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Schnable, J.

Publications and source records attributed to Schnable, J..

12 recordsLinked to original sources

Predicting complex phenotypes using multi-omics data in maize

Understanding and predicting complex traits in plants remains a fundamental challenge due to the emergent nature of most phenotypes and their dependence on genetic, regulatory, and environmental interactions. Accurate prediction of traits and identification of underlying genetic elements has broad applications for plant breeding, systems biology, and biotechnology. Here, we tested if multi-omic datasets could improve predictive accuracy of 129 diverse maize phenotypes across nine environments using genomic markers, field based transcriptomic data from two locations, and drone-derived phenomic data of vegetative indices. We trained and compared linear (rrBLUP) and nonlinear (support vector regression) models using single- and multi-omics inputs. Multi-omics models consistently outperformed single-omics models for most traits, with genomic and transcriptomic inputs contributing distinct biological features. Phenomic features alone yielded the lowest predictive power but improved predictions for specific trait categories like root architecture. Transcriptomic datasets enabled cross-environment prediction, demonstrating that gene expression patterns from one field site could accurately predict traits measured in another. Environment-specific expression of benchmark flowering time genes highlighted the value of transcriptomics in capturing genotype-by-environment (GxE) interactions not detectable through genomic data alone. These findings demonstrate that integrating transcriptomic and phenomic data with genotypes enhances trait prediction, improves model generalizability across environments, and provides deeper insight into the genetic and regulatory architecture of agriculturally important traits in maize.

plant biology↗

Quantitative genetics of photosynthetic trait variation in maize

Natural genetic variation in photosynthesis-related traits can aid both in identifying genes involved in regulating photosynthetic processes and developing crops with improved productivity and photosynthetic efficiency. However, rapidly fluctuating environmental parameters create challenges for measuring photosynthetic parameters in large populations under field conditions. We measured chlorophyll fluorescence and absorbance-based photosynthetic traits in a maize diversity panel in the field using an experimental design that allowed us to estimate and control multiple confounding factors. Controlling the impact of day of measurement and light intensity as well as patterns of two-dimensional spatial variation in the field substantially increased heritability with the heritability of 7 out of 14 traits measured exceeding 0.4. We were able to identify high confidence GWAS signals associated with variation in four spatially corrected traits (the quantum yield of photosystem II, non-photochemical quenching, redox state of QA, and relative chlorophyll content). Insertion alleles for Arabidopsis orthologs of three candidate genes exhibited phenotypes consistent with our GWAS results. Collectively these results illustrate the potential of applying best practices from quantitative genetics research to address outstanding questions in plant physiology and understand the mechanisms underlying natural variation in photosynthesis. Highlights[bullet] Controlling spatial and environmental confounding factors increased heritability of photosynthetic traits. [bullet]GWAS identified high confidence signals associated with variation in relative chlorophyll, {Phi}PSII, {Phi}NPQ, and qL. [bullet]Insertion alleles of the Arabidopsis orthologs of maize candidate genes exhibited photosynthesis related phenotypes consistent with the GWAS results.

plant biology↗

Sorghum Association Panel Whole-Genome Sequencing Establishes Pivotal Resource for Dissecting Genomic Diversity

Association mapping panels represent foundational resources for understanding the genetic basis of phenotypic diversity and serve to advance plant breeding by exploring genetic variation across diverse accessions with distinct histories of evolutionary divergence and local adaptation. We report the whole-genome sequencing (WGS) of 400 sorghum [Sorghum bicolor (L.) Moench] accessions from the Sorghum Association Panel (SAP) at an average coverage of 38X (25X-72X), enabling the development of a high-density genomic-marker set of 43,983,694 variants including SNPs (~ 38 million), indels (~ 5 million), and CNVs (170,000). We observe slightly more deletions among indels and a much higher prevalence of deletions among copy number variants compared to insertions. This new marker set enabled the identification of several putatively novel genomic associations for plant height and tannin content, which were not identified when using previous lower-density marker sets. WGS identified and scored variants in 5 kb bins where available genotyping-by-sequencing (GBS) data captured no variants, with half of all bins in the genome falling into this category. The predictive ability of genomic best unbiased linear predictor (GBLUP) models was increased by an average of 30% by using WGS markers rather than GBS markers. We identified 18 selection peaks across subpopulations that formed due to evolutionary divergence during domestication, and we found six Fst peaks resulting from comparisons between converted lines and breeding lines within the SAP that were distinct from the peaks associated with historic selection. This population has been and continues to serve as a significant public resource for sorghum research and demonstrates the value of improving upon existing genomic resources. Author summary

plant biology↗

Predicting transcriptional responses to cold stress across plant species

Although genome sequence assemblies are available for a growing number of plant species, gene expression responses to stimuli have been catalogued for only a subset of these species. Many genes show altered transcription patterns in response to abiotic stresses. However, orthologous genes in related species often exhibit different responses to a given stress. Accordingly, data on the regulation of gene expression in one species are not reliable predictors of orthologous gene responses in a related species. Here, we trained a supervised classification algorithm to identify genes that transcriptionally respond to cold stress. A model trained with only features calculated directly from genome assemblies exhibited only modest decreases in performance relative to models trained using genomic, chromatin, and evolution/diversity features. Models trained with data from one species successfully predicted which genes would respond to cold stress in other related species. Cross-species predictions remained accurate when training was performed in cold-sensitive species and predictions were performed in cold-tolerant species and vice versa. Models trained with data on gene expression in multiple species outperformed models trained with data from any single species. These results suggest that classifiers trained on stress data from well-studied species may suffice for predicting gene expression patterns in related, less-studied species with sequenced genomes.

plant biology↗

Voxel Carving Based 3D Reconstruction of Sorghum Identifies Genetic Determinants of Radiation Interception Efficiency

Changes in canopy architecture traits have been shown to contribute to yield increases. Optimizing both light interception and radiation use efficiency of agricultural crop canopies will be essential to meeting growing needs for food. Canopy architecture is inherently 3D, but many approaches to measuring canopy architecture component traits treat the canopy as a two dimensional structure in order to make large scale measurement, selective breeding, and gene identification logistically feasible. We develop a high throughput voxel carving strategy to reconstruct three dimensional representations of maize and sorghum from a small number of RGB photos. This approach was employed to generate three dimensional reconstructions of a sorghum association population at the late vegetative stage of development. Light interception parameters estimated from these reconstructions enabled the identification of both known and previously unreported loci controlling light interception efficiency in sorghum. The approach described here is generalizable and scalable and it enables 3D reconstructions from existing plant high throughput phenotyping datasets. For future datasets we propose a set of best practices to increase the accuracy of three dimensional reconstructions.

plant biology↗

DCT4 - a new member of the dicarboxylate transporter family in C4 grasses.

Malate transport shuttles atmospheric carbon into the Calvin-Benson cycle during NADP-ME C4 photosynthesis. Previous characterizations of several plant dicarboxylate transporters (DCT) showed that they efficiently exchange malate across membranes. Here we identify and characterize a previously unknown member of the DCT family, DCT4, in Sorghum bicolor. We show that SbDCT4 exchanges malate across membranes and its expression pattern is consistent with a role in malate transport during C4 photosynthesis. SbDCT4 is not syntenic to the characterized photosynthetic gene ZmDCT2, and an ortholog is not detectable in the maize reference genome. We found that the expression patterns of DCT family genes in the leaves of Z. mays, and S. bicolor varied by cell type. Our results suggest that sub-functionalization of members of the DCT family for the transport of malate into the bundle sheath (BS) plastids occurred during the process of independent recurrent evolution of C4 photosynthesis in grasses of the PACMAD clade. This study confirms the value of using both syntenic information and gene expression profiles to assign orthology in evolutionarily related genomes.

plant biology↗

Reconstructed protein sequence evolution consistent with the evolution of C4 photosynthesis via a C2 ancestor in the Paniceae

The grass tribe Paniceae includes a monophyletic subclade of species, the MPC clade, which specialize in each of the three primary C4 sub-pathways NADP-ME, NAD-ME and PCK. The evolutionary history of C4 photosynthesis in this subclade remains ambiguous. Leveraging newly sequenced grass genomes and syntenic orthology data, we estimated rates of protein sequence evolution on ancestral branches for both core enzymes shared across different C4 sub-pathways and enzymes specific to C4 sub-pathways. While core enzymes show elevated rates of protein sequence evolution in ancestral branches consistent with a transition from C3 to C4 photosynthesis in the ancestor for this clade, no subtype specific enzymes showed similar patterns. At least one protein involved in photorespiration also showed elevated rates of protein sequence evolution in the ancestral branch. The set of core C4 enzymes examined here combined with the photorespiratory pathway are necessary for the C2 photosynthetic cycle, a previously proposed intermediate between C3 and C4 photosynthesis. The patterns reported here are consistent with, but not conclusive proof that, C4 photosynthesis in the MPC clade of the Paniceae evolved via a C2 intermediate.

plant biology↗

IsoSeq transcriptome assembly of C3 panicoid grasses provides tools to study evolutionary change in the Panicoideae

The number of plant species with genomic and transcriptomic data has been increasing rapidly. The grasses - Poaceae - have been well represented among species with published reference genomes. However, as a result the genomes of wild grasses are less frequently targeted by sequencing efforts. Sequence data from wild relatives of crop species in the grasses can aid the study of domestication, gene discovery for breeding and crop improvement, and improve our understanding of the evolution of C4 photosynthesis. Here we used long read sequencing technology to characterize the transcriptomes of three C3 panicoid grass species: Dichanthelium oligosanthes, Chasmanthium laxum, and Hymenachne amplexicaulis. Based on alignments to the sorghum genome we estimate that assembled consensus transcripts from each species capture between 54.2 and 65.7% of the conserved syntenic gene space in grasses. Genes co-opted into C4 were also well represented in this dataset, despite concerns that, because these genes might play roles unrelated to photosynthesis in the target species, they would be expressed at low levels and missed by transcript-based sequencing. A combined analysis using syntenic orthologous genes from grasses with published reference genomes and consensus long read sequences from these wild species was consistent with previously published phylogenies. It is hoped that this data, targeting under represented classes of species within the PACMAD grasses - wild species and species utilizing C3 photosynthesis - will aid in futurue studies of domestication and C4 evolution by decreasing the evolutionary distance between C4 and C3 species within this clade, enabling more accurate comparisons associated with evolution of the C4 pathway.

plant biology↗

Distinct characteristics of genes associated with phenome-wide variation in maize (Zea mays)

Naturally occurring functionally variable alleles in specific genes within a population allows the identification of which genes are involved in the determination of which phenotypes. The omnigenetic model proposes that essentially all genes which are expressed in relevant contexts likely play some role in determining phenotypic outcomes. Here, we develop an approach to identify genes where natural functional variation plays a role in shaping many phenotypic traits simultaneously. We demonstrate that this approach identifies a distinct set of genes relative to conventional genome wide association using data for 260 traits scored a maize diversity panel, and the genes identified using this approach are more likely to be independently validated than genes identified by convetional genome wide association. Genes identified by the new approach share a number of features with a gold standard set of genes characterized through forward genetics which separate them from both genes identified by conventional genome wide association and the overall population of annotated gene models. These features include evidence of significantly stronger purifying selection, positional conservation across the genomes of related species, greater length, and a scarcity of presence absence variation for these loci in natural populations. Genes identified by phenome-wide analyses also showed much stronger signals of GO enrichment and purification than genes identified by conventional genome wide association. Overall these findings are consistent with large subset of annotated gene models - despite support from transcriptional and homology evidence - being unlikely to play any role in determining organismal phenotypes.

bioinformatics↗

Functional Modeling of Plant Growth Dynamics

Recent advances in automated plant phenotyping have enabled the collection time series measurements from the same plants of a wide range of traits over different developmental time scales. The availability of time series phenotypic datasets has increased interest in statistical approaches for comparing patterns of change between different plant genotypes and different treatment conditions. Two widely used methods of modeling growth over time are point-wise analysis of variance (ANOVA) and parametric sigmoidal curve fitting. Point-wise ANOVA yields discontinuous growth curves, which do not reflect the true dynamics of growth patterns in plants. In contrast, fitting a parametric model to a time series of observations does capture the trend of growth, however these models require assumptions regarding the true pattern of plant growth. Depending on the species, treatment regime, and subset of the plant lifecycle sampled this assumptions will not always hold true. Here we introduce a different approach - functional ANOVA - which yields continuous growth curves without requiring assumptions regarding patterns of plant growth. We compare and validate this approach using data from an experiment measuring growth of two maize (Zea mays ssp. mays) genotypes under two water availability treatments over a 21-day period. Functional ANOVA enables a nonparametric estimation of the dynamics of changes in plant traits over time without assumptions regarding curve shape. In addition to estimating smooth curves of trait values over time, functional ANOVA also estimates the the derivatives of these curves - e.g. growth rates - simultaneously. Using two different subsampling strategies, we demonstrate that this functional ANOVA method enables the comparison of growth curves between plants phenotyped on non-overlapping days with little reduction in estimation accuracy. This means functional ANOVA based approaches can allow larger numbers of samples and biological replicates to be scored in a single experiment given fixed amounts of phenotyping infrastructure and personnel.

plant biology↗

Largely unlinked gene sets targeted by selection for domestication syndrome phenotypes in maize and sorghum

The domestication of diverse grain crops from wild grasses resulted from artificial selection for a suite of overlapping traits producing changes referred to in aggregate as \"domestication syndrome\". Parallel phenotypic change can be accomplished by either selection on orthologous genes, or selection on non-orthologous genes with parallel phenotypic effects. To determine how often artificial selection for domestication traits in the grasses targeted orthologous genes, we employed resequencing data from wild and domesticated accessions of Zea (maize) and Sorghum (sorghum). Many \"classic\" domestication genes identified through QTL mapping in populations resulting from wild/domesticated crosses indeed show signatures of parallel selection in both maize and sorghum. However, the overall number of genes showing signatures of parallel selection in both species is not significantly different from that expected by chance. This suggests that, while a small number of genes will extremely large phenotypic effects have been targeted repeatedly by artificial selection during domestication, the optimization portion of domestication targeted small and largely non-overlapping subsets of all possible genes which could produce equivalent phenotypic alterations.

plant biology↗

STAG-CNS: An Order-Aware Conserved Non-coding Sequences Discovery Tool For Arbitrary Numbers of Species

One method for identifying noncoding regulatory regions of a genome is to quantify rates of divergence between related species, as functional sequence will generally diverge more slowly. Most approaches to identifying these conserved noncoding sequences (CNS) based on alignment have had relatively large minimum sequence lengths ([>=]15 base pair) compared to the average length of known transcription factor binding sites. To circumvent this constraint, STAG-CNS integrates data from the promoters of conserved orthologous genes in three or more species simultaneously. Using data from up to six grass species made it possible to identify conserved sequences as short at 9 base pairs with FDP [<=] 0.05. These CNS exhibit greater overlap with open chromatin regions identified using DNase I hypersensitivity, and are enriched in the promoters of genes involved in transcriptional regulation. STAG-CNS was further employed to characterize loss of conserved noncoding sequences associated with retained duplicate genes from the ancient maize polyploidy. Genes with fewer retained CNS show lower overall expression, although this bias is more apparent in samples of complex organ systems containing many cell types, suggesting CNS loss may correspond to a reduced number of expression contexts rather than lower expression levels across the entire ancestral expression domain.

bioinformatics↗