TY - JOUR
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
C2 - 35609035
SN - 1544-9173
VL - 20
SP - e3001597
JO - PLoS Biology
JF - PLoS Biology
IS - 5
ER -