TY - JOUR
T1 - Somatic polyploidy supports biosynthesis and tissue function by increasing transcriptional output
AU - Lessenger, Alexander T.
AU - Skotheim, Jan M.
AU - Swaffer, Matthew P.
AU - Feldman, Jessica L.
N1 - We thank Georgi Marinov for sharing of code and Alex Long and Tim Stearns for the use of their confocal microscope. We thank Dominique Bergman, Lucy O’Brien, Lauren Cote, Andrew Fire, Hannah Fung, Kang Shen, Shicong Xie, and members of the Feldman and Skotheim labs for scientific discussions and feedback, and for their comments on the manuscript.
PY - 2024/12/9
Y1 - 2024/12/9
N2 - Cell size and biosynthetic capacity generally increase with increased DNA content. Somatic polyploidy has therefore been proposed to be an adaptive strategy to increase cell size in specialized tissues with high biosynthetic demands. However, if and how DNA concentration limits cellular biosynthesis in vivo is not well understood. Here, we show that polyploidy in the Caenorhabditis elegans intestine is critical for cell growth and yolk biosynthesis, a central role of this organ. Artificially lowering the DNA/cytoplasm ratio by reducing polyploidization in the intestine gave rise to smaller cells with dilute mRNA. Highly expressed transcripts were more sensitive to this mRNA dilution, whereas lowly expressed genes were partially compensated—in part by loading more RNA Polymerase II on the remaining genomes. Polyploidy-deficient animals produced fewer and slower-growing offspring, consistent with reduced synthesis of highly expressed yolk proteins. DNA-dilute cells had normal total protein concentration, which
AB - Cell size and biosynthetic capacity generally increase with increased DNA content. Somatic polyploidy has therefore been proposed to be an adaptive strategy to increase cell size in specialized tissues with high biosynthetic demands. However, if and how DNA concentration limits cellular biosynthesis in vivo is not well understood. Here, we show that polyploidy in the Caenorhabditis elegans intestine is critical for cell growth and yolk biosynthesis, a central role of this organ. Artificially lowering the DNA/cytoplasm ratio by reducing polyploidization in the intestine gave rise to smaller cells with dilute mRNA. Highly expressed transcripts were more sensitive to this mRNA dilution, whereas lowly expressed genes were partially compensated—in part by loading more RNA Polymerase II on the remaining genomes. Polyploidy-deficient animals produced fewer and slower-growing offspring, consistent with reduced synthesis of highly expressed yolk proteins. DNA-dilute cells had normal total protein concentration, which
UR - https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE280911
UR - https://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE280912
UR - https://github.com/atlessenger/lessenger_2024_jcb
U2 - 10.1083/jcb.202403154
DO - 10.1083/jcb.202403154
M3 - Article
SN - 0021-9525
VL - 224
SP - e202403154
JO - Journal of Cell Biology
JF - Journal of Cell Biology
IS - 3
ER -