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- Title
The piRNA cluster torimochi is an expanding transposon in cultured silkworm cells.
- Authors
Shoji, Keisuke; Umemura, Yusuke; Katsuma, Susumu; Tomari, Yukihide
- Abstract
PIWI proteins and PIWI-interacting RNAs (piRNAs) play a central role in repressing transposable elements in animal germ cells. It is thought that piRNAs are mainly produced from discrete genomic loci named piRNA clusters, which often contain many "dead" transposon remnants from past invasions and have heterochromatic features. In the genome of silkworm ovary-derived cultured cells called BmN4, a well-established model for piRNA research, torimochi was previously annotated as a unique and specialized genomic region that can capture transgenes and produce new piRNAs bearing a trans-silencing activity. However, the sequence identity of torimochi has remained elusive. Here, we carefully characterized torimochi by utilizing the updated silkworm genome sequence and the long-read sequencer MinION. We found that torimochi is in fact a full-length gypsy-like LTR retrotransposon, which is exceptionally active and has massively expanded its copy number in BmN4 cells. Many copies of torimochi in BmN4 cells have features of open chromatin and the ability to produce piRNAs. Therefore, torimochi may represent a young, growing piRNA cluster, which is still "alive" and active in transposition yet capable of trapping other transposable elements to produce de novo piRNAs. (185 words) Author summary: Transposons are DNA sequences that can jump from one region to another in the genome. Since transposon insertions can disrupt the genetic information, the hosts need to silence their activity especially in germ cells. PIWI-interacting RNAs (piRNAs) act as the sequence-specific guide to suppress transposons. Many piRNAs are generated from discrete genomic regions, called piRNA clusters, which often contain a variety of fragmented, "dead" transposons. piRNA clusters are thought to act as genomic storage devices that memorize non-self sequences to be suppressed. However, resent findings suggest that piRNA clusters are not stationary entities but can flexibly appear and disappear. BmN4 cells, derived from silkworm ovaries, have been widely used in the piRNA research. A previous study using BmN4 cells identified torimochi (the Japanese word for birdlime) as a representative piRNA cluster, which can trap foreign sequences and produce piRNAs. However, the detailed properties of torimochi have remained unclear. Here, we found that torimochi is in fact a retrotransposon, which is exceptionally active and has massively expanded its copy number in BmN4 cells. Therefore, torimochi may represent a young, growing piRNA cluster, which is still "alive" and active in jumping yet capable of trapping other transposons to produce new piRNAs. (199 words)
- Subjects
TRANSPOSONS; SILKWORMS; GERM cells; DNA sequencing; TRANSGENES; JAPANESE language
- Publication
PLoS Genetics, 2023, Vol 18, Issue 2, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010632