Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans

Gametogenesis is a thermosensitive process in numerous metazoans, ranging from worms to man. In Caenorhabditis elegans, a variety of RNA-binding proteins that associate with germ-line nuage (P granules), including the Piwi-clade argonaute PRG-1, have been implicated in maintaining fertility at eleva...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 107; no. 8; pp. 3588 - 3593
Main Authors Conine, Colin C, Batista, Pedro J, Gu, Weifeng, Claycomb, Julie M, Chaves, Daniel A, Shirayama, Masaki, Mello, Craig C
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 23.02.2010
National Acad Sciences
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Summary:Gametogenesis is a thermosensitive process in numerous metazoans, ranging from worms to man. In Caenorhabditis elegans, a variety of RNA-binding proteins that associate with germ-line nuage (P granules), including the Piwi-clade argonaute PRG-1, have been implicated in maintaining fertility at elevated temperature. Here we describe the role of two AGO-class paralogs, alg-3 (T22B3.2) and alg-4 (ZK757.3), in promoting thermotolerant male fertility. A rescuing GFP::alg-3 transgene is localized to P granules beginning at the late pachytene stage of male gametogenesis. alg-3/4 double mutants lack a subgroup of small RNAs, the 26G-RNAs which target and appear to down-regulate numerous spermatogenesis-expressed mRNAs. These findings add to a growing number of AGO pathways required for thermotolerant fertility in C. elegans and support a model in which AGOs and their small RNA cofactors function to promote robustness in gene-expression networks.
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Author contributions: C.C.C., P.J.B., and J.M.C. designed research; C.C.C., P.J.B., J.M.C., and D.A.C. performed research; C.C.C., P.J.B., and M.S. contributed new reagents/analytic tools; C.C.C., P.J.B., and W.G. analyzed data; and C.C.C., P.J.B., and C.C.M. wrote the paper.
This Direct Submission article had a prearranged editor.
Edited* by Gary Ruvkun, Massachusetts General Hospital, Boston, MA, and approved December 30, 2009 (received for review October 14, 2009)
ISSN:0027-8424
1091-6490
DOI:10.1073/pnas.0911685107