Transposable elements provide a highly informative marker system for analyzing evolutionary histories. To solve controversially discussed topics in strepsirrhine phylogeny, we characterized 61 loci containing short interspersed elements (SINEs) and determined the SINE presence-absence pattern at orthologous loci in a representative strepsirrhine panel. This SINE monolocus study was complemented by a Southern blot analysis tracing multiple loci of two different strepsirrhine specific SINEs. The results thereof were combined with phylogenetic trees reconstructed on the basis of complete mitochondrial cytochrome b sequences from all recognized strepsirrhine genera. Here we present evidence for (i) a sister group relationship of Malagasy Chiromyiformes and Lemuriformes, (ii) Lorisidae being a monophyletic sister clade to the Galagidae, and (iii) common ancestry of African and Asian lorisids. Based on these findings, we conclude that strepsirrhines originated in Africa and that Madagascar and Asia were colonized by respective single immigration events. In agreement with paleocontinental data, the molecular analyses suggest a crossing of the Mozambique channel by rafting between the late Cretaceous and the middle Eocene, whereas Asia was most likely colonized between the early Eocene and the middle Oligocene on a continental route. Furthermore, one SINE integration links the two Lemuriformes families, Lemuridae and Indriidae, indicating a common origin of diurnality or cathemerality and a later reversal to nocturnality by the indriid genus Avahi.
Germ cells of most animals critically depend on piRNAs and Piwi proteins. Surprisingly, piRNAs in mouse oocytes are relatively rare and dispensable. We present compelling evidence for strong Piwi and piRNA expression in oocytes of other mammals. Human fetal oocytes express PIWIL2 and transposon-enriched piRNAs. Oocytes in adult human ovary express PIWIL1 and PIWIL2, whereas those in bovine ovary only express PIWIL1. In human, macaque, and bovine ovaries, we find piRNAs that resemble testis-borne pachytene piRNAs. Isolated bovine follicular oocytes were shown to contain abundant, relatively short piRNAs that preferentially target transposable elements. Using label-free quantitative proteome analysis, we show that these maturing oocytes strongly and specifically express the PIWIL3 protein, alongside other, known piRNA-pathway components. A piRNA pool is still present in early bovine embryos, revealing a potential impact of piRNAs on mammalian embryogenesis. Our results reveal that there are highly dynamic piRNA pathways in mammalian oocytes and early embryos.
BackgroundThroughout the metazoan lineage, typically gonadal expressed Piwi proteins and their guiding piRNAs (~26-32nt in length) form a protective mechanism of RNA interference directed against the propagation of transposable elements (TEs). Most piRNAs are generated from genomic piRNA clusters. Annotation of experimentally obtained piRNAs from small RNA/cDNA-libraries and detection of genomic piRNA clusters are crucial for a thorough understanding of the still enigmatic piRNA pathway, especially in an evolutionary context. Currently, detection of piRNA clusters relies on bioinformatics rather than detection and sequencing of primary piRNA cluster transcripts and the stringency of the methods applied in different studies differs considerably. Additionally, not all important piRNA cluster characteristics were taken into account during bioinformatic processing. Depending on the applied method this can lead to: i) an accidentally underrepresentation of TE related piRNAs, ii) overlook duplicated clusters harboring few or no single-copy loci and iii) false positive annotation of clusters that are in fact just accumulations of multi-copy loci corresponding to frequently mapped reads, but are not transcribed to piRNA precursors.ResultsWe developed a software which detects and analyses piRNA clusters (proTRAC, probabilistic TRacking and Analysis of Clusters) based on quantifiable deviations from a hypothetical uniform distribution regarding the decisive piRNA cluster characteristics. We used piRNA sequences from human, macaque, mouse and rat to identify piRNA clusters in the respective species with proTRAC and compared the obtained results with piRNA cluster annotation from piRNABank and the results generated by different hitherto applied methods.proTRAC identified clusters not annotated at piRNABank and rejected annotated clusters based on the absence of important features like strand asymmetry. We further show, that proTRAC detects clusters that are passed over if a minimum number of single-copy piRNA loci are required and that proTRAC assigns more sequence reads per cluster since it does not preclude frequently mapped reads from the analysis.ConclusionsWith proTRAC we provide a reliable tool for detection, visualization and analysis of piRNA clusters. Detected clusters are well supported by comprehensible probabilistic parameters and retain a maximum amount of information, thus overcoming the present conflict of sensitivity and specificity in piRNA cluster detection.
Mammalian mitochondrial DNA sequences evolve more rapidly than nuclear sequences. Although the rapid rate of evolution is an advantage for the study of closely related species and populations, it presents a problem in situations where related species, used as outgroups in phylogenetic analyses, have accumulated so much change that multiple substitutions obliterate the phylogenetic information. However, mitochondrial DNA sequences are frequently inserted into the nuclear genome, where they presumably evolve as nuclear pseudogene sequences and therefore more slowly than their mitochondrial counterparts. Such sequences thus represent molecular 'fossils' that could shed light on the evolution of the mitochondrial genome and could be used as outgroups in situations where no appropriate outgroup species exist. Here we show that human chromosome 11 carries a recent integration of the mitochondrial control region that can be used to gain further insight into the origin of the human mitochondrial gene pool.
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