A gel phase promotes condensation of liquid P granules in Caenorhabditis elegans embryos

An Author Correction to this article was published on 02 January 2020

This article has been updated

Abstract

RNA granules are subcellular compartments that are proposed to form by liquid–liquid phase separation (LLPS), a thermodynamic process that partitions molecules between dilute liquid phases and condensed liquid phases. The mechanisms that localize liquid phases in cells, however, are not fully understood. P granules are RNA granules that form in the posterior of Caenorhabditis elegans embryos. Theoretical studies have suggested that spontaneous LLPS of the RNA-binding protein PGL-3 with RNA drives the assembly of P granules. We find that the PGL-3 phase is intrinsically labile and requires a second phase for stabilization in embryos. The second phase is formed by gel-like assemblies of the disordered protein MEG-3 that associate with liquid PGL-3 droplets in the embryo posterior. Co-assembly of gel phases and liquid phases confers local stability and long-range dynamics, both of which contribute to localized assembly of P granules. Our findings suggest that condensation of RNA granules can be regulated spatially by gel-like polymers that stimulate LLPS locally in the cytoplasm.

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Fig. 1: P granule proteins exhibit distinct dynamics.
Fig. 2: Effect of temperature on the MEG-3 and PGL-3 phases.
Fig. 3: Effect of dilution on the MEG-3 and PGL-3 phases.
Fig. 4: In vitro assembly of MEG-3 and PGL-3 condensates.
Fig. 5: MEG-3 forms a stable scaffold around the PGL-3 liquid phase.
Fig. 6: Model for regulation of P granule assembly by the MEG-3 gel condensates.

Data availability

Source data for Figs. 1 and 35 and Supplementary Fig. 3 are available in Supplementary Dataset 1. Other data supporting the findings of this study are available from the corresponding author upon reasonable request.

Change history

  • 02 January 2020

    An amendment to this paper has been published and can be accessed via a link at the top of the paper.

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Acknowledgements

We thank D. Rasoloson who provided strains JH3269 and H. Schmidt who provided strain JH3606, and A. Folkmann for comments on the manuscript. Some strains were provided by the CGC, which is funded by National Institutes of Health (NIH) Office of Research Infrastructure Programs (P40 OD010440). Data acquisition using the Zeiss LSM 800 Confocal reported in this publication was supported by Office of the Director, NIH (OD) of the National Institutes of Health (award number S10OD016374). This work was supported by the NIH (grant number R37 HD37047, G.S.). M.C. was supported by a training grant T32 GM007445 and National Science Foundation Graduate Research Fellowship DGE-1746891. G.S. is an investigator of the Howard Hughes Medical Institute.

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A.P., M.C., J.S., and G.S. designed the research. A.P. and M.C. performed all experiments, collected, and analyzed data. G.S. and A.P. prepared the manuscript with contributions from all authors.

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Correspondence to Geraldine Seydoux.

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Integrated supplementary information

Supplementary Figure 1 P granule proteins exhibit distinct dynamics.

a Graph showing MEG-3::GFP (n = 22) and PGL-3::mCherry (n = 12) fluorescence recovery after photobleaching (FRAP) in embryos. Granule intensity was measured every 5 s for 300 s before and after bleaching. Values were normalized to initial fluorescence intensity and plotted as an average from multiple embryos. Error bars represent mean ± SEM. Representative images from FRAP experiments are shown below the graph. b Graph showing GLH-1::GFP (n = 9), LAF-1::GFP (n = 7), or DEPS-1::GFP (n = 7) FRAP in arrested oocytes. Granule intensity was measured every 3 s for 180 s (GLH-1, LAF-1) or every 5 s for 300 s (DEPS-1) before and after bleaching. Values were normalized to initial fluorescence intensity and plotted as an average from multiple embryos. Error bars represent mean ± SEM. Representative images from FRAP experiments are shown below the graph. c Graph showing MEG-3::GFP (n = 10) or PGL-3::mCherry (n = 8) FRAP in arrested oocytes. Granule intensity was measured every 5 s for 300 s before and after bleaching. Values were normalized to initial fluorescence intensity and plotted as an average from multiple oocytes. Error bars represent mean ± SEM. Representative images from FRAP experiments are shown below the graph. d Graph showing MEG-3::mCherry (n = 6) fluorescence recovery after photobleaching (FRAP) in embryos. Granule intensity was measured every 7 s for 300 s before and after bleaching. Values were normalized to initial fluorescence intensity and plotted as an average from multiple embryos. Error bars represent mean ± SEM. Representative images from FRAP experiments are shown below the graph. e Graph showing MEG-3::mCherry (n = 3) or PGL-1::GFP (n = 7) FRAP in arrested oocytes. Granule intensity was measured every 5 s for 300 s before and after bleaching. Values were normalized to initial fluorescence intensity and plotted as an average from multiple oocytes. Error bars represent mean ± SEM. Representative images from FRAP experiments are shown below the graph. f Photomicrographs of 4-cell embryos expressing MEG-3::GFP ± mbk-2 RNAi. Scale bar is 10 μm. Note that P granules do not localize properly in embryos depleted of MBK-2 kinase by RNAi. g Photomicrographs of embryos of the indicated genotypes expressing PGL-1::GFP. PGL-1::GFP ± mbk-2 RNAi photomicrographs are of 4-cell embryos. PGL-1::GFP, meg-3meg-4 photomicrograph is of a 2-cell embryo. Scale bar is 10 μm. Note that P granules do not localize properly in embryos depleted of MBK-2 kinase by RNAi or derived from mothers mutant for meg-3 and meg-4. h Graphs showing MEG-3::GFP FRAP in embryos ± mbk-2(RNAi) (n = 21). Error bars represent mean ± SEM. MEG-3 becomes less dynamic in embryos lacking MBK-2. Representative images from FRAP experiments are shown below the graph. i Graphs showing PGL-1::GFP FRAP in embryos ± mbk-2(RNAi) (n = 11). Error bars represent mean ± SEM. PGL-1 dynamics are not affected in embryos lacking MBK-2. Representative images from FRAP experiments are shown below the graph. j Graphs showing PGL-1::GFP FRAP in wild-type and embryos lacking meg-3meg4 (n = 10). Error bars represent mean ± SEM. PGL-1 dynamics increase in meg-3meg-4 embryos. Representative images from FRAP experiments are shown below the graph.

Supplementary Figure 2

Effect of temperature and dilution of MEG and PGL phases. a Time-lapse photomicrographs of a 2-cell embryo expressing MEG-3::GFP and PGL-3::mCherry fusions and cultured at 20 °C, up-shifted to 34 °C for 15 minutes (same experiment as in Fig. 2, but longer period at 34 °C). MEG-3 remains in granules throughout. PGL-3 disperses at 34 °C. Scale bar is 10 μm. b Time-lapse photomicrographs of a 2-cell embryos expressing MEG-3::mCherry and PGL-1::GFP fusion cultured at 20 °C and then up-shifted to 34 °C for 1 minute. MEG-3 remains in granules throughout. PGL-1 disperses at 34 °C. Scale bar is 10 μm. c Extruded MEG-3::GFP granules over time. Time-lapse photomicrographs of MEG-3::GFP P granules before and after extrusion into egg buffer (top panels). Time after extrusion is indicated in each image. Scale bar is 10 μm. Graph (bottom panel) showing the fraction of MEG-3::GFP retained in the granular phase over time after extrusion. Total GFP fluorescence from granules was measured 1 min after extrusion (IB) and at times indicated after extrusion (IA) and used to calculate a fluorescence ratio (IA/IB) (n = 10). d Time-lapse photomicrographs of a 4-cell embryo expressing MEG-3::mCherry or 2-cell embryos expressing PGL-1::GFP before and 10 s after laser puncture of the eggshell (top panels). Laser puncture causes the contents of the posterior blastomere to spill onto the slide mixing with the aqueous buffer. MEG-3::mCherry persists in the granule phase, whereas PGL-1 becomes dispersed. Scale bar is 10 μm. Graph (bottom panel) showing the fraction of MEG-3::mCherry (n = 5) or PGL-1::GFP (n = 3) retained in the granular phase after extrusion. Total GFP fluorescence from granules was measured before laser puncture (IB) and after laser puncture (IA) and used to calculate a fluorescence ratio (IA/IB). Means are indicated along with error bars representing ± SD.

Supplementary Figure 3 Effect of temperature and dilution on GLH-1, LAF-1 and DEPS-1.

a Time-lapse photomicrographs of a 2-cell embryos expressing GLH-1::GFP (n = 3), LAF-1::GFP (n = 4), and DEPS1::GFP (n = 5) cultured at 20 °C and then up-shifted to 34 °C for 1 minute. GLH-1 disperses whereas LAF-1 remains in granules throughout. DEPS-1 exists in two granule types: small, bright granules that are distributed throughout the cytoplasm and larger, less bright granules in the posterior cytoplasm. Both become reduced in intensity at 34 °C, consistent with partial dispersal. Images are representative of 3 independent experiments. Scale bar is 10 μm. b Time-lapse photomicrographs of 2-cell embryos expressing GLH-1::GFP, LAF-1::GFP, and DEPS1::GFP before and 10 s after laser puncture of the eggshell. Laser puncture causes the contents of the posterior blastomere to spill onto the slide mixing with the aqueous buffer. GLH-1 and LAF-1 immediately disperse. The majority of DEPS-1 also becomes dispersed, but a subset of smaller granules persists in the granule phase. Scale bar is 10 μm. c Graph showing the fraction of GLH-1::GFP (n = 6), LAF-1::GFP (n = 3), and DEPS1::GFP (n = 6) retained in the granular phase after extrusion. Total GFP fluorescence from granules was measured before laser puncture (IB) and after laser puncture (IA) and used to calculate a fluorescence ratio (IA/IB). Means are indicated along with error bars representing ± SD.

Supplementary Figure 4 In vitro assembly of MEG-3 and PGL-3 condensates.

a Coomassie gels of purified MEG-3 and PGL-3 proteins (Methods). b Representative photomicrographs of MEG-3 and PGL-3 images from Fig. 4a. Images were uniformly processed to reveal the small MEG-3 condensates at the onset of co-assembly. Images were taken at indicated time points after initiation of condensate assembly. Scale bar is 5 µm. c Histograms of intensity distributions of MEG-3 and PGL-3 condensates individually or together after 30 mins of condensate formation. These results suggest that in the individual condensation experiments, most PGL-3 condensates, but only a fraction of MEG-3 condensates, are detected under our imaging conditions. d Graph showing fluorescence recovery after photobleaching (FRAP) of PGL-3 condensates assembled as in Fig. 4a and incubated for 30 min. The entire PGL-3 condensate was bleached. Intensity was measured every 3 s for 300 s before and after bleaching. Values were normalized to initial fluorescence intensity, corrected for photobleaching and plotted as an average from multiple experiments (n = 8). Error bars represent mean ± SD. Representative images from FRAP experiments are shown below the graph. Scale bar is 1 µm. e Graphs showing the Pearson’s correlation coefficient comparing the intensity of MEG-3 or PGL-3 in each condensate. MEG-3 and PGL-3 show increased co-localization over time. Each data point represents the mean ± SD of coefficients calculated for a total of 16 images from 4 experimental replicates. f Radial intensity profile plot of the MEG-3 and PGL-3 phases from the co-condensate shown in Fig. 4d (30 min in vitro assembly). Lines represent the relative maximum intensity along radii extending from the condensate in 360°. The resulting plot shows the variation in intensity around the circumference of the condensate. Note that PGL-3 is evenly distributed around the condensate, while MEG-3 intensity varies. g Photomicrographs of selected frames from Supplemental video 4. Co-condensates were assembled as in Fig. 4a and incubated for 15 min. Scale bar is 1 µm. Co-condensates of MEG-3 and PGL-3 fuse. MEG-3 remains enriched on the surface of the PGL-3 phase after fusion. h Photomicrographs of selected frames from Supplemental video 5. Co-condensates were assembled as in Fig. 4a and incubated for 15 min. Arrows indicate the position of MEG-3 condensates as they move relative to each other on the surface of the PGL-3 condensate. Scale bar is 1 µm. i Photomicrographs of selected frames from Supplemental video 6. Co-condensates were assembled as in Fig. 4a and incubated for 15 min. A MEG-3 condensate on the surface of the PGL-3 condensate was FRAPed (panel 2). The photobleached region indicated by the arrow changes position during the recovery period consistent with movement of the MEG-3 phase. Scale bar is 1 µm.

Supplementary Figure 5 MEG-3 and PGL-3 condensates in embryos.

a, b. Representative maximum projection photomicrographs of the posterior of a (a) 1-cell or (b) 4-cell embryo expressing MEG-3::GFP and PGL-3::mCherry fusions. Center Z-slice of indicated granules are enlarged in the panels on the right. Scale bars are 1 µm. In the 1-cell stage, MEG-3 is enriched at the periphery of the granules. In the 4-cell stage, after some granules have undergone fusion, the MEG-3 scaffold assumes more complex configurations, but remains distinct from the PGL-3 core.

Supplementary Figure 6 Effect of salt and other challenges on MEG-3 and PGL-3 condensates.

a Representative images of MEG-3 or MEG-3-IDR and PGL-3 co-assemblies in condensation buffer or buffer with 1M NaCl for 15 min as described in Fig. 5a. Scale bar is 5 µm. b Representative images of MEG-3 and PGL-3 co-assemblies after incubation with 1M NaCl for 15 min as described in Fig. 5a. Scale bar is 2 µm. c Graphs showing the relative proportion of MEG-3 in condensates [calculated as the ratio of fluorescence in condensates (IC) over total fluorescence (IT)] on a log scale. Single condensates are in black and co-condensates are in green. Each data point represents the average from 4 images collected in one experiment. For data points marked by ‘*’, no condensates were detected. Bars represent the mean ± SD. Condensates were incubated for 15 min before challenge with the indicated additive for 15 minutes (7 mM ATP/Mg, 5% 2,5 or 1,6 Hexanediol, 0.5% SDS). d Graphs showing the relative proportion of PGL-3 in condensates determined as described in (c).

Supplementary Figure 7 RNA dependence of MEG-3 and PGL-3 co-condensate formation.

Representative images of MEG-3 and PGL-3 co-assemblies in condensation buffer. All reactions contained 1.8 µM PGL-3 with varying concentrations of MEG-3 on the y-axis and varying concentration of total embryonic RNA on the x-axis. Reactions were incubated for 15 min. Scale bar is 10 µm. Red boxes indicate conditions where both MEG-3 and PGL-3 form round co-condensates. Conditions that included no RNA or low concentrations of RNA (panels on the left) resulted in the co-precipitation of MEG-3/PGL-3 into aggregates of various shapes. Addition of moderate concentrations of RNA induced the formation of round PGL-3/MEG-3 co-condensates. Higher concentrations of RNA were required to induce round condensates with increasing concentrations of MEG-3. The highest concentrations of RNA (≥500 ng/uL, right most panels) seemed to interfere with condensation.

Supplementary information

Supplementary Figures and Supplementary Table

Supplementary Figures 1–7 and Supplementary Table 1

Reporting Summary

Supplementary Dataset 1

Supplementary Video 1

PGL-1::GFP dynamics in wildtype embryos. Time-lapse of a one-cell embryo expressing GFP::PGL-1(strain JH3269). Images are maximum-intensity projections of Z planes spanning the depth of the entire embryo separated by 1-μm steps. Stacks were taken constantly; total video time is 00:17:55; playback speed is six frames per second. Scale bar is 10 μm. Note that PGL-1 granules disassemble and reassemble in the posterior during the progression from the one-cell stage to the two-cell stage.

Supplementary Video 2

PGL-1::GFP dynamics in meg-3meg-4 embryos. Time-lapse of one-cell meg-3meg-4 embryos expressing GFP::PGL-1 (strain JH3606). Images were taken as in Supplemental Video 1. Note that PGL-1::GFP granules fail to assemble in the posterior during the progression from the one-cell stage to the two-cell stage.

Supplementary Video 3

Extrusion of MEG-3::GFP and mCherry::PGL-3 labeled granules in egg buffer. Synchronized maximum projection time-lapse videos showing extrusion of P granules from a C. elegans embryo coexpressing MEG-3::GFP (left) and mCherry::PGL-3 (right) (strain JH3602). Top left corner shows elapsed time in h:min:s. Images are maximum-intensity projections spanning the depth of the entire embryo separated by 1-μm steps. Stacks were taken every 10 s; total video time is 00:01:30; playback speed is four frames per second. Scale bar is 10 μm. Video was acquired as described in Methods and is the same embryo depicted in Fig. 3b.

Supplementary Video 4

Fusion of MEG-3 and PGL-3 co-condensates assembled in vitro. Synchronized single-plane time-lapse video of cocondensates assembled in vitro as in Fig. 4a for 15 min. Channels for MEG-3 (left), PGL-3 (center), and merged (right) are shown. Images were taken every 5 s; total video time is 230 s; playback speed is three frames per second.

Supplementary Video 5

Movement of MEG-3 foci in a co-condensate assembled in vitro. Synchronized single-plane time-lapse video of cocondensates assembled in vitro as in Fig. 4a for 15 min. Channels for MEG-3 (left), PGL-3 (center), and merged (right) are shown. Images were taken every 5 s; total video time is 12 min; playback speed is ten frames per second.

Supplementary Video 6

FRAPed MEG-3 foci in a co-condensate assembled in vitro. Synchronized single-plane time-lapse video of cocondensates assembled in vitro as in Fig. 4d for 15 min. Channels for MEG-3 (left), PGL-3 (center), and merged (right) are shown. FRAP was performed as described in Methods. Images were taken every 1 s; total video time is 3 min; playback speed is five frames per second.

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Putnam, A., Cassani, M., Smith, J. et al. A gel phase promotes condensation of liquid P granules in Caenorhabditis elegans embryos. Nat Struct Mol Biol 26, 220–226 (2019). https://doi.org/10.1038/s41594-019-0193-2

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