Most cited article - PubMed ID 34571879
Degenerated, Undifferentiated, Rearranged, Lost: High Variability of Sex Chromosomes in Geometridae (Lepidoptera) Identified by Sex Chromatin
BACKGROUND: The primary signals of sex determination in insects are diverse and evolve erratically. This also appears to be the case with moths and butterflies. In the silkworm Bombyx mori, female development is triggered by a W chromosome-derived Feminizer (Fem) piRNA that degrades the mRNA of the Z-linked Masculinizer (Masc) gene, which controls male development. We investigated whether this mechanism is conserved in another group of Lepidoptera. RESULTS: We identified a putative feminizing piRNA and many partial copies of the EkMasc gene on the W chromosome of Ephestia kuehniella. The piRNA is generated by a repetitive W-linked sequence named E. kuehniella Moth-overruler-of-masculinization (EkMom). EkMom piRNA shows high similarity to a region of Z-linked EkMasc and is expressed at the onset of female development, but has no relationship to the B. mori Fem piRNA. We then mapped small RNA-seq data from embryos of the related Plodia interpunctella to the PiMasc gene and identified a single small RNA, a PiMom piRNA, able to target PiMasc and with high sequence identity to the EkMom piRNA. Both the PiMom and EkMom repeats are present in high copy number and form a single cluster on the W chromosome. In both species, the Mom piRNA is responsible for Masc mRNA cleavage, clearly demonstrating that the Mom piRNA triggers female development. CONCLUSIONS: Our study provides multiple lines of evidence that Mom piRNA is the primary sex-determining signal in two pyralid moths and highlights a possible pathway for the origin of feminizing piRNAs in Lepidoptera. The similarity in female sex determination between the phylogenetically distant species suggests convergent evolution of feminizing piRNAs in Lepidoptera.
- Keywords
- Ephestia kuehniella, Masculinizer, Plodia interpunctella, Feminizing piRNA, Lepidoptera, Sex chromosomes, Sex determination, Small RNA-seq,
- MeSH
- Biological Evolution * MeSH
- RNA, Small Interfering * genetics MeSH
- Evolution, Molecular * MeSH
- Moths * genetics MeSH
- Piwi-Interacting RNA MeSH
- Sex Chromosomes * genetics MeSH
- Sex Determination Processes * genetics MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- RNA, Small Interfering * MeSH
- Piwi-Interacting RNA MeSH
The cytogenetics of Acanthocephala is a neglected area in the study of this group of endoparasites. Chromosome number and/or karyotypes are known for only 12 of the 1,270 described species, and molecular cytogenetic data are limited to rDNA mapping in two species. The standard karyological technique and mapping of 18S rRNA and H3 histone genes on the chromosomes of Acanthocephalus anguillae individuals from three populations, one of which originated from the unfavorable environmental conditions of the Zemplínska Šírava reservoir in eastern Slovakia, were applied for the first time. All specimens had 2n = 7/8 (male/female); n = 1m + 1m-sm + 1a + 1a (X). Fluorescence in situ hybridization (FISH) revealed three loci of 18S rDNA on two autosomes and dispersion of H3 histone genes on all autosomes and the X chromosome. In addition to the standard A chromosome set, 34% of specimens from Zemplínska Šírava possessed a small acrocentric B chromosome, which was always found to be univalent, with no pairing observed between the B chromosome and the A complement. The B chromosome had a small amount of heterochromatin in the centromeric and telomeric regions of the chromosomal arms and showed two clusters of H3 genes. It is well known that an environment permanently polluted with chemicals leads to an increased incidence of chromosomal rearrangements. As a possible scenario for the B chromosome origin, we propose chromosomal breaks due to the mutagenic effect of pollutants in the aquatic environment. The results are discussed in comparison with previous chromosome data from Echinorhynchida species.
TITLE: Analyse chromosomique et présence de chromosomes B chez le parasite de poisson Acanthocephalus anguillae (Palaeacanthocephala, Echinorhynchida). ABSTRACT: La cytogénétique des Acanthocephala est un domaine négligé dans l’étude de ce groupe d’endoparasites. Le nombre de chromosomes et/ou les caryotypes ne sont connus que pour 12 des 1270 espèces décrites, et les données cytogénétiques moléculaires se limitent à la cartographie de l’ADNr chez deux espèces. La technique caryologique standard et la cartographie des gènes de l’ARNr 18S et de l’histone H3 ont été appliquées pour la première fois sur les chromosomes d’individus d’Acanthocephalus anguillae provenant de trois populations, dont l’une dans les conditions environnementales défavorables du réservoir de Zemplínska Šírava dans l’est de la Slovaquie. Tous les spécimens avaient 2n = 7/8 (mâle/femelle); n = 1m + 1m-sm + 1a + 1a (X). La technique FISH a révélé trois locus d’ADNr 18S sur deux autosomes et une dispersion des gènes de l’histone H3 sur tous les autosomes et sur le chromosome X. En plus de l’ensemble standard de chromosomes A, 34 % des spécimens de Zemplínska Šírava possédaient un petit chromosome B acrocentrique, qui s’est toujours révélé univalent, sans aucun appariement observé entre le chromosome B et le complément A. Le chromosome B avait une petite quantité d’hétérochromatine dans les régions centromériques et télomériques des bras chromosomiques et présentait deux groupes de gènes H3. Il est bien connu qu’un environnement pollué en permanence par des produits chimiques entraîne une incidence accrue de réarrangements chromosomiques. Comme scénario possible pour l’origine du chromosome B, nous proposons des cassures chromosomiques dues à l’effet mutagène des polluants du milieu aquatique. Les résultats sont discutés en comparaison avec les données chromosomiques précédentes des espèces d’Echinorhynchida.
- Keywords
- 18S rDNA, B chromosomes, Fluorescence in situ hybridization, H3 histone, Karyotype, PCB pollution,
- MeSH
- Acanthocephala * genetics MeSH
- Histones genetics MeSH
- In Situ Hybridization, Fluorescence methods MeSH
- Karyotype MeSH
- Humans MeSH
- Chromosome Mapping methods MeSH
- Parasites * genetics MeSH
- DNA, Ribosomal genetics MeSH
- Animals MeSH
- Check Tag
- Humans MeSH
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Histones MeSH
- DNA, Ribosomal MeSH
The W chromosome of Lepidoptera is typically gene-poor, repeat-rich and composed of heterochromatin. Pioneering studies investigating this chromosome reported an abundance of mobile elements. However, the actual composition of the W chromosome varies greatly between species, as repeatedly demonstrated by comparative genomic hybridization (CGH) or fluorescence in situ hybridization (FISH). Here we present an analysis of repeats on the W chromosome in the willow beauty, Peribatodes rhomboidaria (Geometridae), a species in which CGH predicted an abundance of W-enriched or W-specific sequences. Indeed, comparative analysis of male and female genomes using RepeatExplorer identified ten putative W chromosome-enriched repeats, most of which are LTR or LINE mobile elements. We analysed the two most abundant: PRW LINE-like and PRW Bel-Pao. The results of FISH mapping and bioinformatic analysis confirmed their enrichment on the W chromosome, supporting the hypothesis that mobile elements are the driving force of W chromosome differentiation in Lepidoptera. As the W chromosome is highly underrepresented in chromosome-level genome assemblies of Lepidoptera, this recently introduced approach, combining bioinformatic comparative genome analysis with molecular cytogenetics, provides an elegant tool for studying this elusive and rapidly evolving part of the genome.
- MeSH
- In Situ Hybridization, Fluorescence MeSH
- Moths * genetics MeSH
- Sex Chromosomes genetics MeSH
- Retroelements genetics MeSH
- Salix * genetics MeSH
- Comparative Genomic Hybridization MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Retroelements MeSH
Odonata have holokinetic chromosomes. About 95% of species have an XX/X0 sex chromosome system, with heterogametic males. There are species with neo-XX/neo-XY sex chromosomes resulting from an X chromosome/autosome fusion. The genus Rhionaeschna includes 42 species found in the Americas. We analyzed the distribution of the nucleolar organizer region (NOR) using FISH with rDNA probes in Rhionaeschna bonariensis (n = 12 + neo-XY), R. planaltica (n = 7 + neo-XY), and Aeshna cyanea (n = 13 + X0). In R. bonariensis and A. cyanea, the NOR is located on a large pair of autosomes, which have a secondary constriction in the latter species. In R. planaltica, the NOR is located on the ancestral part of the neo-X chromosome. Meiotic analysis and FISH results in R. planaltica led to the conclusion that the neo-XY system arose by insertion of the ancestral X chromosome into an autosome. Genomic in situ hybridization, performed for the first time in Odonata, highlighted the entire neo-Y chromosome in meiosis of R. bonariensis, suggesting that it consists mainly of repetitive DNA. This feature and the terminal chiasma localization suggest an ancient origin of the neo-XY system. Our study provides new information on the origin and evolution of neo-sex chromosomes in Odonata, including new types of chromosomal rearrangements, NOR transposition, and heterochromatin accumulation.
- Keywords
- FISH, GISH, dragonflies, holokinetic chromosomes, meiosis, neo-sex chromosome evolution, nucleolar organizer region, ribosomal DNA, structural rearrangements,
- Publication type
- Journal Article MeSH
Moths of the family Crambidae include a number of pests that cause economic losses to agricultural crops. Despite their economic importance, little is known about their genome architecture and chromosome evolution. Here, we characterized the chromosomes and repetitive DNA of the sugarcane borer Diatraea saccharalis using a combination of low-pass genome sequencing, bioinformatics, and cytogenetic methods, focusing on the sex chromosomes. Diploid chromosome numbers differed between the sexes, i.e., 2n = 33 in females and 2n = 34 in males. This difference was caused by the occurrence of a WZ1Z2 trivalent in female meiosis, indicating a multiple sex-chromosome system WZ1Z2/Z1Z1Z2Z2. A strong interstitial telomeric signal was observed on the W chromosome, indicating a fusion of the ancestral W chromosome with an autosome. Among repetitive DNAs, transposable elements (TEs) accounted for 39.18% (males) to 41.35% (females), while satDNAs accounted for only 0.214% (males) and 0.215% (females) of the genome. FISH mapping revealed different chromosomal organization of satDNAs, such as single localized clusters, spread repeats, and non-clustered repeats. Two TEs mapped by FISH were scattered. Although we found a slight enrichment of some satDNAs in the female genome, they were not differentially enriched on the W chromosome. However, we found enriched FISH signals for TEs on the W chromosome, suggesting their involvement in W chromosome degeneration and differentiation. These data shed light on karyotype and repetitive DNA dynamics due to multiple chromosome fusions in D. saccharalis, contribute to the understanding of genome structure in Lepidoptera and are important for future genomic studies.
- Keywords
- Chromosome fusion, FISH, Holocentric chromosome, Multiple sex chromosomes, W chromatin, satDNA,
- MeSH
- Karyotype MeSH
- Evolution, Molecular MeSH
- Moths * genetics MeSH
- Sex Chromosomes genetics MeSH
- Saccharum * genetics MeSH
- DNA Transposable Elements MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- DNA Transposable Elements MeSH