Endomitosis controls tissue-specific gene expression during development

Lotte M van Rijnberk; Ramon Barrull-Mascaró; Reinier L van der Palen; Erik S Schild; Hendrik C Korswagen; Matilde Galli

doi:10.1371/journal.pbio.3001597

Endomitosis controls tissue-specific gene expression during development

Lotte M van Rijnberk, Ramon Barrull-Mascaró, Reinier L van der Palen, Erik S Schild, Hendrik C Korswagen, Matilde Galli

Hubrecht Institute

Onderzoeksoutput: Bijdrage aan wetenschappelijk tijdschrift/periodieke uitgave › Artikel › Wetenschappelijk › peer review

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Polyploid cells contain more than 2 copies of the genome and are found in many plant and animal tissues. Different types of polyploidy exist, in which the genome is confined to either 1 nucleus (mononucleation) or 2 or more nuclei (multinucleation). Despite the widespread occurrence of polyploidy, the functional significance of different types of polyploidy is largely unknown. Here, we assess the function of multinucleation in Caenorhabditis elegans intestinal cells through specific inhibition of binucleation without altering genome ploidy. Through single-worm RNA sequencing, we find that binucleation is important for tissue-specific gene expression, most prominently for genes that show a rapid up-regulation at the transition from larval development to adulthood. Regulated genes include vitellogenins, which encode yolk proteins that facilitate nutrient transport to the germline. We find that reduced expression of vitellogenins in mononucleated intestinal cells leads to progeny with developmental delays and reduced fitness. Together, our results show that binucleation facilitates rapid up-regulation of intestine-specific gene expression during development, independently of genome ploidy, underscoring the importance of spatial genome organization for polyploid cell function.

Originele taal-2	Engels
Pagina's (van-tot)	e3001597
Tijdschrift	PLoS Biology
Volume	20
Nummer van het tijdschrift	5
DOI's	https://doi.org/10.1371/journal.pbio.3001597
Status	Gepubliceerd - mei 2022

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@article{289a43420f2342dd9712f6038ffbf2b8,

title = "Endomitosis controls tissue-specific gene expression during development",

abstract = "Polyploid cells contain more than 2 copies of the genome and are found in many plant and animal tissues. Different types of polyploidy exist, in which the genome is confined to either 1 nucleus (mononucleation) or 2 or more nuclei (multinucleation). Despite the widespread occurrence of polyploidy, the functional significance of different types of polyploidy is largely unknown. Here, we assess the function of multinucleation in Caenorhabditis elegans intestinal cells through specific inhibition of binucleation without altering genome ploidy. Through single-worm RNA sequencing, we find that binucleation is important for tissue-specific gene expression, most prominently for genes that show a rapid up-regulation at the transition from larval development to adulthood. Regulated genes include vitellogenins, which encode yolk proteins that facilitate nutrient transport to the germline. We find that reduced expression of vitellogenins in mononucleated intestinal cells leads to progeny with developmental delays and reduced fitness. Together, our results show that binucleation facilitates rapid up-regulation of intestine-specific gene expression during development, independently of genome ploidy, underscoring the importance of spatial genome organization for polyploid cell function.",

keywords = "Animals, Caenorhabditis elegans/genetics, Cell Division, Cell Nucleus/genetics, Gene Expression, Polyploidy, Vitellogenins/genetics",

author = "{van Rijnberk}, {Lotte M} and Ramon Barrull-Mascar{\'o} and {van der Palen}, {Reinier L} and Schild, {Erik S} and Korswagen, {Hendrik C} and Matilde Galli",

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month = may,

doi = "10.1371/journal.pbio.3001597",

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T1 - Endomitosis controls tissue-specific gene expression during development

AU - van Rijnberk, Lotte M

AU - Barrull-Mascaró, Ramon

AU - van der Palen, Reinier L

AU - Schild, Erik S

AU - Korswagen, Hendrik C

AU - Galli, Matilde

PY - 2022/5

Y1 - 2022/5

N2 - Polyploid cells contain more than 2 copies of the genome and are found in many plant and animal tissues. Different types of polyploidy exist, in which the genome is confined to either 1 nucleus (mononucleation) or 2 or more nuclei (multinucleation). Despite the widespread occurrence of polyploidy, the functional significance of different types of polyploidy is largely unknown. Here, we assess the function of multinucleation in Caenorhabditis elegans intestinal cells through specific inhibition of binucleation without altering genome ploidy. Through single-worm RNA sequencing, we find that binucleation is important for tissue-specific gene expression, most prominently for genes that show a rapid up-regulation at the transition from larval development to adulthood. Regulated genes include vitellogenins, which encode yolk proteins that facilitate nutrient transport to the germline. We find that reduced expression of vitellogenins in mononucleated intestinal cells leads to progeny with developmental delays and reduced fitness. Together, our results show that binucleation facilitates rapid up-regulation of intestine-specific gene expression during development, independently of genome ploidy, underscoring the importance of spatial genome organization for polyploid cell function.

AB - Polyploid cells contain more than 2 copies of the genome and are found in many plant and animal tissues. Different types of polyploidy exist, in which the genome is confined to either 1 nucleus (mononucleation) or 2 or more nuclei (multinucleation). Despite the widespread occurrence of polyploidy, the functional significance of different types of polyploidy is largely unknown. Here, we assess the function of multinucleation in Caenorhabditis elegans intestinal cells through specific inhibition of binucleation without altering genome ploidy. Through single-worm RNA sequencing, we find that binucleation is important for tissue-specific gene expression, most prominently for genes that show a rapid up-regulation at the transition from larval development to adulthood. Regulated genes include vitellogenins, which encode yolk proteins that facilitate nutrient transport to the germline. We find that reduced expression of vitellogenins in mononucleated intestinal cells leads to progeny with developmental delays and reduced fitness. Together, our results show that binucleation facilitates rapid up-regulation of intestine-specific gene expression during development, independently of genome ploidy, underscoring the importance of spatial genome organization for polyploid cell function.

KW - Animals

KW - Caenorhabditis elegans/genetics

KW - Cell Division

KW - Cell Nucleus/genetics

KW - Gene Expression

KW - Polyploidy

KW - Vitellogenins/genetics

U2 - 10.1371/journal.pbio.3001597

DO - 10.1371/journal.pbio.3001597

M3 - Article

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SN - 1544-9173

VL - 20

SP - e3001597

JO - PLoS Biology

JF - PLoS Biology

IS - 5

ER -

Endomitosis controls tissue-specific gene expression during development

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