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PMID: 33049212 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

Emerging Roles for Phase Separation in Plants.

Developmental cell ·Vol. 55 ·No. 1 ·2020-00-12 ·Pages 69-83

Emenecker RJ, Holehouse AS, Strader LC

Abstract

The plant cell internal environment is a dynamic, intricate landscape composed of many intracellular compartments. Cells organize some cellular components through formation of biomolecular condensates-non-stoichiometric assemblies of protein and/or nucleic acids. In many cases, phase separation appears to either underly or contribute to the formation of biomolecular condensates. Many canonical membraneless compartments within animal cells form in a manner that is at least consistent with phase separation, including nucleoli, stress granules, Cajal bodies, and numerous additional bodies, regulated by developmental and environmental stimuli. In this Review, we examine the emerging roles for phase separation in plants. Further, drawing on studies carried out in other organisms, we identify cellular phenomenon in plants that might also arise via phase separation. We propose that plants make use of phase separation to a much greater extent than has been previously appreciated, implicating phase separation as an evolutionarily ancient mechanism for cellular organization.

Keywords
biomolecular condensates condensates phase separation phase separation in plants
MeSH Terms
Animals Cell Nucleolus/metabolism Cytoplasm/metabolism Humans Organelles/metabolism Plant Physiological Phenomena Plant Proteins/metabolism Plants
Chemicals
Plant Proteins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Emenecker Ryan J
Department of Biology, Washington University, St. Louis, MO 63130, USA; Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, MO 63110, USA; Center for Science and Engineering Living Systems (CSELS), Washington University, St. Louis, MO 63130, USA; Center for Engineering Mechanobiology, Washington University, St. Louis, MO 63130, USA.
Holehouse Alex S
Department of Biochemistry and Molecular Biophysics, Washington University School of Medicine, St. Louis, MO 63110, USA; Center for Science and Engineering Living Systems (CSELS), Washington University, St. Louis, MO 63130, USA. Electronic address: alex.holehouse@wustl.edu.
Strader Lucia C
Center for Science and Engineering Living Systems (CSELS), Washington University, St. Louis, MO 63130, USA; Center for Engineering Mechanobiology, Washington University, St. Louis, MO 63130, USA; Department of Biology, Duke University, Durham, NC 27708, USA. Electronic address: lucia.strader@duke.edu.
Conflict of Interest

Declaration of Interests A.S.H. is a scientific consultant with Dewpoint Therapeutics. R.J.E. and L.C.S. declare no competing interests.

References (155)
155 references, click to expand
  1. Ligand effects on phase separation of multivalent macromolecules.
    Proc Natl Acad Sci U S A. 2021 Mar 9;118(10): PMID: 33653957
  2. Composition-dependent thermodynamics of intracellular phase separation.
    Nature. 2020 May;581(7807):209-214 PMID: 32405004
  3. Composition and function of P bodies in Arabidopsis thaliana.
    Front Plant Sci. 2014 May 14;5:201 PMID: 24860588
  4. Polyubiquitin chain-induced p62 phase separation drives autophagic cargo segregation.
    Cell Res. 2018 Apr;28(4):405-415 PMID: 29507397
  5. FCA mediates thermal adaptation of stem growth by attenuating auxin action in Arabidopsis.
    Nat Commun. 2014 Nov 17;5:5473 PMID: 25400039
  6. Paraspeckles: Where Long Noncoding RNA Meets Phase Separation.
    Trends Biochem Sci. 2018 Feb;43(2):124-135 PMID: 29289458
  7. Tudor-SN, a component of stress granules, regulates growth under salt stress by modulating GA20ox3 mRNA levels in Arabidopsis.
    J Exp Bot. 2014 Nov;65(20):5933-44 PMID: 25205572
  8. Phase separation of 53BP1 determines liquid-like behavior of DNA repair compartments.
    EMBO J. 2019 Aug 15;38(16):e101379 PMID: 31267591
  9. Live Cell Imaging Reveals the Relocation of dsRNA Binding Proteins Upon Viral Infection.
    Mol Plant Microbe Interact. 2017 Jun;30(6):435-443 PMID: 28296575
  10. Organization and Function of Non-dynamic Biomolecular Condensates.
    Trends Biochem Sci. 2018 Feb;43(2):81-94 PMID: 29258725
  11. Nuclear localization and in vivo dynamics of a plant-specific serine/arginine-rich protein.
    Plant J. 2003 Dec;36(6):883-93 PMID: 14675452
  12. ELF4 regulates GIGANTEA chromatin access through subnuclear sequestration.
    Cell Rep. 2013 Mar 28;3(3):671-7 PMID: 23523352
  13. Nucleoli: composition, function, and dynamics.
    Plant Physiol. 2012 Jan;158(1):44-51 PMID: 22082506
  14. Local Translation in Axons: When Membraneless RNP Granules Meet Membrane-Bound Organelles.
    Front Mol Biosci. 2019 Nov 22;6:129 PMID: 31824961
  15. The functional interplay between protein kinase CK2 and CCA1 transcriptional activity is essential for clock temperature compensation in Arabidopsis.
    PLoS Genet. 2010 Nov 04;6(11):e1001201 PMID: 21079791
  16. Phase separation drives heterochromatin domain formation.
    Nature. 2017 Jul 13;547(7662):241-245 PMID: 28636597
  17. PWWP-DOMAIN INTERACTOR OF POLYCOMBS1 Interacts with Polycomb-Group Proteins and Histones and Regulates Arabidopsis Flowering and Development.
    Plant Cell. 2018 Jan;30(1):117-133 PMID: 29330200
  18. Dehydration stress activates Arabidopsis MPK6 to signal DCP1 phosphorylation.
    EMBO J. 2012 Apr 18;31(8):1975-84 PMID: 22407295
  19. The splicing factor U1-70K interacts with the SMN complex and is required for nuclear gem integrity.
    J Cell Sci. 2014 Sep 15;127(Pt 18):3909-15 PMID: 25052091
  20. PCH1 integrates circadian and light-signaling pathways to control photoperiod-responsive growth in Arabidopsis.
    Elife. 2016 Feb 03;5:e13292 PMID: 26839287
  21. The Cajal body and histone locus body.
    Cold Spring Harb Perspect Biol. 2010 Jul;2(7):a000653 PMID: 20504965
  22. The SR protein family of splicing factors: master regulators of gene expression.
    Biochem J. 2009 Jan 1;417(1):15-27 PMID: 19061484
  23. Photobodies in light signaling.
    Plant Physiol. 2012 Jan;158(1):52-60 PMID: 21951469
  24. Shining a light on the Arabidopsis circadian clock.
    Plant Cell Environ. 2017 Nov;40(11):2571-2585 PMID: 28732105
  25. Coactivator condensation at super-enhancers links phase separation and gene control.
    Science. 2018 Jul 27;361(6400): PMID: 29930091
  26. Formation of cytoplasmic heat shock granules in tomato cell cultures and leaves.
    Mol Cell Biol. 1983 Sep;3(9):1648-55 PMID: 6633535
  27. Plant coilin: structural characteristics and RNA-binding properties.
    PLoS One. 2013;8(1):e53571 PMID: 23320094
  28. Intrinsically disordered proteins and intrinsically disordered protein regions.
    Annu Rev Biochem. 2014;83:553-84 PMID: 24606139
  29. Proteomic analysis of interchromatin granule clusters.
    Mol Biol Cell. 2004 Aug;15(8):3876-90 PMID: 15169873
  30. P-Bodies: Composition, Properties, and Functions.
    Biochemistry. 2018 May 1;57(17):2424-2431 PMID: 29381060
  31. Plant nuclear bodies.
    Curr Opin Plant Biol. 2004 Dec;7(6):614-20 PMID: 15491908
  32. ATPase-Modulated Stress Granules Contain a Diverse Proteome and Substructure.
    Cell. 2016 Jan 28;164(3):487-98 PMID: 26777405
  33. Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses.
    Plant Mol Biol. 2005 Jul;58(4):585-96 PMID: 16021341
  34. Tardigrades Use Intrinsically Disordered Proteins to Survive Desiccation.
    Mol Cell. 2017 Mar 16;65(6):975-984.e5 PMID: 28306513
  35. PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition.
    Bioinformatics. 2014 Sep 1;30(17):2501-2 PMID: 24825614
  36. HP1 reshapes nucleosome core to promote phase separation of heterochromatin.
    Nature. 2019 Nov;575(7782):390-394 PMID: 31618757
  37. Biomolecular condensates: organizers of cellular biochemistry.
    Nat Rev Mol Cell Biol. 2017 May;18(5):285-298 PMID: 28225081
  38. Liquid droplet formation by HP1α suggests a role for phase separation in heterochromatin.
    Nature. 2017 Jul 13;547(7662):236-240 PMID: 28636604
  39. LASSI: A lattice model for simulating phase transitions of multivalent proteins.
    PLoS Comput Biol. 2019 Oct 21;15(10):e1007028 PMID: 31634364
  40. Arabidopsis DCP2, DCP1, and VARICOSE form a decapping complex required for postembryonic development.
    Plant Cell. 2006 Dec;18(12):3386-98 PMID: 17158604
  41. Diversity of Polycomb group complexes in plants: same rules, different players?
    Trends Genet. 2009 Sep;25(9):414-23 PMID: 19716619
  42. Blue-light-dependent interaction of cryptochrome 1 with SPA1 defines a dynamic signaling mechanism.
    Genes Dev. 2011 May 15;25(10):1023-8 PMID: 21511872
  43. Regulation of auxin transcriptional responses.
    Dev Dyn. 2020 Apr;249(4):483-495 PMID: 31774605
  44. DNA repair by Rad52 liquid droplets.
    Nat Commun. 2020 Feb 4;11(1):695 PMID: 32019927
  45. The molecular language of membraneless organelles.
    J Biol Chem. 2019 May 3;294(18):7115-7127 PMID: 30045872
  46. Poly-dipeptides encoded by the C9orf72 repeats bind nucleoli, impede RNA biogenesis, and kill cells.
    Science. 2014 Sep 5;345(6201):1139-45 PMID: 25081482
  47. A view of nuclear Polycomb bodies.
    Curr Opin Genet Dev. 2012 Apr;22(2):101-9 PMID: 22178420
  48. Dynamic regulation of ARGONAUTE4 within multiple nuclear bodies in Arabidopsis thaliana.
    PLoS Genet. 2008 Feb;4(2):e27 PMID: 18266474
  49. Organization of Chromatin by Intrinsic and Regulated Phase Separation.
    Cell. 2019 Oct 3;179(2):470-484.e21 PMID: 31543265
  50. RNA transcription modulates phase transition-driven nuclear body assembly.
    Proc Natl Acad Sci U S A. 2015 Sep 22;112(38):E5237-45 PMID: 26351690
  51. Coordinated regulation of Arabidopsis microRNA biogenesis and red light signaling through Dicer-like 1 and phytochrome-interacting factor 4.
    PLoS Genet. 2018 Mar 9;14(3):e1007247 PMID: 29522510
  52. Fibrillarin genes encode both a conserved nucleolar protein and a novel small nucleolar RNA involved in ribosomal RNA methylation in Arabidopsis thaliana.
    J Biol Chem. 2000 Sep 1;275(35):27212-20 PMID: 10829025
  53. Molecular structure in biomolecular condensates.
    Curr Opin Struct Biol. 2020 Feb;60:17-26 PMID: 31790873
  54. Transcription Factors Activate Genes through the Phase-Separation Capacity of Their Activation Domains.
    Cell. 2018 Dec 13;175(7):1842-1855.e16 PMID: 30449618
  55. ABI5-binding proteins (AFPs) alter transcription of ABA-induced genes via a variety of interactions with chromatin modifiers.
    Plant Mol Biol. 2017 Mar;93(4-5):403-418 PMID: 27942958
  56. Valence and patterning of aromatic residues determine the phase behavior of prion-like domains.
    Science. 2020 Feb 7;367(6478):694-699 PMID: 32029630
  57. PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis.
    Proc Natl Acad Sci U S A. 2019 Apr 23;116(17):8603-8608 PMID: 30948632
  58. Phosphorylation regulates in vivo interaction and molecular targeting of serine/arginine-rich pre-mRNA splicing factors.
    J Cell Biol. 1999 May 3;145(3):447-55 PMID: 10225947
  59. Nuclear speckles: molecular organization, biological function and role in disease.
    Nucleic Acids Res. 2017 Oct 13;45(18):10350-10368 PMID: 28977640
  60. Nucleo-cytoplasmic Partitioning of ARF Proteins Controls Auxin Responses in Arabidopsis thaliana.
    Mol Cell. 2019 Oct 3;76(1):177-190.e5 PMID: 31421981
  61. The SMN complex.
    Exp Cell Res. 2004 May 15;296(1):51-6 PMID: 15120993
  62. Liquid-Liquid Phase Transition Drives Intra-chloroplast Cargo Sorting.
    Cell. 2020 Mar 19;180(6):1144-1159.e20 PMID: 32169217
  63. Memories from the polycomb group proteins.
    Annu Rev Genet. 2012;46:561-89 PMID: 22994356
  64. Stress granule assembly is mediated by prion-like aggregation of TIA-1.
    Mol Biol Cell. 2004 Dec;15(12):5383-98 PMID: 15371533
  65. Compositional Control of Phase-Separated Cellular Bodies.
    Cell. 2016 Jul 28;166(3):651-663 PMID: 27374333
  66. Nuclear condensates of the Polycomb protein chromobox 2 (CBX2) assemble through phase separation.
    J Biol Chem. 2019 Feb 1;294(5):1451-1463 PMID: 30514760
  67. Arginine-Enriched Mixed-Charge Domains Provide Cohesion for Nuclear Speckle Condensation.
    Mol Cell. 2020 Mar 19;77(6):1237-1250.e4 PMID: 32048997
  68. The Arabidopsis aberrant growth and death2 mutant shows resistance to Pseudomonas syringae and reveals a role for NPR1 in suppressing hypersensitive cell death.
    Plant J. 2001 Aug;27(3):203-11 PMID: 11532166
  69. Context-Dependent and Disease-Specific Diversity in Protein Interactions within Stress Granules.
    Cell. 2018 Jan 25;172(3):590-604.e13 PMID: 29373831
  70. Low-complexity domain of U1-70K modulates phase separation and aggregation through distinctive basic-acidic motifs.
    Sci Adv. 2019 Nov 06;5(11):eaax5349 PMID: 31723601
  71. Focusing on the nuclear and subnuclear dynamics of light and circadian signalling.
    Plant Cell Environ. 2019 Oct;42(10):2871-2884 PMID: 31369151
  72. Selective mRNA sequestration by OLIGOURIDYLATE-BINDING PROTEIN 1 contributes to translational control during hypoxia in Arabidopsis.
    Proc Natl Acad Sci U S A. 2014 Feb 11;111(6):2373-8 PMID: 24469793
  73. Special focus on the Cajal Body.
    RNA Biol. 2017 Jun 3;14(6):669-670 PMID: 28486008
  74. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants.
    Curr Biol. 2007 May 1;17(9):818-23 PMID: 17442570
  75. Liquid phase condensation in cell physiology and disease.
    Science. 2017 Sep 22;357(6357): PMID: 28935776
  76. Arabidopsis FLL2 promotes liquid-liquid phase separation of polyadenylation complexes.
    Nature. 2019 May;569(7755):265-269 PMID: 31043738
  77. ATPase activity of the DEAD-box protein Dhh1 controls processing body formation.
    Elife. 2016 Oct 03;5: PMID: 27692063
  78. Signals controlling Cajal body assembly and function.
    Int J Biochem Cell Biol. 2013 Jul;45(7):1314-7 PMID: 23583661
  79. Stress granule formation is induced by a threshold temperature rather than a temperature difference in Arabidopsis.
    J Cell Sci. 2018 Aug 20;131(16): PMID: 30030372
  80. Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities.
    Nat Commun. 2020 Apr 3;11(1):1660 PMID: 32245953
  81. Nuclear speckles.
    Cold Spring Harb Perspect Biol. 2011 Feb 01;3(2): PMID: 20926517
  82. Considerations and Challenges in Studying Liquid-Liquid Phase Separation and Biomolecular Condensates.
    Cell. 2019 Jan 24;176(3):419-434 PMID: 30682370
  83. All about the RNA after all.
    Elife. 2017 Jan 24;6: PMID: 28117660
  84. DNA damage foci: Meaning and significance.
    Environ Mol Mutagen. 2015 Jul;56(6):491-504 PMID: 25773265
  85. Phase separation by low complexity domains promotes stress granule assembly and drives pathological fibrillization.
    Cell. 2015 Sep 24;163(1):123-33 PMID: 26406374
  86. Competing Protein-RNA Interaction Networks Control Multiphase Intracellular Organization.
    Cell. 2020 Apr 16;181(2):306-324.e28 PMID: 32302570
  87. Dynamic nucleocytoplasmic shuttling of an Arabidopsis SR splicing factor: role of the RNA-binding domains.
    Plant Physiol. 2010 May;153(1):273-84 PMID: 20237019
  88. A distant coilin homologue is required for the formation of cajal bodies in Arabidopsis.
    Mol Biol Cell. 2006 Jul;17(7):2942-51 PMID: 16624863
  89. The Arabidopsis tandem zinc finger protein AtTZF1 traffics between the nucleus and cytoplasmic foci and binds both DNA and RNA.
    Plant Physiol. 2010 Jan;152(1):151-65 PMID: 19897605
  90. The Clk/Sty protein kinase phosphorylates SR splicing factors and regulates their intranuclear distribution.
    EMBO J. 1996 Jan 15;15(2):265-75 PMID: 8617202
  91. Coilin-dependent snRNP assembly is essential for zebrafish embryogenesis.
    Nat Struct Mol Biol. 2010 Apr;17(4):403-9 PMID: 20357773
  92. Formation of NPR1 Condensates Promotes Cell Survival during the Plant Immune Response.
    Cell. 2020 Sep 3;182(5):1093-1108.e18 PMID: 32810437
  93. Phase separation directs ubiquitination of gene-body nucleosomes.
    Nature. 2020 Mar;579(7800):592-597 PMID: 32214243
  94. Liquid-liquid phase separation in biology.
    Annu Rev Cell Dev Biol. 2014;30:39-58 PMID: 25288112
  95. Diffuse decapping enzyme DCP2 accumulates in DCP1 foci under heat stress in Arabidopsis thaliana.
    Plant Cell Physiol. 2015 Jan;56(1):107-15 PMID: 25339350
  96. A Molecular Grammar Governing the Driving Forces for Phase Separation of Prion-like RNA Binding Proteins.
    Cell. 2018 Jul 26;174(3):688-699.e16 PMID: 29961577
  97. Functional Implications of Intracellular Phase Transitions.
    Biochemistry. 2018 May 1;57(17):2415-2423 PMID: 29323488
  98. Light Triggers the miRNA-Biogenetic Inconsistency for De-etiolated Seedling Survivability in Arabidopsis thaliana.
    Mol Plant. 2020 Mar 2;13(3):431-445 PMID: 31678531
  99. Dicing bodies.
    Plant Physiol. 2012 Jan;158(1):61-6 PMID: 22025607
  100. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion.
    Nat Commun. 2017 Dec 20;8(1):2221 PMID: 29263319
  101. RNA-Induced Conformational Switching and Clustering of G3BP Drive Stress Granule Assembly by Condensation.
    Cell. 2020 Apr 16;181(2):346-361.e17 PMID: 32302572
  102. Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes.
    Cell. 2010 Jun 25;141(7):1230-40 PMID: 20603003
  103. Cajal bodies and their role in plant stress and disease responses.
    RNA Biol. 2017 Jun 3;14(6):779-790 PMID: 27726481
  104. Co-localisation studies of Arabidopsis SR splicing factors reveal different types of speckles in plant cell nuclei.
    Exp Cell Res. 2008 Oct 15;314(17):3175-86 PMID: 18674533
  105. The Multiple Functions of the Nucleolus in Plant Development, Disease and Stress Responses.
    Front Plant Sci. 2018 Feb 09;9:132 PMID: 29479362
  106. PARylation regulates stress granule dynamics, phase separation, and neurotoxicity of disease-related RNA-binding proteins.
    Cell Res. 2019 Mar;29(3):233-247 PMID: 30728452
  107. Protocol Update for large-scale genome and gene function analysis with the PANTHER classification system (v.14.0).
    Nat Protoc. 2019 Mar;14(3):703-721 PMID: 30804569
  108. Protein Phase Separation: A New Phase in Cell Biology.
    Trends Cell Biol. 2018 Jun;28(6):420-435 PMID: 29602697
  109. Intrinsically disordered linkers determine the interplay between phase separation and gelation in multivalent proteins.
    Elife. 2017 Nov 01;6: PMID: 29091028
  110. Formation of nuclear bodies of Arabidopsis CRY2 in response to blue light is associated with its blue light-dependent degradation.
    Plant Cell. 2009 Jan;21(1):118-30 PMID: 19141709
  111. The movement of coiled bodies visualized in living plant cells by the green fluorescent protein.
    Mol Biol Cell. 1999 Jul;10(7):2297-307 PMID: 10397766
  112. Identification of Coilin Mutants in a Screen for Enhanced Expression of an Alternatively Spliced GFP Reporter Gene in Arabidopsis thaliana.
    Genetics. 2016 Aug;203(4):1709-20 PMID: 27317682
  113. Nuclear speckles: a model for nuclear organelles.
    Nat Rev Mol Cell Biol. 2003 Aug;4(8):605-12 PMID: 12923522
  114. Sequence-encoded material properties dictate the structure and function of nuclear bodies.
    Curr Opin Cell Biol. 2017 Jun;46:62-71 PMID: 28343140
  115. Characterization of wound-responsive RNA-binding proteins and their splice variants in Arabidopsis.
    Plant Mol Biol. 2008 May;67(1-2):71-88 PMID: 18278441
  116. Cytoplasmic ribonucleoprotein (RNP) bodies and their relationship to GW/P bodies.
    Int J Biochem Cell Biol. 2010 Jun;42(6):828-43 PMID: 19944184
  117. Plant snRNP Biogenesis: A Perspective from the Nucleolus and Cajal Bodies.
    Front Plant Sci. 2018 Jan 04;8:2184 PMID: 29354141
  118. UBA1 and UBA2, two proteins that interact with UBP1, a multifunctional effector of pre-mRNA maturation in plants.
    Mol Cell Biol. 2002 Jun;22(12):4346-57 PMID: 12024044
  119. Evaluating phase separation in live cells: diagnosis, caveats, and functional consequences.
    Genes Dev. 2019 Dec 1;33(23-24):1619-1634 PMID: 31594803
  120. Localization and dynamics of nuclear speckles in plants.
    Plant Physiol. 2012 Jan;158(1):67-77 PMID: 22045923
  121. The involvement of stress granules in aging and aging-associated diseases.
    Aging Cell. 2020 Apr;19(4):e13136 PMID: 32170904
  122. The Cryptochrome Blue Light Receptors.
    Arabidopsis Book. 2010 Sep 23;8:e0135 PMID: 21841916
  123. Phase separation of the C. elegans Polycomb protein SOP-2 is modulated by RNA and sumoylation.
    Protein Cell. 2020 Mar;11(3):202-207 PMID: 31894537
  124. Phase Separation of Intrinsically Disordered Proteins.
    Methods Enzymol. 2018;611:1-30 PMID: 30471685
  125. Selection of mitochondria in female germline cells: is Balbiani body implicated in this process?
    J Assist Reprod Genet. 2017 Nov;34(11):1405-1412 PMID: 28755153
  126. Stress-Triggered Phase Separation Is an Adaptive, Evolutionarily Tuned Response.
    Cell. 2017 Mar 9;168(6):1028-1040.e19 PMID: 28283059
  127. Extreme disorder in an ultrahigh-affinity protein complex.
    Nature. 2018 Mar 1;555(7694):61-66 PMID: 29466338
  128. Phase separation of Polycomb-repressive complex 1 is governed by a charged disordered region of CBX2.
    Genes Dev. 2019 Jul 1;33(13-14):799-813 PMID: 31171700
  129. AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation.
    Genes Dev. 2003 Feb 1;17(3):410-8 PMID: 12569131
  130. TIA-1 Self-Multimerization, Phase Separation, and Recruitment into Stress Granules Are Dynamically Regulated by Zn2.
    Cell Rep. 2018 Jan 2;22(1):59-71 PMID: 29298433
  131. DEAD-box ATPases are global regulators of phase-separated organelles.
    Nature. 2019 Sep;573(7772):144-148 PMID: 31435012
  132. The selective autophagy receptor p62 forms a flexible filamentous helical scaffold.
    Cell Rep. 2015 May 5;11(5):748-58 PMID: 25921531
  133. PANTHER version 14: more genomes, a new PANTHER GO-slim and improvements in enrichment analysis tools.
    Nucleic Acids Res. 2019 Jan 8;47(D1):D419-D426 PMID: 30407594
  134. PML Nuclear Body Biogenesis, Carcinogenesis, and Targeted Therapy.
    Trends Cancer. 2020 Oct;6(10):889-906 PMID: 32527650
  135. Transport Selectivity of Nuclear Pores, Phase Separation, and Membraneless Organelles.
    Trends Biochem Sci. 2016 Jan;41(1):46-61 PMID: 26705895
  136. The Role of Post-Translational Modifications in the Phase Transitions of Intrinsically Disordered Proteins.
    Int J Mol Sci. 2019 Nov 05;20(21): PMID: 31694155
  137. Coilin is essential for Cajal body organization in Drosophila melanogaster.
    Mol Biol Cell. 2009 Mar;20(6):1661-70 PMID: 19158395
  138. Processing bodies control the selective translation for optimal development of Arabidopsis young seedlings.
    Proc Natl Acad Sci U S A. 2019 Mar 26;116(13):6451-6456 PMID: 30850529
  139. Protein and metabolite composition of Arabidopsis stress granules.
    New Phytol. 2019 May;222(3):1420-1433 PMID: 30664249
  140. TIA1 Mutations in Amyotrophic Lateral Sclerosis and Frontotemporal Dementia Promote Phase Separation and Alter Stress Granule Dynamics.
    Neuron. 2017 Aug 16;95(4):808-816.e9 PMID: 28817800
  141. Principles and Properties of Stress Granules.
    Trends Cell Biol. 2016 Sep;26(9):668-679 PMID: 27289443
  142. Interactions of Arabidopsis RS domain containing cyclophilins with SR proteins and U1 and U11 small nuclear ribonucleoprotein-specific proteins suggest their involvement in pre-mRNA Splicing.
    J Biol Chem. 2004 Aug 6;279(32):33890-8 PMID: 15166240
  143. Posttranslational Modifications of the Master Transcriptional Regulator NPR1 Enable Dynamic but Tight Control of Plant Immune Responses.
    Cell Host Microbe. 2015 Aug 12;18(2):169-82 PMID: 26269953
  144. Amyloid-like Self-Assembly of a Cellular Compartment.
    Cell. 2016 Jul 28;166(3):637-650 PMID: 27471966
  145. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis.
    Nature. 2020 Sep;585(7824):256-260 PMID: 32848244
  146. Modulation of an RNA-binding protein by abscisic-acid-activated protein kinase.
    Nature. 2002 Aug 15;418(6899):793-7 PMID: 12181571
  147. Coexisting Liquid Phases Underlie Nucleolar Subcompartments.
    Cell. 2016 Jun 16;165(7):1686-1697 PMID: 27212236
  148. Coiled body numbers in the Arabidopsis root epidermis are regulated by cell type, developmental stage and cell cycle parameters.
    J Cell Sci. 1998 Dec 18;111 ( Pt 24):3687-94 PMID: 9819359
  149. Cellular sensing by phase separation: Using the process, not just the products.
    J Biol Chem. 2019 May 3;294(18):7151-7159 PMID: 30877200
  150. G3BP1 Is a Tunable Switch that Triggers Phase Separation to Assemble Stress Granules.
    Cell. 2020 Apr 16;181(2):325-345.e28 PMID: 32302571
  151. The UPF1 interactome reveals interaction networks between RNA degradation and translation repression factors in Arabidopsis.
    Plant J. 2018 Oct;96(1):119-132 PMID: 29983000
  152. A Phase Separation Model for Transcriptional Control.
    Cell. 2017 Mar 23;169(1):13-23 PMID: 28340338
  153. An ARGONAUTE4-containing nuclear processing center colocalized with Cajal bodies in Arabidopsis thaliana.
    Cell. 2006 Jul 14;126(1):93-106 PMID: 16839879
  154. EARLY FLOWERING4 recruitment of EARLY FLOWERING3 in the nucleus sustains the Arabidopsis circadian clock.
    Plant Cell. 2012 Feb;24(2):428-43 PMID: 22327739
  155. The continuing conundrum of the LEA proteins.
    Naturwissenschaften. 2007 Oct;94(10):791-812 PMID: 17479232
Article Info
Journal
Developmental cell
Abbr.
Dev Cell
ISSN
1878-1551
DOI
10.1016/j.devcel.2020.09.010
Email
alex.holehouse@wustl.edu
lucia.strader@duke.edu
Published
2020-00-12
Pages
69-83
Language
English
Region
United States
NLM ID
101120028
PMCID
PMC7577370
Subset
IM
Grants
NIGMS NIH HHS · R35 GM136338 · United States
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PubMed source DOI: 10.1016/j.devcel.2020.09.010 PMC Full Text View journal details
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