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Male differentiation in the marine copepod Oithona nana reveals the development of a new nervous ganglion linked to Lin12-Notch-Repeat protein-associated proteolysis
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  • Kevin Sugier,
  • Romuald Laso-Jadart,
  • Benoit Vacherie,
  • Jos Käfer,
  • Laurie Bertrand,
  • Céline Orvain,
  • Nathalie Martins,
  • Karine Labadie,
  • Julie Poulain,
  • Emmanuelle Petit,
  • Patrick Wincker,
  • Jean-Louis Jamet,
  • Adriana Alberti,
  • Mohammed-Amin Madoui
Kevin Sugier
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay

Corresponding Author:[email protected]

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Romuald Laso-Jadart
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Benoit Vacherie
Genoscope, Institut de biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay, F-91000 Evry, France
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Jos Käfer
4 Université de Lyon, Université Lyon 1, CNRS, Laboratoire de Biométrie et Biologie Evolutive UMR 5558
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Laurie Bertrand
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Céline Orvain
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Nathalie Martins
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Karine Labadie
Genoscope, Institut de biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay, F-91000 Evry, France
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Julie Poulain
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Emmanuelle Petit
Genoscope, Institut de biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay, F-91000 Evry, France
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Patrick Wincker
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Jean-Louis Jamet
Université de Toulon, Aix-Marseille Université, CNRS/INSU/IRD, Mediterranean Institute of Oceanography MIO UMR 7294, EMBIO, CS 60584, 83041
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Adriana Alberti
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Mohammed-Amin Madoui
Génomique Métabolique, Genoscope, Institut François Jacob, CEA, CNRS, Univ Evry, Université Paris-Saclay
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Abstract

Copepods are the most numerous animals and play an essential role in the marine trophic web and biogeochemical cycles. The genus Oithona is described as having the highest numerical density, as the most cosmopolite copepod. The Oithona male paradox obliges it to alternate immobile and mobile phases for ambushed feeding and mate search respectively, while the female is less mobile and often feeding. To characterize the molecular basis of this sexual dimorphism, we combined immunofluorescence, genomics, transcriptomics and protein-protein interactions approaches. Tubulin-β3 and α immunofluorescence analysis revealed two lateral male-specific nervous ganglions in the first segment of the Oithona nana male’s prosome. In parallel, the transcriptomic analysis showed male-specific enrichment for nervous system development related transcripts. Twenty seven Lin12-Notch Repeat domains-containing proteins coding genes (LDPGs) over the 75 LDPGs found in the genome were specifically expressed in male. Furthermore, most of the LDPGs (27%) code for proteins having a predicted proteolytic activity and non-LDPGs proteolysis associated transcripts showed a male specific enrichment. Using yeast double–hybrid assays, we constructed a protein-protein interaction network involving two LDPs with proteases, extracellular matrix proteins and neurogenesis related proteins. In our study, the lateral nervous ganglion of O. nana male is described for the first time and is unique in copepods. We also demonstrated a role of the LDPGs and its associated proteolysis to participate to the male-specific physiology and we hypothesize a role of the LDPGs in the lateral ganglions development through guiding lysis of extracellular matrix for the neurites and synapse genesis.