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Exome resequencing and GWAS for growth, ecophysiology, and chemical and metabolomic composition of wood of Populus trichocarpa
Populus trichocarpa is an important forest tree species for the generation of lignocellulosic ethanol. Understanding the genomic basis of biomass production and chemical composition of wood is fundamental in supporting genetic improvement programs. Considerable variation has been observed in this species for complex traits related to growth, phenology, ecophysiology and wood chemistry. Those traits are influenced by both polygenic control and environmental effects, and their genome architecture and regulation are only partially understood. Genome wide association studies (GWAS) represent an approach to advance that aim using thousands of single nucleotide polymorphisms (SNPs). Genotyping using exome capture methodologies represent an efficient approach to identify specific functional regions of genomes underlying phenotypic variation. We identified 813 K SNPs, which were utilized for genotyping 461 P. trichocarpa clones, representing 101 provenances collected from Oregon and Washington, and established in California. A GWAS performed on 20 traits, considering single SNP-marker tests identified a variable number of significant SNPs ( p -value < 6.1479E-8) in association with diameter, height, leaf carbon and nitrogen contents, and δ 15 N. The number of significant SNPs ranged from 2 to 220 per trait. Additionally, multiple-marker analyses by sliding-windows tests detected between 6 and 192 significant windows for the analyzed traits. The significant SNPs resided within genes that encode proteins belonging to different functional classes as such protein synthesis, energy/metabolism and DNA/RNA metabolism, among others. SNP-markers within genes associated with traits of importance for biomass production were detected. They contribute to characterize the genomic architecture of P. trichocarpa biomass required to support the development and application of marker breeding technologies.
Novel candidate genes for lignin structure identified through genome-wide association study of naturally varying Populus trichocarpa
Populus is a promising lignocellulosic feedstock for biofuels and bioproducts. However, the cell wall biopolymer lignin is a major barrier in conversion of biomass to biofuels. To investigate the variability and underlying genetic basis of the complex structure of lignin, a population of 409 three-year-old, naturally varying Populus trichocarpa genotypes were characterized by heteronuclear single quantum coherence (HSQC) nuclear magnetic resonance (NMR). A subsequent genome-wide association study (GWAS) was conducted using approximately 8.3 million single nucleotide polymorphisms (SNPs), which identified 756 genes that were significantly associated (−log 10 ( p -value)>6) with at least one lignin phenotype. Several promising candidate genes were identified, many of which have not previously been reported to be associated with lignin or cell wall biosynthesis. These results provide a resource for gaining insights into the molecular mechanisms of lignin biosynthesis and new targets for future genetic improvement in poplar.
Chronic drought differentially alters the belowground microbiome of drought tolerant and drought susceptible genotypes of Populus trichocarpa
Populus trichocarpa is an ecologically important tree species and economically important biofeedstock. Belowground, P. trichocarpa interacts with diverse microorganisms in the rhizosphere and root endosphere. These plant-microbial interactions can bolster a variety of plant processes, ranging from pathogen suppression to drought tolerance, yet we know little about the impact of chronic drought stress on P. trichocarpa’s belowground microbiomes. To investigate the interactive effect of chronic drought on belowground microbial communities across genetically different P. trichocarpa hosts, we assessed archaeal/bacterial and fungal communities within the root endosphere, rhizosphere, and surrounding bulk soil of selected genotypes in a long-term drought experiment in Boardman, OR, USA. We sequenced the 16S rRNA and ITS2 gene region on samples collected from 16 distinct P. trichocarpa genotypes in plots with full or reduced irrigation. Eight of these genotypes have been previously identified as drought tolerant while the other eight genotypes were drought susceptible. While reduced irrigation influenced the composition of every archaeal/bacterial microbiome compartment, fungal communities were only affected in the rhizosphere and bulk soil compartments. Drought-tolerant bacteria, such as Actinobacteria, were differentially abundant in reduced irrigation across all belowground microbiomes. Host drought-tolerance influenced plant-associated microbiome compartments but had little impact on the bulk soil compartment. Drought-tolerant trees were enriched for potential growth-promoting microorganisms in the root endosphere and rhizosphere, including Sphingomonas bacteria and ectomycorrhizal fungi. Overall, associations of growth-promoting microbes in drought resistant P. trichocarpa genotypes can be leveraged to improve biofeedstock productivity in regions prone to periodic drought.
Populus trichocarpa and Populus deltoides Exhibit Different Metabolomic Responses to Colonization by the Symbiotic fungus Laccaria bicolor
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Significance of Lignin S/G Ratio in Biomass Recalcitrance of Populus trichocarpa Variants for Bioethanol Production
Lignin S/G ratio has been investigated as an important factor in biomass recalcitrance to bioethanol production. Because of the complexity and variety of biomass, recalcitrance was also reportedly influenced by several other factors, such as total lignin content, degree of cellulose polymerization, etc. In addition, the effect of S/G ratio on biomass conversion is not uniform across plant species. Herein, 11 Populus trichocarpa natural variants grown under the same conditions with similar total lignin content were selected to minimize the effects of other factors. The lignin S/G ratio of the selected P. trichocarpa natural variants showed negative correlations with p-hydroxybenzoate (PB) and ..beta..-5 linkage contents, while it had positive ones with ..beta..-O-4 linkage, lignin molecular weight, and ethanol production. This study showed the importance of lignin S/G ratio as an independent recalcitrance factor that may aid future energy crop engineering and biomass conversion strategies.
Identification of quantitative trait loci affecting ectomycorrhizal symbiosis in an interspecific F1 poplar cross and differential expression of genes in ectomycorrhizas of the two parents: Populus deltoides and Populus trichocarpa
A Populus deltoides Populus trichocarpa F1 pedigree was analyzed for quantitative trait loci (QTLs) affecting ectomycorrhizal development and for microarray characterization of gene networks involved in this symbiosis. A 300 genotype progeny set was evaluated for its ability to form ectomycorrhiza with the basidiomycete Laccaria bicolor. The percentage of mycorrhizal root tips was determined on the root systems of all 300 progeny and their two parents. QTL analysis identified four significant QTLs, one on the P. deltoides and three on the P. trichocarpa genetic maps. These QTLs were aligned to the P. trichocarpa genome and each contained several megabases and encompass numerous genes. NimbleGen whole-genome microarray, using cDNA from RNA extracts of ectomycorrhizal root tips from the parental genotypes P. trichocarpa and P. deltoides, was used to narrow the candidate gene list. Among the 1,543 differentially expressed genes (p value 0.05; 5.0-fold change in transcript level) having different transcript levels in mycorrhiza of the two parents, 41 transcripts were located in the QTL intervals: 20 in Myc_d1, 14 in Myc_t1, and seven in Myc_t2, while no significant differences among transcripts were found in Myc_t3. Among these 41 transcripts, 25 were overrepresented in P. deltoides relative to P. trichocarpa; 16 were overrepresented in P. trichocarpa. The transcript showing the highest overrepresentation in P. trichocarpa mycorrhiza libraries compared to P. deltoides mycorrhiza codes for an ethylene-sensitive EREBP-4 protein which may repress defense mechanisms in P. trichocarpa while the highest overrepresented transcripts in P. deltoides code for proteins/genes typically associated with pathogen resistance.
Insights of biomass recalcitrance in natural Populus trichocarpa variants for biomass conversion
Populus has been investigated as a promising biomass feedstock for alternative fuels and chemicals. Physicochemical characteristics and genomic information of biomass feedstocks are among the essential information that can help not only advance our understanding of biomass recalcitrance but also in its efficient utilization. Here in this paper, the recalcitrance of natural Populus variants was elucidated in three aspects: (1) sugar release, (2) physicochemical properties, and (3) relative variation of gene expression within natural poplar variants. The sugar release performance of natural Populus variants was evaluated with their correlation with biomass recalcitrance-related characteristics. Among the physicochemical properties of poplar, the lignin content, lignin molecular weight, lignin S/G ratio, and cellulose accessibility were found to correlate with sugar release. The results demonstrated that the lignin content was negatively correlated with sugar release, whereas the lignin molecular weight, lignin S/G ratio, and cellulose accessibility were positively associated with poplar sugar release. The trend of differential gene expression of each variant also supports the characterization results and their effects on biomass conversion.
Enhancing a Pathway-Genome Database (PGDB) to capture subcellular localization of metabolites and enzymes: the nucleotide-sugar biosynthetic pathways of Populus trichocarpa
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Association Genetics of Populus trichocarpa or Resequencing in Populus: Towards Genome Wide Association Genetics (2011 JGI User Meeting)
The U.S. Department of Energy Joint Genome Institute (JGI) invited scientists interested in the application of genomics to bioenergy and environmental issues, as well as all current and prospective users and collaborators, to attend the annual DOE JGI Genomics of Energy Environment Meeting held March 22-24, 2011 in Walnut Creek, Calif. The emphasis of this meeting was on the genomics of renewable energy strategies, carbon cycling, environmental gene discovery, and engineering of fuel-producing organisms. The meeting features presentations by leading scientists advancing these topics. Gerry Tuskan of Oak Ridge National Laboratory on Resequencing in Populus: Towards Genome Wide Association Genetics at the 6th annual Genomics of Energy Environment Meeting on March 23, 2011.
Fungal Pretreatment and Enzymatic Hydrolysis of Genetically-Modified Populus trichocarpa
Fungal pretreatment of Populus trichocarpa wood genetically modified to reduce lignin and alter lignin chemistry is investigated for its effectiveness as an alternative to common pretreatment methods. The goal of this work is to improve biomass utilization for biofuel and biochemical applications by increasing sugar release. Sugar release after enzymatic hydrolysis was measured after various biomass pretreatments (including wood-rot fungus, hot water, and dilute acid). In the wildtype, and in constructs downregulated in PAL, 4CL, and C3H, the fungal pretreatment resulted in substantial improvements in sugar yields, up to 2.4-fold increase in glucose yield and 6-fold increase in xylose yield after enzymatic hydrolysis compared to the unpretreated control. However, the effects of fungal pretreatment were inconsistent, and in genetic lines down-regulated in 4CL, CCoAOMT, CAld5H, and C3H, fungal pretreatment yielded similar or decreased sugar release after enzymatic hydrolysis.
Physicochemical Changes of Cellulose and Their Influences on Populus trichocarpa Digestibility after Different Pretreatments
Pretreatment is commonly used to reduce recalcitrance of the lignin-carbohydrate matrix. In this study, leading pretreatment technologies, including dilute sulfuric acid, liquid hot water, alkaline, and organosolv pretreatments, were applied to the selected Populus trichocarpa genotype with relatively low lignin content to elucidate cellulose physicochemical property changes and digestibility-related factors. Pretreated Populus trichocarpa (BESC 131) exhibited higher accessibility and glucose yield than the untreated biomass. Chemical composition and Fourier transform infrared (FTIR) analysis results revealed that hemicellulose and lignin were removed to a varying extent depending on the pretreatment techniques applied. Here, the degree of polymerization of the cellulose was decreased to the largest extent after dilute acid pretreatment, followed by organosolv, alkaline, and liquid hot water pretreatments. Cellulose crystallinity index was slightly changed after the pretreatments; however, its differences were not remarkable between those pretreatment techniques. Among four different pretreatments, organosolv was the most effective pretreatment technology in terms of sugar release, which was three times higher than that of the untreated native biomass. Among all of the tested cell wall traits, the lignin content of Populus trichocarpa was the most remarkable feature associated with glucose release, though Populus trichocarpa recalcitrance was not solely dependent on any single factor.
Expanded genetic variation (SNP) and phenomics (image based) dataset for Populus trichocarpa
The image dataset consists of 11,791 images representing 1,219 genotypes of Populus trichocarpa undergoing in planta regeneration. Genotypes were imaged with a median of four weekly timepoints and a median of two replicates each. A representative and diverse subset of 249 images was annotated using the IDEAS annotation interface (ideas.eecs.oregonstate.edu) and these annotated images were used to train a deep semantic segmentation model (PSPNet), which was deployed for inference over the entire dataset. Annotated classes include specific stages of regeneration (callus and shoot) in addition to unregenerated plant material and background. Statistics of relative tissue area were extracted and used for downstream genetic association mapping in a genome-wide association study. The SNP dataset consists of over 40 million single-nucleotide polymorphisms across 1,323 wild accessions of Populus trichocarpa
Correlating laser-induced breakdown spectroscopy with neutron activation analysis to determine the elemental concentration in the ionome of the Populus trichocarpa leaf
The black cottonwood poplar (Populus trichocarpa) leaf ionome (inorganic trace elements and mineral nutrients) is an important aspect for determining the physiological and developmental processes contributing to biomass production. A number of techniques are used to measure the ionome, yet characterizing the leaf spatial heterogeneity remains a challenge, especially in solid samples. Laser-induced breakdown spectroscopy (LIBS) has been used to determine the elemental composition of leaves and is able to raster across solid matrixes at 10 μm resolution. Here, we evaluate the use of LIBS for solid sample leaf elemental characterization in relation to neutron activation. In fact, neutron activation analysis is a laboratory-based technique which is used by the National Institute of Standards and Technology (NIST) to certify trace elements in candidate reference materials including plant leaf matrices. Introduction to the techniques used in this research has been presented in this manuscript. Neutron activation analysis (NAA) data has been correlated to the LIBS spectra to achieve quantification of the elements or ions present within poplar leaves. The regression coefficients of calibration and validation using multivariate analysis (MVA) methodology for six out of seven elements have been determined and vary between 0.810 and 0.998. LIBS and NAA data has been presented for the elements such as, calcium, magnesium, manganese, aluminum, copper, and potassium. Chlorine was also detected but it did not show good correlation between the LIBS and NAA techniques. This research shows that LIBS can be used as a fast, high-spatial resolution technique to quantify elements as part of large-scale field phenotyping projects.
Corresponding Standard Reference Material Data used in Partial Least Squares Regression Models for Sugar Composition Estimates in Biomass in: Economic Impact of Yield and Composition Variation in Bioenergy Crops: Populus trichocarpa
Corresponding Standard Reference Material Data used in Partial Least Squares Regression Models for Sugar Composition Estimates in Biomass in: Economic Impact of Yield and Composition Variation in Bioenergy Crops: Populus trichocarpa (for corresponding manuscript: DOI: 10.1002/bbb.2148) PDF Files: Images of 1H NMR spectra for neutralized 2-stage acid hydrolysates of 4 NIST Standard Reference Material biomass samples (Monterey Pine 8493, Sugarcane Bagasse 8491, Wheat Straw 8494, and Eastern Cottonwood/Poplar 8492) and 2 Center for Bioenergy Innovation reference biomass samples (Poplar - Populus trichocarpa and Switchgrass - Panicum Virgatum). Suppression of the water peak was achieved using a NOESY-1D with presaturation, a recycle delay of 5 s, and a total of 64 scans. Spectra were acquired at 298 K and processed with automatic phase correction, baseline correction, and chemical shift referencing to TSP-d4. Images show all 1H data from 10 to 1ppm with inset spectra of region of interest (4.0 to 3.1 ppm). Text Files: Spectra for neutralized 2-stage acid hydrolysates of 4 NIST Standard Reference Material biomass samples (Monterey Pine 8493, Sugarcane Bagasse 8491, Wheat Straw 8494, and Eastern Cottonwood/Poplar 8492) and 2 Center for Bioenergy Innovation reference biomass samples (Poplar - Populus trichocarpa and Switchgrass - Panicum Virgatum) were converted into text files for plotting. Files contain 8192 points of raw spectral data from 12.23 to -2.78 ppm. The text file contains 4 columns of data and includes: Point number, Intensity, Hz, and ppm. Xcel Spreadsheet: HPLC measured monomeric sugar concentrations and bucketed 1H NMR data used to build monomeric sugar composition prediction models. Sugar composition in biomass determined from HPLC analyses are given in mg sugar/mg of biomass. Spectral bucketing was performed using Bruker’s AMIX software. Spectra were divided into 0.005 ppm buckets in the region of 3.10– 4.15 ppm for a total of 210 buckets. Headers for the bucketed data are the chemical shift in ppm of the center of the bucket. Bucketed data was used to build partial least squares models for subsequent predictions in The Unscrambler v. 10.5(CAMO A/S, Trondheim, Norway). The formation of methanol during hydrolysis interferes with the quantitative NMR analysis of sugars, so the methanol peak centered at 3.37 ppm and spanning four buckets (3.2925 – 3.2775 ppm) was set to zero for all spectra.
Telomere-to-telomere assemblies of chromosome 10 reveal complex adaptive variation of 3-ketoacyl-CoA-synthases in Populus trichocarpa likely driven by Helitrons
The model woody plant Populus trichocarpa displays an atypical alkene-diverse wax cuticle likely driven by copy number variation (CNV) of 3-ketoacyl-CoA synthases ( KCS ), which has been difficult to confirm with short-read assemblies. Long-read sequencing enables the development of telomere-to-telomere resources to detect cryptic variation, including CNVs, which are currently missed. Integrating this information can improve genomic prediction for breeding and provide insights into the evolutionary basis of important traits. Our analysis of 78 long-read haplotypes from chromosome 10 identified more than twice as many KCS genes as previously reported, and numerous intragenic non-synonymous substitutions. Random Forest predictive models highlighted the importance of Potri.010G079500 in producing very long chain alkenes; however, its absence did not predict previously reported alkene-deficient phenotypes. Instead, alkene levels are best predicted by the combinations of KCS copies. Additionally, amino acid substitutions clustered around ligand and donor binding pockets, suggesting they contribute to differing wax cuticle composition. Finally, each KCS gene and copy was linked to a Helitron transposon. A phylogenetic analysis suggests Helitrons are the evolutionary mechanism for generating KCS tandem arrays. Long-read generated telomere-to-telomere assemblies of P. trichocarpa chromosome 10 revealed large-effect loci critical to genetic studies that are unattainable from short-reads. This new resource produced novel insights into genome structure and function, and a novel mechanism for generating tandem gene duplication. Our results highlight that, given current challenges in annotation and assembly, detailed and focused long-read sequences are key to interpreting complex genomic regions that contain tandem copy number variants.
Populus_trichocarpa_Breeding_Population_SNPs
These data are from the manuscript “Application of Genomic Prediction in a Populus trichocarpa Breeding Program”, by Brian J. Stanton, David Macaya-Sanz, Chanaka Roshan Abeyratne, David Kainer, Kathy Haiby, Austin Himes, Carlos Gantz, Gerald A. Tuskan, and Stephen P. DiFazio. The data are based on genome resequencing to approximately 10X depth on two collections of Populus trichocarpa trees from Oregon, Washington, California, and British Columbia. The first collection consists of 293 genets collected by Poplar Innovations LLC for a breeding program. The second collection consists of 961 trees collected for the purpose of genome-wide association studies. These genets were sequenced using short, paired-end Illumina sequence reads (Chhetri et al. 2019). Reads were aligned to the P. trichocarpa ′Stettler-14′ reference (Hofmeister et al. 2020), with minor modifications to correct mis-assemblies (Zhou et al. 2020), and variants were called as per methods described in (Abeyratne et al. 2023). Identified variants were filtered using GATK’s VariantFiltration tool (DePristo et al. 2011), with filter expression flag set to “AF < 0.01 || AF > 0.99 || QD < 10.0 || ExcessHet > 20.0 || FS > 10.0 || MQ < 58.0”. SNPs with severe departures from Hardy−Weinberg expectations (exact-test p< 0.01) were also removed using vcftools --hwe flag (Danecek et al. 2011), resulting in 15,627,211 bi-allelic SNPs. The data included here consist of 141,903 high quality bi-allelic genome-wide SNPs obtained by further filtering the original SNP dataset using vcftools with flags --maf 0.05, --max-maf 0.95, --max-missing 0.95, --min-meanDP 10.75, --max-meanDP 43.00, --thin 2000. Collectively, these filtering parameters removed SNPs with 1) a minor allele frequency ≤ 0.05; 2) proportion of missing data for individual loci exceeding 5%; 3) sequencing depth more than 2X mean-depth or less than 0.5X mean-depth; or 4) a distance of