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ROS regulated reversible protein phase separation synchronizes plant flowering

Abstract

How aerobic organisms exploit inevitably generated but potentially dangerous reactive oxygen species (ROS) to benefit normal life is a fundamental biological question. Locally accumulated ROS have been reported to prime stem cell differentiation. However, the underlying molecular mechanism is unclear. Here, we reveal that developmentally produced H2O2 in plant shoot apical meristem (SAM) triggers reversible protein phase separation of TERMINATING FLOWER (TMF), a transcription factor that times flowering transition in the tomato by repressing pre-maturation of SAM. Cysteine residues within TMF sense cellular redox to form disulfide bonds that concatenate multiple TMF molecules and elevate the amount of intrinsically disordered regions to drive phase separation. Oxidation triggered phase separation enables TMF to bind and sequester the promoter of a floral identity gene ANANTHA to repress its expression. The reversible transcriptional condensation via redox-regulated phase separation endows aerobic organisms with the flexibility of gene control in dealing with developmental cues.

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Fig. 1: H2O2 represses flowering transition through TMF.
Fig. 2: TMF undergoes phase separation in vitro and in vivo.
Fig. 3: Redox-regulated disulfide bonding determines phase status of TMF.
Fig. 4: TMF directly targets the AN gene.
Fig. 5: H2O2 promoted formation of TMF transcriptional condensates regulate flowering.

Data availability

Source data are provided with this paper. All other data supporting the findings of this study are available within the paper and its Supplementary information files, or are available from the corresponding author upon reasonable request.

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Acknowledgements

We thank C.-C. Wang and L. Wang from the Institute of Biophysics, CAS for sharing PDI enzyme and valuable suggestions for related experiments, Z. B. Lippman (Cold Spring Harbor Laboratory), S. J. Park (Wonkwang University) and J. V. Eck (Boyce Thompson Institute) for sharing seeds, in situ images and the tomato transformation protocol, respectively. We thank J. Y. Li, Z. B. Lippman, J. Yang, K. Jiang and Q. Y. Wu for valuable comments and discussions; S. H. Yang and J. G. Li for sharing transformation vectors; Y. B. Tian, L. Fu, Z. Lu and S. Q. Jia for technical support and Y. F. Chen, W. X. Dong, Q. L. Guo, Y. Yu, Y. Xie, T. H. Zhang and X. Tong in the Xu laboratory for their help in this study. We are grateful to the staff from facilities of State Key Laboratory of Plant Genomics, Institute of Genetics and Developmental Biology, CAS; Institute of Botany, CAS and Tsinghua University for technical assistance. This study was financially supported by the Key Research Program of Frontier Sciences of the Chinese Academy of Science (grant no. ZDBS-LY-SM021) and the Strategic Priority Research Program of Chinese Academy of Sciences (grant no. XDA24030503) to C.X., a National Key R&D grant (no. 2019YFA0508403) and a NSFC grant (no. 31871443) to P.L. and start-up funding from State Key Laboratory of Plant Genomics and Institute of Genetics and Developmental Biology to C.X. and a NSFC grant (no. 31900174) to X.H.

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Authors

Contributions

C.X. and P.L. designed the research. X.H. performed in vivo condensate assays, chemical treatments, gene expression, immunoblots, ChIP–qPCR and transcriptional activity assays with help from N.X., S.C. and W. Li performed in vitro phase separation assays. S.C. performed EMSA, protein sedimentation assays and PDI treatments. X.H. and N.X. produced CRISPR mutants and transgenic lines with the help from X.Z. L.T. performed the yeast one-hybrid assay. Y. Zhang and W. Liu performed in situ hybridization and H2O2 staining. N.Y. performed mass spectrometric analysis. Y. Zou performed bioinformatic analysis. C.X. and P.L. wrote the paper with input from all other authors.

Corresponding authors

Correspondence to Pilong Li or Cao Xu.

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Extended data

Extended Data Fig. 1 Images and quantification data for hydrogen peroxide staining and redox chemical treatments.

a, DAB staining and stereoscope imaging showing the accumulation of H2O2 in tomato young leaves treated with or without H2O2 (10 mM) for 36 h. b,c, HPF staining (b) and quantitative data (c) showing the accumulation of H2O2 in the meristem treated with or without H2O2 (10 mM) for 48 h. (n=3). d,e, Stereoscope images (d) and quantitative data (e) comparing flowering transition indicated by leaf production until floral meristem stage transition from mock and H2O2 (10 mM) treated WT (upper) and tmf-2 (bottom). Leaf production is indicated by leaf number. L, Leaf. Scale bar, 100 μm. Data are presented as means (± s.d.). Sample size used for statistics of mock and H2O2 treatment for WT and tmf-2 is 19, 16, 43, 44, respectively. f, Phylogeny tree showing RBOH gene family in tomato. g, Expression of SlRBOH genes during meristem maturation of tomato. h, CRISPR/Cas9 gRNAs for targeting SlRBOH genes. i, DAB staining showing decreased H2O2 level in CRISPR mutant of slrboh1 slrboh2. Scale bar, 0.9 cm. j, Stereoscope images comparing flowering transition indicated by leaf production until floral meristem stage transition from WT and slrboh1 slrboh2 mutant, L, leaf. Scale bar, 100 μm. Three independent assays with similar results were carried out. In c and e, data are presented as means (± s.d.)(two-tailed t-test). Source data

Extended Data Fig. 2 Droplet property and FRAP analysis of TMF-GFP condensates.

a, Amino acid sequence of TMF indicating IDRs, putative DNA binding domain and cysteine residues. b, Aspect ratios (maximal diameter/ minimal diameter) of droplets formed GFP-TMF. Gray ellipses show a guide to the eye of different aspect ratios. Totally, 202 droplets were measured for aspect ratio calculation. c, Quantification of TMF-GFP transfected tomato protoplast cells with or without condensates in nuclei. Three independent experiments were performed for quantification. Data are presented as (± s.d.) (n = 48). d,e, Image (d) and quantitative data (e) showing the recovery of TMF-GFP condensates after photobleaching in tomato protoplasts. The bleached (green line) event occurs at time = 0 s. The unbleached (blue line) was used as control. Quantitative data are representative of three independent photobleaching events. Data are presented as (± s.d.) (n = 3). Source data

Extended Data Fig. 3 Quantification data and representative images for protein behavior of TMF and its mutated variants after redox chemicals treatment.

a, Quantification of integrated fluorescence density of the liquid-like droplets formed by GFP-TMF protein under various concentration combinations of H2O2 and DTT with constant protein concentration (25 μM). b,c, Representative confocal images (b) and quantification data (c) showing effects of TCEP treatment on droplet formation of GFP-TMF proteins. Protein concentration, 20 μM; Salt concentration, 25 mM. Scale bar, 20 μm. d, Schematic sedimentation assay for redox regulated phase separation. e,f, Immunoblotting (e) and quantification data (f) showing the distribution of TMF proteins between aqueous-solution/supernatant (S) and condensed liquid phase/pellet (P) fractions after H2O2 or DTT treatments. g, Schematics showing TMF variants with IDR or cysteine mutations. h, Quantification of integrated fluorescence density of the droplets formed by TMF variants with IDR or cysteine mutations. i, Immunoblot analysis showing the expression for TMF and variants with IDR or cysteine mutations in tomato protoplast. Actin serves as a loading control. In a,c,f,h, three technical replicates data are presented as means (± s.d.) (n = 3, two-tailed t-test). Source data

Extended Data Fig. 4 Inter- and intramolecular disulfide bonds identified by LC-MS/MS.

a, LC-MS/MS spectrum of intramolecular and intermolecular disulfide bonds from normal TMF. b, Schematic diagrams showing the working model of PDI in different redox status. c, LC-MS/MS spectrum of intramolecular and intermolecular disulfide bonds from PDI treated TMF protein.

Extended Data Fig. 5 Representative colonies and quantification data of yeast one-hybrid assay.

a, Promoter regions upstream of the AN gene selected for yeast one hybrid assays in (b-d). b-d, Colony growth assessment (b) and quantification of β-galactosidase activity (c,d) in yeast one-hybrid assay. e, Promoter regions upstream of the AN gene selected for evaluating the ChIP enrichments. In c and d, three biological replicates data are presented as means (± s.d.) (n = 3, two-tailed t-test). Source data

Extended Data Fig. 6 Quantification data for droplets, phase sedimentation assay and leaf production for flower transition.

a, Phase diagram showing droplets formed by GFP-TMF protein and Cy-3 labeled DNA fragments under various concentration combinations of H2O2 and DTT with constant protein concentration. Scale bar, 5 μm. b,c, Immunoblotting (b) and quantification data (c) showing the distribution of TMF-DNA complex between aqueous-solution/supernatant (S) and condensed liquid phase/pellet (P) fractions after H2O2 or DTT treatments. Three technical replicates data are presented. d, Western blot analysis showing expression of proteins in transgenic plants. The Wild-type (WT) plant sample served as a negative control, actin served as a loading control. e, Quantification of leaf number to flower transition on primary shoots. In c and e, data are means(± s.d.) (n = 3 for c, n = 8 for e, two-tailed t-test). Source data

Supplementary information

Supplementary Information

Supplementary Fig. 1 and Table 1.

Reporting Summary

Supplementary Video 1

Fusion process of two separated GFP–TMF droplets for Fig. 2f.

Supplementary Video 2

FRAP analysis of recombinantly expressed GFP–TMF droplets for Fig. 2g.

Supplementary Video 3

FRAP analysis of TMF–GFP condensates in tomato protoplasts for Extended Data Fig. 2d.

Supplementary Video 4

FRAP analysis of TMF–GFP condensates in the young leaf of 35S:TMFGFP transgenic tomato plants for Fig. 2j.

Supplementary Video 5

FRAP analysis of droplets formed by GFP–TMF–DNA complex for Fig. 4e.

Source data

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Huang, X., Chen, S., Li, W. et al. ROS regulated reversible protein phase separation synchronizes plant flowering. Nat Chem Biol (2021). https://doi.org/10.1038/s41589-021-00739-0

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