Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis
Copepods are among the most numerous animals, and they play an essential role in the marine trophic web and biogeochemical cycles. The genus Oithona is described as having the highest density of copepods. The Oithona male paradox describes the activity states of males, which are obliged to alternate...
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MDPI AG
2021-07-01
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| author | Kevin Sugier Romuald Laso-Jadart Benoît Vacherie Jos Käfer Laurie Bertrand Karine Labadie Nathalie Martins Céline Orvain Emmanuelle Petit Patrick Wincker Jean-Louis Jamet Adriana Alberti Mohammed-Amin Madoui |
| author_facet | Kevin Sugier Romuald Laso-Jadart Benoît Vacherie Jos Käfer Laurie Bertrand Karine Labadie Nathalie Martins Céline Orvain Emmanuelle Petit Patrick Wincker Jean-Louis Jamet Adriana Alberti Mohammed-Amin Madoui |
| author_sort | Kevin Sugier |
| collection | DOAJ |
| description | Copepods are among the most numerous animals, and they play an essential role in the marine trophic web and biogeochemical cycles. The genus Oithona is described as having the highest density of copepods. The Oithona male paradox describes the activity states of males, which are obliged to alternate between immobile and mobile phases for ambush feeding and mate searching, respectively, while the female is less mobile and feeds less. To characterize the molecular basis of this sexual dimorphism, we combined immunofluorescence, genomics, transcriptomics, and protein–protein interaction approaches and revealed the presence of a male-specific nervous ganglion. Transcriptomic analysis showed male-specific enrichment for nervous system development-related transcripts. Twenty-seven Lin12-Notch Repeat domain-containing protein coding genes (LDPGs) of the 75 LDPGs identified in the genome were specifically expressed in males. Furthermore, some LDPGs coded for proteins with predicted proteolytic activity, and proteases-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. We also hypothesized possible roles of the LDPGs in the development of the lateral ganglia through helping in extracellular matrix lysis, neurites growth guidance, and synapses genesis. |
| first_indexed | 2024-03-10T09:45:11Z |
| format | Article |
| id | doaj.art-92896c91b9ee473ba87582b2071b53f3 |
| institution | Directory Open Access Journal |
| issn | 2079-7737 |
| language | English |
| last_indexed | 2024-03-10T09:45:11Z |
| publishDate | 2021-07-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Biology |
| spelling | doaj.art-92896c91b9ee473ba87582b2071b53f32023-11-22T03:16:03ZengMDPI AGBiology2079-77372021-07-0110765710.3390/biology10070657Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated ProteolysisKevin Sugier0Romuald Laso-Jadart1Benoît Vacherie2Jos Käfer3Laurie Bertrand4Karine Labadie5Nathalie Martins6Céline Orvain7Emmanuelle Petit8Patrick Wincker9Jean-Louis Jamet10Adriana Alberti11Mohammed-Amin Madoui12Génomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceGenoscope, Institut de Biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay, 91000 Evry, FranceLaboratoire de Biométrie et Biologie Evolutive UMR 5558, Université Lyon 1, Université de Lyon, 69622 Villeurbanne, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceGenoscope, Institut de Biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay, 91000 Evry, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceGenoscope, Institut de Biologie François-Jacob, Commissariat à l’Energie Atomique (CEA), Université Paris-Saclay, 91000 Evry, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceMediterranean Institute of Oceanography, Université de Toulon, Aix-Marseille Université, CEDEX 9, 83041 Toulon, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceGénomique Métabolique, Genoscope, Institut François Jacob, Univ Evry, Université Paris-Saclay, 91000 Evry, FranceCopepods are among the most numerous animals, and they play an essential role in the marine trophic web and biogeochemical cycles. The genus Oithona is described as having the highest density of copepods. The Oithona male paradox describes the activity states of males, which are obliged to alternate between immobile and mobile phases for ambush feeding and mate searching, respectively, while the female is less mobile and feeds less. To characterize the molecular basis of this sexual dimorphism, we combined immunofluorescence, genomics, transcriptomics, and protein–protein interaction approaches and revealed the presence of a male-specific nervous ganglion. Transcriptomic analysis showed male-specific enrichment for nervous system development-related transcripts. Twenty-seven Lin12-Notch Repeat domain-containing protein coding genes (LDPGs) of the 75 LDPGs identified in the genome were specifically expressed in males. Furthermore, some LDPGs coded for proteins with predicted proteolytic activity, and proteases-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. We also hypothesized possible roles of the LDPGs in the development of the lateral ganglia through helping in extracellular matrix lysis, neurites growth guidance, and synapses genesis.https://www.mdpi.com/2079-7737/10/7/657copepodssexual differentiationnervous systemLin12-Notch-RepeatOithonaprotein–protein interaction |
| spellingShingle | Kevin Sugier Romuald Laso-Jadart Benoît Vacherie Jos Käfer Laurie Bertrand Karine Labadie Nathalie Martins Céline Orvain Emmanuelle Petit Patrick Wincker Jean-Louis Jamet Adriana Alberti Mohammed-Amin Madoui Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis Biology copepods sexual differentiation nervous system Lin12-Notch-Repeat Oithona protein–protein interaction |
| title | Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis |
| title_full | Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis |
| title_fullStr | Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis |
| title_full_unstemmed | Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis |
| title_short | Male Differentiation in the Marine Copepod <i>Oithona nana</i> Reveals the Development of a New Nervous Ganglion and Lin12-Notch-Repeat Protein-Associated Proteolysis |
| title_sort | male differentiation in the marine copepod i oithona nana i reveals the development of a new nervous ganglion and lin12 notch repeat protein associated proteolysis |
| topic | copepods sexual differentiation nervous system Lin12-Notch-Repeat Oithona protein–protein interaction |
| url | https://www.mdpi.com/2079-7737/10/7/657 |
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