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HOP-1 Presenilin Deficiency Causes a Late-Onset Notch Signaling Phenotype that Affects Adult Germline Function in C. elegans

Ipsita Agarwal, Cassandra Farnow, Joshua Jiang, Kyung-Sik Kim, Donna E. Leet, Ruth Z. Solomon, Valerie A. Hale and Caroline Goutte
Genetics Early online December 14, 2017; https://doi.org/10.1534/genetics.117.300605
Ipsita Agarwal
Amherst College
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Cassandra Farnow
Amherst College
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Joshua Jiang
Amherst College
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Kyung-Sik Kim
Amherst College
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Donna E. Leet
Amherst College
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Ruth Z. Solomon
Amherst College
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Valerie A. Hale
Amherst College
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Caroline Goutte
Amherst College
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Abstract

Functionally redundant genes present a puzzle as to their evolutionary preservation, and offer an interesting opportunity for molecular specialization. In Caenorhabditis elegans, either one of two presenilin genes (sel-12 or hop-1) facilitate Notch activation, providing the catalytic subunit for the gamma secretase proteolytic enzyme complex.  For all known Notch signaling events, sel-12 can mediate Notch activation, so the conservation of hop-1 remains a mystery. Here, we uncover a novel "late-onset" germline Notch phenotype in which HOP-1-deficient worms fail to maintain proliferating germline stem cells during adulthood.  Either SEL-12 or HOP-1 presenilin can impart sufficient Notch signaling for establishment and expansion of the germ line, but maintenance of an adult stem cell pool relies exclusively on HOP-1-mediated Notch signaling. We also show that HOP-1 is necessary for maximum fecundity and reproductive span. The low fecundity phenotype of hop-1 mutants can be phenocopied by switching off glp-1/Notch function during the last stage of larval development.  We propose that at the end of larval development, dual presenilin usage switches exclusively to HOP-1, perhaps offering opportunities for differential regulation of the germ line during adulthood.  Additional defects in oocyte size and production rate in hop-1 and glp-1 mutants indicate that the process of oogenesis is compromised when germline Notch signaling is switched off. We calculate that in wild-type adults, as much as 86% of cells derived from the stem cell pool function to support oogenesis.  This work suggests that an important role for Notch signaling in the adult germ line is to furnish a large and continuous supply of nurse cells to support the efficiency of oogenesis.

  • presenilin
  • Notch signaling
  • gene redundancy
  • oogenesis
  • germ line
  • nurse cells
  • proliferation
  • Received September 14, 2017.
  • Accepted December 11, 2017.
  • Copyright © 2017, Genetics
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Volume 208 Issue 4, April 2018

Genetics: 208 (4)

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HOP-1 Presenilin Deficiency Causes a Late-Onset Notch Signaling Phenotype that Affects Adult Germline Function in C. elegans

Ipsita Agarwal, Cassandra Farnow, Joshua Jiang, Kyung-Sik Kim, Donna E. Leet, Ruth Z. Solomon, Valerie A. Hale and Caroline Goutte
Genetics Early online December 14, 2017; https://doi.org/10.1534/genetics.117.300605
Ipsita Agarwal
Amherst College
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Cassandra Farnow
Amherst College
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Joshua Jiang
Amherst College
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Kyung-Sik Kim
Amherst College
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Donna E. Leet
Amherst College
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Ruth Z. Solomon
Amherst College
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Valerie A. Hale
Amherst College
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Caroline Goutte
Amherst College
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  • For correspondence: cegoutte@amherst.edu
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Citation

HOP-1 Presenilin Deficiency Causes a Late-Onset Notch Signaling Phenotype that Affects Adult Germline Function in C. elegans

Ipsita Agarwal, Cassandra Farnow, Joshua Jiang, Kyung-Sik Kim, Donna E. Leet, Ruth Z. Solomon, Valerie A. Hale and Caroline Goutte
Genetics Early online December 14, 2017; https://doi.org/10.1534/genetics.117.300605
Ipsita Agarwal
Amherst College
  • Find this author on Google Scholar
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  • Search for this author on this site
Cassandra Farnow
Amherst College
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Joshua Jiang
Amherst College
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Kyung-Sik Kim
Amherst College
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Donna E. Leet
Amherst College
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Ruth Z. Solomon
Amherst College
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Valerie A. Hale
Amherst College
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Caroline Goutte
Amherst College
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  • For correspondence: cegoutte@amherst.edu

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