Abstract
Just as organ size typically increases with body size, the size of intracellular structures changes as cells grow and divide. Indeed, many organelles, such as the nucleus [1, 2], mitochondria [3], mitotic spindle [4, 5], and centrosome [6], exhibit size scaling, a phenomenon in which organelle size depends linearly on cell size. However, the mechanisms of organelle size scaling remain unclear. Here, we show that the size of the nucleolus, a membraneless organelle important for cell-size homeostasis [7], is coupled to cell size by an intracellular phase transition. We find that nucleolar size directly scales with cell size in early C. elegans embryos. Surprisingly, however, when embryo size is altered, we observe inverse scaling: nucleolar size increases in small cells and decreases in large cells. We demonstrate that this seemingly contradictory result arises from maternal loading of a fixed number rather than a fixed concentration of nucleolar components, which condense into nucleoli only above a threshold concentration. Our results suggest that the physics of phase transitions can dictate whether an organelle assembles, and, if so, its size, providing a mechanistic link between organelle assembly and cell size. Since the nucleolus is known to play a key role in cell growth, this biophysical readout of cell size could provide a novel feedback mechanism for growth control.
MeSH Terms
Animals
Caenorhabditis elegans/cytology,embryology
Cell Nucleolus/physiology,ultrastructure
Cell Size
Feedback, Physiological
Fluorescence
Image Processing, Computer-Assisted
Microscopy, Confocal
Models, Biological
RNA Interference
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Weber Stephanie C
Department of Chemical and Biological Engineering, Princeton University, Princeton, NJ 08544, USA.
Brangwynne Clifford P
Department of Chemical and Biological Engineering, Princeton University, Princeton, NJ 08544, USA. Electronic address: cbrangwy@princeton.edu.
References (26)
26 references, click to expand
-
Phase transitions and size scaling of membrane-less organelles.
J Cell Biol. 2013 Dec 23;203(6):875-81
PMID: 24368804
-
Germline and developmental roles of the nuclear transport factor importin alpha3 in C. elegans.
Development. 2001 May;128(10):1817-30
PMID: 11311162
-
Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast.
J Cell Biol. 1991 May;113(4):715-29
PMID: 2026646
-
ncl-1 is required for the regulation of cell size and ribosomal RNA synthesis in Caenorhabditis elegans.
J Cell Biol. 1998 Mar 23;140(6):1321-9
PMID: 9508766
-
Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans.
Nature. 2005 Mar 24;434(7032):462-9
PMID: 15791247
-
Distinct roles for two C. elegans anillins in the gonad and early embryo.
Development. 2005 Jun;132(12):2837-48
PMID: 15930113
-
Cajal body number and nucleolar size correlate with the cell body mass in human sensory ganglia neurons.
J Struct Biol. 2007 Jun;158(3):410-20
PMID: 17275332
-
Actin-dependent cytoplasmic streaming in C. elegans oogenesis.
Development. 2007 Jun;134(12):2227-36
PMID: 17507392
-
The size of the nucleus increases as yeast cells grow.
Mol Biol Cell. 2007 Sep;18(9):3523-32
PMID: 17596521
-
Nuclear size control in fission yeast.
J Cell Biol. 2007 Nov 19;179(4):593-600
PMID: 17998401
-
Germline P granules are liquid droplets that localize by controlled dissolution/condensation.
Science. 2009 Jun 26;324(5935):1729-32
PMID: 19460965
-
Cell-size-dependent spindle elongation in the Caenorhabditis elegans early embryo.
Curr Biol. 2009 Sep 29;19(18):1549-54
PMID: 19682904
-
Active liquid-like behavior of nucleoli determines their size and shape in Xenopus laevis oocytes.
Proc Natl Acad Sci U S A. 2011 Mar 15;108(11):4334-9
PMID: 21368180
-
Limiting amounts of centrosome material set centrosome size in C. elegans embryos.
Curr Biol. 2011 Aug 9;21(15):1259-67
PMID: 21802300
-
Centrosome size: scaling without measuring.
Curr Biol. 2011 Aug 9;21(15):R594-6
PMID: 21820626
-
Phase transitions in the assembly of multivalent signalling proteins.
Nature. 2012 Mar 15;483(7389):336-40
PMID: 22398450
-
Organelle growth control through limiting pools of cytoplasmic components.
Curr Biol. 2012 May 8;22(9):R330-9
PMID: 22575475
-
Getting RNA and protein in phase.
Cell. 2012 Jun 8;149(6):1188-91
PMID: 22682242
-
Nucleologenesis in the Caenorhabditis elegans embryo.
PLoS One. 2012;7(7):e40290
PMID: 22768349
-
Cell biology. Beyond oil and water--phase transitions in cells.
Science. 2012 Aug 31;337(6098):1047-9
PMID: 22936764
-
Mitochondrial network size scaling in budding yeast.
Science. 2012 Nov 9;338(6108):822-4
PMID: 23139336
-
A nuclear F-actin scaffold stabilizes ribonucleoprotein droplets against gravity in large cells.
Nat Cell Biol. 2013 Oct;15(10):1253-9
PMID: 23995731
-
Changes in cytoplasmic volume are sufficient to drive spindle scaling.
Science. 2013 Nov 15;342(6160):853-6
PMID: 24233723
-
Cytoplasmic volume modulates spindle size during embryogenesis.
Science. 2013 Nov 15;342(6160):856-60
PMID: 24233724
-
Systematic identification of pathways that couple cell growth and division in yeast.
Science. 2002 Jul 19;297(5580):395-400
PMID: 12089449
-
ScanImage: flexible software for operating laser scanning microscopes.
Biomed Eng Online. 2003 May 17;2:13
PMID: 12801419