Coupling of growth rate and developmental tempo reduces body size heterogeneity in C. elegans

• Published in: Nature communications Vol. 13; no. 1; p. 3132
• Main Authors: Stojanovski, Klement, Großhans, Helge, Towbin, Benjamin D.
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 06-06-2022; Nature Publishing Group; Nature Portfolio
• Subjects: 14/35; 14/63; 631/136/83; 631/553/2693; 631/553/2715; 64/11; Amplification; Animals; Body size; Body volume (biology); Cell division; Coupling; Developmental stages; Genetic engineering; Growth rate; Heterogeneity; Humanities and Social Sciences; Larval development; Mathematical models; Molting; multidisciplinary; Nematodes; Oscillators; Perturbation; Science; Science (multidisciplinary); Stochasticity
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-022-29720-8

Animals increase by orders of magnitude in volume during development. Therefore, small variations in growth rates among individuals could amplify to a large heterogeneity in size. By live imaging of
C. elegans
, we show that amplification of size heterogeneity is prevented by an inverse coupling of the volume growth rate to the duration of larval stages and does not involve strict size thresholds for larval moulting. We perturb this coupling by changing the developmental tempo through manipulation of a transcriptional oscillator that controls the duration of larval development. As predicted by a mathematical model, this perturbation alters the body volume. Model analysis shows that an inverse relation between the period length and the growth rate is an intrinsic property of genetic oscillators and can occur independently of additional complex regulation. This property of genetic oscillators suggests a parsimonious mechanism that counteracts the amplification of size differences among individuals during development.
Animals must reach the correct size during development, despite stochastic differences in their growth rate. Here, Stojanovski et al. show that a coupling of growth and development by an oscillatory timer buffers fluctuations in the growth of the nematode C. elegans to ensure its correct size.