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Article: Stronger evidence for relaxed selection than adaptive evolution in high-elevation animal mtDNA.

Iverson, Erik N K / Criswell, Abby / Havird, Justin C

bioRxiv : the preprint server for biology

2024

Abstract: Mitochondrial (mt) genes are the subject of many adaptive hypotheses due to the key role of mitochondria in energy production and metabolism. One widespread adaptive hypothesis is that selection imposed by life at high elevation leads to the rapid ... ...

Abstract	Mitochondrial (mt) genes are the subject of many adaptive hypotheses due to the key role of mitochondria in energy production and metabolism. One widespread adaptive hypothesis is that selection imposed by life at high elevation leads to the rapid fixation of beneficial alleles in mtDNA, reflected in the increased rates of mtDNA evolution documented in many high-elevation species. However, the assumption that fast mtDNA evolution is caused by positive, rather than relaxed purifying selection has rarely been tested. Here, we calculated the
Language	English
Publishing date	2024-01-23
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.20.576402
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Article: The revised reference genome of the leopard gecko (

Pinto, Brendan J / Gamble, Tony / Smith, Chase H / Keating, Shannon E / Havird, Justin C / Chiari, Ylenia

bioRxiv : the preprint server for biology

2023

Abstract: Genomic resources across squamate reptiles (lizards and snakes) have lagged behind other vertebrate systems and high-quality reference genomes remain scarce. Of the 23 chromosome-scale reference genomes across the order, only 12 of the ~60 squamate ... ...

Abstract	Genomic resources across squamate reptiles (lizards and snakes) have lagged behind other vertebrate systems and high-quality reference genomes remain scarce. Of the 23 chromosome-scale reference genomes across the order, only 12 of the ~60 squamate families are represented. Within geckos (infraorder Gekkota), a species-rich clade of lizards, chromosome-level genomes are exceptionally sparse representing only two of the seven extant families. Using the latest advances in genome sequencing and assembly methods, we generated one of the highest quality squamate genomes to date for the leopard gecko,
Language	English
Publishing date	2023-02-13
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.01.20.523807
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Article ; Online: The revised reference genome of the leopard gecko (Eublepharis macularius) provides insight into the considerations of genome phasing and assembly.

Pinto, Brendan J / Gamble, Tony / Smith, Chase H / Keating, Shannon E / Havird, Justin C / Chiari, Ylenia

The Journal of heredity

2023 Volume 114, Issue 5, Page(s) 513–520

Abstract	Genomic resources across squamate reptiles (lizards and snakes) have lagged behind other vertebrate systems and high-quality reference genomes remain scarce. Of the 23 chromosome-scale reference genomes across the order, only 12 of the ~60 squamate families are represented. Within geckos (infraorder Gekkota), a species-rich clade of lizards, chromosome-level genomes are exceptionally sparse representing only two of the seven extant families. Using the latest advances in genome sequencing and assembly methods, we generated one of the highest-quality squamate genomes to date for the leopard gecko, Eublepharis macularius (Eublepharidae). We compared this assembly to the previous, short-read only, E. macularius reference genome published in 2016 and examined potential factors within the assembly influencing contiguity of genome assemblies using PacBio HiFi data. Briefly, the read N50 of the PacBio HiFi reads generated for this study was equal to the contig N50 of the previous E. macularius reference genome at 20.4 kilobases. The HiFi reads were assembled into a total of 132 contigs, which was further scaffolded using HiC data into 75 total sequences representing all 19 chromosomes. We identified 9 of the 19 chromosomal scaffolds were assembled as a near-single contig, whereas the other 10 chromosomes were each scaffolded together from multiple contigs. We qualitatively identified that the percent repeat content within a chromosome broadly affects its assembly contiguity prior to scaffolding. This genome assembly signifies a new age for squamate genomics where high-quality reference genomes rivaling some of the best vertebrate genome assemblies can be generated for a fraction of previous cost estimates. This new E. macularius reference assembly is available on NCBI at JAOPLA010000000.
MeSH term(s)	Humans ; Animals ; Genome ; Genomics/methods ; Chromosome Mapping/methods ; Chromosomes ; Lizards/genetics
Language	English
Publishing date	2023-03-03
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	3044-2
ISSN	1465-7333 ; 0022-1503
ISSN (online)	1465-7333
ISSN	0022-1503
DOI	10.1093/jhered/esad016
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Article ; Online: Genomic Signatures of Mitonuclear Coevolution in Mammals.

Weaver, Ryan J / Rabinowitz, Samantha / Thueson, Kiley / Havird, Justin C

Molecular biology and evolution

2022 Volume 39, Issue 11

Abstract: Mitochondrial (mt) and nuclear-encoded proteins are integrated in aerobic respiration, requiring co-functionality among gene products from fundamentally different genomes. Different evolutionary rates, inheritance mechanisms, and selection pressures set ... ...

Abstract	Mitochondrial (mt) and nuclear-encoded proteins are integrated in aerobic respiration, requiring co-functionality among gene products from fundamentally different genomes. Different evolutionary rates, inheritance mechanisms, and selection pressures set the stage for incompatibilities between interacting products of the two genomes. The mitonuclear coevolution hypothesis posits that incompatibilities may be avoided if evolution in one genome selects for complementary changes in interacting genes encoded by the other genome. Nuclear compensation, in which deleterious mtDNA changes are offset by compensatory nuclear changes, is often invoked as the primary mechanism for mitonuclear coevolution. Yet, direct evidence supporting nuclear compensation is rare. Here, we used data from 58 mammalian species representing eight orders to show strong correlations between evolutionary rates of mt and nuclear-encoded mt-targeted (N-mt) proteins, but not between mt and non-mt-targeted nuclear proteins, providing strong support for mitonuclear coevolution across mammals. N-mt genes with direct mt interactions also showed the strongest correlations. Although most N-mt genes had elevated dN/dS ratios compared to mt genes (as predicted under nuclear compensation), N-mt sites in close contact with mt proteins were not overrepresented for signs of positive selection compared to noncontact N-mt sites (contrary to predictions of nuclear compensation). Furthermore, temporal patterns of N-mt and mt amino acid substitutions did not support predictions of nuclear compensation, even in positively selected, functionally important residues with direct mitonuclear contacts. Overall, our results strongly support mitonuclear coevolution across ∼170 million years of mammalian evolution but fail to support nuclear compensation as the major mode of mitonuclear coevolution.
MeSH term(s)	Animals ; DNA, Mitochondrial/genetics ; Genes, Mitochondrial ; Mammals/genetics ; Cell Nucleus/genetics ; Mitochondrial Proteins/genetics ; Genomics
Chemical Substances	DNA, Mitochondrial ; Mitochondrial Proteins
Language	English
Publishing date	2022-10-26
Publishing country	United States
Document type	Journal Article ; Research Support, U.S. Gov't, Non-P.H.S. ; Research Support, N.I.H., Extramural
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msac233
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Article ; Online: Disentangling Positive Selection from Relaxed Selection in Animal Mitochondrial Genomes.

Zwonitzer, Kendra D / Iverson, Erik N K / Sterling, Jess E / Weaver, Ryan J / Maclaine, Bradley A / Havird, Justin C

The American naturalist

2023 Volume 202, Issue 4, Page(s) E121–E129

Abstract: AbstractDisentangling different types of selection is a common goal in molecular evolution. ... ...

Abstract	AbstractDisentangling different types of selection is a common goal in molecular evolution. Elevated
MeSH term(s)	Animals ; Genome, Mitochondrial ; Phylogeny ; Selection, Genetic ; Evolution, Molecular ; Primates/genetics ; DNA, Mitochondrial/genetics
Chemical Substances	DNA, Mitochondrial
Language	English
Publishing date	2023-08-31
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	207092-3
ISSN	1537-5323 ; 0003-0147
ISSN (online)	1537-5323
ISSN	0003-0147
DOI	10.1086/725805
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Article ; Online: Mitochondrial mutations in Caenorhabditis elegans show signatures of oxidative damage and an AT-bias.

Waneka, Gus / Svendsen, Joshua M / Havird, Justin C / Sloan, Daniel B

Genetics

2021 Volume 219, Issue 2

Abstract: ... extreme AT bias in the C. elegans mtDNA (75.6% AT), we found that a significant majority of mutations ... resolution view of mitochondrial mutations in C. elegans highlights the value of this system ...

Abstract	Rapid mutation rates are typical of mitochondrial genomes (mtDNAs) in animals, but it is not clear why. The difficulty of obtaining measurements of mtDNA mutation that are not biased by natural selection has stymied efforts to distinguish between competing hypotheses about the causes of high mtDNA mutation rates. Several studies which have measured mtDNA mutations in nematodes have yielded small datasets with conflicting conclusions about the relative abundance of different substitution classes (i.e., the mutation spectrum). We therefore leveraged Duplex Sequencing, a high-fidelity DNA sequencing technique, to characterize de novo mtDNA mutations in Caenorhabditis elegans. This approach detected nearly an order of magnitude more mtDNA mutations than documented in any previous nematode mutation study. Despite an existing extreme AT bias in the C. elegans mtDNA (75.6% AT), we found that a significant majority of mutations increase genomic AT content. Compared to some prior studies in nematodes and other animals, the mutation spectrum reported here contains an abundance of CG→AT transversions, supporting the hypothesis that oxidative damage may be a driver of mtDNA mutations in nematodes. Furthermore, we found an excess of G→T and C→T changes on the coding DNA strand relative to the template strand, consistent with increased exposure to oxidative damage. Analysis of the distribution of mutations across the mtDNA revealed significant variation among protein-coding genes and as well as among neighboring nucleotides. This high-resolution view of mitochondrial mutations in C. elegans highlights the value of this system for understanding relationships among oxidative damage, replication error, and mtDNA mutation.
MeSH term(s)	AT Rich Sequence ; Animals ; Base Composition ; Caenorhabditis elegans ; DNA, Mitochondrial/genetics ; Mutation ; Oxidative Stress
Chemical Substances	DNA, Mitochondrial
Language	English
Publishing date	2021-11-30
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2167-2
ISSN	1943-2631 ; 0016-6731
ISSN (online)	1943-2631
ISSN	0016-6731
DOI	10.1093/genetics/iyab116
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Article: Mitonuclear sex determination? Empirical evidence from bivalves.

Smith, Chase H / Mejia-Trujillo, Raquel / Breton, Sophie / Pinto, Brendan J / Kirkpatrick, Mark / Havird, Justin C

bioRxiv : the preprint server for biology

2023

Abstract: Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In bivalves, however, mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination in lineages that possess doubly uniparental inheritance ( ... ...

Abstract	Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In bivalves, however, mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination in lineages that possess doubly uniparental inheritance (DUI). In these cases, females transmit a female mtDNA (F mtDNA) to all offspring, while male mtDNA (M mtDNA) is transmitted only from fathers to sons. Because M mtDNA is inherited in the same way as Y chromosomes, it has been hypothesized that mtDNA may be responsible for sex determination. However, the role of mitochondrial and nuclear genes in sex determination has yet to be validated in DUI bivalves. In this study, we used DNA, RNA, and mitochondrial short non-coding RNA (sncRNA) sequencing to explore the role of mitochondrial and nuclear elements in the sexual development pathway of the freshwater mussel
Language	English
Publishing date	2023-07-07
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.05.547839
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Article ; Online: Did doubly uniparental inheritance (DUI) of mtDNA originate as a cytoplasmic male sterility (CMS) system?

Breton, Sophie / Stewart, Donald T / Brémaud, Julie / Havird, Justin C / Smith, Chase H / Hoeh, Walter R

BioEssays : news and reviews in molecular, cellular and developmental biology

2022 Volume 44, Issue 4, Page(s) e2100283

Abstract: Animal and plant species exhibit an astonishing diversity of sexual systems, including environmental and genetic determinants of sex, with the latter including genetic material in the mitochondrial genome. In several hermaphroditic plants for example, ... ...

Abstract	Animal and plant species exhibit an astonishing diversity of sexual systems, including environmental and genetic determinants of sex, with the latter including genetic material in the mitochondrial genome. In several hermaphroditic plants for example, sex is determined by an interaction between mitochondrial cytoplasmic male sterility (CMS) genes and nuclear restorer genes. Specifically, CMS involves aberrant mitochondrial genes that prevent pollen development and specific nuclear genes that restore it, leading to a mixture of female (male-sterile) and hermaphroditic individuals in the population (gynodioecy). Such a mitochondrial-nuclear sex determination system is thought to be rare outside plants. Here, we present one possible case of CMS in animals. We hypothesize that the only exception to the strict maternal mtDNA inheritance in animals, the doubly uniparental inheritance (DUI) system in bivalves, might have originated as a mitochondrial-nuclear sex-determination system. We document and explore similarities that exist between DUI and CMS, and we propose various ways to test our hypothesis.
MeSH term(s)	Animals ; DNA, Mitochondrial/genetics ; Female ; Genes, Mitochondrial/genetics ; Genome, Mitochondrial/genetics ; Inheritance Patterns/genetics ; Plant Infertility
Chemical Substances	DNA, Mitochondrial
Language	English
Publishing date	2022-02-16
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	50140-2
ISSN	1521-1878 ; 0265-9247
ISSN (online)	1521-1878
ISSN	0265-9247
DOI	10.1002/bies.202100283
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Article ; Online: The mtDNA mutation spectrum in the PolG mutator mouse reveals germline and somatic selection.

Maclaine, Kendra D / Stebbings, Kevin A / Llano, Daniel A / Havird, Justin C

BMC genomic data

2021 Volume 22, Issue 1, Page(s) 52

Abstract: ... and missense C to T mutations primarily resulted in increased protein hydrophobicity. Unlike wild type ...

Abstract	Background: Mitochondrial DNA (mtDNA) codes for products necessary for electron transport and mitochondrial gene translation. mtDNA mutations can lead to human disease and influence organismal fitness. The PolG mutator mouse lacks mtDNA proofreading function and rapidly accumulates mtDNA mutations, making it a model for examining the causes and consequences of mitochondrial mutations. Premature aging in PolG mice and their physiology have been examined in depth, but the location, frequency, and diversity of their mtDNA mutations remain understudied. Identifying the locations and spectra of mtDNA mutations in PolG mice can shed light on how selection shapes mtDNA, both within and across organisms. Results: Here, we characterized somatic and germline mtDNA mutations in brain and liver tissue of PolG mice to quantify mutation count (number of unique mutations) and frequency (mutation prevalence). Overall, mtDNA mutation count and frequency were the lowest in the D-loop, where an mtDNA origin of replication is located, but otherwise uniform across the mitochondrial genome. Somatic mtDNA mutations have a higher mutation count than germline mutations. However, germline mutations maintain a higher frequency and were also more likely to be silent. Cytosine to thymine mutations characteristic of replication errors were the plurality of basepair changes, and missense C to T mutations primarily resulted in increased protein hydrophobicity. Unlike wild type mice, PolG mice do not appear to show strand asymmetry in mtDNA mutations. Indel mutations had a lower count and frequency than point mutations and tended to be short, frameshift deletions. Conclusions: Our results provide strong evidence that purifying selection plays a major role in the mtDNA of PolG mice. Missense mutations were less likely to be passed down in the germline, and they were less likely to spread to high frequencies. The D-loop appears to have resistance to mutations, either through selection or as a by-product of replication processes. Missense mutations that decrease hydrophobicity also tend to be selected against, reflecting the membrane-bound nature of mtDNA-encoded proteins. The abundance of mutations from polymerase errors compared with reactive oxygen species (ROS) damage supports previous studies suggesting ROS plays a minimal role in exacerbating the PolG phenotype, but our findings on strand asymmetry provide discussion for the role of polymerase errors in wild type organisms. Our results provide further insight on how selection shapes mtDNA mutations and on the aging mechanisms in PolG mice.
MeSH term(s)	Aging, Premature/genetics ; Animals ; DNA Mutational Analysis ; DNA Polymerase gamma/genetics ; DNA, Mitochondrial/genetics ; Germ Cells/metabolism ; Male ; Mice ; Mutation ; Reactive Oxygen Species/metabolism
Chemical Substances	DNA, Mitochondrial ; Reactive Oxygen Species ; DNA Polymerase gamma (EC 2.7.7.7) ; Polg protein, mouse (EC 2.7.7.7)
Language	English
Publishing date	2021-11-26
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	2730-6844
ISSN (online)	2730-6844
DOI	10.1186/s12863-021-01005-x
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Article ; Online: Mitonuclear Sex Determination? Empirical Evidence from Bivalves.

Smith, Chase H / Mejia-Trujillo, Raquel / Breton, Sophie / Pinto, Brendan J / Kirkpatrick, Mark / Havird, Justin C

Molecular biology and evolution

2023 Volume 40, Issue 11

Abstract: Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In certain bivalve lineages that possess doubly uniparental inheritance (DUI), mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination. ...

Abstract	Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In certain bivalve lineages that possess doubly uniparental inheritance (DUI), mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination. In these cases, females transmit a female mtDNA to all offspring, while male mtDNA (M mtDNA) is transmitted only from fathers to sons. Because M mtDNA is inherited in the same way as Y chromosomes, it has been hypothesized that mtDNA may be responsible for sex determination. However, the role of mitochondrial and nuclear genes in sex determination has yet to be validated in DUI bivalves. In this study, we used DNA, RNA, and mitochondrial short noncoding RNA (sncRNA) sequencing to explore the role of mitochondrial and nuclear elements in the sexual development pathway of the freshwater mussel Potamilus streckersoni (Bivalvia: Unionida). We found that the M mtDNA sheds a sncRNA partially within a male-specific mitochondrial gene that targets a pathway hypothesized to be involved in female development and mitophagy. RNA-seq confirmed the gene target was significantly upregulated in females, supporting a direct role of mitochondrial sncRNAs in gene silencing. These findings support the hypothesis that M mtDNA inhibits female development. Genome-wide patterns of genetic differentiation and heterozygosity did not support a nuclear sex-determining region, although we cannot reject that nuclear factors are involved with sex determination. Our results provide further evidence that mitochondrial loci contribute to diverse, nonrespiratory functions and additional insights into an unorthodox sex-determining system.
MeSH term(s)	Female ; Animals ; Bivalvia/genetics ; DNA, Mitochondrial/genetics ; Mitochondria/genetics ; Genes, Mitochondrial ; RNA, Small Untranslated
Chemical Substances	DNA, Mitochondrial ; RNA, Small Untranslated
Language	English
Publishing date	2023-11-05
Publishing country	United States
Document type	Journal Article
ZDB-ID	998579-7
ISSN	1537-1719 ; 0737-4038
ISSN (online)	1537-1719
ISSN	0737-4038
DOI	10.1093/molbev/msad240
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