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1.
Proc Natl Acad Sci U S A ; 120(10): e2216894120, 2023 03 07.
Article in English | MEDLINE | ID: mdl-36848555

ABSTRACT

Drought tolerance is a highly complex trait controlled by numerous interconnected pathways with substantial variation within and across plant species. This complexity makes it difficult to distill individual genetic loci underlying tolerance, and to identify core or conserved drought-responsive pathways. Here, we collected drought physiology and gene expression datasets across diverse genotypes of the C4 cereals sorghum and maize and searched for signatures defining water-deficit responses. Differential gene expression identified few overlapping drought-associated genes across sorghum genotypes, but using a predictive modeling approach, we found a shared core drought response across development, genotype, and stress severity. Our model had similar robustness when applied to datasets in maize, reflecting a conserved drought response between sorghum and maize. The top predictors are enriched in functions associated with various abiotic stress-responsive pathways as well as core cellular functions. These conserved drought response genes were less likely to contain deleterious mutations than other gene sets, suggesting that core drought-responsive genes are under evolutionary and functional constraints. Our findings support a broad evolutionary conservation of drought responses in C4 grasses regardless of innate stress tolerance, which could have important implications for developing climate resilient cereals.


Subject(s)
Sorghum , Zea mays , Zea mays/genetics , Sorghum/genetics , Droughts , Edible Grain/genetics , Poaceae
2.
Theor Appl Genet ; 135(1): 273-290, 2022 Jan.
Article in English | MEDLINE | ID: mdl-34661697

ABSTRACT

KEY MESSAGE: Two read depth methods were jointly used in next-generation sequencing data to identify deletions in maize population. GWAS by deletions were analyzed for gene expression pattern and classical traits, respectively. Many studies have confirmed that structural variation (SV) is pervasive throughout the maize genome. Deletion is one type of SV that may impact gene expression and cause phenotypic changes in quantitative traits. In this study, two read count approaches were used to analyze the deletions in the whole-genome sequencing data of 270 maize inbred lines. A total of 19,754 deletion windows overlapped 12,751 genes, which were unevenly distributed across the genome. The deletions explained population structure well and correlated with genomic features. The deletion proportion of genes was determined to be negatively correlated with its expression. The detection of gene expression quantitative trait loci (eQTL) indicated that local eQTL were fewer but had larger effects than distant ones. The common associated genes were related to basic metabolic processes, whereas unique associated genes with eQTL played a role in the stress or stimulus responses in multiple tissues. Compared with the eQTL detected by SNPs derived from the same sequencing data, 89.4% of the associated genes could be detected by both markers. The effect of top eQTL detected by SNPs was usually larger than that detected by deletions for the same gene. A genome-wide association study (GWAS) on flowering time and plant height illustrated that only a few loci could be consistently captured by SNPs, suggesting that combining deletion and SNP for GWAS was an excellent strategy to dissect trait architecture. Our findings will provide insights into characteristic and biological function of genome-wide deletions in maize.


Subject(s)
Gene Deletion , Genetic Variation , Genome, Plant , Zea mays/genetics , Genome-Wide Association Study , Polymorphism, Single Nucleotide , Quantitative Trait Loci , Whole Genome Sequencing , Zea mays/physiology
3.
G3 (Bethesda) ; 11(2)2021 02 09.
Article in English | MEDLINE | ID: mdl-33604670

ABSTRACT

Gene expression links genotypes to phenotypes, so identifying genes whose expression is shaped by selection will be important for understanding the traits and processes underlying local adaptation. However, detecting local adaptation for gene expression will require distinguishing between divergence due to selection and divergence due to genetic drift. Here, we adapt a QST-FST framework to detect local adaptation for transcriptome-wide gene expression levels in a population of diverse maize genotypes. We compare the number and types of selected genes across a wide range of maize populations and tissues, as well as selection on cold-response genes, drought-response genes, and coexpression clusters. We identify a number of genes whose expression levels are consistent with local adaptation and show that genes involved in stress response show enrichment for selection. Due to its history of intense selective breeding and domestication, maize evolution has long been of interest to researchers, and our study provides insight into the genes and processes important for in local adaptation of maize.


Subject(s)
Selection, Genetic , Zea mays , Adaptation, Physiological , Genetic Drift , Transcriptome , Zea mays/genetics
4.
BMC Genomics ; 21(1): 689, 2020 Oct 06.
Article in English | MEDLINE | ID: mdl-33023467

ABSTRACT

BACKGROUND: MiRNAs play essential roles in plant development and response to biotic and abiotic stresses through interaction with their target genes. The expression level of miRNAs shows great variations among different plant accessions, developmental stages, and tissues. Little is known about the content within the plant genome contributing to the variations in plants. This study aims to identify miRNA expression-related quantitative trait loci (miR-QTLs) in the maize genome. RESULTS: The miRNA expression level from next generation sequencing (NGS) small RNA libraries derived from mature leaf samples of the maize panel (200 maize lines) was estimated as phenotypes, and maize Hapmap v3.2.1 was chosen as the genotype for the genome-wide association study (GWAS). A total of four significant miR-eQTLs were identified contributing to miR156k-5p, miR159a-3p, miR390a-5p and miR396e-5p, and all of them are trans-eQTLs. In addition, a strong positive coexpression of miRNA was found among five miRNA families. Investigation of the effects of these miRNAs on the expression levels and target genes provided evidence that miRNAs control the expression of their targets by suppression and enhancement. CONCLUSIONS: These identified significant miR-eQTLs contribute to the diversity of miRNA expression in the maize penal at the developmental stages of mature leaves in maize, and the positive and negative regulation between miRNA and its target genes has also been uncovered.


Subject(s)
MicroRNAs/genetics , Quantitative Trait Loci , Zea mays/genetics , Gene Expression Regulation, Plant , Genome-Wide Association Study/methods , MicroRNAs/metabolism , Plant Leaves/genetics , Plant Leaves/metabolism
5.
Nat Plants ; 6(11): 1375-1388, 2020 11.
Article in English | MEDLINE | ID: mdl-33106639

ABSTRACT

Specialized metabolites constitute key layers of immunity that underlie disease resistance in crops; however, challenges in resolving pathways limit our understanding of the functions and applications of these metabolites. In maize (Zea mays), the inducible accumulation of acidic terpenoids is increasingly considered to be a defence mechanism that contributes to disease resistance. Here, to understand maize antibiotic biosynthesis, we integrated association mapping, pan-genome multi-omic correlations, enzyme structure-function studies and targeted mutagenesis. We define ten genes in three zealexin (Zx) gene clusters that encode four sesquiterpene synthases and six cytochrome P450 proteins that collectively drive the production of diverse antibiotic cocktails. Quadruple mutants in which the ability to produce zealexins (ZXs) is blocked exhibit a broad-spectrum loss of disease resistance. Genetic redundancies ensuring pathway resiliency to single null mutations are combined with enzyme substrate promiscuity, creating a biosynthetic hourglass pathway that uses diverse substrates and in vivo combinatorial chemistry to yield complex antibiotic blends. The elucidated genetic basis of biochemical phenotypes that underlie disease resistance demonstrates a predominant maize defence pathway and informs innovative strategies for transferring chemical immunity between crops.


Subject(s)
Anti-Bacterial Agents/biosynthesis , Disease Resistance/genetics , Immunity, Innate/genetics , Metabolic Networks and Pathways/genetics , Zea mays/genetics , Disease Resistance/physiology , Gene Expression Profiling , Genes, Plant/genetics , Genes, Plant/physiology , Metabolomics , Multigene Family/genetics , Multigene Family/physiology , Proteomics , Zea mays/immunology , Zea mays/metabolism , Zea mays/microbiology
6.
Nat Plants ; 5(10): 1043-1056, 2019 10.
Article in English | MEDLINE | ID: mdl-31527844

ABSTRACT

Duplication and divergence of primary pathway genes underlie the evolution of plant specialized metabolism; however, mechanisms partitioning parallel hormone and defence pathways are often speculative. For example, the primary pathway intermediate ent-kaurene is essential for gibberellin biosynthesis and is also a proposed precursor for maize antibiotics. By integrating transcriptional coregulation patterns, genome-wide association studies, combinatorial enzyme assays, proteomics and targeted mutant analyses, we show that maize kauralexin biosynthesis proceeds via the positional isomer ent-isokaurene formed by a diterpene synthase pair recruited from gibberellin metabolism. The oxygenation and subsequent desaturation of ent-isokaurene by three promiscuous cytochrome P450s and a new steroid 5α reductase indirectly yields predominant ent-kaurene-associated antibiotics required for Fusarium stalk rot resistance. The divergence and differential expression of pathway branches derived from multiple duplicated hormone-metabolic genes minimizes dysregulation of primary metabolism via the circuitous biosynthesis of ent-kaurene-related antibiotics without the production of growth hormone precursors during defence.


Subject(s)
Diterpenes, Kaurane/metabolism , Genes, Plant , Plant Growth Regulators/genetics , Zea mays/genetics , Ascomycota , Cytochrome P-450 Enzyme System/metabolism , Disease Resistance/genetics , Genome-Wide Association Study , Gibberellins/metabolism , Metabolic Networks and Pathways/genetics , Plant Diseases/immunology , Plant Diseases/microbiology , Zea mays/immunology , Zea mays/metabolism , Zea mays/microbiology
7.
G3 (Bethesda) ; 9(9): 3023-3033, 2019 09 04.
Article in English | MEDLINE | ID: mdl-31337639

ABSTRACT

Modern improvement of complex traits in agricultural species relies on successful associations of heritable molecular variation with observable phenotypes. Historically, this pursuit has primarily been based on easily measurable genetic markers. The recent advent of new technologies allows assaying and quantifying biological intermediates (hereafter endophenotypes) which are now readily measurable at a large scale across diverse individuals. The usefulness of endophenotypes for delineating the regulatory landscape of the genome and genetic dissection of complex trait variation remains underexplored in plants. The work presented here illustrated the utility of a large-scale (299-genotype and seven-tissue) gene expression resource to dissect traits across multiple levels of biological organization. Using single-tissue- and multi-tissue-based transcriptome-wide association studies (TWAS), we revealed that about half of the functional variation acts through altered transcript abundance for maize kernel traits, including 30 grain carotenoid abundance traits, 20 grain tocochromanol abundance traits, and 22 field-measured agronomic traits. Comparing the efficacy of TWAS with genome-wide association studies (GWAS) and an ensemble approach that combines both GWAS and TWAS, we demonstrated that results of TWAS in combination with GWAS increase the power to detect known genes and aid in prioritizing likely causal genes. Using a variance partitioning approach in the largely independent maize Nested Association Mapping (NAM) population, we also showed that the most strongly associated genes identified by combining GWAS and TWAS explain more heritable variance for a majority of traits than the heritability captured by the random genes and the genes identified by GWAS or TWAS alone. This not only improves the ability to link genes to phenotypes, but also highlights the phenotypic consequences of regulatory variation in plants.


Subject(s)
Genome-Wide Association Study/methods , Transcriptome , Zea mays/genetics , Analysis of Variance , Gene Expression Regulation, Plant , Genome-Wide Association Study/statistics & numerical data , Phenotype , Plant Proteins/genetics , Quantitative Trait Loci
8.
Proc Natl Acad Sci U S A ; 116(12): 5542-5549, 2019 03 19.
Article in English | MEDLINE | ID: mdl-30842277

ABSTRACT

Deep learning methodologies have revolutionized prediction in many fields and show potential to do the same in molecular biology and genetics. However, applying these methods in their current forms ignores evolutionary dependencies within biological systems and can result in false positives and spurious conclusions. We developed two approaches that account for evolutionary relatedness in machine learning models: (i) gene-family-guided splitting and (ii) ortholog contrasts. The first approach accounts for evolution by constraining model training and testing sets to include different gene families. The second approach uses evolutionarily informed comparisons between orthologous genes to both control for and leverage evolutionary divergence during the training process. The two approaches were explored and validated within the context of mRNA expression level prediction and have the area under the ROC curve (auROC) values ranging from 0.75 to 0.94. Model weight inspections showed biologically interpretable patterns, resulting in the hypothesis that the 3' UTR is more important for fine-tuning mRNA abundance levels while the 5' UTR is more important for large-scale changes.


Subject(s)
Base Sequence/genetics , Deep Learning , Evolution, Molecular , Transcription, Genetic/genetics , DNA/genetics , DNA/metabolism , Gene Expression Regulation/genetics , Models, Theoretical , Sequence Analysis, DNA
9.
Plant Cell ; 31(5): 937-955, 2019 05.
Article in English | MEDLINE | ID: mdl-30923231

ABSTRACT

Cultivated maize (Zea mays) has retained much of the genetic diversity of its wild ancestors. Here, we performed nontargeted liquid chromatography-mass spectrometry metabolomics to analyze the metabolomes of the 282 maize inbred lines in the Goodman Diversity Panel. This analysis identified a bimodal distribution of foliar metabolites. Although 15% of the detected mass features were present in >90% of the inbred lines, the majority were found in <50% of the samples. Whereas leaf bases and tips were differentiated by flavonoid abundance, maize varieties (stiff-stalk, nonstiff-stalk, tropical, sweet maize, and popcorn) showed differential accumulation of benzoxazinoid metabolites. Genome-wide association studies (GWAS), performed for 3,991 mass features from the leaf tips and leaf bases, showed that 90% have multiple significantly associated loci scattered across the genome. Several quantitative trait locus hotspots in the maize genome regulate the abundance of multiple, often structurally related mass features. The utility of maize metabolite GWAS was demonstrated by confirming known benzoxazinoid biosynthesis genes, as well as by mapping isomeric variation in the accumulation of phenylpropanoid hydroxycitric acid esters to a single linkage block in a citrate synthase-like gene. Similar to gene expression databases, this metabolomic GWAS data set constitutes an important public resource for linking maize metabolites with biosynthetic and regulatory genes.


Subject(s)
Gene Expression Regulation, Plant/genetics , Genetic Variation , Genome-Wide Association Study , Metabolome , Zea mays/genetics , Metabolomics , Phenotype , Quantitative Trait Loci/genetics , Zea mays/chemistry , Zea mays/metabolism
10.
New Phytol ; 221(4): 2096-2111, 2019 03.
Article in English | MEDLINE | ID: mdl-30289553

ABSTRACT

The production and regulation of defensive specialized metabolites play a central role in pathogen resistance in maize (Zea mays) and other plants. Therefore, identification of genes involved in plant specialized metabolism can contribute to improved disease resistance. We used comparative metabolomics to identify previously unknown antifungal metabolites in maize seedling roots, and investigated the genetic and physiological mechanisms underlying their natural variation using quantitative trait locus mapping and comparative transcriptomics approaches. Two maize metabolites, smilaside A (3,6-diferuloyl-3',6'-diacetylsucrose) and smiglaside C (3,6-diferuloyl-2',3',6'-triacetylsucrose), were identified that could contribute to maize resistance against Fusarium graminearum and other fungal pathogens. Elevated expression of an ethylene signaling gene, ETHYLENE INSENSITIVE 2 (ZmEIN2), co-segregated with a decreased smilaside A : smiglaside C ratio. Pharmacological and genetic manipulation of ethylene availability and sensitivity in vivo indicated that, whereas ethylene was required for the production of both metabolites, the smilaside A : smiglaside C ratio was negatively regulated by ethylene sensitivity. This ratio, rather than the absolute abundance of these two metabolites, was important for maize seedling root defense against F. graminearum. Ethylene signaling regulates the relative abundance of the two F. graminearum-resistance-related metabolites and affects resistance against F. graminearum in maize seedling roots.


Subject(s)
Disease Resistance , Ethylenes/metabolism , Fusarium/physiology , Plant Roots/microbiology , Seedlings/microbiology , Signal Transduction , Sucrose/metabolism , Zea mays/microbiology , Acetylation , Antifungal Agents/pharmacology , Inbreeding , Metabolome , Models, Biological , Plant Diseases/microbiology , Plant Proteins/metabolism , Plant Roots/growth & development , Quantitative Trait Loci/genetics , Zea mays/metabolism
11.
Plant Genome ; 11(3)2018 11.
Article in English | MEDLINE | ID: mdl-30512036

ABSTRACT

Plant genomes reduce in size following a whole-genome duplication event, and one gene in a duplicate gene pair can lose function in absence of selective pressure to maintain duplicate gene copies. Maize ( L.) and its sister genus, , share a genome duplication event that occurred 5 to 26 million years ago. Because few genomic resources for exist, it is unknown whether grasses and maize have maintained a similar set of genes that have resisted decay into pseudogenes. Here we present high-quality de novo transcriptome assemblies for two species: (L.) L. and Porter ex Vasey. Genes with experimental protein evidence in maize were good candidates for genes resistant to pseudogenization in both genera because pseudogenes by definition do not produce protein. We tested whether 15,160 maize genes with protein evidence are resisting gene loss and whether their homologs are also resisting gene loss. Protein-encoding maize transcripts and their homologs have higher guanine-cytosine (GC) content, higher gene expression levels, and more conserved expression levels than putatively untranslated maize transcripts and their homologs. These results suggest that similar genes may be decaying into pseudogenes in both genera after a shared ancient polyploidy event. The transcriptome assemblies provide a high-quality genomic resource that can provide insight into the evolution of maize, a highly valuable crop worldwide.


Subject(s)
Evolution, Molecular , Poaceae/genetics , Zea mays/genetics , Gene Deletion , Genes, Plant , Polyploidy , Transcriptome
12.
Genome Res ; 28(10): 1555-1565, 2018 10.
Article in English | MEDLINE | ID: mdl-30166407

ABSTRACT

Ribosomal repeats occupy 5% of a plant genome, yet there has been little study of their diversity in the modern age of genomics. Ribosomal copy number and expression variation present an opportunity to tap a novel source of diversity. In the present study, we estimated the ribosomal DNA (rDNA) copy number and ribosomal RNA (rRNA) expression for a population of maize inbred lines and investigated the potential role of rDNA and rRNA dosage in regulating global gene expression. Extensive variation was found in both ribosomal DNA copy number and ribosomal RNA expression among maize inbred lines. However, rRNA abundance was not consistent with the copy number of the rDNA. We have not found that the rDNA gene dosage has a regulatory role in gene expression; however, thousands of genes are identified to be coregulated with rRNA expression, including genes participating in ribosome biogenesis and other functionally relevant pathways. We further investigated the potential roles of copy number and the expression level of rDNA on agronomic traits and found that both correlated with flowering time but through different regulatory mechanisms. This comprehensive analysis suggested that rRNA expression variation is a valuable source of functional diversity that affects gene expression variation and field-based phenotypic changes.


Subject(s)
DNA, Ribosomal/genetics , Plant Proteins/genetics , RNA, Ribosomal/genetics , Zea mays/genetics , DNA, Plant/genetics , Flowers/genetics , Gene Dosage , Gene Expression Profiling , Gene Expression Regulation, Plant , Phenotype
13.
Nature ; 555(7697): 520-523, 2018 03 22.
Article in English | MEDLINE | ID: mdl-29539638

ABSTRACT

Here we report a multi-tissue gene expression resource that represents the genotypic and phenotypic diversity of modern inbred maize, and includes transcriptomes in an average of 255 lines in seven tissues. We mapped expression quantitative trait loci and characterized the contribution of rare genetic variants to extremes in gene expression. Some of the new mutations that arise in the maize genome can be deleterious; although selection acts to keep deleterious variants rare, their complete removal is impeded by genetic linkage to favourable loci and by finite population size. Modern maize breeders have systematically reduced the effects of this constant mutational pressure through artificial selection and self-fertilization, which have exposed rare recessive variants in elite inbred lines. However, the ongoing effect of these rare alleles on modern inbred maize is unknown. By analysing this gene expression resource and exploiting the extreme diversity and rapid linkage disequilibrium decay of maize, we characterize the effect of rare alleles and evolutionary history on the regulation of expression. Rare alleles are associated with the dysregulation of expression, and we correlate this dysregulation to seed-weight fitness. We find enrichment of ancestral rare variants among expression quantitative trait loci mapped in modern inbred lines, which suggests that historic bottlenecks have shaped regulation. Our results suggest that one path for further genetic improvement in agricultural species lies in purging the rare deleterious variants that have been associated with crop fitness.


Subject(s)
Alleles , Gene Expression Regulation, Plant/genetics , Genetic Fitness/genetics , Zea mays/genetics , Crops, Agricultural/genetics , Genetic Variation/genetics , Genome, Plant/genetics , Genotype , Linkage Disequilibrium , Phenotype , Population Density , Quantitative Trait Loci/genetics , RNA, Plant/genetics , Seeds/genetics , Sequence Analysis, RNA
14.
G3 (Bethesda) ; 5(11): 2229-39, 2015 Sep 01.
Article in English | MEDLINE | ID: mdl-26333837

ABSTRACT

The transfer of mitochondrial DNA (mtDNA) into nuclear genomes is a regularly occurring process that has been observed in many species. Few studies, however, have focused on the variation of nuclear-mtDNA sequences (NUMTs) within a species. This study examined mtDNA insertions within chromosomes of a diverse set of Zea mays ssp. mays (maize) inbred lines by the use of fluorescence in situ hybridization. A relatively large NUMT on the long arm of chromosome 9 (9L) was identified at approximately the same position in four inbred lines (B73, M825, HP301, and Oh7B). Further examination of the similarly positioned 9L NUMT in two lines, B73 and M825, indicated that the large size of these sites is due to the presence of a majority of the mitochondrial genome; however, only portions of this NUMT (~252 kb total) were found in the publically available B73 nuclear sequence for chromosome 9. Fiber-fluorescence in situ hybridization analysis estimated the size of the B73 9L NUMT to be ~1.8 Mb and revealed that the NUMT is methylated. Two regions of mtDNA (2.4 kb and 3.3 kb) within the 9L NUMT are not present in the B73 mitochondrial NB genome; however, these 2.4-kb and 3.3-kb segments are present in other Zea mitochondrial genomes, including that of Zea mays ssp. parviglumis, a progenitor of domesticated maize.


Subject(s)
Chromosomes, Plant/genetics , DNA, Mitochondrial/genetics , Mutagenesis, Insertional , Zea mays/genetics , In Situ Hybridization, Fluorescence , Sequence Analysis, DNA
15.
Planta ; 236(2): 463-76, 2012 Aug.
Article in English | MEDLINE | ID: mdl-22411508

ABSTRACT

Inhibition of photosynthesis by heat stress is accompanied by functional impairment of Rubisco's chaperone, activase (RCA), resulting in deactivation of Rubisco. Since activase is extremely sensitive to thermal denaturation, changes in expression of RCA at the transcript or protein level could provide a mechanism for acclimation of photosynthesis to prolonged heat stress. Using quantitative real-time PCR (qPCR) we show steady-state RCA transcript levels in Arabidopsis thaliana are stabilized during prolonged exposure to moderate heat (35  °C). A survey of RCA transcripts indicates heat stress did not alter the relative abundance of transcripts encoding α and ß-isoforms of activase that are produced by alternative splicing of the pre-mRNA. Instead, mRNA stabilization in heat-stressed plants coincided with a significant reduction in the average length of activase 3'-untranslated regions, and was associated with enrichment of an uncharacterized activase mRNA splice variant, AtRCAß2. Transcript-specific qPCR revealed AtRCAß2 mRNA was more stable than AtRCAα and AtRCAß mRNA in heat-stressed plants. Using an inducible transgenic system, we found that RCA transcripts lacking their native 3'-untranslated region were significantly more stable than their full-length counterparts in vivo. Using this system, stability of the RCA protein was examined over 24 h in vivo, in the absence of RCA transcription. At both optimal and elevated temperatures, RCA protein levels remained stable in plants lacking RCA mRNA, but increased when RCA mRNA was present, particularly in heat-stressed plants. This study reveals a possible mechanism, involving post-transcriptional regulation of an important photosynthesis regulatory gene, for acclimation of photosynthesis to heat stress.


Subject(s)
3' Untranslated Regions/genetics , Arabidopsis/enzymology , Hot Temperature/adverse effects , Plant Proteins/genetics , Acclimatization/genetics , Arabidopsis/genetics , Arabidopsis/physiology , Gene Expression Regulation, Plant/genetics , Mutagenesis, Insertional , Photosynthesis/genetics , Photosynthesis/physiology , Plant Proteins/metabolism , Plant Shoots/enzymology , Plant Shoots/genetics , Plant Shoots/physiology , Plants, Genetically Modified , Protein Isoforms/genetics , Protein Isoforms/metabolism , RNA, Messenger/genetics , RNA, Messenger/metabolism , RNA, Plant/genetics , RNA, Plant/metabolism , Seedlings/enzymology , Seedlings/genetics , Seedlings/physiology , Stress, Physiological/genetics , Transgenes
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