Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline

Haspin is a histone kinase that promotes error-free chromosome segregation by recruiting the chromosomal passenger complex (CPC) to mitotic and meiotic chromosomes. Haspin remains less well studied than other M-phase kinases, and the models explaining Haspin function have been developed primarily in...

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Main Authors: Jommel Macaraeg, Isaac Reinhard, Matthew Ward, Danielle Carmeci, Madison Stanaway, Amy Moore, Ethan Hagmann, Katherine Brown, David J. Wynne
Format: Article
Language:English
Published: The Company of Biologists 2022-07-01
Series:Biology Open
Subjects:
Online Access:http://bio.biologists.org/content/11/7/bio059277
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author Jommel Macaraeg
Isaac Reinhard
Matthew Ward
Danielle Carmeci
Madison Stanaway
Amy Moore
Ethan Hagmann
Katherine Brown
David J. Wynne
author_facet Jommel Macaraeg
Isaac Reinhard
Matthew Ward
Danielle Carmeci
Madison Stanaway
Amy Moore
Ethan Hagmann
Katherine Brown
David J. Wynne
author_sort Jommel Macaraeg
collection DOAJ
description Haspin is a histone kinase that promotes error-free chromosome segregation by recruiting the chromosomal passenger complex (CPC) to mitotic and meiotic chromosomes. Haspin remains less well studied than other M-phase kinases, and the models explaining Haspin function have been developed primarily in mitotic cells. Here, we generate strains containing new conditional or nonsense mutations in the Caenorhabditis elegans Haspin homologs hasp-1 and hasp-2 and characterize their phenotypes. We show that hasp-1 is responsible for all predicted functions of Haspin and that loss of function of hasp-1 using classical and conditional alleles produces defects in germline stem cell proliferation and spermatogenesis, and confirms its role in oocyte meiosis. Genetic analysis suggests that hasp-1 acts downstream of the Polo-like kinase plk-2 and shows synthetic interactions between hasp-1 and two genes expected to promote recruitment of the CPC by a parallel pathway that depends on the kinase Bub1. This work adds to the growing understanding of Haspin function by characterizing a variety of roles in an intact animal.
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spelling doaj.art-a48db24ec5194adfb8a90537f5e50b222022-12-22T02:05:25ZengThe Company of BiologistsBiology Open2046-63902022-07-0111710.1242/bio.059277059277Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germlineJommel Macaraeg0Isaac Reinhard1Matthew Ward2Danielle Carmeci3Madison Stanaway4Amy Moore5Ethan Hagmann6Katherine Brown7David J. Wynne8 Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Department of Biology, University of Portland, 5000 N Willamette Blvd, Portland, OR 97203, USA Haspin is a histone kinase that promotes error-free chromosome segregation by recruiting the chromosomal passenger complex (CPC) to mitotic and meiotic chromosomes. Haspin remains less well studied than other M-phase kinases, and the models explaining Haspin function have been developed primarily in mitotic cells. Here, we generate strains containing new conditional or nonsense mutations in the Caenorhabditis elegans Haspin homologs hasp-1 and hasp-2 and characterize their phenotypes. We show that hasp-1 is responsible for all predicted functions of Haspin and that loss of function of hasp-1 using classical and conditional alleles produces defects in germline stem cell proliferation and spermatogenesis, and confirms its role in oocyte meiosis. Genetic analysis suggests that hasp-1 acts downstream of the Polo-like kinase plk-2 and shows synthetic interactions between hasp-1 and two genes expected to promote recruitment of the CPC by a parallel pathway that depends on the kinase Bub1. This work adds to the growing understanding of Haspin function by characterizing a variety of roles in an intact animal.http://bio.biologists.org/content/11/7/bio059277chromosome segregationinner centromeregermlinemeiosisspermatogenesisoogenesis
spellingShingle Jommel Macaraeg
Isaac Reinhard
Matthew Ward
Danielle Carmeci
Madison Stanaway
Amy Moore
Ethan Hagmann
Katherine Brown
David J. Wynne
Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
Biology Open
chromosome segregation
inner centromere
germline
meiosis
spermatogenesis
oogenesis
title Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_full Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_fullStr Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_full_unstemmed Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_short Genetic analysis of Caenorhabditis elegans Haspin-like genes shows that hasp-1 plays multiple roles in the germline
title_sort genetic analysis of caenorhabditis elegans haspin like genes shows that hasp 1 plays multiple roles in the germline
topic chromosome segregation
inner centromere
germline
meiosis
spermatogenesis
oogenesis
url http://bio.biologists.org/content/11/7/bio059277
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