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 in	Proceedings 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
Language	English
Published	United States National Academy of Sciences 23.02.2010 National Acad Sciences
Subjects	Animals Binding sites Biological Sciences Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cell division Fertility - genetics Fertility - physiology Gametogenesis Gene expression Gene expression regulation Germ cells Hot Temperature Male Male animals Messenger RNA Metazoa Mutation Nematodes Proteins Ribonucleic acid RNA RNA, Small Interfering - biosynthesis RNA, Small Interfering - genetics RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism Spermatids Spermatogenesis Spermatogenesis - genetics Spermatogenesis - physiology Spermatozoa Spermatozoa - metabolism
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Abstract	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.
AbstractList	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. 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 nuagè (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 para logs, 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. 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. [PUBLICATION ABSTRACT] 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.
Author	Conine, Colin C Claycomb, Julie M Gu, Weifeng Shirayama, Masaki Chaves, Daniel A Batista, Pedro J Mello, Craig C
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Notes	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 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)
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Snippet	Gametogenesis is a thermosensitive process in numerous metazoans, ranging from worms to man. In Caenorhabditis elegans, a variety of RNA-binding proteins that... Gametogenesis is a thermosensitive process in numerous metazoans, ranging from worms to man. In Caenorhabditis elegans. a variety of RNA-binding proteins that... Gametogenesis is a thermosensitive process in numerous metazoans, ranging from worms to man. In Caenorhabditis elegans , a variety of RNA-binding proteins that... Gametogenesis is a thermosensitive process in numerous metazoans, ranging from worms to man. In Caenorhabditis elegans , a variety of RNA-binding proteins that...
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SubjectTerms	Animals Binding sites Biological Sciences Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - metabolism Cell division Fertility - genetics Fertility - physiology Gametogenesis Gene expression Gene expression regulation Germ cells Hot Temperature Male Male animals Messenger RNA Metazoa Mutation Nematodes Proteins Ribonucleic acid RNA RNA, Small Interfering - biosynthesis RNA, Small Interfering - genetics RNA-Binding Proteins - genetics RNA-Binding Proteins - metabolism Spermatids Spermatogenesis Spermatogenesis - genetics Spermatogenesis - physiology Spermatozoa Spermatozoa - metabolism
Title	Argonautes ALG-3 and ALG-4 are required for spermatogenesis-specific 26G-RNAs and thermotolerant sperm in Caenorhabditis elegans
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