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1.
Curr Biol ; 25(5): 613-20, 2015 Mar 02.
Article in English | MEDLINE | ID: mdl-25660540

ABSTRACT

Gall-forming arthropods are highly specialized herbivores that, in combination with their hosts, produce extended phenotypes with unique morphologies [1]. Many are economically important, and others have improved our understanding of ecology and adaptive radiation [2]. However, the mechanisms that these arthropods use to induce plant galls are poorly understood. We sequenced the genome of the Hessian fly (Mayetiola destructor; Diptera: Cecidomyiidae), a plant parasitic gall midge and a pest of wheat (Triticum spp.), with the aim of identifying genic modifications that contribute to its plant-parasitic lifestyle. Among several adaptive modifications, we discovered an expansive reservoir of potential effector proteins. Nearly 5% of the 20,163 predicted gene models matched putative effector gene transcripts present in the M. destructor larval salivary gland. Another 466 putative effectors were discovered among the genes that have no sequence similarities in other organisms. The largest known arthropod gene family (family SSGP-71) was also discovered within the effector reservoir. SSGP-71 proteins lack sequence homologies to other proteins, but their structures resemble both ubiquitin E3 ligases in plants and E3-ligase-mimicking effectors in plant pathogenic bacteria. SSGP-71 proteins and wheat Skp proteins interact in vivo. Mutations in different SSGP-71 genes avoid the effector-triggered immunity that is directed by the wheat resistance genes H6 and H9. Results point to effectors as the agents responsible for arthropod-induced plant gall formation.


Subject(s)
Chromosomes/genetics , Diptera/genetics , Multigene Family/genetics , Phylogeny , Plant Tumors/genetics , Triticum/parasitology , Adaptation, Biological/genetics , Amino Acid Sequence , Animals , Base Sequence , Diptera/metabolism , Larva/metabolism , Models, Genetic , Molecular Sequence Data , Sequence Analysis, DNA , Sequence Homology , Sexual Behavior, Animal/physiology , Two-Hybrid System Techniques , Ubiquitin-Protein Ligases/genetics
2.
PLoS Biol ; 12(11): e1002005, 2014 Nov.
Article in English | MEDLINE | ID: mdl-25423365

ABSTRACT

Myriapods (e.g., centipedes and millipedes) display a simple homonomous body plan relative to other arthropods. All members of the class are terrestrial, but they attained terrestriality independently of insects. Myriapoda is the only arthropod class not represented by a sequenced genome. We present an analysis of the genome of the centipede Strigamia maritima. It retains a compact genome that has undergone less gene loss and shuffling than previously sequenced arthropods, and many orthologues of genes conserved from the bilaterian ancestor that have been lost in insects. Our analysis locates many genes in conserved macro-synteny contexts, and many small-scale examples of gene clustering. We describe several examples where S. maritima shows different solutions from insects to similar problems. The insect olfactory receptor gene family is absent from S. maritima, and olfaction in air is likely effected by expansion of other receptor gene families. For some genes S. maritima has evolved paralogues to generate coding sequence diversity, where insects use alternate splicing. This is most striking for the Dscam gene, which in Drosophila generates more than 100,000 alternate splice forms, but in S. maritima is encoded by over 100 paralogues. We see an intriguing linkage between the absence of any known photosensory proteins in a blind organism and the additional absence of canonical circadian clock genes. The phylogenetic position of myriapods allows us to identify where in arthropod phylogeny several particular molecular mechanisms and traits emerged. For example, we conclude that juvenile hormone signalling evolved with the emergence of the exoskeleton in the arthropods and that RR-1 containing cuticle proteins evolved in the lineage leading to Mandibulata. We also identify when various gene expansions and losses occurred. The genome of S. maritima offers us a unique glimpse into the ancestral arthropod genome, while also displaying many adaptations to its specific life history.


Subject(s)
Arthropods/genetics , Genome , Synteny , Animals , Circadian Rhythm Signaling Peptides and Proteins/genetics , DNA Methylation , Evolution, Molecular , Female , Genome, Mitochondrial , Hormones/genetics , Male , Multigene Family , Phylogeny , Polymorphism, Genetic , Protein Kinases/genetics , RNA, Untranslated/genetics , Receptors, Odorant/genetics , Selenoproteins/genetics , Sex Chromosomes , Transcription Factors/genetics
3.
Genome Res ; 24(7): 1209-23, 2014 Jul.
Article in English | MEDLINE | ID: mdl-24985915

ABSTRACT

Accurate gene model annotation of reference genomes is critical for making them useful. The modENCODE project has improved the D. melanogaster genome annotation by using deep and diverse high-throughput data. Since transcriptional activity that has been evolutionarily conserved is likely to have an advantageous function, we have performed large-scale interspecific comparisons to increase confidence in predicted annotations. To support comparative genomics, we filled in divergence gaps in the Drosophila phylogeny by generating draft genomes for eight new species. For comparative transcriptome analysis, we generated mRNA expression profiles on 81 samples from multiple tissues and developmental stages of 15 Drosophila species, and we performed cap analysis of gene expression in D. melanogaster and D. pseudoobscura. We also describe conservation of four distinct core promoter structures composed of combinations of elements at three positions. Overall, each type of genomic feature shows a characteristic divergence rate relative to neutral models, highlighting the value of multispecies alignment in annotating a target genome that should prove useful in the annotation of other high priority genomes, especially human and other mammalian genomes that are rich in noncoding sequences. We report that the vast majority of elements in the annotation are evolutionarily conserved, indicating that the annotation will be an important springboard for functional genetic testing by the Drosophila community.


Subject(s)
Computational Biology/methods , Drosophila melanogaster/genetics , Gene Expression Profiling , Molecular Sequence Annotation , Transcriptome , Animals , Cluster Analysis , Drosophila melanogaster/classification , Evolution, Molecular , Exons , Female , Genome, Insect , Humans , Male , Nucleotide Motifs , Phylogeny , Position-Specific Scoring Matrices , Promoter Regions, Genetic , RNA Editing , RNA Splice Sites , RNA Splicing , Reproducibility of Results , Transcription Initiation Site
4.
Genome Res ; 24(7): 1193-208, 2014 Jul.
Article in English | MEDLINE | ID: mdl-24714809

ABSTRACT

The Drosophila melanogaster Genetic Reference Panel (DGRP) is a community resource of 205 sequenced inbred lines, derived to improve our understanding of the effects of naturally occurring genetic variation on molecular and organismal phenotypes. We used an integrated genotyping strategy to identify 4,853,802 single nucleotide polymorphisms (SNPs) and 1,296,080 non-SNP variants. Our molecular population genomic analyses show higher deletion than insertion mutation rates and stronger purifying selection on deletions. Weaker selection on insertions than deletions is consistent with our observed distribution of genome size determined by flow cytometry, which is skewed toward larger genomes. Insertion/deletion and single nucleotide polymorphisms are positively correlated with each other and with local recombination, suggesting that their nonrandom distributions are due to hitchhiking and background selection. Our cytogenetic analysis identified 16 polymorphic inversions in the DGRP. Common inverted and standard karyotypes are genetically divergent and account for most of the variation in relatedness among the DGRP lines. Intriguingly, variation in genome size and many quantitative traits are significantly associated with inversions. Approximately 50% of the DGRP lines are infected with Wolbachia, and four lines have germline insertions of Wolbachia sequences, but effects of Wolbachia infection on quantitative traits are rarely significant. The DGRP complements ongoing efforts to functionally annotate the Drosophila genome. Indeed, 15% of all D. melanogaster genes segregate for potentially damaged proteins in the DGRP, and genome-wide analyses of quantitative traits identify novel candidate genes. The DGRP lines, sequence data, genotypes, quality scores, phenotypes, and analysis and visualization tools are publicly available.


Subject(s)
Drosophila melanogaster/genetics , Genetic Variation , Genome, Insect , Phenotype , Animals , Chromatin/genetics , Chromatin/metabolism , Drosophila melanogaster/microbiology , Female , Genetic Linkage , Genome Size , Genome-Wide Association Study , Genotype , Genotyping Techniques , High-Throughput Nucleotide Sequencing , INDEL Mutation , Linkage Disequilibrium , Male , Molecular Sequence Annotation , Polymorphism, Single Nucleotide , Quantitative Trait, Heritable , Reproducibility of Results
5.
Proc Natl Acad Sci U S A ; 109(39): 15553-9, 2012 Sep 25.
Article in English | MEDLINE | ID: mdl-22949659

ABSTRACT

Epistasis-nonlinear genetic interactions between polymorphic loci-is the genetic basis of canalization and speciation, and epistatic interactions can be used to infer genetic networks affecting quantitative traits. However, the role that epistasis plays in the genetic architecture of quantitative traits is controversial. Here, we compared the genetic architecture of three Drosophila life history traits in the sequenced inbred lines of the Drosophila melanogaster Genetic Reference Panel (DGRP) and a large outbred, advanced intercross population derived from 40 DGRP lines (Flyland). We assessed allele frequency changes between pools of individuals at the extremes of the distribution for each trait in the Flyland population by deep DNA sequencing. The genetic architecture of all traits was highly polygenic in both analyses. Surprisingly, none of the SNPs associated with the traits in Flyland replicated in the DGRP and vice versa. However, the majority of these SNPs participated in at least one epistatic interaction in the DGRP. Despite apparent additive effects at largely distinct loci in the two populations, the epistatic interactions perturbed common, biologically plausible, and highly connected genetic networks. Our analysis underscores the importance of epistasis as a principal factor that determines variation for quantitative traits and provides a means to uncover genetic networks affecting these traits. Knowledge of epistatic networks will contribute to our understanding of the genetic basis of evolutionarily and clinically important traits and enhance predictive ability at an individualized level in medicine and agriculture.


Subject(s)
Epistasis, Genetic/physiology , Genes, Insect/physiology , Quantitative Trait, Heritable , Animals , Drosophila melanogaster , Polymorphism, Single Nucleotide
6.
Nature ; 482(7384): 173-8, 2012 Feb 08.
Article in English | MEDLINE | ID: mdl-22318601

ABSTRACT

A major challenge of biology is understanding the relationship between molecular genetic variation and variation in quantitative traits, including fitness. This relationship determines our ability to predict phenotypes from genotypes and to understand how evolutionary forces shape variation within and between species. Previous efforts to dissect the genotype-phenotype map were based on incomplete genotypic information. Here, we describe the Drosophila melanogaster Genetic Reference Panel (DGRP), a community resource for analysis of population genomics and quantitative traits. The DGRP consists of fully sequenced inbred lines derived from a natural population. Population genomic analyses reveal reduced polymorphism in centromeric autosomal regions and the X chromosome, evidence for positive and negative selection, and rapid evolution of the X chromosome. Many variants in novel genes, most at low frequency, are associated with quantitative traits and explain a large fraction of the phenotypic variance. The DGRP facilitates genotype-phenotype mapping using the power of Drosophila genetics.


Subject(s)
Drosophila melanogaster/genetics , Genome-Wide Association Study , Genomics , Quantitative Trait Loci/genetics , Alleles , Animals , Centromere/genetics , Chromosomes, Insect/genetics , Genotype , Phenotype , Polymorphism, Single Nucleotide/genetics , Selection, Genetic/genetics , Starvation/genetics , Telomere/genetics , X Chromosome/genetics
7.
Dev Biol ; 354(1): 1-8, 2011 Jun 01.
Article in English | MEDLINE | ID: mdl-21458440

ABSTRACT

We present a genetic map for Xenopus tropicalis, consisting of 2886 Simple Sequence Length Polymorphism (SSLP) markers. Using a bioinformatics-based strategy, we identified unique SSLPs within the X. tropicalis genome. Scaffolds from X. tropicalis genome assembly 2.0 (JGI) were scanned for Simple Sequence Repeats (SSRs); unique SSRs were then tested for amplification and polymorphisms using DNA from inbred Nigerian and Ivory Coast individuals. Thus identified, the SSLPs were genotyped against a mapping cross panel of DNA samples from 190 F2 individuals. Nearly 4000 SSLPs were genotyped, yielding a 2886-marker genetic map consisting of 10 major linkage groups between 73 and 132cM in length, and 4 smaller linkage groups between 7 and 40cM. The total effective size of the map is 1658cM, and the average intermarker distance for each linkage group ranged from 0.27 to 0.75cM. Fluorescence In Situ Hybridization (FISH) was carried out using probes for genes located on mapped scaffolds to assign linkage groups to chromosomes. Comparisons of this map with the X. tropicalis genome Assembly 4.1 (JGI) indicate that the map provides representation of a minimum of 66% of the X. tropicalis genome, incorporating 758 of the approximately 1300 scaffolds over 100,000bp. The genetic map and SSLP marker database constitute an essential resource for genetic and genomic analyses in X. tropicalis.


Subject(s)
Chromosome Mapping/methods , Genetic Markers/genetics , Spectral Karyotyping/methods , Xenopus/genetics , Animals , Chromosome Banding , Genome/genetics , Genotype , Internet , Minisatellite Repeats/genetics , Polymorphism, Genetic , Xenopus Proteins/genetics
8.
Nature ; 452(7190): 949-55, 2008 Apr 24.
Article in English | MEDLINE | ID: mdl-18362917

ABSTRACT

Tribolium castaneum is a member of the most species-rich eukaryotic order, a powerful model organism for the study of generalized insect development, and an important pest of stored agricultural products. We describe its genome sequence here. This omnivorous beetle has evolved the ability to interact with a diverse chemical environment, as shown by large expansions in odorant and gustatory receptors, as well as P450 and other detoxification enzymes. Development in Tribolium is more representative of other insects than is Drosophila, a fact reflected in gene content and function. For example, Tribolium has retained more ancestral genes involved in cell-cell communication than Drosophila, some being expressed in the growth zone crucial for axial elongation in short-germ development. Systemic RNA interference in T. castaneum functions differently from that in Caenorhabditis elegans, but nevertheless offers similar power for the elucidation of gene function and identification of targets for selective insect control.


Subject(s)
Genes, Insect/genetics , Genome, Insect/genetics , Tribolium/genetics , Animals , Base Composition , Body Patterning/genetics , Cytochrome P-450 Enzyme System/genetics , DNA Transposable Elements/genetics , Growth and Development/genetics , Humans , Insecticides/pharmacology , Neurotransmitter Agents/genetics , Oogenesis/genetics , Phylogeny , Proteome/genetics , RNA Interference , Receptors, G-Protein-Coupled/genetics , Receptors, Odorant/genetics , Repetitive Sequences, Nucleic Acid/genetics , Taste/genetics , Telomere/genetics , Tribolium/classification , Tribolium/embryology , Tribolium/physiology , Vision, Ocular/genetics
9.
Nature ; 440(7088): 1194-8, 2006 Apr 27.
Article in English | MEDLINE | ID: mdl-16641997

ABSTRACT

After the completion of a draft human genome sequence, the International Human Genome Sequencing Consortium has proceeded to finish and annotate each of the 24 chromosomes comprising the human genome. Here we describe the sequencing and analysis of human chromosome 3, one of the largest human chromosomes. Chromosome 3 comprises just four contigs, one of which currently represents the longest unbroken stretch of finished DNA sequence known so far. The chromosome is remarkable in having the lowest rate of segmental duplication in the genome. It also includes a chemokine receptor gene cluster as well as numerous loci involved in multiple human cancers such as the gene encoding FHIT, which contains the most common constitutive fragile site in the genome, FRA3B. Using genomic sequence from chimpanzee and rhesus macaque, we were able to characterize the breakpoints defining a large pericentric inversion that occurred some time after the split of Homininae from Ponginae, and propose an evolutionary history of the inversion.


Subject(s)
Chromosomes, Human, Pair 3/genetics , Animals , Base Sequence , Chromosome Breakage/genetics , Chromosome Inversion/genetics , Contig Mapping , CpG Islands/genetics , DNA, Complementary/genetics , Evolution, Molecular , Expressed Sequence Tags , Human Genome Project , Humans , Macaca mulatta/genetics , Molecular Sequence Data , Pan troglodytes/genetics , Sequence Analysis, DNA , Synteny/genetics
10.
Nature ; 440(7082): 346-51, 2006 Mar 16.
Article in English | MEDLINE | ID: mdl-16541075

ABSTRACT

Human chromosome 12 contains more than 1,400 coding genes and 487 loci that have been directly implicated in human disease. The q arm of chromosome 12 contains one of the largest blocks of linkage disequilibrium found in the human genome. Here we present the finished sequence of human chromosome 12, which has been finished to high quality and spans approximately 132 megabases, representing approximately 4.5% of the human genome. Alignment of the human chromosome 12 sequence across vertebrates reveals the origin of individual segments in chicken, and a unique history of rearrangement through rodent and primate lineages. The rate of base substitutions in recent evolutionary history shows an overall slowing in hominids compared with primates and rodents.


Subject(s)
Chromosomes, Human, Pair 12/genetics , Animals , Base Composition , CpG Islands/genetics , Evolution, Molecular , Expressed Sequence Tags , Genes/genetics , Humans , Linkage Disequilibrium/genetics , Microsatellite Repeats/genetics , Molecular Sequence Data , Mutagenesis, Insertional/genetics , Pan troglodytes/genetics , Sequence Analysis, DNA , Sequence Deletion/genetics , Short Interspersed Nucleotide Elements/genetics , Synteny/genetics
11.
Genome Res ; 15(1): 1-18, 2005 Jan.
Article in English | MEDLINE | ID: mdl-15632085

ABSTRACT

We have sequenced the genome of a second Drosophila species, Drosophila pseudoobscura, and compared this to the genome sequence of Drosophila melanogaster, a primary model organism. Throughout evolution the vast majority of Drosophila genes have remained on the same chromosome arm, but within each arm gene order has been extensively reshuffled, leading to a minimum of 921 syntenic blocks shared between the species. A repetitive sequence is found in the D. pseudoobscura genome at many junctions between adjacent syntenic blocks. Analysis of this novel repetitive element family suggests that recombination between offset elements may have given rise to many paracentric inversions, thereby contributing to the shuffling of gene order in the D. pseudoobscura lineage. Based on sequence similarity and synteny, 10,516 putative orthologs have been identified as a core gene set conserved over 25-55 million years (Myr) since the pseudoobscura/melanogaster divergence. Genes expressed in the testes had higher amino acid sequence divergence than the genome-wide average, consistent with the rapid evolution of sex-specific proteins. Cis-regulatory sequences are more conserved than random and nearby sequences between the species--but the difference is slight, suggesting that the evolution of cis-regulatory elements is flexible. Overall, a pattern of repeat-mediated chromosomal rearrangement, and high coadaptation of both male genes and cis-regulatory sequences emerges as important themes of genome divergence between these species of Drosophila.


Subject(s)
Chromosomes/genetics , Drosophila/genetics , Evolution, Molecular , Genes, Insect/genetics , Genome , Sequence Analysis, DNA/methods , Animals , Chromosome Breakage/genetics , Chromosome Inversion/genetics , Chromosome Mapping/methods , Conserved Sequence/genetics , Drosophila melanogaster/genetics , Enhancer Elements, Genetic , Gene Rearrangement/genetics , Genetic Variation/genetics , Molecular Sequence Data , Predictive Value of Tests , Repetitive Sequences, Nucleic Acid/genetics
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