1932

Abstract

A surge in research focused on understanding the physical principles governing the formation, properties, and function of membraneless compartments has occurred over the past decade. Compartments such as the nucleolus, stress granules, and nuclear speckles have been designated as biomolecular condensates to describe their shared property of spatially concentrating biomolecules. Although this research has historically been carried out in animal and fungal systems, recent work has begun to explore whether these same principles are relevant in plants. Effectively understanding and studying biomolecular condensates require interdisciplinary expertise that spans cell biology, biochemistry, and condensed matter physics and biophysics. As such, some involved concepts may be unfamiliar to any given individual. This review focuses on introducing concepts essential to the study of biomolecular condensates and phase separation for biologists seeking to carry out research in this area and further examines aspects of biomolecular condensates that are relevant to plant systems.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081720-015238
2021-06-17
2024-05-06
Loading full text...

Full text loading...

/deliver/fulltext/arplant/72/1/annurev-arplant-081720-015238.html?itemId=/content/journals/10.1146/annurev-arplant-081720-015238&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Alberti S, Dormann D. 2019. Liquid-liquid phase separation in disease. Annu. Rev. Genet. 53:171–94
    [Google Scholar]
  2. 2. 
    Alberti S, Gladfelter A, Mittag T. 2019. Considerations and challenges in studying liquid-liquid phase separation and biomolecular condensates. Cell 176:419–34
    [Google Scholar]
  3. 3. 
    Alberti S, Saha S, Woodruff JB, Franzmann TM, Wang J, Hyman AA 2018. A user's guide for phase separation assays with purified proteins. J. Mol. Biol. 430:4806–20
    [Google Scholar]
  4. 4. 
    Banani SF, Lee HO, Hyman AA, Rosen MK. 2017. Biomolecular condensates: organizers of cellular biochemistry. Nat. Rev. Mol. Cell Biol 18:285–98Comprehensively reviews biomolecular condensates.
    [Google Scholar]
  5. 5. 
    Banani SF, Rice AM, Peeples WB, Lin Y, Jain S et al. 2016. Compositional control of phase-separated cellular bodies. Cell 166:651–63
    [Google Scholar]
  6. 6. 
    Banjade S, Rosen MK 2014. Phase transitions of multivalent proteins can promote clustering of membrane receptors. eLife 3:e04123
    [Google Scholar]
  7. 7. 
    Barnes AC, Elowsky CG, Roston RL. 2019. An Arabidopsis protoplast isolation method reduces cytosolic acidification and activation of the chloroplast stress sensor SENSITIVE TO FREEZING 2. Plant Signal. Behav. 14:1629270
    [Google Scholar]
  8. 8. 
    Bashandy H, Jalkanen S, Teeri TH. 2015. Within leaf variation is the largest source of variation in agroinfiltration of Nicotiana benthamiana. Plant Methods 11:47
    [Google Scholar]
  9. 9. 
    Berry J, Brangwynne CP, Haataja M. 2018. Physical principles of intracellular organization via active and passive phase transitions. Rep. Prog. Phys. 81:046601
    [Google Scholar]
  10. 10. 
    Bishof I, Dammer EB, Duong DM, Kundinger SR, Gearing M et al. 2018. RNA-binding proteins with basic-acidic dipeptide (BAD) domains self-assemble and aggregate in Alzheimer's disease. J. Biol. Chem. 293:11047–66
    [Google Scholar]
  11. 11. 
    Boeynaems S, Alberti S, Fawzi NL, Mittag T, Polymenidou M et al. 2018. Protein phase separation: a new phase in cell biology. Trends Cell Biol 28:420–35
    [Google Scholar]
  12. 12. 
    Boeynaems S, Holehouse AS, Weinhardt V, Kovacs D, Van Lindt J et al. 2019. Spontaneous driving forces give rise to protein-RNA condensates with coexisting phases and complex material properties. PNAS 116:7889–98
    [Google Scholar]
  13. 13. 
    Boisvert FM, van Koningsbruggen S, Navascues J, Lamond AI. 2007. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 8:574–85
    [Google Scholar]
  14. 14. 
    Boke E, Ruer M, Wuhr M, Coughlin M, Lemaitre R et al. 2016. Amyloid-like self-assembly of a cellular compartment. Cell 166:637–50
    [Google Scholar]
  15. 15. 
    Brady JP, Farber PJ, Sekhar A, Lin YH, Huang R et al. 2017. Structural and hydrodynamic properties of an intrinsically disordered region of a germ cell–specific protein on phase separation. PNAS 114:E8194–203
    [Google Scholar]
  16. 16. 
    Brangwynne CP, Eckmann CR, Courson DS, Rybarska A, Hoege C et al. 2009. Germline P granules are liquid droplets that localize by controlled dissolution/condensation. Science 324:1729–32The original paper to propose that liquid-liquid phase separation can drive cellular organization.
    [Google Scholar]
  17. 17. 
    Brangwynne CP, Tompa P, Pappu RV. 2015. Polymer physics of intracellular phase transitions. Nat. Phys 11:899–904Reviews the process of biological phase separation from the perspective of polymer physics.
    [Google Scholar]
  18. 18. 
    Burke KA, Janke AM, Rhine CL, Fawzi NL. 2015. Residue-by-residue view of in vitro FUS granules that bind the C-terminal domain of RNA polymerase II. Mol. Cell 60:231–41
    [Google Scholar]
  19. 19. 
    Cao X, Jin X, Liu B 2020. The involvement of stress granules in aging and aging-associated diseases. Aging Cell 19:e13136
    [Google Scholar]
  20. 20. 
    Cascarina SM, Elder MR, Ross ED. 2020. Atypical structural tendencies among low-complexity domains in the Protein Data Bank proteome. PLOS Comput. Biol. 16:e1007487
    [Google Scholar]
  21. 21. 
    Chen M, Galvao RM, Li M, Burger B, Bugea J et al. 2010. Arabidopsis HEMERA/pTAC12 initiates photomorphogenesis by phytochromes. Cell 141:1230–40
    [Google Scholar]
  22. 22. 
    Choi J-M, Dar F, Pappu RV. 2019. LASSI: a lattice model for simulating phase transitions of multivalent proteins. PLOS Comput. Biol. 15:e1007028
    [Google Scholar]
  23. 23. 
    Choi J-M, Holehouse AS, Pappu RV. 2020. Physical principles underlying the complex biology of intracellular phase transitions. Annu. Rev. Biophys 49:107–33Key review outlines the thermodynamic principles that underlie phase separation in multivalent biomolecules.
    [Google Scholar]
  24. 24. 
    Choi J-M, Hyman AA, Pappu RV. 2020. Generalized models for bond percolation transitions of associative polymers. Phys. Rev. E 102:042403
    [Google Scholar]
  25. 25. 
    Clemson CM, Hutchinson JN, Sara SA, Ensminger AW, Fox AH et al. 2009. An architectural role for a nuclear noncoding RNA: NEAT1 RNA is essential for the structure of paraspeckles. Mol. Cell 33:717–26
    [Google Scholar]
  26. 26. 
    Collier S, Pendle A, Boudonck K, van Rij T, Dolan L, Shaw P. 2006. A distant coilin homologue is required for the formation of Cajal bodies in Arabidopsis. Mol. Biol. Cell 17:2942–51
    [Google Scholar]
  27. 27. 
    Cutrale F, Rodriguez D, Hortiguela V, Chiu CL, Otterstrom J et al. 2019. Using enhanced number and brightness to measure protein oligomerization dynamics in live cells. Nat. Protoc. 14:616–38
    [Google Scholar]
  28. 28. 
    Dignon GL, Best RB, Mittal J. 2020. Biomolecular phase separation: from molecular driving forces to macroscopic properties. Annu. Rev. Phys. Chem. 71:53–75
    [Google Scholar]
  29. 29. 
    Duan Y, Du A, Gu J, Duan G, Wang C et al. 2019. PARylation regulates stress granule dynamics, phase separation, and neurotoxicity of disease-related RNA-binding proteins. Cell Res 29:233–47
    [Google Scholar]
  30. 30. 
    Dzuricky M, Rogers BA, Shahid A, Cremer PS, Chilkoti A. 2020. De novo engineering of intracellular condensates using artificial disordered proteins. Nat. Chem. 12:814–25
    [Google Scholar]
  31. 31. 
    Elbaum-Garfinkle S, Kim Y, Szczepaniak K, Chen CC, Eckmann CR et al. 2015. The disordered P granule protein LAF-1 drives phase separation into droplets with tunable viscosity and dynamics. PNAS 112:7189–94
    [Google Scholar]
  32. 32. 
    Emenecker RJ, Holehouse AS, Strader LC. 2020. Emerging roles for phase separation in plants. Dev. Cell 55:69–83
    [Google Scholar]
  33. 33. 
    Enderle B, Sheerin DJ, Paik I, Kathare PK, Schwenk P et al. 2017. PCH1 and PCHL promote photomorphogenesis in plants by controlling phytochrome B dark reversion. Nat. Commun. 8:2221
    [Google Scholar]
  34. 34. 
    Erdos G, Dosztanyi Z. 2020. Analyzing protein disorder with IUPred2A. Curr. Protoc. Bioinform. 70:e99
    [Google Scholar]
  35. 35. 
    Fang X, Wang L, Ishikawa R, Li Y, Fiedler M et al. 2019. Arabidopsis FLL2 promotes liquid-liquid phase separation of polyadenylation complexes. Nature 569:265–69Discusses the role of phase separation in the formation of subnuclear condensates involved in polyadenylation.
    [Google Scholar]
  36. 36. 
    Fang Y, Spector DL. 2007. Identification of nuclear dicing bodies containing proteins for microRNA biogenesis in living Arabidopsis plants. Curr. Biol. 17:818–23
    [Google Scholar]
  37. 37. 
    Faraco M, Di Sansebastiano GP, Spelt K, Koes RE, Quattrocchio FM. 2011. One protoplast is not the other!. Plant Physiol 156:474–78
    [Google Scholar]
  38. 38. 
    Feric M, Vaidya N, Harmon TS, Mitrea DM, Zhu L et al. 2016. Coexisting liquid phases underlie nucleolar subcompartments. Cell 165:1686–97
    [Google Scholar]
  39. 39. 
    Franzmann TM, Alberti S. 2019. Prion-like low-complexity sequences: key regulators of protein solubility and phase behavior. J. Biol. Chem. 294:7128–36
    [Google Scholar]
  40. 40. 
    Fujioka Y, Alam JM, Noshiro D, Mouri K, Ando T et al. 2020. Phase separation organizes the site of autophagosome formation. Nature 578:301–5
    [Google Scholar]
  41. 41. 
    Galganski L, Urbanek MO, Krzyzosiak WJ. 2017. Nuclear speckles: molecular organization, biological function and role in disease. Nucleic Acids Res 45:10350–68
    [Google Scholar]
  42. 42. 
    Ginell GM, Holehouse AS. 2020. Analyzing the sequences of intrinsically disordered regions with CIDER and localCIDER. Methods Mol. Biol. 2141:103–26
    [Google Scholar]
  43. 43. 
    Greig JA, Nguyen TA, Lee M, Holehouse AS, Posey AE et al. 2020. Arginine-enriched mixed-charge domains provide cohesion for nuclear speckle condensation. Mol. Cell 77:1237–50.e4
    [Google Scholar]
  44. 44. 
    Hahm J, Kim K, Qiu Y, Chen M. 2020. Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. Nat. Commun. 11:1660
    [Google Scholar]
  45. 45. 
    Hanazawa M, Yonetani M, Sugimoto A. 2011. PGL proteins self associate and bind RNPs to mediate germ granule assembly in C. elegans. J. Cell Biol. 192:929–37
    [Google Scholar]
  46. 46. 
    Harmon TS, Holehouse AS, Rosen MK, Pappu RV. 2017. Intrinsically disordered linkers determine the interplay between phase separation and gelation in multivalent proteins. eLife 6:e30294
    [Google Scholar]
  47. 47. 
    Hebert MD. 2013. Signals controlling Cajal body assembly and function. Int. J. Biochem. Cell Biol. 45:1314–17
    [Google Scholar]
  48. 48. 
    Hirakawa T, Matsunaga S. 2019. Characterization of DNA repair foci in root cells of Arabidopsis in response to DNA damage. Front. Plant Sci. 10:990
    [Google Scholar]
  49. 49. 
    Holehouse AS 2019. IDPs and IDRs in biomolecular condensates. Intrinsically Disordered Proteins N Salvi 209–55 Cambridge, MA: Elsevier
    [Google Scholar]
  50. 50. 
    Holehouse AS, Das RK, Ahad JN, Richardson MO, Pappu RV. 2017. CIDER: resources to analyze sequence-ensemble relationships of intrinsically disordered proteins. Biophys. J. 112:16–21
    [Google Scholar]
  51. 51. 
    Hondele M, Sachdev R, Heinrich S, Wang J, Vallotton P et al. 2019. DEAD-box ATPases are global regulators of phase-separated organelles. Nature 573:144–48
    [Google Scholar]
  52. 52. 
    Huang H, McLoughlin KE, Sorkin ML, Burgie ES, Bindbeutel RK et al. 2019. PCH1 regulates light, temperature, and circadian signaling as a structural component of phytochrome B-photobodies in Arabidopsis. PNAS 116:8603–8
    [Google Scholar]
  53. 53. 
    Hubstenberger A, Courel M, Benard M, Souquere S, Ernoult-Lange M et al. 2017. P-body purification reveals the condensation of repressed mRNA regulons. Mol. Cell 68:144–57.e5
    [Google Scholar]
  54. 54. 
    Hyman AA, Weber CA, Jülicher F. 2014. Liquid-liquid phase separation in biology. Annu. Rev. Cell Dev. Biol. 30:39–58Reviews various physical concepts that are foundational to understanding condensate formation.
    [Google Scholar]
  55. 55. 
    Ishida T, Kinoshita K. 2007. PrDOS: prediction of disordered protein regions from amino acid sequence. Nucleic Acids Res 35:W460–64
    [Google Scholar]
  56. 56. 
    Jacobs WM, Frenkel D. 2013. Predicting phase behavior in multicomponent mixtures. J. Chem. Phys. 139:024108
    [Google Scholar]
  57. 57. 
    Jung JH, Barbosa AD, Hutin S, Kumita JR, Gao M et al. 2020. A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 585:256–60Arpion-like domain–containing protein forms condensates in response to temperature fluctuation in plants.
    [Google Scholar]
  58. 58. 
    Kalinina NO, Makarova S, Makhotenko A, Love AJ, Taliansky M. 2018. The multiple functions of the nucleolus in plant development, disease and stress responses. Front. Plant Sci. 9:132
    [Google Scholar]
  59. 59. 
    Kao YT, Gonzalez KL, Bartel B 2018. Peroxisome function, biogenesis, and dynamics in plants. Plant Physiol 176:162–77
    [Google Scholar]
  60. 60. 
    Khong A, Matheny T, Jain S, Mitchell SF, Wheeler JR, Parker R. 2017. The stress granule transcriptome reveals principles of mRNA accumulation in stress granules. Mol. Cell 68:808–20.e5
    [Google Scholar]
  61. 61. 
    Kosmacz M, Gorka M, Schmidt S, Luzarowski M, Moreno JC et al. 2019. Protein and metabolite composition of Arabidopsis stress granules. New Phytol 222:1420–33
    [Google Scholar]
  62. 62. 
    Kulkarni M, Ozgur S, Stoecklin G. 2010. On track with P-bodies. Biochem. Soc. Trans. 38:242–51
    [Google Scholar]
  63. 63. 
    Lancaster AK, Nutter-Upham A, Lindquist S, King OD. 2014. PLAAC: a web and command-line application to identify proteins with prion-like amino acid composition. Bioinformatics 30:2501–2
    [Google Scholar]
  64. 64. 
    Langdon EM, Gladfelter AS. 2018. A new lens for RNA localization: liquid-liquid phase separation. Annu. Rev. Microbiol. 72:255–71
    [Google Scholar]
  65. 65. 
    Lee HJ, Jung JH, Cortes Llorca L, Kim SG, Lee S et al. 2014. FCA mediates thermal adaptation of stem growth by attenuating auxin action in Arabidopsis. Nat. Commun. 5:5473
    [Google Scholar]
  66. 66. 
    Leuzinger K, Dent M, Hurtado J, Stahnke J, Lai H et al. 2013. Efficient agroinfiltration of plants for high-level transient expression of recombinant proteins. J. Vis. Exp. 23:50521
    [Google Scholar]
  67. 67. 
    Li P, Banjade S, Cheng HC, Kim S, Chen B et al. 2012. Phase transitions in the assembly of multivalent signalling proteins. Nature 483:336–40
    [Google Scholar]
  68. 68. 
    Lin YH, Chan HS. 2017. Phase separation and single-chain compactness of charged disordered proteins are strongly correlated. Biophys. J. 112:2043–46
    [Google Scholar]
  69. 69. 
    Liu JL, Wu Z, Nizami Z, Deryusheva S, Rajendra TK et al. 2009. Coilin is essential for Cajal body organization in Drosophila melanogaster. Mol. Biol. Cell 20:1661–70
    [Google Scholar]
  70. 70. 
    Liu Q, Shi L, Fang Y. 2012. Dicing bodies. Plant Physiol 158:61–66
    [Google Scholar]
  71. 71. 
    Lopez-Molina L, Mongrand S, Kinoshita N, Chua NH. 2003. AFP is a novel negative regulator of ABA signaling that promotes ABI5 protein degradation. Genes Dev 17:410–18
    [Google Scholar]
  72. 72. 
    Luo Y, Na Z, Slavoff SA 2018. P-bodies: composition, properties, and functions. Biochemistry 57:2424–31
    [Google Scholar]
  73. 73. 
    Mackenzie IR, Nicholson AM, Sarkar M, Messing J, Purice MD et al. 2017. TIA1 mutations in amyotrophic lateral sclerosis and frontotemporal dementia promote phase separation and alter stress granule dynamics. Neuron 95:808–16.e9
    [Google Scholar]
  74. 74. 
    Mackenzie S, McIntosh L. 1999. Higher plant mitochondria. Plant Cell 11:571–86
    [Google Scholar]
  75. 75. 
    Maldonado-Bonilla LD. 2014. Composition and function of P bodies in Arabidopsis thaliana. Front. Plant Sci. 5:201
    [Google Scholar]
  76. 76. 
    Mao Y, Botella JR, Liu Y, Zhu J-K. 2019. Gene editing in plants: progress and challenges. Natl. Sci. Rev. 6:421–37
    [Google Scholar]
  77. 77. 
    Martin EW, Holehouse AS. 2020. Intrinsically disordered protein regions and phase separation: sequence determinants of assembly or lack thereof. Emerg. Top. Life Sci. 4:307–29
    [Google Scholar]
  78. 78. 
    Martin EW, Holehouse AS, Peran I, Farag M, Incicco JJ et al. 2020. Valence and patterning of aromatic residues determine the phase behavior of prion-like domains. Science 367:694–99
    [Google Scholar]
  79. 79. 
    Martin EW, Mittag T. 2018. Relationship of sequence and phase separation in protein low-complexity regions. Biochemistry 57:2478–87
    [Google Scholar]
  80. 80. 
    McSwiggen DT, Mir M, Darzacq X, Tjian R. 2019. Evaluating phase separation in live cells: diagnosis, caveats, and functional consequences. Genes Dev 33:1619–34
    [Google Scholar]
  81. 81. 
    Milkovic NM, Mittag T. 2020. Determination of protein phase diagrams by centrifugation. Methods Mol. Biol. 2141:685–702
    [Google Scholar]
  82. 82. 
    Mitrea DM, Chandra B, Ferrolino MC, Gibbs EB, Tolbert M et al. 2018. Methods for physical characterization of phase-separated bodies and membrane-less organelles. J. Mol. Biol. 430:4773–805
    [Google Scholar]
  83. 83. 
    Murthy AC, Dignon GL, Kan Y, Zerze GH, Parekh SH et al. 2019. Molecular interactions underlying liquid-liquid phase separation of the FUS low-complexity domain. Nat. Struct. Mol. Biol. 26:637–48
    [Google Scholar]
  84. 84. 
    Nakagawa C, Nishimura S, Senda-Murata K, Sugimoto K. 2012. A rapid and simple method of evaluating the dimeric tendency of fluorescent proteins in living cells using a truncated protein of importin alpha as fusion tag. Biosci. Biotechnol. Biochem. 76:388–90
    [Google Scholar]
  85. 85. 
    Norkunas K, Harding R, Dale J, Dugdale B. 2018. Improving agroinfiltration-based transient gene expression in Nicotiana benthamiana. Plant Methods 14:71
    [Google Scholar]
  86. 86. 
    Nott TJ, Petsalaki E, Farber P, Jervis D, Fussner E et al. 2015. Phase transition of a disordered nuage protein generates environmentally responsive membraneless organelles. Mol. Cell 57:936–47
    [Google Scholar]
  87. 87. 
    Oates ME, Romero P, Ishida T, Ghalwash M, Mizianty MJ et al. 2013. D2P2: database of disordered protein predictions. Nucleic Acids Res 41:D508–16
    [Google Scholar]
  88. 88. 
    Ohtani M. 2017. Plant snRNP biogenesis: a perspective from the nucleolus and Cajal bodies. Front. Plant Sci. 8:2184
    [Google Scholar]
  89. 89. 
    Oldfield CJ, Dunker AK. 2014. Intrinsically disordered proteins and intrinsically disordered protein regions. Annu. Rev. Biochem. 83:553–84
    [Google Scholar]
  90. 90. 
    Oshidari R, Huang R, Medghalchi M, Tse EYW, Ashgriz N et al. 2020. DNA repair by Rad52 liquid droplets. Nat. Commun. 11:695
    [Google Scholar]
  91. 91. 
    Ouyang M, Li X, Zhang J, Feng P, Pu H et al. 2020. Liquid-liquid phase transition drives intra-chloroplast cargo sorting. Cell 180:1144–59.e20Phase separation is involved in intrachloroplast cargo sorting.
    [Google Scholar]
  92. 92. 
    Owen I, Shewmaker F. 2019. The role of post-translational modifications in the phase transitions of intrinsically disordered proteins. Int. J. Mol. Sci. 20:5501
    [Google Scholar]
  93. 93. 
    Pak CW, Kosno M, Holehouse AS, Padrick SB, Mittal A et al. 2016. Sequence determinants of intracellular phase separation by complex coacervation of a disordered protein. Mol. Cell 63:72–85
    [Google Scholar]
  94. 94. 
    Patel A, Lee HO, Jawerth L, Maharana S, Jahnel M et al. 2015. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell 162:1066–77
    [Google Scholar]
  95. 95. 
    Pavlovic M, Plucinski A, Zhang J, Antonietti M, Zeininger L, Schmidt B. 2020. Cascade kinetics in an enzyme-loaded aqueous two-phase system. Langmuir 36:1401–8
    [Google Scholar]
  96. 96. 
    Pederson T. 2011. The nucleolus. Cold Spring Harb. Perspect. Biol. 3:a000638
    [Google Scholar]
  97. 97. 
    Peran I, Martin EW, Mittag T. 2020. Walking along a protein phase diagram to determine coexistence points by static light scattering. Methods Mol. Biol. 2141:715–30
    [Google Scholar]
  98. 98. 
    Pérez-González A, Elena C 2016. Hindrances to the efficient and stable expression of transgenes in plant synthetic biology approaches. Systems Biology Application in Synthetic Biology S Singh 79–89 New Delhi: Springer
    [Google Scholar]
  99. 99. 
    Peskett TR, Rau F, O'Driscoll J, Patani R, Lowe AR, Saibil HR. 2018. A liquid to solid phase transition underlying pathological huntingtin exon1 aggregation. Mol. Cell 70:588–601.e6
    [Google Scholar]
  100. 100. 
    Piovesan D, Tabaro F, Paladin L, Necci M, Micetic I et al. 2018. MobiDB 3.0: more annotations for intrinsic disorder, conformational diversity and interactions in proteins. Nucleic Acids Res 46:D471–76
    [Google Scholar]
  101. 101. 
    Posey AE, Holehouse AS, Pappu RV. 2018. Phase separation of intrinsically disordered proteins. Methods Enzymol 611:1–30
    [Google Scholar]
  102. 102. 
    Powers SK, Holehouse AS, Korasick DA, Schreiber KH, Clark NM et al. 2019. Nucleo-cytoplasmic partitioning of ARF proteins controls auxin responses in Arabidopsis thaliana. Mol. Cell 76:177–90.e5Biomolecular condensates regulate tissue responsiveness to the plant hormone auxin.
    [Google Scholar]
  103. 103. 
    Protter DSW, Parker R. 2016. Principles and properties of stress granules. Trends Cell Biol 26:668–79
    [Google Scholar]
  104. 104. 
    Pruss GJ, Nester EW, Vance V 2008. Infiltration with Agrobacterium tumefaciens induces host defense and development-dependent responses in the infiltrated zone. Mol. Plant Microbe Interact. 21:1528–38
    [Google Scholar]
  105. 105. 
    Qu W, Wang Z, Zhang H. 2020. Phase separation of the C. elegans Polycomb protein SOP-2 is modulated by RNA and sumoylation. Protein Cell 11:202–7
    [Google Scholar]
  106. 106. 
    Quiroz FG, Chilkoti A. 2015. Sequence heuristics to encode phase behaviour in intrinsically disordered protein polymers. Nat. Mater. 14:1164–71
    [Google Scholar]
  107. 107. 
    Reddy AS, Day IS, Gohring J, Barta A. 2012. Localization and dynamics of nuclear speckles in plants. Plant Physiol 158:67–77
    [Google Scholar]
  108. 108. 
    Riback JA, Katanski CD, Kear-Scott JL, Pilipenko EV, Rojek AE et al. 2017. Stress-triggered phase separation is an adaptive, evolutionarily tuned response. Cell 168:1028–40.e19
    [Google Scholar]
  109. 109. 
    Riback JA, Zhu L, Ferrolino MC, Tolbert M, Mitrea DM et al. 2020. Composition-dependent thermodynamics of intracellular phase separation. Nature 581:209–14
    [Google Scholar]
  110. 110. 
    Rico A, Bennett MH, Forcat S, Huang WE, Preston GM. 2010. Agroinfiltration reduces ABA levels and suppresses Pseudomonas syringae–elicited salicylic acid production in Nicotiana tabacum. PLOS ONE 5:e8977
    [Google Scholar]
  111. 111. 
    Ronald J, Davis SJ. 2019. Focusing on the nuclear and subnuclear dynamics of light and circadian signalling. Plant Cell Environ 42:2871–84
    [Google Scholar]
  112. 112. 
    Rothkamm K, Barnard S, Moquet J, Ellender M, Rana Z, Burdak-Rothkamm S. 2015. DNA damage foci: meaning and significance. Environ. Mol. Mutagen. 56:491–504
    [Google Scholar]
  113. 113. 
    Rubinstein M, Dobrynin AV. 1997. Solutions of associative polymers. Trends Polym. Sci. 5:181–86
    [Google Scholar]
  114. 114. 
    Ruff KM, Dar F, Pappu RV. 2020. Ligand effects on phase separation of multivalent macromolecules. bioRxiv 252346 https://doi.org/10.1101/2020.08.15.252346
    [Crossref] [Google Scholar]
  115. 115. 
    Ruff KM, Roberts S, Chilkoti A, Pappu RV. 2018. Advances in understanding stimulus-responsive phase behavior of intrinsically disordered protein polymers. J. Mol. Biol. 430:4619–35
    [Google Scholar]
  116. 116. 
    Saitoh N, Spahr CS, Patterson SD, Bubulya P, Neuwald AF, Spector DL. 2004. Proteomic analysis of interchromatin granule clusters. Mol. Biol. Cell 15:3876–90
    [Google Scholar]
  117. 117. 
    Santner AA, Croy CH, Vasanwala FH, Uversky VN, Van YY, Dunker AK 2012. Sweeping away protein aggregation with entropic bristles: Intrinsically disordered protein fusions enhance soluble expression. Biochemistry 51:7250–62
    [Google Scholar]
  118. 118. 
    Schmidt HB, Görlich D 2015. Nup98 FG domains from diverse species spontaneously phase-separate into particles with nuclear pore–like permselectivity. eLife 4:e04251
    [Google Scholar]
  119. 119. 
    Schuster BS, Dignon GL, Tang WS, Kelley FM, Ranganath AK et al. 2020. Identifying sequence perturbations to an intrinsically disordered protein that determine its phase-separation behavior. PNAS 117:11421–31
    [Google Scholar]
  120. 120. 
    Semenov AN, Rubinstein M 1998. Thermoreversible gelation in solutions of associative polymers. 1. Statics. Macromolecules 31:1373–85
    [Google Scholar]
  121. 121. 
    Shimada T, Takagi J, Ichino T, Shirakawa M, Hara-Nishimura I. 2018. Plant vacuoles. Annu. Rev. Plant Biol. 69:123–45
    [Google Scholar]
  122. 122. 
    Snapp EL. 2009. Fluorescent proteins: a cell biologist's user guide. Trends Cell Biol 19:649–55
    [Google Scholar]
  123. 123. 
    Spector DL, Lamond AI. 2011. Nuclear speckles. Cold Spring Harb. Perspect. Biol. 3:a000646
    [Google Scholar]
  124. 124. 
    Su X, Ditlev JA, Hui E, Xing W, Banjade S et al. 2016. Phase separation of signaling molecules promotes T cell receptor signal transduction. Science 352:595–99
    [Google Scholar]
  125. 125. 
    Tada Y, Spoel SH, Pajerowska-Mukhtar K, Mou Z, Song J et al. 2008. Plant immunity requires conformational changes of NPR1 via S-nitrosylation and thioredoxins. Science 321:952–56
    [Google Scholar]
  126. 126. 
    Taylor NO, Wei MT, Stone HA, Brangwynne CP. 2019. Quantifying dynamics in phase-separated condensates using fluorescence recovery after photobleaching. Biophys. J. 117:1285–300
    [Google Scholar]
  127. 127. 
    UniProt Consort 2019. UniProt: a worldwide hub of protein knowledge. Nucleic Acids Res 47:D506–15
    [Google Scholar]
  128. 128. 
    Uversky VN 2019. Intrinsically disordered proteins and their “mysterious” (meta)physics. Front. Phys. 7:10 https://doi.org/10.3389/fphy.2019.00010
    [Crossref] [Google Scholar]
  129. 129. 
    Van Buskirk EK, Decker PV, Chen M. 2012. Photobodies in light signaling. Plant Physiol 158:52–60
    [Google Scholar]
  130. 130. 
    Vernon RM, Chong PA, Tsang B, Kim TH, Bah A et al. 2018. Pi-pi contacts are an overlooked protein feature relevant to phase separation. eLife 7:e31486
    [Google Scholar]
  131. 131. 
    Vernon RM, Forman-Kay JD. 2019. First-generation predictors of biological protein phase separation. Curr. Opin. Struct. Biol. 58:88–96
    [Google Scholar]
  132. 132. 
    Voronina E, Seydoux G, Sassone-Corsi P, Nagamori I. 2011. RNA granules in germ cells. Cold Spring Harb. Perspect. Biol. 3:a002774
    [Google Scholar]
  133. 133. 
    Walsh I, Martin AJ, Di Domenico T, Tosatto SC. 2012. ESpritz: accurate and fast prediction of protein disorder. Bioinformatics 28:503–9
    [Google Scholar]
  134. 134. 
    Wang J, Choi J-M, Holehouse AS, Lee HO, Zhang X et al. 2018. A molecular grammar governing the driving forces for phase separation of prion-like RNA binding proteins. Cell 174:688–99.e16
    [Google Scholar]
  135. 135. 
    Wang Z, Zhang G, Zhang H. 2018. Protocol for analyzing protein liquid–liquid phase separation. Biophys. Rep. 5:1–9
    [Google Scholar]
  136. 136. 
    Weber SC. 2017. Sequence-encoded material properties dictate the structure and function of nuclear bodies. Curr. Opin. Cell Biol. 46:62–71
    [Google Scholar]
  137. 137. 
    Wei M-T, Elbaum-Garfinkle S, Holehouse AS, Chen CC-H, Feric M et al. 2017. Phase behaviour of disordered proteins underlying low density and high permeability of liquid organelles. Nat. Chem 9:1118–25
    [Google Scholar]
  138. 138. 
    Weihs D, Mason TG, Teitell MA. 2006. Bio-microrheology: a frontier in microrheology. Biophys. J. 91:4296–305
    [Google Scholar]
  139. 139. 
    Woodruff JB, Ferreira Gomes B, Widlund PO, Mahamid J, Honigmann A, Hyman AA 2017. The centrosome is a selective condensate that nucleates microtubules by concentrating tubulin. Cell 169:1066–77.e10
    [Google Scholar]
  140. 140. 
    Woodruff JB, Hyman AA, Boke E. 2018. Organization and function of non-dynamic biomolecular condensates. Trends Biochem. Sci. 43:81–94
    [Google Scholar]
  141. 141. 
    Xue S, Gong R, He F, Li Y, Wang Y et al. 2019. Low-complexity domain of U1-70K modulates phase separation and aggregation through distinctive basic-acidic motifs. Sci. Adv. 5:eaax5349
    [Google Scholar]
  142. 142. 
    Yang Z, Tian L, Latoszek-Green M, Brown D, Wu K. 2005. Arabidopsis ERF4 is a transcriptional repressor capable of modulating ethylene and abscisic acid responses. Plant Mol. Biol. 58:585–96
    [Google Scholar]
  143. 143. 
    Yoo H, Triandafillou C, Drummond DA. 2019. Cellular sensing by phase separation: using the process, not just the products. J. Biol. Chem. 294:7151–59
    [Google Scholar]
  144. 144. 
    Yoo SD, Cho YH, Sheen J. 2007. Arabidopsis mesophyll protoplasts: a versatile cell system for transient gene expression analysis. Nat. Protoc. 2:1565–72
    [Google Scholar]
  145. 145. 
    Youn JY, Dunham WH, Hong SJ, Knight JDR, Bashkurov M et al. 2018. High-density proximity mapping reveals the subcellular organization of mRNA-associated granules and bodies. Mol. Cell 69:517–32.e11
    [Google Scholar]
  146. 146. 
    Zavaliev R, Mohan R, Chen T, Dong X 2020. Formation of NPR1 condensates promotes cell survival during the plant immune response. Cell 182:1093–108.e18The formation of biomolecular condensates induced by salicylic acid is involved in the regulation of effector-triggered immunity.
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-081720-015238
Loading
/content/journals/10.1146/annurev-arplant-081720-015238
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error