1932

Abstract

Anionic phospholipids, which include phosphatidic acid, phosphatidylserine, and phosphoinositides, represent a small percentage of membrane lipids. They are able to modulate the physical properties of membranes, such as their surface charges, curvature, or clustering of proteins. Moreover, by mediating interactions with numerous membrane-associated proteins, they are key components in the establishment of organelle identity and dynamics. Finally, anionic lipids also act as signaling molecules, as they are rapidly produced or interconverted by a set of dedicated enzymes. As such, anionic lipids are major regulators of many fundamental cellular processes, including cell signaling, cell division, membrane trafficking, cell growth, and gene expression. In this review, we describe the functions of anionic lipids from a cellular perspective. Using the localization of each anionic lipid and its related metabolic enzymes as starting points, we summarize their roles within the different compartments of the endomembrane system and address their associated developmental and physiological consequences.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-081519-035910
2020-04-29
2024-11-06
Loading full text...

Full text loading...

/deliver/fulltext/arplant/71/1/annurev-arplant-081519-035910.html?itemId=/content/journals/10.1146/annurev-arplant-081519-035910&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Ambrose C, Ruan Y, Gardiner J, Tamblyn LM, Catching A et al. 2013. CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana.. Dev. Cell 24:6649–59
    [Google Scholar]
  2. 2. 
    Antignani V, Klocko AL, Bak G, Chandrasekaran SD, Dunivin T, Nielsen E 2015. Recruitment of PLANT U-BOX13 and the PI4Kβ1/β2 phosphatidylinositol-4 kinases by the small GTPase RabA4B plays important roles during salicylic acid-mediated plant defense signaling in Arabidopsis. Plant Cell 27:1243–61
    [Google Scholar]
  3. 3. 
    Antonny B, Bigay J, Mesmin B 2018. The oxysterol-binding protein cycle: burning off PI(4)P to transport cholesterol. Annu. Rev. Biochem. 87:1809–37
    [Google Scholar]
  4. 4. 
    Azouaoui H, Montigny C, Dieudonné T, Champeil P, Jacquot A et al. 2017. High phosphatidylinositol 4-phosphate (PI4P)-dependent ATPase activity for the Drs2p-Cdc50p flippase after removal of its N- and C-terminal extensions. J. Biol. Chem. 292:197954–70
    [Google Scholar]
  5. 5. 
    Barbosa ICR, Shikata H, Zourelidou M, Heilmann M, Heilmann I, Schwechheimer C 2016. Phospholipid composition and a polybasic motif determine D6 PROTEIN KINASE polar association with the plasma membrane and tropic responses. Development 143:4687–700
    [Google Scholar]
  6. 6. 
    Bayer EM, Sparkes I, Vanneste S, Rosado A 2017. From shaping organelles to signalling platforms: the emerging functions of plant ER-PM contact sites. Curr. Opin. Plant Biol. 40:89–96
    [Google Scholar]
  7. 7. 
    Bigay J, Antonny B. 2012. Curvature, lipid packing, and electrostatics of membrane organelles: defining cellular territories in determining specificity. Dev. Cell 23:5886–95
    [Google Scholar]
  8. 8. 
    Bloch D, Pleskot R, Pejchar P, Potocký M, Trpkošová P et al. 2016. Exocyst SEC3 and phosphoinositides define sites of exocytosis in pollen tube initiation and growth. Plant Physiol 172:2980–1002
    [Google Scholar]
  9. 9. 
    Botella C, Sautron E, Boudiere L, Michaud M, Dubots E et al. 2016. ALA10, a phospholipid flippase, controls FAD2/FAD3 desaturation of phosphatidylcholine in the ER and affects chloroplast lipid composition in Arabidopsis thaliana. Plant Physiol 170:31300–14
    [Google Scholar]
  10. 10. 
    Boutté Y, Moreau P. 2014. Modulation of endomembranes morphodynamics in the secretory/retrograde pathways depends on lipid diversity. Curr. Opin. Plant Biol. 22:22–29
    [Google Scholar]
  11. 11. 
    Brault ML, Petit JD, Immel F, Nicolas WJ, Glavier M et al. 2019. Multiple C2 domains and transmembrane region proteins (MCTPs) tether membranes at plasmodesmata. EMBO Rep 20:e47182Proposes MCTP proteins, a class of putative PS/PI4P binding proteins, as tethering factors at PD-EPCSs.
    [Google Scholar]
  12. 12. 
    Brillada C, Zheng J, Krüger F, Rovira-Diaz E, Askani JC et al. 2018. Phosphoinositides control the localization of HOPS subunit VPS41, which together with VPS33 mediates vacuole fusion in plants. PNAS 15:35E8305–14
    [Google Scholar]
  13. 13. 
    Caillaud M-C. 2019. Anionic lipids: a pipeline connecting key players of plant cell division. Front. Plant Sci. 10:419
    [Google Scholar]
  14. 14. 
    Cole RA, Synek L, Zarsky V, Fowler JE 2005. SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol 138:42005–18
    [Google Scholar]
  15. 15. 
    Colin LA, Jaillais Y. 2020. Phospholipids across scales: lipid patterns and plant development. Curr. Opin. Plant Biol. 53:1–9
    [Google Scholar]
  16. 16. 
    de Campos MKF, Schaaf G 2017. The regulation of cell polarity by lipid transfer proteins of the SEC14 family. Curr. Opin. Plant Biol. 40:158–68
    [Google Scholar]
  17. 17. 
    Diao J, Liu R, Rong Y, Zhao M, Zhang J et al. 2015. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature 520:7548563–66
    [Google Scholar]
  18. 18. 
    Doumane M, Lionnet C, Bayle V, Jaillais Y, Caillaud M-C 2017. Automated tracking of root for confocal time-lapse imaging of cellular processes. Bio-Protoc 7:8e2245
    [Google Scholar]
  19. 19. 
    Dowd PE, Coursol S, Skirpan AL, Kao T, Gilroy S 2006. Petunia phospholipase C1 is involved in pollen tube growth. Plant Cell 18:61438–53
    [Google Scholar]
  20. 20. 
    Drdová EJ, Synek L, Pečenková T, Hála M, Kulich I et al. 2013. The exocyst complex contributes to PIN auxin efflux carrier recycling and polar auxin transport in Arabidopsis. Plant J 73:5709–19
    [Google Scholar]
  21. 21. 
    Dubeaux G, Vert G. 2017. Zooming into plant ubiquitin-mediated endocytosis. Curr. Opin. Plant Biol. 40:56–62
    [Google Scholar]
  22. 22. 
    Enrique Gomez R, Joubès J, Valentin N, Batoko H, Satiat-Jeunemaître B, Bernard A 2018. Lipids in membrane dynamics during autophagy in plants. J. Exp. Bot. 69:61287–99
    [Google Scholar]
  23. 23. 
    Galvan-Ampudia CS, Julkowska MM, Darwish E, Gandullo J, Korver RA et al. 2013. Halotropism is a response of plant roots to avoid a saline environment. Curr. Biol. 23:202044–50
    [Google Scholar]
  24. 24. 
    Gao C, Luo M, Zhao Q, Yang R, Cui Y et al. 2014. A unique plant ESCRT component, FREE1, regulates multivesicular body protein sorting and plant growth. Curr. Biol. 24:212556–63
    [Google Scholar]
  25. 25. 
    Gao C, Zhuang X, Cui Y, Fu X, He Y et al. 2015. Dual roles of an Arabidopsis ESCRT component FREE1 in regulating vacuolar protein transport and autophagic degradation. PNAS 112:61886–91
    [Google Scholar]
  26. 26. 
    Gerth K, Lin F, Menzel W, Krishnamoorthy P, Stenzel I et al. 2017. Guilt by association: a phenotype-based view of the plant phosphoinositide network. Annu. Rev. Plant Biol. 68:1349–74
    [Google Scholar]
  27. 27. 
    Ghosh R, de Campos MKF, Huang J, Huh SK, Orlowski A et al. 2015. Sec14-nodulin proteins and the patterning of phosphoinositide landmarks for developmental control of membrane morphogenesis. Mol. Biol. Cell 26:91764–81Proposes a model for Sec14-nodulin function as phosphatidylinositol kinase helper proteins mediating PI(4,5)P2 polar localization.
    [Google Scholar]
  28. 28. 
    Giordano F, Saheki Y, Idevall-Hagren O, Colombo SF, Pirruccello M et al. 2013. PI(4,5)P(2)-dependent and Ca2+-regulated ER-PM interactions mediated by the extended synaptotagmins. Cell 153:71494–509
    [Google Scholar]
  29. 29. 
    Gomès E, Jakobsen MK, Axelsen KB, Geisler M, Palmgren MG 2000. Chilling tolerance in Arabidopsis involves ALA1, a member of a new family of putative aminophospholipid translocases. Plant Cell 12:122441–53
    [Google Scholar]
  30. 30. 
    Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V et al. 2015. Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:41228–50
    [Google Scholar]
  31. 31. 
    Gronnier J, Crowet J-M, Habenstein B, Nasir MN, Bayle V et al. 2017. Structural basis for plant plasma membrane protein dynamics and organization into functional nanodomains. eLife 6:e26404Describes how anionic lipids and sterol influence REMORIN conformation, localization, and activity by forming nanoclusters.
    [Google Scholar]
  32. 32. 
    Gujas B, Cruz TMD, Kastanaki E, Vermeer JEM, Munnik T, Rodriguez-Villalon A 2017. Perturbing phosphoinositide homeostasis oppositely affects vascular differentiation in Arabidopsis thaliana roots. Development 144:193578–89
    [Google Scholar]
  33. 33. 
    Harrison MJ, Ivanov S. 2017. Exocytosis for endosymbiosis: membrane trafficking pathways for development of symbiotic membrane compartments. Curr. Opin. Plant Biol. 38:101–8
    [Google Scholar]
  34. 34. 
    Helling D, Possart A, Cottier S, Klahre U, Kost B 2006. Pollen tube tip growth depends on plasma membrane polarization mediated by tobacco PLC3 activity and endocytic membrane recycling. Plant Cell 18:123519–34
    [Google Scholar]
  35. 35. 
    Hempel F, Stenzel I, Heilmann M, Krishnamoorthy P, Menzel W et al. 2017. MAPKs influence pollen tube growth by controlling the formation of phosphatidylinositol 4,5-bisphosphate in an apical plasma membrane domain. Plant Cell 29:123030–50
    [Google Scholar]
  36. 36. 
    Hirano T, Konno H, Takeda S, Dolan L, Kato M et al. 2018. PtdIns(3,5)P2 mediates root hair shank hardening in Arabidopsis. Nat. Plants 4:11888–97
    [Google Scholar]
  37. 37. 
    Hirano T, Matsuzawa T, Takegawa K, Sato MH 2011. Loss-of-function and gain-of-function mutations in FAB1A/B impair endomembrane homeostasis, conferring pleiotropic developmental abnormalities in Arabidopsis. Plant Physiol 155:2797–807
    [Google Scholar]
  38. 38. 
    Hirano T, Munnik T, Sato MH 2015. Phosphatidylinositol 3-phosphate 5-kinase, FAB1/PIKfyve mediates endosome maturation to establish endosome-cortical microtubule interaction in Arabidopsis. Plant Physiol 169:31961–74
    [Google Scholar]
  39. 39. 
    Hirano T, Munnik T, Sato MH 2016. Inhibition of phosphatidylinositol 3,5-bisphosphate production has pleiotropic effects on various membrane trafficking routes in Arabidopsis. Plant Cell Physiol 58:1120–29
    [Google Scholar]
  40. 40. 
    Hirano T, Stecker K, Munnik T, Xu H, Sato MH 2017. Visualization of phosphatidylinositol 3,5-bisphosphate dynamics by tandem ML1N-based fluorescent protein probe in Arabidopsis. Plant Cell Physiol 58:71185–95
    [Google Scholar]
  41. 41. 
    Hiruma K, Onozawa-Komori M, Takahashi F, Asakura M, Bednarek P et al. 2010. Entry mode–dependent function of an indole glucosinolate pathway in Arabidopsis for nonhost resistance against anthracnose pathogens. Plant Cell 22:72429–43
    [Google Scholar]
  42. 42. 
    Huang J, Ghosh R, Tripathi A, Lönnfors M, Somerharju P, Bankaitis VA 2016. Two-ligand priming mechanism for potentiated phosphoinositide synthesis is an evolutionarily conserved feature of Sec14-like phosphatidylinositol and phosphatidylcholine exchange proteins. Mol. Biol. Cell 27:142317–30
    [Google Scholar]
  43. 43. 
    Ischebeck T, Stenzel I, Heilmann I 2008. Type B phosphatidylinositol-4-phosphate 5-kinases mediate Arabidopsis and Nicotiana tabacum pollen tube growth by regulating apical pectin secretion. Plant Cell 20:123312–30
    [Google Scholar]
  44. 44. 
    Ischebeck T, Stenzel I, Hempel F, Jin X, Mosblech A, Heilmann I 2011. Phosphatidylinositol-4,5-bisphosphate influences Nt-Rac5-mediated cell expansion in pollen tubes of Nicotiana tabacum. Plant J 65:3453–68
    [Google Scholar]
  45. 45. 
    Ischebeck T, Werner S, Krishnamoorthy P, Lerche J, Meijón M et al. 2013. Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis. Plant Cell 25:124894–911
    [Google Scholar]
  46. 46. 
    Ivanov S, Harrison MJ. 2019. Accumulation of phosphoinositides in distinct regions of the periarbuscular membrane. New Phytol 221:42213–27
    [Google Scholar]
  47. 47. 
    Jaillais Y, Ott T. 2019. The nanoscale organization of the plasma membrane and its importance in signaling—a proteolipid perspective. Plant Physiol 2019.pp.01349.2019
    [Google Scholar]
  48. 48. 
    Jaillais Y, Santambrogio M, Rozier F, Fobis-Loisy I, Miège C, Gaude T 2007. The retromer protein VPS29 links cell polarity and organ initiation in plants. Cell 130:61057–70
    [Google Scholar]
  49. 49. 
    Jarsch IK, Konrad SSA, Stratil TF, Urbanus SL, Szymanski W et al. 2014. Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:41698–711
    [Google Scholar]
  50. 50. 
    Jarsch IK, Ott T. 2011. Perspectives on remorin proteins, membrane rafts, and their role during plant-microbe interactions. Mol. Plant-Microbe Interact. 24:17–12
    [Google Scholar]
  51. 51. 
    Kalmbach L, Hématy K, De Bellis D, Barberon M, Fujita S et al. 2017. Transient cell-specific EXO70A1 activity in the CASP domain and Casparian strip localization. Nat. Plants. 3:17058
    [Google Scholar]
  52. 52. 
    Kang B-H, Nielsen E, Preuss ML, Mastronarde D, Staehelin LA 2011. Electron tomography of RabA4b- and PI-4Kβ1-labeled trans Golgi network compartments in Arabidopsis. Traffic 12:3313–29Uses electron tomography to reveal distinct TGN subdomains, with PI4Kβ1 highlighting the secretory vesicle subdomain.
    [Google Scholar]
  53. 53. 
    Katsiarimpa A, Kalinowska K, Anzenberger F, Weis C, Ostertag M et al. 2013. The deubiquitinating enzyme AMSH1 and the ESCRT-III subunit VPS2.1 are required for autophagic degradation in Arabidopsis. Plant Cell 25:62236–52
    [Google Scholar]
  54. 54. 
    Kelly BT, Graham SC, Liska N, Dannhauser PN, Höning S et al. 2014. AP2 controls clathrin polymerization with a membrane-activated switch. Science 345:6195459–63
    [Google Scholar]
  55. 55. 
    Kim H, Kwon H, Kim S, Kim MK, Botella MA et al. 2016. Synaptotagmin 1 negatively controls the two distinct immune secretory pathways to powdery mildew fungi in Arabidopsis. Plant Cell Physiol 57:61133–41
    [Google Scholar]
  56. 56. 
    Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L et al. 2008. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. PNAS 105:4617812–17
    [Google Scholar]
  57. 57. 
    Kolb C, Nagel M-K, Kalinowska K, Hagmann J, Ichikawa M et al. 2015. FYVE1 is essential for vacuole biogenesis and intracellular trafficking in Arabidopsis. Plant Physiol 167:41361–73
    [Google Scholar]
  58. 58. 
    König S, Ischebeck T, Lerche J, Stenzel I, Heilmann I 2008. Salt-stress-induced association of phosphatidylinositol 4,5-bisphosphate with clathrin-coated vesicles in plants. Biochem. J. 415:3387–99
    [Google Scholar]
  59. 59. 
    Kubátová Z, Pejchar P, Potocký M, Sekereš J, Žárský V, Kulich I 2019. Arabidopsis trichome contains two plasma membrane domains with different lipid composition which attract distinct EXO70 subunits. Int. J. Mol. Sci. 20:153803
    [Google Scholar]
  60. 60. 
    Kulich I, Vojtíková Z, Glanc M, Ortmannová J, Rasmann S, Žárský V 2015. Cell wall maturation of Arabidopsis trichomes is dependent on exocyst subunit EXO70H4 and involves callose deposition. Plant Physiol 168:1120–31
    [Google Scholar]
  61. 61. 
    Kulich I, Vojtíková Z, Sabol P, Ortmannová J, Neděla V et al. 2018. Exocyst subunit EXO70H4 has a specific role in callose synthase secretion and silica accumulation. Plant Physiol 176:32040–51
    [Google Scholar]
  62. 62. 
    Kusano H, Testerink C, Vermeer JEM, Tsuge T, Shimada H et al. 2008. The Arabidopsis phosphatidylinositol phosphate 5-kinase PIP5K3 is a key regulator of root hair tip growth. Plant Cell 20:2367–80
    [Google Scholar]
  63. 63. 
    Lee BH, Weber ZT, Zourelidou M, Hofmeister BT, Schmitz RJ et al. 2018. Arabidopsis protein kinase D6PKL3 is involved in the formation of distinct plasma membrane aperture domains on the pollen surface. Plant Cell 30:92038–56
    [Google Scholar]
  64. 64. 
    Lee E, Vanneste S, Pérez-Sancho J, Benitez-Fuente F, Strelau M et al. 2019. Ionic stress enhances ER-PM connectivity via phosphoinositide-associated SYT1 contact site expansion in Arabidopsis. PNAS 116:41420–29Proposes that S-EPCS dynamics is regulated by PI(4,5)P2-SYT interactions and is remodeled during osmotic stresses.
    [Google Scholar]
  65. 65. 
    Lemmon MA. 2008. Membrane recognition by phospholipid-binding domains. Nat. Rev. Mol. Cell Biol. 9:299–111
    [Google Scholar]
  66. 66. 
    Levy A, Zheng JY, Lazarowitz SG 2015. Synaptotagmin SYTA forms ER-plasma membrane junctions that are recruited to plasmodesmata for plant virus movement. Curr. Biol. 25:152018–25
    [Google Scholar]
  67. 67. 
    Lewis JD, Lazarowitz SG. 2010. Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. PNAS 107:62491–96
    [Google Scholar]
  68. 68. 
    Li G, Xue H-W. 2007. Arabidopsis PLDζ2 regulates vesicle trafficking and is required for auxin response. Plant Cell 19:1281–95
    [Google Scholar]
  69. 69. 
    Li W, Song T, Wallrad L, Kudla J, Wang X, Zhang W 2019. Tissue-specific accumulation of pH-sensing phosphatidic acid determines plant stress tolerance. Nat. Plants 5:91012–21
    [Google Scholar]
  70. 70. 
    Li Y, Tan X, Wang M, Li B, Zhao Y et al. 2017. Exocyst subunit SEC3A marks the germination site and is essential for pollen germination in Arabidopsis thaliana. Sci. Rep 7:40279
    [Google Scholar]
  71. 71. 
    Lin F, Krishnamoorthy P, Schubert V, Hause G, Heilmann M, Heilmann I 2019. A dual role for cell plate-associated PI4Kβ in endocytosis and phragmoplast dynamics during plant somatic cytokinesis. EMBO J 38:4e100303Establishes that PI4P production at the cell plate contributes to cytokinesis and phragmoplast dynamics.
    [Google Scholar]
  72. 72. 
    Löfke C, Dünser K, Scheuring D, Kleine-Vehn J 2015. Auxin regulates SNARE-dependent vacuolar morphology restricting cell size. eLife 4:e05868
    [Google Scholar]
  73. 73. 
    López-Marqués RL, Poulsen LR, Hanisch S, Meffert K, Buch-Pedersen MJ et al. 2010. Intracellular targeting signals and lipid specificity determinants of the ALA/ALIS P4-ATPase complex reside in the catalytic ALA α-subunit. Mol. Biol. Cell 21:5791–801
    [Google Scholar]
  74. 74. 
    López-Marqués RL, Poulsen LR, Palmgren MG 2012. A putative plant aminophospholipid flippase, the Arabidopsis P4 ATPase ALA1, localizes to the plasma membrane following association with a β-subunit. PLOS ONE 7:4e33042
    [Google Scholar]
  75. 75. 
    Lynch DV, Steponkus PL. 1987. Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 83:4761–67
    [Google Scholar]
  76. 76. 
    Marhava P, Aliaga Fandino AC, Koh SWH, Jelínková A, Kolb M et al. 2020. Plasma membrane domain patterning and self-reinforcing polarity in Arabidopsis. Dev. Cell 52:2223–35.e5
    [Google Scholar]
  77. 77. 
    Martinière A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L et al. 2012. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. PNAS 109:3112805–10
    [Google Scholar]
  78. 78. 
    McDowell SC, López-Marqués RL, Cohen T, Brown E, Rosenberg A et al. 2015. Loss of the Arabidopsis thaliana P4-ATPases ALA6 and ALA7 impairs pollen fitness and alters the pollen tube plasma membrane. Front. Plant Sci. 6:197
    [Google Scholar]
  79. 79. 
    McKenna JF, Rolfe DJ, Webb SED, Tolmie AF, Botchway SW et al. 2019. The cell wall regulates dynamics and size of plasma-membrane nanodomains in Arabidopsis. PNAS 116:2612857–62
    [Google Scholar]
  80. 80. 
    McLaughlin S. 1989. The electrostatic properties of membranes. Annu. Rev. Biophys. Biophys. Chem. 18:1113–36
    [Google Scholar]
  81. 81. 
    McLoughlin F, Arisz SA, Dekker HL, Kramer G, de Koster CG et al. 2013. Identification of novel candidate phosphatidic acid-binding proteins involved in the salt-stress response of Arabidopsis thaliana roots. Biochem. J. 450:3573–81
    [Google Scholar]
  82. 82. 
    McMahon HT, Gallop JL. 2005. Membrane curvature and mechanisms of dynamic cell membrane remodelling. Nature 438:7068590–96
    [Google Scholar]
  83. 83. 
    Mei Y, Jia W-J, Chu Y-J, Xue H-W 2012. Arabidopsis phosphatidylinositol monophosphate 5-kinase 2 is involved in root gravitropism through regulation of polar auxin transport by affecting the cycling of PIN proteins. Cell Res 22:3581–97
    [Google Scholar]
  84. 84. 
    Menzel W, Stenzel I, Helbig L-M, Krishnamoorthy P, Neumann S et al. 2019. A PAMP-triggered MAPK-cascade inhibits phosphatidylinositol 4,5-bisphosphate production by PIP5K6 in Arabidopsis thaliana. New Phytol 224:833–47
    [Google Scholar]
  85. 85. 
    Mettlen M, Chen P-H, Srinivasan S, Danuser G, Schmid SL 2018. Regulation of clathrin-mediated endocytosis. Annu. Rev. Biochem. 87:1871–96
    [Google Scholar]
  86. 86. 
    Mishkind M, Vermeer JEM, Darwish E, Munnik T 2009. Heat stress activates phospholipase D and triggers PIP accumulation at the plasma membrane and nucleus. Plant J. Cell Mol. Biol. 60:110–21
    [Google Scholar]
  87. 87. 
    Munnik T, Meijer HJ, Ter Riet B, Hirt H, Frank W et al. 2000. Hyperosmotic stress stimulates phospholipase D activity and elevates the levels of phosphatidic acid and diacylglycerol pyrophosphate. Plant J. Cell Mol. Biol. 22:2147–54
    [Google Scholar]
  88. 88. 
    Munnik T, Nielsen E. 2011. Green light for polyphosphoinositide signals in plants. Curr. Opin. Plant Biol. 14:5489–97
    [Google Scholar]
  89. 89. 
    Nintemann SJ, Palmgren M, López-Marqués RL 2019. Catch you on the flip side: a critical review of flippase mutant phenotypes. Trends Plant Sci 24:5468–78
    [Google Scholar]
  90. 90. 
    Noack LC, Jaillais Y. 2017. Precision targeting by phosphoinositides: how PIs direct endomembrane trafficking in plants. Curr. Opin. Plant Biol. 40:22–33
    [Google Scholar]
  91. 91. 
    Nováková P, Hirsch S, Feraru E, Tejos R, van Wijk R et al. 2014. SAC phosphoinositide phosphatases at the tonoplast mediate vacuolar function in Arabidopsis. PNAS 111:72818–23
    [Google Scholar]
  92. 92. 
    Novick P, Field C, Schekman R 1980. Identification of 23 complementation groups required for post-translational events in the yeast secretory pathway. Cell 21:1205–15
    [Google Scholar]
  93. 93. 
    Ogura T, Goeschl C, Filiault D, Mirea M, Slovak R et al. 2019. Root system depth in Arabidopsis is shaped by EXOCYST70A3 via the dynamic modulation of auxin transport. Cell 178:2400–412.e16
    [Google Scholar]
  94. 94. 
    Ott T. 2017. Membrane nanodomains and microdomains in plant-microbe interactions. Curr. Opin. Plant Biol. 40:82–88
    [Google Scholar]
  95. 95. 
    Pérez-Sancho J, Vanneste S, Lee E, McFarlane HE, del Valle AE et al. 2015. The Arabidopsis Synaptotagmin1 is enriched in endoplasmic reticulum-plasma membrane contact sites and confers cellular resistance to mechanical stresses. Plant Physiol 168:1132–43
    [Google Scholar]
  96. 96. 
    Platre MP, Bayle V, Armengot L, Bareille J, del Mar Marquès-Bueno M et al. 2019. Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine. Science 364:643557–62Visualizes and functionally characterizes nanoclusters of anionic lipids (i.e., PS) in live plant cells.
    [Google Scholar]
  97. 97. 
    Platre MP, Jaillais Y. 2016. Guidelines for the use of protein domains in acidic phospholipid imaging. Methods Mol. Biol. 1376:175–94
    [Google Scholar]
  98. 98. 
    Platre MP, Noack LC, Doumane M, Bayle V, Simon MLA et al. 2018. A combinatorial lipid code shapes the electrostatic landscape of plant endomembranes. Dev. Cell 45:4465–480.e11Proposes the concept of an electrostatic membrane territory in plants that corresponds to post-Golgi membranes.
    [Google Scholar]
  99. 99. 
    Pokotylo I, Kravets V, Martinec J, Ruelland E 2018. The phosphatidic acid paradox: too many actions for one molecule class? Lessons from plants. Prog. Lipid Res. 71:43–53
    [Google Scholar]
  100. 100. 
    Posor Y, Eichhorn-Grünig M, Haucke V 2015. Phosphoinositides in endocytosis. Biochim. Biophys. Acta (BBA) Mol. Cell Biol. Lipids 1851:6794–804
    [Google Scholar]
  101. 101. 
    Poulsen LR, López-Marqués RL, McDowell SC, Okkeri J, Licht D et al. 2008. The Arabidopsis P4-ATPase ALA3 localizes to the Golgi and requires a β-subunit to function in lipid translocation and secretory vesicle formation. Plant Cell 20:3658–76
    [Google Scholar]
  102. 102. 
    Poulsen LR, López-Marqués RL, Pedas PR, McDowell SC, Brown E et al. 2015. A phospholipid uptake system in the model plant Arabidopsis thaliana. Nat. Commun 6:7649
    [Google Scholar]
  103. 103. 
    Pourcher M, Santambrogio M, Thazar N, Thierry A-M, Fobis-Loisy I et al. 2010. Analyses of sorting nexins reveal distinct retromer-subcomplex functions in development and protein sorting in Arabidopsis thaliana. Plant Cell 22:123980–91
    [Google Scholar]
  104. 104. 
    Preuss ML, Schmitz AJ, Thole JM, Bonner HKS, Otegui MS, Nielsen E 2006. A role for the RabA4b effector protein PI-4Kβ1 in polarized expansion of root hair cells in Arabidopsis thaliana. J. Cell Biol 172:7991–98
    [Google Scholar]
  105. 105. 
    Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S et al. 2009. Remorin, a solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21:51541–55
    [Google Scholar]
  106. 106. 
    Rodriguez-Villalon A, Gujas B, van Wijk R, Munnik T, Hardtke CS 2015. Primary root protophloem differentiation requires balanced phosphatidylinositol-4,5-biphosphate levels and systemically affects root branching. Development 142:81437–46
    [Google Scholar]
  107. 107. 
    Saravanan RS, Slabaugh E, Singh VR, Lapidus LJ, Haas T, Brandizzi F 2009. The targeting of the oxysterol-binding protein ORP3a to the endoplasmic reticulum relies on the plant VAP33 homolog PVA12. Plant J 58:5817–30
    [Google Scholar]
  108. 108. 
    Schaaf G, Ortlund EA, Tyeryar KR, Mousley CJ, Ile KE et al. 2008. Functional anatomy of phospholipid binding and regulation of phosphoinositide homeostasis by proteins of the Sec14 superfamily. Mol. Cell 29:2191–206
    [Google Scholar]
  109. 109. 
    Schapire AL, Voigt B, Jasik J, Rosado A, Lopez-Cobollo R et al. 2008. Arabidopsis Synaptotagmin 1 is required for the maintenance of plasma membrane integrity and cell viability. Plant Cell 20:123374–88
    [Google Scholar]
  110. 110. 
    Schauder CM, Wu X, Saheki Y, Narayanaswamy P, Torta F et al. 2014. Structure of a lipid-bound extended-synaptotagmin indicates a role in lipid transfer. Nature 510:7506552–55
    [Google Scholar]
  111. 111. 
    Scheuring D, Löfke C, Krüger F, Kittelmann M, Eisa A et al. 2016. Actin-dependent vacuolar occupancy of the cell determines auxin-induced growth repression. PNAS 113:2452–57
    [Google Scholar]
  112. 112. 
    Scorrano L, Matteis MAD, Emr S, Giordano F, Hajnóczky G et al. 2019. Coming together to define membrane contact sites. Nat. Commun. 10:11287
    [Google Scholar]
  113. 113. 
    Sekereš J, Pejchar P, Šantrůček J, Vukašinović N, Žárský V, Potocký M 2017. Analysis of exocyst subunit EXO70 family reveals distinct membrane polar domains in tobacco pollen tubes. Plant Physiol 173:31659–75
    [Google Scholar]
  114. 114. 
    Shimada C, Lipka V, O'Connell R, Okuno T, Schulze-Lefert P, Takano Y 2006. Nonhost resistance in Arabidopsis-Colletotrichum interactions acts at the cell periphery and requires actin filament function. Mol. Plant-Microbe Interact. 19:3270–79
    [Google Scholar]
  115. 115. 
    Shimada TL, Betsuyaku S, Inada N, Ebine K, Fujimoto M et al. 2019. Enrichment of phosphatidylinositol 4,5-bisphosphate in the extra-invasive hyphal membrane promotes Colletotrichum infection of Arabidopsis thaliana. Plant Cell Physiol 60:71514–24
    [Google Scholar]
  116. 116. 
    Siao W, Wang P, Voigt B, Hussey PJ, Baluska F 2016. Arabidopsis SYT1 maintains stability of cortical endoplasmic reticulum networks and VAP27-1-enriched endoplasmic reticulum–plasma membrane contact sites. J. Exp. Bot. 67:216161–71
    [Google Scholar]
  117. 117. 
    Simon MLA, Platre MP, Assil S, van Wijk R, Chen WY et al. 2014. A multi-colour/multi-affinity marker set to visualize phosphoinositide dynamics in Arabidopsis. Plant J. Cell Mol. Biol. 77:2322–37
    [Google Scholar]
  118. 118. 
    Simon MLA, Platre MP, Marquès-Bueno MM, Armengot L, Stanislas T et al. 2016. A PtdIns(4)P-driven electrostatic field controls cell membrane identity and signalling in plants. Nat. Plants. 2:7201689Establishes the importance of membrane electrostatics and PI4P in defining the plant PM identity.
    [Google Scholar]
  119. 119. 
    Singh MK, Krüger F, Beckmann H, Brumm S, Vermeer JEM et al. 2014. Protein delivery to vacuole requires SAND protein-dependent Rab GTPase conversion for MVB-vacuole fusion. Curr. Biol. 24:121383–89
    [Google Scholar]
  120. 120. 
    Sousa E, Kost B, Malhó R 2008. Arabidopsis phosphatidylinositol-4-monophosphate 5-kinase 4 regulates pollen tube growth and polarity by modulating membrane recycling. Plant Cell 20:113050–64
    [Google Scholar]
  121. 121. 
    Stefano G, Renna L, Wormsbaecher C, Gamble J, Zienkiewicz K, Brandizzi F 2018. Plant endocytosis requires the ER membrane-anchored proteins VAP27-1 and VAP27-3. Cell Rep 23:82299–307Demonstrates that plant VAP27 proteins directly interact with anionic phospholipids and regulate endocytic trafficking.
    [Google Scholar]
  122. 122. 
    Stenzel I, Ischebeck T, König S, Hołubowska A, Sporysz M et al. 2008. The type B phosphatidylinositol-4-phosphate 5-kinase 3 is essential for root hair formation in Arabidopsis thaliana. Plant Cell 20:1124–41
    [Google Scholar]
  123. 123. 
    Synek L, Schlager N, Eliás M, Quentin M, Hauser M-T, Zárský V 2006. AtEXO70A1, a member of a family of putative exocyst subunits specifically expanded in land plants, is important for polar growth and plant development. Plant J. Cell Mol. Biol. 48:154–72
    [Google Scholar]
  124. 124. 
    Tan X, Feng Y, Liu Y, Bao Y 2016. Mutations in exocyst complex subunit SEC6 gene impaired polar auxin transport and PIN protein recycling in Arabidopsis primary root. Plant Sci 250:97–104
    [Google Scholar]
  125. 125. 
    Tejos R, Sauer M, Vanneste S, Palacios-Gomez M, Li H et al. 2014. Bipolar plasma membrane distribution of phosphoinositides and their requirement for auxin-mediated cell polarity and patterning in Arabidopsis. Plant Cell 26:52114–28
    [Google Scholar]
  126. 126. 
    Testerink C, Munnik T. 2011. Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J. Exp. Bot. 62:72349–61
    [Google Scholar]
  127. 127. 
    Thole JM, Vermeer JEM, Zhang Y, Gadella TWJ, Nielsen E 2008. ROOT HAIR DEFECTIVE4 encodes a phosphatidylinositol-4-phosphate phosphatase required for proper root hair development in Arabidopsis thaliana. Plant Cell 20:2381–95
    [Google Scholar]
  128. 128. 
    Timcenko M, Lyons JA, Januliene D, Ulstrup JJ, Dieudonné T et al. 2019. Structure and autoregulation of a P4-ATPase lipid flippase. Nature 571:776536670
    [Google Scholar]
  129. 129. 
    Uemura T, Ueda T. 2014. Plant vacuolar trafficking driven by RAB and SNARE proteins. Curr. Opin. Plant Biol. 22:116–21
    [Google Scholar]
  130. 130. 
    Uličná L, Paprčková D, Fáberová V, Hozák P 2018. Phospholipids and inositol phosphates linked to the epigenome. Histochem. Cell Biol. 150:3245–53
    [Google Scholar]
  131. 131. 
    van Leeuwen W, Okrész L, Bögre L, Munnik T 2004. Learning the lipid language of plant signalling. Trends Plant Sci 9:8378–84
    [Google Scholar]
  132. 132. 
    van Leeuwen W, Vermeer JEM, Gadella TWJ Jr, Munnik T 2007. Visualization of phosphatidylinositol 4,5-bisphosphate in the plasma membrane of suspension-cultured tobacco BY-2 cells and whole Arabidopsis seedlings. Plant J. Cell Mol. Biol. 52:61014–26
    [Google Scholar]
  133. 133. 
    Vermeer JEM, Thole JM, Goedhart J, Nielsen E, Munnik T, Gadella TWJ Jr 2009. Imaging phosphatidylinositol 4-phosphate dynamics in living plant cells. Plant J 57:2356–72
    [Google Scholar]
  134. 134. 
    Vermeer JEM, van Leeuwen W, Tobeña-Santamaria R, Laxalt AM, Jones DR et al. 2006. Visualization of PtdIns3P dynamics in living plant cells. Plant J. Cell Mol. Biol. 47:5687–700
    [Google Scholar]
  135. 135. 
    Vincent P, Chua M, Nogue F, Fairbrother A, Mekeel H et al. 2005. A Sec14p-nodulin domain phosphatidylinositol transfer protein polarizes membrane growth of Arabidopsis thaliana root hairs. J. Cell Biol. 168:5801–12
    [Google Scholar]
  136. 136. 
    Vollmer AH, Youssef NN, DeWald DB 2011. Unique cell wall abnormalities in the putative phosphoinositide phosphatase mutant AtSAC9. Planta 234:5993–1005
    [Google Scholar]
  137. 137. 
    Wang P, Hawes C, Hussey PJ 2016. Plant endoplasmic reticulum–plasma membrane contact sites. Trends Plant Sci 22:4289–97
    [Google Scholar]
  138. 138. 
    Wang P, Hawkins TJ, Richardson C, Cummins I, Deeks MJ et al. 2014. The plant cytoskeleton, NET3C, and VAP27 mediate the link between the plasma membrane and endoplasmic reticulum. Curr. Biol. 24:121397–405
    [Google Scholar]
  139. 139. 
    Wang P, Richardson C, Hawkins TJ, Sparkes I, Hawes C, Hussey PJ 2016. Plant VAP27 proteins: domain characterization, intracellular localization and role in plant development. New Phytol 210:41311–26
    [Google Scholar]
  140. 140. 
    Welti R, Li W, Li M, Sang Y, Biesiada H et al. 2002. Profiling membrane lipids in plant stress responses: role of phospholipase Dα in freezing-induced lipid changes in Arabidopsis. J. Biol. Chem 277:3531994–2002
    [Google Scholar]
  141. 141. 
    Wen T-J, Hochholdinger F, Sauer M, Bruce W, Schnable PS 2005. The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol 138:31637–43
    [Google Scholar]
  142. 142. 
    Whitley P, Hinz S, Doughty J 2009. Arabidopsis FAB1/PIKfyve proteins are essential for development of viable pollen. Plant Physiol 151:41812–22
    [Google Scholar]
  143. 143. 
    Wu H, Carvalho P, Voeltz GK 2018. Here, there, and everywhere: the importance of ER membrane contact sites. Science 361:6401eaan5835
    [Google Scholar]
  144. 144. 
    Xu P, Baldridge RD, Chi RJ, Burd CG, Graham TR 2013. Phosphatidylserine flipping enhances membrane curvature and negative charge required for vesicular transport. J. Cell Biol. 202:6875–86
    [Google Scholar]
  145. 145. 
    Yamaoka Y, Yu Y, Mizoi J, Fujiki Y, Saito K et al. 2011. PHOSPHATIDYLSERINE SYNTHASE1 is required for microspore development in Arabidopsis thaliana. Plant J 67:4648–61
    [Google Scholar]
  146. 146. 
    Yamazaki T, Kawamura Y, Minami A, Uemura M 2008. Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via synaptotagmin SYT1. Plant Cell 20:123389–404
    [Google Scholar]
  147. 147. 
    Yang X, Bassham DC. 2015. New insight into the mechanism and function of autophagy in plant cells. Int. Rev. Cell Mol. Biol. 320:1–40
    [Google Scholar]
  148. 148. 
    Yoo C-M, Quan L, Cannon AE, Wen J, Blancaflor EB 2012. AGD1, a class 1 ARF-GAP, acts in common signaling pathways with phosphoinositide metabolism and the actin cytoskeleton in controlling Arabidopsis root hair polarity. Plant J. Cell Mol. Biol. 69:61064–76
    [Google Scholar]
  149. 149. 
    Yu H, Liu Y, Gulbranson DR, Paine A, Rathore SS, Shen J 2016. Extended synaptotagmins are Ca2+-dependent lipid transfer proteins at membrane contact sites. PNAS 113:164362–67
    [Google Scholar]
  150. 150. 
    Zhang X, Pumplin N, Ivanov S, Harrison MJ 2015. EXO70I is required for development of a sub-domain of the periarbuscular membrane during arbuscular mycorrhizal symbiosis. Curr. Biol. 25:162189–95
    [Google Scholar]
  151. 151. 
    Zhao Y, Yan A, Feijó JA, Furutani M, Takenawa T et al. 2010. Phosphoinositides regulate clathrin-dependent endocytosis at the tip of pollen tubes in Arabidopsis and tobacco. Plant Cell 22:124031–44
    [Google Scholar]
  152. 152. 
    Zheng J, Han SW, Rodriguez-Welsh MF, Rojas-Pierce M 2014. Homotypic vacuole fusion requires VTI11 and is regulated by phosphoinositides. Mol. Plant. 7:61026–40
    [Google Scholar]
  153. 153. 
    Zhong R, Burk DH, Nairn CJ, Wood-Jones A, Morrison WH, Ye Z-H 2005. Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization. Plant Cell 17:51449–66
    [Google Scholar]
  154. 154. 
    Zhuang X, Wang H, Lam SK, Gao C, Wang X et al. 2013. A BAR-domain protein SH3P2, which binds to phosphatidylinositol 3-phosphate and ATG8, regulates autophagosome formation in Arabidopsis. Plant Cell 25:114596–615
    [Google Scholar]
/content/journals/10.1146/annurev-arplant-081519-035910
Loading
/content/journals/10.1146/annurev-arplant-081519-035910
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