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- Title
Non-gonadal somatic piRNA pathways ensure sexual differentiation, larval growth, and wing development in silkworms.
- Authors
Kiuchi, Takashi; Shoji, Keisuke; Izumi, Natsuko; Tomari, Yukihide; Katsuma, Susumu
- Abstract
PIWI-interacting RNAs (piRNAs) guide PIWI proteins to target transposons in germline cells, thereby suppressing transposon activity to preserve genome integrity in metazoans' gonadal tissues. Piwi, one of three Drosophila PIWI proteins, is expressed in the nucleus and suppresses transposon activity by forming heterochromatin in an RNA cleavage-independent manner. Recently, Piwi was reported to control cell metabolism in Drosophila fat body, providing an example of piRNAs acting in non-gonadal somatic tissues. However, mutant flies of the other two PIWI proteins, Aubergine (Aub) and Argonaute3 (Ago3), show no apparent phenotype except for infertility, blurring the importance of the piRNA pathway in non-gonadal somatic tissues. The silkworm, Bombyx mori, possesses two PIWI proteins, Siwi (Aub homolog) and BmAgo3 (Ago3 homolog), whereas B. mori does not have a Piwi homolog. Siwi and BmAgo3 are mainly expressed in gonadal tissues and play a role in repressing transposon activity by cleaving transposon RNA in the cytoplasm. Here, we generated Siwi and BmAgo3 loss-of-function mutants of B. mori and found that they both showed delayed larval growth and failed to become adult moths. They also exhibited defects in wing development and sexual differentiation. Transcriptome analysis revealed that loss of somatic piRNA biogenesis pathways results in abnormal expression of not only transposons but also host genes, presumably causing severe growth defects. Our results highlight the roles of non-gonadal somatic piRNAs in B. mori development. Author summary: In animal germ cells, PIWI proteins and piRNAs play an important role in the defense system against selfish elements such as transposons. The fruit fly Drosophila possesses two PIWI proteins, Aub and Ago3, both of which are required for piRNA production and transposon repression in the cytoplasm of germ cells. However, their roles in somatic cells are unclear. Using a lepidopteran model insect, the silkworm Bombyx mori, we established Siwi (Aub homolog) and BmAgo3 (Ago3 homolog) germline knockout mutants and characterized non-gonadal somatic piRNA functions in B. mori development. We found that somatic piRNAs are utilized to suppress transposon activity and maintain normal gene expression in several somatic tissues. Unlike Drosophila, disruption of somatic piRNA pathways severely inhibited normal development in somatic tissues of B. mori: both mutants grew slowly, did not develop to adult moths, and exhibited defects in wing development and sexual differentiation. This study is the first to generate germline knockout insects of PIWI genes in non-Drosophila insects and expands the knowledge on the ancestral or universal functions of piRNAs in arthropods.
- Subjects
SEX differentiation (Embryology); PIWI genes; SILKWORMS; GENE expression; INSECT genes; LARVAE
- Publication
PLoS Genetics, 2023, Vol 19, Issue 9, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010912