Teosinte Pollen Drive guides maize domestication and evolution by RNA interference [small RNA-seq]
Ontology highlight
ABSTRACT: Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Cryptic drive is thought to be pervasive and can be unleashed following hybridization with a naïve genome, resulting in sterility and hybrid incompatibility. Using single molecule and single pollen genome sequencing, we describe an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi) in the male germline. Multiple hairpin-derived small RNA from mexicana target a novel domestication gene, Teosinte Drive Responder, that is required for pollen fertility and has undergone selection for immunity to RNAi. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas. A survey of maize landraces and sympatric populations of teosinte mexicana reveals allelic bias at genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication, and offers an explanation for the widespread abundance of hairpin-encoded and other endogenous small RNA in the germlines of plants and animals.
ORGANISM(S): Zea mays subsp. mays x Zea mays subsp. mexicana
Project description:Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Cryptic drive is thought to be pervasive and can be unleashed following hybridization with a naïve genome, resulting in sterility and hybrid incompatibility. Using single molecule and single pollen genome sequencing, we describe an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi) in the male germline. Multiple hairpin-derived small RNA from mexicana target a novel domestication gene, Teosinte Drive Responder, that is required for pollen fertility and has undergone selection for immunity to RNAi. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas. A survey of maize landraces and sympatric populations of teosinte mexicana reveals allelic bias at genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication, and offers an explanation for the widespread abundance of hairpin-encoded and other endogenous small RNA in the germlines of plants and animals.
Project description:Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Cryptic drive is thought to be pervasive and can be unleashed following hybridization with a naïve genome, resulting in sterility and hybrid incompatibility. Using single molecule and single pollen genome sequencing, we describe an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi) in the male germline. Multiple hairpin-derived small RNA from mexicana target a novel domestication gene, Teosinte Drive Responder, that is required for pollen fertility and has undergone selection for immunity to RNAi. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas. A survey of maize landraces and sympatric populations of teosinte mexicana reveals allelic bias at genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication, and offers an explanation for the widespread abundance of hairpin-encoded and other endogenous small RNA in the germlines of plants and animals.
Project description:Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Cryptic drive is thought to be pervasive and can be unleashed following hybridization with a naïve genome, resulting in sterility and hybrid incompatibility. Using single molecule and single pollen genome sequencing, we describe an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi) in the male germline. Multiple hairpin-derived small RNA from mexicana target a novel domestication gene, Teosinte Drive Responder, that is required for pollen fertility and has undergone selection for immunity to RNAi. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas. A survey of maize landraces and sympatric populations of teosinte mexicana reveals allelic bias at genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication, and offers an explanation for the widespread abundance of hairpin-encoded and other endogenous small RNA in the germlines of plants and animals.
Project description:Meiotic drivers subvert Mendelian expectations by manipulating reproductive development to bias their own transmission. Chromosomal drive typically functions in asymmetric female meiosis, while gene drive is normally postmeiotic and typically found in males. Cryptic drive is thought to be pervasive and can be unleashed following hybridization with a naïve genome, resulting in sterility and hybrid incompatibility. Using single molecule and single pollen genome sequencing, we describe an instance of gene drive in hybrids between maize (Zea mays ssp. mays) and teosinte mexicana (Zea mays ssp. mexicana), that depends on RNA interference (RNAi) in the male germline. Multiple hairpin-derived small RNA from mexicana target a novel domestication gene, Teosinte Drive Responder, that is required for pollen fertility and has undergone selection for immunity to RNAi. Introgression of mexicana into early cultivated maize is thought to have been critical to its geographical dispersal throughout the Americas. A survey of maize landraces and sympatric populations of teosinte mexicana reveals allelic bias at genes required for RNAi on at least 4 chromosomes that are also subject to gene drive in pollen from synthetic hybrids. Teosinte Pollen Drive likely played a major role in maize domestication, and offers an explanation for the widespread abundance of hairpin-encoded and other endogenous small RNA in the germlines of plants and animals.
Project description:In this work, we performed high throughput sequencing of small RNA libraries in maize (Zea mays ssp. mays) and teosinte (Zea mays ssp. parviglumis) to investigate the response mediated by miRNAs in these plants under control conditions, submergence, drought and alternated drought-submergence or submergence-drought stress. After Illumina sequencing of 8 small RNA libraries, we obtained from 16,139,354 to 46,522,229 raw reads across the libraries. Bioinformatic analysis identified 88 maize miRNAs and 76 miRNAs from other plants differentially expressed in maize and/or in teosinte in response to at least one of the treatments, and revealed that a larger set of miRNAs were regulated in maize than in teosinte in response to submergence and drought stress.
Project description:Through domestication, humans have substantially altered the morphology of Zea mays ssp. parviglumis (teosinte) into the currently recognizable maize. A wealth of archeological and population genetic data has established maize as a model system for studying domestication , genome evolution and the genetics and evolution of complex traits. We used expression profiling of 18,242 genes for 38 diverse maize genotypes and 18 teosinte genotypes to examine how domestication has re-shaped the transcriptome of maize seedlings. We detected evidence for more than 600 genes having significantly different expression levels in maize compared to teosinte as well as 800 genes with significantly altered co-expression profiles reflective of substantial rewiring of the transcriptome since domestication. These genes likely include loci with altered expression due to domestication. The genes with altered expression show a significant enrichment for genes located in regions that previous population genetic analyses have identified as having undergone a selective sweep during maize domestication; thirty-two genes previously identified as putative targets of selection also exhibit altered expression levels and co-expression relationships. We also identified 45 genes with altered, primarily higher, expression in inbred relative to out-crossed teosinte. These genes are over-represented for genes that function in response to biotic stress and may reflect responses to the effects of inbreeding. This study not only documents alterations in the maize transcriptome following domestication and identifies several genes that may have contributed to the evolution of maize but also highlights the complementary information that can be gained by combining gene expression with population genetic analyses.
Project description:Purpose: The goals of this study are studies the response of annual Zea mays ssp. mexicana L. under cold and drought stress Methods: The seedlings of zea may ssp. mexicana L. were generated by Illumina HiSeq2500 deep-sequencing. In order to generate a global overview of Zea mexicana transcriptome data, 3 of complement DNA (cDNA) libraries were prepared from RNA isolated from root, stem, and leave mixed tissues of Zea Mexicana from Control (24℃), Cold (4℃) and Drought (PEG2000, 20%) treatments and each teatment has two repetitions. The sequence reads that passed quality filters were merged and de novo to generate all transcripts set by Trinity with default parameter, which will be treated as reference genome. The number of paired-reads of each sample were mapped to reference genome by Bowtie software v1.1.1 and the number of mapped reads were calculated by RSEM. qRT-PCR validation was performed using BIO-RAD CFX96 sequence detection system and SYBR Green assays. Results: Using RNA-Seq technology with the Trinity assembled method, we generated a seedling plant transcriptome at a sequencing size of 51.78Gb of Zea mays ssp. mexicana L. from pooled RNA samples which included control (CK), cold (4℃) and drought (PEG2000, 20%) stressed plant samples. A total of 414,232,462 high quality clean reads were used to conduct de novo assembly and annotation of genes without reference genome information. All of these reads were assembled into 251,145 transcripts (N50 = 1,269 bp) and 184,280 unigenes (N50 = 923 bp). A total of 3,504 up-regulated and 1,220 down-regulated genes were detected under cold stress and 532 up-regulated and 82 down-regulated genes were detected under drought stress. A Venn diagram indicated that 208 genes were affected by both cold and drought stresses. 3 cold stress pathways and 5 drought related pathways showed significant KEGG pathways. Functional enrichment analyses identified many common or specific biological processes and gene sets in response to drought and cold stresses. The ABA dependent pathway, trehalose synthetic pathway and CBF6 gene of ICE1-CBF pathway may play important roles in the DEGs co-up-regulated by both stresses of Zea mays ssp. mexicana L. Conclusions: We analyzed transcriptome data and gene expression profile information from seedlings of Zea mays ssp. mexicana L. under cold and drought stresses. Together these data provides the most comprehensive sequence study available for Zea mays ssp. mexicana L. and provides some important functional genes and molecular mechanism information for improving the quality characteristic of maize in the future.
Project description:DNA methylation is a ubiquitous chromatin feature — in maize, more than 25% of cytosines in the genome are methylated. Recently, major progress has been made in describing the molecular mechanisms driving methylation, yet variation and evolution of the methylation landscape during maize domestication remain largely unknown. Here we leveraged whole-genome sequencing (WGS) and whole-genome bisulfite sequencing (WGBS) on populations of modern maize, landrace, and teosinte (Zea mays ssp. parviglumis) to investigate the adaptive and phenotypic consequences of methylation variations in maize. By using a novel estimation approach, we inferred the methylome site frequency spectrum (mSFS) to estimate forward and backward methylation mutation rates and selection coefficients. We only found weak evidence for direct selection on DNA methylation in any context, but thousands of differentially methylated regions (DMRs) were identified in population-wide that are correlated with recent selection. Further investigation revealed that DMRs are enriched in 5’ untranslated regions, and that maize hypomethylated DMRs likely helped rewire distal gene regulation. For two trait-associated DMRs, vgt1-DMR and tb1DMR, our HiChIP data indicated that the interactive loops between DMRs and respective downstream genes were present in B73, a modern maize line, but absent in teosinte. Functional analyses suggested that these DMRs likely served as cis-acting elements that modulated gene regulation after domestication. Our results enable a better understanding of the evolutionary forces acting on patterns of DNA methylation and suggest a role of methylation variation in adaptive evolution.
Project description:Modern maize was domesticated from Teosinte parviglumis, with subsequent introgressions from Teosinte mexicana, yielding increased kernel row number, loss of the hard fruit case and dissociation from the cob upon maturity, as well as fewer tillers. Molecular approaches have identified several transcription factors involved in the development of these traits, yet revealed that a complex regulatory network is at play. MaizeCODE deploys ENCODE strategies to catalog regulatory regions in the maize genome, generating histone modification and transcription factor ChIP-seq in parallel with transcriptomics datasets in 5 tissues of 3 inbred lines which span the phenotypic diversity of maize, as well as the teosinte inbred TIL11. Integrated analysis of these datasets resulted in the identification of a comprehensive set of regulatory regions in each inbred, and notably of distal enhancers which were differentiated from gene bodies by their lack of H3K4me1. Many of these distal enhancers expressed noncoding enhancer RNAs bi-directionally, reminiscent of “super enhancers” in animal genomes. We show that pollen grains are the most differentiated tissue at the transcriptomic level, and share features with endosperm that may be related to McClintock’s chromosome breakagefusion-bridge cycle. Conversely, ears have the least conservation between maize and teosinte, both in gene expression and within regulatory regions, reflecting conspicuous morphological differences selected during domestication. The identification of molecular signatures of domestication in transcriptional regulatory regions provides a framework for directed breeding strategies in maize.
Project description:Modern maize was domesticated from Teosinte parviglumis, with subsequent introgressions from Teosinte mexicana, yielding increased kernel row number, loss of the hard fruit case and dissociation from the cob upon maturity, as well as fewer tillers. Molecular approaches have identified several transcription factors involved in the development of these traits, yet revealed that a complex regulatory network is at play. MaizeCODE deploys ENCODE strategies to catalog regulatory regions in the maize genome, generating histone modification and transcription factor ChIP-seq in parallel with transcriptomics datasets in 5 tissues of 3 inbred lines which span the phenotypic diversity of maize, as well as the teosinte inbred TIL11. Integrated analysis of these datasets resulted in the identification of a comprehensive set of regulatory regions in each inbred, and notably of distal enhancers which were differentiated from gene bodies by their lack of H3K4me1. Many of these distal enhancers expressed noncoding enhancer RNAs bi-directionally, reminiscent of “super enhancers” in animal genomes. We show that pollen grains are the most differentiated tissue at the transcriptomic level, and share features with endosperm that may be related to McClintock’s chromosome breakagefusion-bridge cycle. Conversely, ears have the least conservation between maize and teosinte, both in gene expression and within regulatory regions, reflecting conspicuous morphological differences selected during domestication. The identification of molecular signatures of domestication in transcriptional regulatory regions provides a framework for directed breeding strategies in maize.