Malone JH et al. (2007), Sterility and gene expression in hybrid males o...

XB-ART-36379

PLoS One 2007 Aug 08;28:e781. doi: 10.1371/journal.pone.0000781.

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Sterility and gene expression in hybrid males of Xenopus laevis and X. muelleri.

Malone JH , Chrzanowski TH , Michalak P .

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Reproductive isolation is a defining characteristic of populations that represent unique biological species, yet we know very little about the gene expression basis for reproductive isolation. The advent of powerful molecular biology tools provides the ability to identify genes involved in reproductive isolation and focuses attention on the molecular mechanisms that separate biological species. Herein we quantify the sterility pattern of hybrid males in African Clawed Frogs (Xenopus) and apply microarray analysis of the expression pattern found in testes to identify genes that are misexpressed in hybrid males relative to their two parental species (Xenopus laevis and X. muelleri). Phenotypic characteristics of spermatogenesis in sterile male hybrids (X. laevis x X. muelleri) were examined using a novel sperm assay that allowed quantification of live, dead, and undifferentiated sperm cells, the number of motile vs. immotile sperm, and sperm morphology. Hybrids exhibited a dramatically lower abundance of mature sperm relative to the parental species. Hybrid spermatozoa were larger in size and accompanied by numerous undifferentiated sperm cells. Microarray analysis of gene expression in testes was combined with a correction for sequence divergence derived from genomic hybridizations to identify candidate genes involved in the sterility phenotype. Analysis of the transcriptome revealed a striking asymmetric pattern of misexpression. There were only about 140 genes misexpressed in hybrids compared to X. laevis but nearly 4,000 genes misexpressed in hybrids compared to X. muelleri. Our results provide an important correlation between phenotypic characteristics of sperm and gene expression in sterile hybrid males. The broad pattern of gene misexpression suggests intriguing mechanisms creating the dominance pattern of the X. laevis genome in hybrids. These findings significantly contribute to growing evidence for allelic dominance in hybrids and have implications for the mechanism of species differentiation at the transcriptome level.

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References [+] :

Adams, Novel patterns of gene expression in polyploid plants. 2005, Pubmed

Adams, Novel patterns of gene expression in polyploid plants. 2005, Pubmed
Altschul, Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. 1997, Pubmed
Appels, The wheat ribosomal DNA spacer region: Its structure and variation in populations and among species. 1982, Pubmed
Auger, Nonadditive gene expression in diploid and triploid hybrids of maize. 2005, Pubmed
Barbash, Lethality in Drosophila melanogaster/Drosophila simulans species hybrids is not associated with substantial transcriptional misregulation. 2007, Pubmed
Bauer-Dantoin, Neuropeptide Y potentiates luteinizing hormone (LH)-releasing hormone-induced LH secretion only under conditions leading to preovulatory LH surges. 1992, Pubmed
Birchler, Dosage balance in gene regulation: biological implications. 2005, Pubmed
Blackler, Transmission of sex cells of one species through the body of a second species in the genus Xenopus. II. Interspecific matings. 1972, Pubmed , Xenbase
Boseley, Sequence organization of the spacer DNA in a ribosomal gene unit of Xenopus laevis. 1979, Pubmed , Xenbase
Bramwell, Ribosomal RNA synthesis in human-mouse hybrid cells. 1971, Pubmed
Brandeis, Cyclin B2-null mice develop normally and are fertile whereas cyclin B1-null mice die in utero. 1998, Pubmed
Brown, Xenopus borealis misidentified as Xenopus mulleri. 1977, Pubmed , Xenbase
Brun, Functional haplodiploidy: a mechanism for the spread of insecticide resistance in an important international insect pest. 1995, Pubmed
Busby, Spacer sequences regulate transcription of ribosomal gene plasmids injected into Xenopus embryos. 1983, Pubmed , Xenbase
Cassidy, Repression of nucleolar organizer activity in an interspecific hybrid of the genus Xenopus. 1974, Pubmed , Xenbase
Chain, Multiple mechanisms promote the retained expression of gene duplicates in the tetraploid frog Xenopus laevis. 2006, Pubmed , Xenbase
Chen, Epigenetic silencing of RNA polymerase I transcription: a role for DNA methylation and histone modification in nucleolar dominance. 1997, Pubmed
Chen, Transcriptional analysis of nucleolar dominance in polyploid plants: biased expression/silencing of progenitor rRNA genes is developmentally regulated in Brassica. 1997, Pubmed
Chen, Gene dosage and stochastic effects determine the severity and direction of uniparental ribosomal RNA gene silencing (nucleolar dominance) in Arabidopsis allopolyploids. 1998, Pubmed
Chen, Mechanisms of genomic rearrangements and gene expression changes in plant polyploids. 2006, Pubmed
Comai, Do the different parental 'heteromes' cause genomic shock in newly formed allopolyploids? 2003, Pubmed
Croce, Suppression of production of mouse 28S ribosomal RNA in mouse-human hybrids segregating mouse chromosomes. 1977, Pubmed
Crouse, The Controlling Element in Sex Chromosome Behavior in Sciara. 1960, Pubmed
Diederichs, Expression patterns of mitotic and meiotic cell cycle regulators in testicular cancer and development. 2005, Pubmed
Dobson, Evidence for a genomic imprinting sex determination mechanism in Nasonia vitripennis (Hymenoptera; Chalcidoidea). 1998, Pubmed
Doelling, Species-specificity of rRNA gene transcription in plants manifested as a switch in RNA polymerase specificity. 1996, Pubmed
Dover, Molecular coevolution: DNA divergence and the maintenance of function. 1984, Pubmed , Xenbase
Durica, Studies on the ribosomal RNA cistrons in interspecific Drosophila hybrids. I. Nucleolar dominance. 1977, Pubmed
Durica, Studies on the Ribosomal RNA Cistrons in Interspecific Drosophila Hybrids. II. Heterochromatic Regions Mediating Nucleolar Dominance. 1978, Pubmed
Eliceiri, Ribosomal RNA synthesis in human-mouse hybrid cells. 1969, Pubmed
Evans, A mitochondrial DNA phylogeny of African clawed frogs: phylogeography and implications for polyploid evolution. 2004, Pubmed , Xenbase
Evans, Evolution of RAG-1 in polyploid clawed frogs. 2005, Pubmed , Xenbase
Fan, In vitro transcription of plant RNA polymerase I-dependent rRNA genes is species-specific. 1995, Pubmed
Flavell, Regulation of cytosine methylation in ribosomal DNA and nucleolus organizer expression in wheat. 1988, Pubmed
Frieman, RNA polymerase I transcription in a Brassica interspecific hybrid and its progenitors: Tests of transcription factor involvement in nucleolar dominance. 1999, Pubmed
Galili, Rnf4, a RING protein expressed in the developing nervous and reproductive systems, interacts with Gscl, a gene within the DiGeorge critical region. 2000, Pubmed
Gehring, DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. 2006, Pubmed
Gilad, Using DNA microarrays to study natural variation. 2006, Pubmed
Gilad, Multi-species microarrays reveal the effect of sequence divergence on gene expression profiles. 2005, Pubmed
Goday, Chromosome elimination in sciarid flies. 2001, Pubmed
Graves, Molecular cloning, expression, and characterization of a 49-kilodalton casein kinase I isoform from rat testis. 1993, Pubmed
Grummt, Ribosomal RNA transcription in vitro is species specific. 1982, Pubmed
Gye, Expression of occludin in canine testis and epididymis. 2004, Pubmed
Haerty, Gene regulation divergence is a major contributor to the evolution of Dobzhansky-Muller incompatibilities between species of Drosophila. 2006, Pubmed
Hammond, Using genomic DNA-based probe-selection to improve the sensitivity of high-density oligonucleotide arrays when applied to heterologous species. 2005, Pubmed
Hayes, Sex determination and primary sex differentiation in amphibians: genetic and developmental mechanisms. 1998, Pubmed
Heard, X-chromosome inactivation in mammals. 1997, Pubmed
Hegarty, Transcriptome shock after interspecific hybridization in senecio is ameliorated by genome duplication. 2006, Pubmed
Honjo, Preferential transcription of Xenopus laevis ribosomal RNA in interspecies hybrids between Xenopus laevis and Xenopus mulleri. 1973, Pubmed , Xenbase
Hsu, Mouse type-2 retinaldehyde dehydrogenase (RALDH2): genomic organization, tissue-dependent expression, chromosome assignment and comparison to other types. 2000, Pubmed
Jenuwein, Translating the histone code. 2001, Pubmed
Jin, Size-selective junctional barrier and Ca(2+)-independent cell adhesion in the testis of Cynops pyrrhogaster: expression and function of occludin. 2008, Pubmed
Josefsson, Parent-dependent loss of gene silencing during interspecies hybridization. 2006, Pubmed
Kajiura-Kobayashi, The cloning of cyclin B3 and its gene expression during hormonally induced spermatogenesis in the teleost, Anguilla japonica. 2004, Pubmed
Kanzaki, Expression and regulation of neuropeptide Y messenger ribonucleic acid in cultured immature rat Leydig and Sertoli cells. 1996, Pubmed
Kaulen, The Xenopus B1 factor is closely related to the mammalian activator USF and is implicated in the developmental regulation of TFIIIA gene expression. 1991, Pubmed , Xenbase
Knox, Unmasking of neuropeptide-Y inhibitory effects on in vitro gonadotropin secretion from pituitaries of metestrous, but not proestrous, rats. 1995, Pubmed
LEVINE, A screening technique for photosynthetic mutants in unicellular algae. 1960, Pubmed
Labhart, Enhancer-like properties of the 60/81 bp elements in the ribosomal gene spacer of Xenopus laevis. 1984, Pubmed , Xenbase
Lai, Microarray analysis reveals differential gene expression in hybrid sunflower species. 2006, Pubmed
Landry, Compensatory cis-trans evolution and the dysregulation of gene expression in interspecific hybrids of Drosophila. 2005, Pubmed
MIKAMO, FUNCTIONAL SEX-REVERSAL IN GENETIC FEMALES OF XENOPUS LAEVIS, INDUCED BY IMPLANTED TESTES. 1963, Pubmed , Xenbase
Mable, Hybridization between tetraploid and diploid species of treefrogs (Genus hyla). 1995, Pubmed
Malone, Sex-biased gene expression in a ZW sex determination system. 2006, Pubmed , Xenbase
McStay, Nucleolar dominance: a model for rRNA gene silencing. 2006, Pubmed
Michalak, RNA world - the dark matter of evolutionary genomics. 2006, Pubmed
Michalak, Genome-wide patterns of expression in Drosophila pure species and hybrid males. 2003, Pubmed
Miesfeld, Species-specific rDNA transcription is due to promoter-specific binding factors. 1984, Pubmed
Miesfeld, The absence of a human-specific ribosomal DNA transcription factor leads to nucleolar dominance in mouse greater than human hybrid cells. 1984, Pubmed
Mikamo, Masculinization and breeding of the WW Xenopus. 1964, Pubmed , Xenbase
Miller, Expression of human and suppression of mouse nucleolus organizer activity in mouse-human somatic cell hybrids. 1976, Pubmed
Missirlis, Characterization of mitochondrial ferritin in Drosophila. 2006, Pubmed
Moehring, Genome-wide patterns of expression in Drosophila pure species and hybrid males. II. Examination of multiple-species hybridizations, platforms, and life cycle stages. 2007, Pubmed
Moss, A transcriptional function for the repetitive ribosomal spacer in Xenopus laevis. , Pubmed , Xenbase
Nicoloff, 'Nucleolar dominance' as observed in barley translocation lines with specifically reconstructed SAT chromosomes. 1979, Pubmed
Nielsen, Functional constraint underlies 60 million year stasis of Dipteran testis-specific beta-tubulin. 2006, Pubmed
Nuzhdin, Common pattern of evolution of gene expression level and protein sequence in Drosophila. 2004, Pubmed
Onishi, On the mechanism of nucleolar dominance in mouse-human somatic cell hybrids. 1984, Pubmed
Ortíz-Barrientos, Gene expression divergence and the origin of hybrid dysfunctions. 2007, Pubmed
Osborn, Understanding mechanisms of novel gene expression in polyploids. 2003, Pubmed
Pikaard, Nucleolar dominance: uniparental gene silencing on a multi-megabase scale in genetic hybrids. 2000, Pubmed
Pikaard, Sequence elements essential for function of the Xenopus laevis ribosomal DNA enhancers. 1988, Pubmed , Xenbase
Pilder, Hst7: a male sterility mutation perturbing sperm motility, flagellar assembly, and mitochondrial sheath differentiation. 1997, Pubmed
Porter, Speciation despite gene flow when developmental pathways evolve. 2002, Pubmed
Pozzi, Effect of human gonadotropins on spermiation and androgen biosynthesis in the testis of the toad Bufo arenarum (Amphibia, Anura). 2006, Pubmed
Presgraves, Adaptive evolution drives divergence of a hybrid inviability gene between two species of Drosophila. 2003, Pubmed
Presgraves, Haldane's rule in taxa lacking a hemizygous X. 1998, Pubmed
Presgraves, Patterns of postzygotic isolation in Lepidoptera. 2002, Pubmed
Ranz, Anomalies in the expression profile of interspecific hybrids of Drosophila melanogaster and Drosophila simulans. 2004, Pubmed
Reeder, Spacer regulation of Xenopus ribosomal gene transcription: competition in oocytes. 1983, Pubmed , Xenbase
Reeder, Enhancers and ribosomal gene spacers. 1984, Pubmed , Xenbase
Reeder, Mechanisms of nucleolar dominance in animals and plants. 1985, Pubmed
Reeder, The mechanism of nucleolar dominance in Xenopus hybrids. 1984, Pubmed , Xenbase
Reiland, Little qualitative RNA misexpression in sterile male F1 hybrids of Drosophila pseudoobscura and D. persimilis. 2002, Pubmed
Richards, Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. 2002, Pubmed
Rosemblit, Relationship between steroidogenesis and spermiation in Rana catesbeiana and Leptodactylus ocellatus. 2006, Pubmed
Sardana, Correlation between the size of the intergenic regulatory region, the status of cytosine methylation of rRNA genes and nucleolar expression in wheat. 1993, Pubmed
Schmid, Chromosome banding in Amphibia. XVI. High-resolution replication banding patterns in Xenopus laevis. 1991, Pubmed , Xenbase
Schnapp, Trans-acting factors involved in species-specificity and control of mouse ribosomal gene transcription. , Pubmed
Shilatifard, Chromatin modifications by methylation and ubiquitination: implications in the regulation of gene expression. 2006, Pubmed
Siu, Sertoli-germ cell anchoring junction dynamics in the testis are regulated by an interplay of lipid and protein kinases. 2005, Pubmed
Smith, HMG box transcription factor gene Hbp1 is expressed in germ cells of the developing mouse testis. 2004, Pubmed
Smith, Testis-specific expression of the beta2 tubulin promoter of Aedes aegypti and its application as a genetic sex-separation marker. 2007, Pubmed
Smyth, Linear models and empirical bayes methods for assessing differential expression in microarray experiments. 2004, Pubmed
Sollner-Webb, The nucleotide sequence of the initiation and termination sites for ribosomal RNA transcription in X. laevis. 1979, Pubmed , Xenbase
Soprano, Reactivation of ribosomal RNA genes in human-mouse hybrid cells by 12-O-tetradecanoylphorbol 13-acetate. 1980, Pubmed
Soprano, Reactivation of silent rRNA genes by simian virus 40 in human-mouse hybrid cells. 1979, Pubmed
Terado, Expression of Neuropeptide Y gene in mouse testes during testicular development. 2006, Pubmed
Thompson, DNase I sensitivity of ribosomal RNA genes in chromatin and nucleolar dominance in wheat. 1988, Pubmed , Xenbase
Tymowska, Karyotype analysis of Xenopus muelleri (Peters) and Xenopus laevis (Daudin), Pipidae. 1972, Pubmed , Xenbase
Vinogradov, Genome elimination in diploid and triploid Rana esculenta males: cytological evidence from DNA flow cytometry. 1990, Pubmed
Vonwyl, Expression of the lactate dehydrogenase genes of Xenopus species and interspecies hybrids during early development. 1983, Pubmed , Xenbase
Wall, Enzyme patterns in two species of Xenopus and their hybrids. 1974, Pubmed , Xenbase
Wang, Genomewide nonadditive gene regulation in Arabidopsis allotetraploids. 2006, Pubmed
Wang, Stochastic and epigenetic changes of gene expression in Arabidopsis polyploids. 2004, Pubmed
Wang, Stage-specific expression of dynein light chain-1 and its interacting kinase, p21-activated kinase-1, in rodent testes: implications in spermiogenesis. 2005, Pubmed
Wu, Evolution of postmating reproductive isolation: the composite nature of Haldane's rule and its genetic bases. 1993, Pubmed
Wu, Haldane's rule and its legacy: Why are there so many sterile males? 1996, Pubmed
de Robertis, Hybrids of Xenopus laevis and Xenopus borealis express proteins from both parents. 1979, Pubmed , Xenbase
de la Casa-Esperón, Natural selection and the evolution of genome imprinting. 2003, Pubmed

	Figure 1. Visualization of live (green) and dead (red) sperm in sperm density assay using dual emission filter for SYBR14 and propidium iodide.Xenopus laevis (A); hybrid (B); X. muelleri (C); and brightfield combined with fluorescent image of undifferentiated cells of hybrids (D).
	Figure 2. The number of total sperm cells in Xenopus laevis (black circles) and hybrids (striped squares) in uninjected sexually mature males and hCG injected sexually mature males.Error bars represent±1 standard error.
	Figure 3. Proportion of live (green circles), dead (red squares), and undifferentiated (black triangles) sperm cells in Xenopus laevis (A) and hybrids (B) in normal/uninjected compared to hCG injected males.Error bars represent±1 standard error.
	Figure 4. Numbers of motile (green circles) and immotile (red x's) sperm in Xenopus laevis and hybrids in normal/uninjected compared to hCG injected males.Error bars represent±1 standard error.
	Figure 5. Comparison of sperm area (µm2) in Xenopus laevis, X. muelleri, and hybrids and representative brightfield images of sperm.Error bars represent±1 standard error and * denotes significance from a Bonferroni multiple comparison test. Hybrids have larger sperm compared to X. laevis and X. muelleri but sperm area does not differ between X. laevis and X. muelleri.
	Figure 6. Number of probesets remaining at various thresholds from comparing the hybridization intensity of Xenopus muelleri vs. X. laevis.
	Figure 7. Volcano plots from FDR corrected t-tests of statistical significance (vertical axis) against magnitude of expression change (horizontal axis), where each point corresponds to a gene/transcript.Expression change (fold-change) is defined as a log2-transformed ratio of mean nonhybrid to mean hybrid expression level. (A) Xenopus laevis vs. Hybrids; (B) Xenpous muelleri vs. Hybrids. The red line denotes FDR adjusted alpha 0.05. The horizontal deviation from 0 towards the right or left reflects hybrid underexpression or overexpression, respectively.