Non-gonadal somatic piRNA pathways ensure sexual differentiation, larval growth, and wing development in silkworms

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 acti...

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Bibliographic Details
Published in:PLoS genetics 2023-09, Vol.19 (9), p.e1010912-e1010912
Main Authors: Kiuchi, Takashi, Shoji, Keisuke, Izumi, Natsuko, Tomari, Yukihide, Katsuma, Susumu
Format: Article
Language:English
Subjects:
Analysis
Biology and Life Sciences
Biosynthesis
Bombyx mori
CRISPR
Cytoplasm
Drosophila
Fat body
Fat metabolism
Females
Genetic aspects
Genomes
Genomics
Growth
Heterochromatin
Infertility
Insects
Medicine and Health Sciences
Morphology
Mutants
Ovaries
Phenotypes
Physiological aspects
Proteins
Research and analysis methods
RNA
Sex differentiation
Silkworms
Table tennis
Testes
Transcriptomes
Transposons
Wings
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Summary: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.
ISSN:1553-7404
1553-7390
1553-7404
DOI:10.1371/journal.pgen.1010912