Genome‐wide atlas of transcription during maize development
TL;DR: A comprehensive atlas of global transcription profiles across developmental stages and plant organs is presented, and it is found that expansion of distinct gene families was accompanied by divergent, tissue-specific transcription patterns of the paralogs.
Abstract: Maize is an important model species and a major constituent of human and animal diets. It has also emerged as a potential feedstock and model system for bioenergy research due to recent worldwide interest in developing plant biomass-based, carbon-neutral liquid fuels. To understand how the underlying genome sequence results in specific plant phenotypes, information on the temporal and spatial transcription patterns of genes is crucial. Here we present a comprehensive atlas of global transcription profiles across developmental stages and plant organs. We used a NimbleGen microarray containing 80,301 probe sets to profile transcription patterns in 60 distinct tissues representing 11 major organ systems of inbred line B73. Of the 30,892 probe sets representing the filtered B73 gene models, 91.4% were expressed in at least one tissue. Interestingly, 44.5% of the probe sets were expressed in all tissues, indicating a substantial overlap of gene expression among plant organs. Clustering of maize tissues based on global gene expression profiles resulted in formation of groups of biologically related tissues. We utilized this dataset to examine the expression of genes that encode enzymes in the lignin biosynthetic pathway, and found that expansion of distinct gene families was accompanied by divergent, tissue-specific transcription patterns of the paralogs. This comprehensive expression atlas represents a valuable resource for gene discovery and functional characterization in maize.
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TL;DR: A comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines finds evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement.
Abstract: Domestication and plant breeding are ongoing 10,000-year-old evolutionary experiments that have radically altered wild species to meet human needs. Maize has undergone a particularly striking transformation. Researchers have sought for decades to identify the genes underlying maize evolution, but these efforts have been limited in scope. Here, we report a comprehensive assessment of the evolution of modern maize based on the genome-wide resequencing of 75 wild, landrace and improved maize lines. We find evidence of recovery of diversity after domestication, likely introgression from wild relatives, and evidence for stronger selection during domestication than improvement. We identify a number of genes with stronger signals of selection than those previously shown to underlie major morphological changes. Finally, through transcriptome-wide analysis of gene expression, we find evidence both consistent with removal of cis-acting variation during maize domestication and improvement and suggestive of modern breeding having increased dominance in expression while targeting highly expressed genes.
788 citations
TL;DR: The results show that characterization of the maize B73 transcriptome is far from complete, and that maize gene expression is more complex than previously thought.
Abstract: Zea mays is an important genetic model for elucidating transcriptional networks. Uncertainties about the complete structure of mRNA transcripts limit the progress of research in this system. Here, using single-molecule sequencing technology, we produce 111,151 transcripts from 6 tissues capturing ∼70% of the genes annotated in maize RefGen_v3 genome. A large proportion of transcripts (57%) represent novel, sometimes tissue-specific, isoforms of known genes and 3% correspond to novel gene loci. In other cases, the identified transcripts have improved existing gene models. Averaging across all six tissues, 90% of the splice junctions are supported by short reads from matched tissues. In addition, we identified a large number of novel long non-coding RNAs and fusion transcripts and found that DNA methylation plays an important role in generating various isoforms. Our results show that characterization of the maize B73 transcriptome is far from complete, and that maize gene expression is more complex than previously thought.
466 citations
TL;DR: The dynamic nature of the maize pan-genome was revealed and it was demonstrated that a substantial portion of variation may lie outside the single reference genome for a species.
Abstract: Genomes at the species level are dynamic, with genes present in every individual (core) and genes in a subset of individuals (dispensable) that collectively constitute the pan-genome. Using transcriptome sequencing of seedling RNA from 503 maize (Zea mays) inbred lines to characterize the maize pan-genome, we identified 8681 representative transcript assemblies (RTAs) with 16.4% expressed in all lines and 82.7% expressed in subsets of the lines. Interestingly, with linkage disequilibrium mapping, 76.7% of the RTAs with at least one single nucleotide polymorphism (SNP) could be mapped to a single genetic position, distributed primarily throughout the nonpericentromeric portion of the genome. Stepwise iterative clustering of RTAs suggests, within the context of the genotypes used in this study, that the maize genome is restricted and further sampling of seedling RNA within this germplasm base will result in minimal discovery. Genome-wide association studies based on SNPs and transcript abundance in the pan-genome revealed loci associated with the timing of the juvenile-to-adult vegetative and vegetative-to-reproductive developmental transitions, two traits important for fitness and adaptation. This study revealed the dynamic nature of the maize pan-genome and demonstrated that a substantial portion of variation may lie outside the single reference genome for a species.
461 citations
Cites background from "Genome‐wide atlas of transcription ..."
...…associated with variation for flowering time. zmm22 encodes a StMADS-11-like transcription factor, and this clade of proteins act as a repressor of flowering in several species including wheat (Triticum aestivum) and rice (Kane et al., 2005; Sentoku et al., 2005; Kikuchi et al., 2008)....
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TL;DR: A comprehensive study of maize metabolism, combining genetic, metabolite and expression profiling methodologies to dissect the genetic basis of metabolic diversity in maize kernels, finds metabolite features associated with kernel weight could be used as biomarkers to facilitate genetic improvement of maize.
Abstract: Plants produce a variety of metabolites that have a critical role in growth and development. Here we present a comprehensive study of maize metabolism, combining genetic, metabolite and expression profiling methodologies to dissect the genetic basis of metabolic diversity in maize kernels. We quantify 983 metabolite features in 702 maize genotypes planted at multiple locations. We identify 1,459 significant locus-trait associations (P≤1.8 × 10(-6)) across three environments through metabolite-based genome-wide association mapping. Most (58.5%) of the identified loci are supported by expression QTLs, and some (14.7%) are validated through linkage mapping. Re-sequencing and candidate gene association analysis identifies potential causal variants for five candidate genes involved in metabolic traits. Two of these genes were further validated by mutant and transgenic analysis. Metabolite features associated with kernel weight could be used as biomarkers to facilitate genetic improvement of maize.
376 citations
TL;DR: It is suggested that TEs provide an important source of allelic regulatory variation in gene response to abiotic stress in maize and may provide local enhancer activities that stimulate stress-responsive gene expression.
Abstract: Transposable elements (TEs) account for a large portion of the genome in many eukaryotic species. Despite their reputation as “junk” DNA or genomic parasites deleterious for the host, TEs have complex interactions with host genes and the potential to contribute to regulatory variation in gene expression. It has been hypothesized that TEs and genes they insert near may be transcriptionally activated in response to stress conditions. The maize genome, with many different types of TEs interspersed with genes, provides an ideal system to study the genome-wide influence of TEs on gene regulation. To analyze the magnitude of the TE effect on gene expression response to environmental changes, we profiled gene and TE transcript levels in maize seedlings exposed to a number of abiotic stresses. Many genes exhibit up- or down-regulation in response to these stress conditions. The analysis of TE families inserted within upstream regions of up-regulated genes revealed that between four and nine different TE families are associated with up-regulated gene expression in each of these stress conditions, affecting up to 20% of the genes up-regulated in response to abiotic stress, and as many as 33% of genes that are only expressed in response to stress. Expression of many of these same TE families also responds to the same stress conditions. The analysis of the stress-induced transcripts and proximity of the transposon to the gene suggests that these TEs may provide local enhancer activities that stimulate stress-responsive gene expression. Our data on allelic variation for insertions of several of these TEs show strong correlation between the presence of TE insertions and stress-responsive up-regulation of gene expression. Our findings suggest that TEs provide an important source of allelic regulatory variation in gene response to abiotic stress in maize.
352 citations
Cites methods from "Genome‐wide atlas of transcription ..."
...Analysis of developmental expression patterns for these genes using the B73 expression atlas [48] reveals that only 7% of the TE influenced genes are expressed in at least 5 tissues, compared to 41% of the non-TE influenced genes....
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References
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TL;DR: A new approach to rapid sequence comparison, basic local alignment search tool (BLAST), directly approximates alignments that optimize a measure of local similarity, the maximal segment pair (MSP) score.
88,255 citations
"Genome‐wide atlas of transcription ..." refers methods in this paper
...The FGENESH gene models were aligned to each other using BLAST (Altschul et al., 1990), and the shorter model was discarded for pairs of models with sequence identity >95% and at least a 300 bp overlap....
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TL;DR: There is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities, and the exploratory data analyses of the probe level data motivate a new summary measure that is a robust multi-array average (RMA) of background-adjusted, normalized, and log-transformed PM values.
Abstract: SUMMARY In this paper we report exploratory analyses of high-density oligonucleotide array data from the Affymetrix GeneChip R � system with the objective of improving upon currently used measures of gene expression. Our analyses make use of three data sets: a small experimental study consisting of five MGU74A mouse GeneChip R � arrays, part of the data from an extensive spike-in study conducted by Gene Logic and Wyeth’s Genetics Institute involving 95 HG-U95A human GeneChip R � arrays; and part of a dilution study conducted by Gene Logic involving 75 HG-U95A GeneChip R � arrays. We display some familiar features of the perfect match and mismatch probe ( PM and MM )v alues of these data, and examine the variance–mean relationship with probe-level data from probes believed to be defective, and so delivering noise only. We explain why we need to normalize the arrays to one another using probe level intensities. We then examine the behavior of the PM and MM using spike-in data and assess three commonly used summary measures: Affymetrix’s (i) average difference (AvDiff) and (ii) MAS 5.0 signal, and (iii) the Li and Wong multiplicative model-based expression index (MBEI). The exploratory data analyses of the probe level data motivate a new summary measure that is a robust multiarray average (RMA) of background-adjusted, normalized, and log-transformed PM values. We evaluate the four expression summary measures using the dilution study data, assessing their behavior in terms of bias, variance and (for MBEI and RMA) model fit. Finally, we evaluate the algorithms in terms of their ability to detect known levels of differential expression using the spike-in data. We conclude that there is no obvious downside to using RMA and attaching a standard error (SE) to this quantity using a linear model which removes probe-specific affinities. ∗ To whom correspondence should be addressed
10,711 citations
TL;DR: The calculation of the q‐value is discussed, the pFDR analogue of the p‐value, which eliminates the need to set the error rate beforehand as is traditionally done, and can yield an increase of over eight times in power compared with the Benjamini–Hochberg FDR method.
Abstract: Summary. Multiple-hypothesis testing involves guarding against much more complicated errors than single-hypothesis testing. Whereas we typically control the type I error rate for a single-hypothesis test, a compound error rate is controlled for multiple-hypothesis tests. For example, controlling the false discovery rate FDR traditionally involves intricate sequential p-value rejection methods based on the observed data. Whereas a sequential p-value method fixes the error rate and estimates its corresponding rejection region, we propose the opposite approach—we fix the rejection region and then estimate its corresponding error rate. This new approach offers increased applicability, accuracy and power. We apply the methodology to both the positive false discovery rate pFDR and FDR, and provide evidence for its benefits. It is shown that pFDR is probably the quantity of interest over FDR. Also discussed is the calculation of the q-value, the pFDR analogue of the p-value, which eliminates the need to set the error rate beforehand as is traditionally done. Some simple numerical examples are presented that show that this new approach can yield an increase of over eight times in power compared with the Benjamini–Hochberg FDR method.
5,414 citations
"Genome‐wide atlas of transcription ..." refers methods in this paper
...A Fisher’s exact test with the false discovery rate (FDR) set at 5% as defined by the Q-value program (Storey, 2002) was used to identify enriched GO Slim annotations for each subset of the maize genes: non-expressed genes, constitutively expressed genes and stably expressed genes....
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TL;DR: The sequence of the maize genome reveals it to be the most complex genome known to date and the correlation of methylation-poor regions with Mu transposon insertions and recombination and how uneven gene losses between duplicated regions were involved in returning an ancient allotetraploid to a genetically diploid state is reported.
Abstract: We report an improved draft nucleotide sequence of the 2.3-gigabase genome of maize, an important crop plant and model for biological research. Over 32,000 genes were predicted, of which 99.8% were placed on reference chromosomes. Nearly 85% of the genome is composed of hundreds of families of transposable elements, dispersed nonuniformly across the genome. These were responsible for the capture and amplification of numerous gene fragments and affect the composition, sizes, and positions of centromeres. We also report on the correlation of methylation-poor regions with Mu transposon insertions and recombination, and copy number variants with insertions and/or deletions, as well as how uneven gene losses between duplicated regions were involved in returning an ancient allotetraploid to a genetically diploid state. These analyses inform and set the stage for further investigations to improve our understanding of the domestication and agricultural improvements of maize.
3,761 citations
"Genome‐wide atlas of transcription ..." refers background or methods in this paper
...We have demonstrated that the dataset is of high quality and that the results of biological replicates are highly repeatable, based on an analysis of 30 892 probe sets that represented high-confidence maize genes from the filtered maize gene set (Schnable et al., 2009)....
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...After release of the higher-quality B73 maize genome (Schnable et al., 2009), all probes were further searched against the official maize genome sequence and the mRNA...
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...recent sequencing of the maize genome (Schnable et al., 2009) has provided a framework for the identification and functional characterization of genes and genetic networks for crop improvement and basic research....
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15 Dec 2005
TL;DR: The U.S. Department of Energy and the United States Department of Agriculture have both strongly committed to expanding the role of biomass as an energy source as mentioned in this paper, and they support biomass fuels and products as a way to reduce the need for oil and gas imports; to support the growth of agriculture, forestry, and rural economies; and to foster major new domestic industries making a variety of fuels, chemicals, and other products.
Abstract: The U.S. Department of Energy (DOE) and the U.S. Department of Agriculture (USDA) are both strongly committed to expanding the role of biomass as an energy source. In particular, they support biomass fuels and products as a way to reduce the need for oil and gas imports; to support the growth of agriculture, forestry, and rural economies; and to foster major new domestic industries--biorefineries--making a variety of fuels, chemicals, and other products. As part of this effort, the Biomass R&D Technical Advisory Committee, a panel established by the Congress to guide the future direction of federally funded biomass R&D, envisioned a 30 percent replacement of the current U.S. petroleum consumption with biofuels by 2030. Biomass--all plant and plant-derived materials including animal manure, not just starch, sugar, oil crops already used for food and energy--has great potential to provide renewable energy for America's future. Biomass recently surpassed hydropower as the largest domestic source of renewable energy and currently provides over 3 percent of the total energy consumption in the United States. In addition to the many benefits common to renewable energy, biomass is particularly attractive because it is the only current renewable source of liquid transportation fuel. This, of course, makes it invaluable in reducing oil imports--one of our most pressing energy needs. A key question, however, is how large a role could biomass play in responding to the nation's energy demands. Assuming that economic and financial policies and advances in conversion technologies make biomass fuels and products more economically viable, could the biorefinery industry be large enough to have a significant impact on energy supply and oil imports? Any and all contributions are certainly needed, but would the biomass potential be sufficiently large to justify the necessary capital replacements in the fuels and automobile sectors? The purpose of this report is to determine whether the land resources of the United States are capable of producing a sustainable supply of biomass sufficient to displace 30 percent or more of the country's present petroleum consumption--the goal set by the Advisory Committee in their vision for biomass technologies. Accomplishing this goal would require approximately 1 billion dry tons of biomass feedstock per year.
2,637 citations