, and also for the DNA content averages and distributions of the F2 seeds. To identify genetic variation for tolerance of aneuploidy in F2 seeds, we carried out a GWAS which identifed two SNPs, termed MOT and POT, which represent candidate loci for genetic control of the proportion of normal F2 seeds obtained from selfed F1 triploids. Parental and grandparental efects on F2 seeds obtained from selfed F1 triploids can have transgenerational consequences for asymmetric gene fow, emergence of novel genotypes in polyploid populations, and for control of F2 seed set in triploid crops.
Khasanova A, Lovell J, Bonnette J, Weng X, Jenkins J, Yoshinga Y, Schmutz J, Juenger T. The genetic architecture of shoot and root trait divergence between mesic and xeric ecotypes of a perennial grass. Frontiers in Plant Science [Internet]. 2019. Publisher's VersionAbstract
Environmental heterogeneity can drive patterns of functional trait variation and lead to the formation of locally adapted ecotypes. Plant ecotypes are often differentiated by suites of correlated root and shoot traits that share common genetic, developmental, and physiological relationships. For instance, although plant water loss is largely governed by shoot systems, root systems determine water access and constrain shoot water status. To evaluate the genetic basis of root and shoot trait divergence, we developed a recombinant inbred population derived from mesic and xeric ecotypes of the perennial grass Panicum hallii. Our study sheds light on the genetic architecture underlying the relationships between root and shoot traits. We identified several genomic ‘hotspots’ which control suites of correlated root and shoot traits, thus indicating genetic coordination between plant organ systems in the process of ecotypic divergence. Genomic regions of colocalized quantitative trait locus (QTL) for the majority of shoot and root growth related traits were independent of colocalized QTL for shoot and root resource acquisition traits. The allelic effects of individual QTL underscore ecological specialization for drought adaptation between ecotypes and reveal possible hybrid breakdown through epistatic interactions. These results have implications for understanding the factors constraining or facilitating local adaptation in plants.

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