1932

Abstract

Cell polarity in plants operates across a broad range of spatial and temporal scales to control processes from acute cell growth to systemic hormone distribution. Similar to other eukaryotes, plants generate polarity at both the subcellular and tissue levels, often through polarization of membrane-associated protein complexes. However, likely due to the constraints imposed by the cell wall and their extremely plastic development, plants possess novel polarity molecules and mechanisms highly tuned to environmental inputs. Considerable progress has been made in identifying key plant polarity regulators, but detailed molecular understanding of polarity mechanisms remains incomplete in plants. Here, we emphasize the striking similarities in the conceptual frameworks that generate polarity in both animals and plants. To this end, we highlight how novel, plant-specific proteins engage in common themes of positive feedback, dynamic intracellular trafficking, and posttranslational regulation to establish polarity axes in development. We end with a discussion of how environmental signals control intrinsic polarity to impact postembryonic organogenesis and growth.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-100818-125211
2019-10-06
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/35/1/annurev-cellbio-100818-125211.html?itemId=/content/journals/10.1146/annurev-cellbio-100818-125211&mimeType=html&fmt=ahah

Literature Cited

  1. Abas L, Benjamins R, Malenica N, Paciorek T, Wisniewska J et al. 2006. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism. Nat. Cell Biol. 8:249–56
    [Google Scholar]
  2. Adamowski M, Friml J. 2015. PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32
    [Google Scholar]
  3. Alassimone J, Naseer S, Geldner N 2010. A developmental framework for endodermal differentiation and polarity. PNAS 107:5214–19
    [Google Scholar]
  4. Anne P, Azzopardi M, Gissot L, Beaubiat S, Hematy K, Palauqui JC 2015. OCTOPUS negatively regulates BIN2 to control phloem differentiation in Arabidopsis thaliana. Curr. Biol 25:2584–90
    [Google Scholar]
  5. Bainbridge K, Guyomarc'h S, Bayer E, Swarup R, Bennett M et al. 2008. Auxin influx carriers stabilize phyllotactic patterning. Genes Dev 22:810–23
    [Google Scholar]
  6. Barberon M, Dubeaux G, Kolb C, Isono E, Zelazny E, Vert G 2014. Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. PNAS 111:8293–98
    [Google Scholar]
  7. Barbosa IC, 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]
  8. Barbosa IC, Zourelidou M, Willige BC, Weller B, Schwechheimer C 2014. D6 PROTEIN KINASE activates auxin transport–dependent growth and PIN-FORMED phosphorylation at the plasma membrane. Development 29:674–85
    [Google Scholar]
  9. Benjamins R, Quint A, Weijers D, Hooykaas P, Offringa R 2001. The PINOID protein kinase regulates organ development in Arabidopsis by enhancing polar auxin transport. Development 128:4057–67
    [Google Scholar]
  10. Benkova E, Michniewicz M, Sauer M, Teichmann T, Seifertova D et al. 2003. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115:591–602
    [Google Scholar]
  11. Bennett MJ, Marchant A, Green HG, May ST, Ward SP et al. 1996. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–50
    [Google Scholar]
  12. Bergmann DC, Lukowitz W, Somerville CR 2004. Stomatal development and pattern controlled by a MAPKK kinase. Science 304:1494–97
    [Google Scholar]
  13. Berken A, Thomas C, Wittinghofer A 2005. A new family of RhoGEFs activates the Rop molecular switch in plants. Nature 436:1176–80
    [Google Scholar]
  14. Bischoff F, Vahlkamp L, Molendijk A, Palme K 2000. Localization of AtROP4 and AtROP6 and interaction with the guanine nucleotide dissociation inhibitor AtRhoGDI1 from Arabidopsis. Plant Mol. Biol 42:515–30
    [Google Scholar]
  15. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I 2005. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433:39–44
    [Google Scholar]
  16. Bonifacino JS, Traub LM. 2003. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu. Rev. Biochem. 72:395–447
    [Google Scholar]
  17. Boutte Y, Crosnier MT, Carraro N, Traas J, Satiat-Jeunemaitre B 2006. The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J. Cell Sci. 119:1255–65
    [Google Scholar]
  18. Boyd L, Guo S, Levitan D, Stinchcomb DT, Kemphues KJ 1996. PAR-2 is asymmetrically distributed and promotes association of P granules and PAR-1 with the cortex in C. elegans embryos. Development 122:3075–84
    [Google Scholar]
  19. Breda AS, Hazak O, Hardtke CS 2017. Phosphosite charge rather than shootward localization determines OCTOPUS activity in root protophloem. PNAS 114:E5721.e30
    [Google Scholar]
  20. Bringmann M, Bergmann DC. 2017. Tissue-wide mechanical forces influence the polarity of stomatal stem cells in Arabidopsis. Curr. Biol 27:877–83
    [Google Scholar]
  21. Brunoud G, Wells DM, Oliva M, Larrieu A, Mirabet V et al. 2012. A novel sensor to map auxin response and distribution at high spatio-temporal resolution. Nature 482:103–6
    [Google Scholar]
  22. Butty AC, Perrinjaquet N, Petit A, Jaquenoud M, Segall JE et al. 2002. A positive feedback loop stabilizes the guanine-nucleotide exchange factor Cdc24 at sites of polarization. EMBO J 21:1565–76
    [Google Scholar]
  23. Carol RJ, Takeda S, Linstead P, Durrant MC, Kakesova H et al. 2005. A RhoGDP dissociation inhibitor spatially regulates growth in root hair cells. Nature 438:1013–16
    [Google Scholar]
  24. Cartwright HN, Humphries JA, Smith LG 2009. PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science 323:649–51
    [Google Scholar]
  25. Chau AH, Walter JM, Gerardin J, Tang C, Lim WA 2012. Designing synthetic regulatory networks capable of self-organizing cell polarization. Cell 151:320–32
    [Google Scholar]
  26. Chiou JG, Balasubramanian MK, Lew DJ 2017. Cell polarity in yeast. Annu. Rev. Cell Dev. Biol. 33:77–101
    [Google Scholar]
  27. Christensen SK, Dagenais N, Chory J, Weigel D 2000. Regulation of auxin response by the protein kinase PINOID. Cell 100:469–78
    [Google Scholar]
  28. De Smet I, Beeckman T 2011. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nat. Rev. Mol. Cell Biol. 12:177–88
    [Google Scholar]
  29. Ding Z, Galvan-Ampudia CS, Demarsy E, Langowski L, Kleine-Vehn J et al. 2011. Light-mediated polarization of the PIN3 auxin transporter for the phototropic response in Arabidopsis. Nat. Cell Biol 13:447–52
    [Google Scholar]
  30. Donaldson JG, Jackson CL. 2011. ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat. Rev. Mol. Cell Biol. 12:362–75
    [Google Scholar]
  31. Dong J, MacAlister CA, Bergmann DC 2009. BASL controls asymmetric cell division in Arabidopsis. Cell 137:1320–30
    [Google Scholar]
  32. Etemad-Moghadam B, Guo S, Kemphues KJ 1995. Asymmetrically distributed PAR-3 protein contributes to cell polarity and spindle alignment in early C. elegans embryos. Cell 83:743–52
    [Google Scholar]
  33. Endler A, Persson S. 2011. Cellulose synthases and synthesis in Arabidopsis. Mol. Plant 4:199–211
    [Google Scholar]
  34. Facette MR, Park Y, Sutimantanapi D, Luo A, Cartwright HN et al. 2015. The SCAR/WAVE complex polarizes PAN receptors and promotes division asymmetry in maize. Nat. Plants 1:14024
    [Google Scholar]
  35. Fendrych M, Akhmanova M, Merrin J, Glanc M, Hagihara S et al. 2018. Rapid and reversible root growth inhibition by TIR1 auxin signalling. Nat. Plants 4:453–59
    [Google Scholar]
  36. Feraru E, Feraru MI, Kleine-Vehn J, Martiniere A, Mouille G et al. 2011. PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol 21:338–43
    [Google Scholar]
  37. Frank MJ, Cartwright HN, Smith LG 2003. Three Brick genes have distinct functions in a common pathway promoting polarized cell division and cell morphogenesis in the maize leaf epidermis. Development 130:753–62
    [Google Scholar]
  38. Frank MJ, Smith LG. 2002. A small, novel protein highly conserved in plants and animals promotes the polarized growth and division of maize leaf epidermal cells. Curr. Biol. 12:849–53
    [Google Scholar]
  39. Freisinger T, Klunder B, Johnson J, Muller N, Pichler G et al. 2013. Establishment of a robust single axis of cell polarity by coupling multiple positive feedback loops. Nat. Commun. 4:1807
    [Google Scholar]
  40. Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T et al. 2002a. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 108:661–73
    [Google Scholar]
  41. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H et al. 2003. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426:147–53
    [Google Scholar]
  42. Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K 2002b. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature 415:806–9
    [Google Scholar]
  43. Friml J, Yang X, Michniewicz M, Weijers D, Quint A et al. 2004. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 306:862–65
    [Google Scholar]
  44. Fu Y, Gu Y, Zheng Z, Wasteneys G, Yang Z 2005. Arabidopsis interdigitating cell growth requires two antagonistic pathways with opposing action on cell morphogenesis. Cell 120:687–700
    [Google Scholar]
  45. Fu Y, Li H, Yang Z 2002. The ROP2 GTPase controls the formation of cortical fine F-actin and the early phase of directional cell expansion during Arabidopsis organogenesis. Plant Cell 14:777–94
    [Google Scholar]
  46. Galweiler L, Guan C, Muller A, Wisman E, Mendgen K et al. 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:2226–30
    [Google Scholar]
  47. Geisler M, Nadeau J, Sack FD 2000. Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–86
    [Google Scholar]
  48. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W et al. 2003. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 112:219–30
    [Google Scholar]
  49. Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K 2001. Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–28
    [Google Scholar]
  50. Gordon-Weeks R, Tong Y, Davies TG, Leggewie G 2003. Restricted spatial expression of a high-affinity phosphate transporter in potato roots. J. Cell Sci. 116:3135–44
    [Google Scholar]
  51. Grebe M, Friml J, Swarup R, Ljung K, Sandberg G et al. 2002. Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway. Curr. Biol. 12:329–34
    [Google Scholar]
  52. Grones P, Abas M, Hajny J, Jones A, Waidmann S et al. 2018. PID/WAG-mediated phosphorylation of the Arabidopsis PIN3 auxin transporter mediates polarity switches during gravitropism. Sci. Rep. 8:10279
    [Google Scholar]
  53. Gu Y, Fu Y, Dowd P, Li S, Vernoud V et al. 2005. A Rho family GTPase controls actin dynamics and tip growth via two counteracting downstream pathways in pollen tubes. J. Cell Biol. 169:127–38
    [Google Scholar]
  54. Gu Y, Li S, Lord EM, Yang Z 2006. Members of a novel class of Arabidopsis Rho guanine nucleotide exchange factors control Rho GTPase–dependent polar growth. Plant Cell 18:366–81
    [Google Scholar]
  55. Gudesblat GE, Schneider-Pizon J, Betti C, Mayerhofer J, Vanhoutte I et al. 2012. SPEECHLESS integrates brassinosteroid and stomata signalling pathways. Nat. Cell Biol. 14:548–54
    [Google Scholar]
  56. Hable WE, Miller NR, Kropf DL 2003. Polarity establishment requires dynamic actin in fucoid zygotes. Protoplasma 221:193–204
    [Google Scholar]
  57. Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F 2006. Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol. Biol. 62:305–23
    [Google Scholar]
  58. Harrison BR, Masson PH. 2008. ARL2, ARG1 and PIN3 define a gravity signal transduction pathway in root statocytes. Plant J 53:380–92
    [Google Scholar]
  59. Heisler MG, Ohno C, Das P, Sieber P, Reddy GV et al. 2005. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 15:1899–911
    [Google Scholar]
  60. 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 18:3519–34
    [Google Scholar]
  61. Houbaert A, Zhang C, Tiwari M, Wang K, de Marcos Serrano A et al. 2018. POLAR-guided signalling complex assembly and localization drive asymmetric cell division. Nature 563:574–78
    [Google Scholar]
  62. Howell AS, Jin M, Wu CF, Zyla TR, Elston TC, Lew DJ 2012. Negative feedback enhances robustness in the yeast polarity establishment circuit. Cell 149:322–33
    [Google Scholar]
  63. Huang F, Zago MK, Abas L, van Marion A, Galvan-Ampudia CS, Offringa R 2010. Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell 22:1129–42
    [Google Scholar]
  64. Humphries JA, Vejlupkova Z, Luo A, Meeley RB, Sylvester AW et al. 2011. ROP GTPases act with the receptor-like protein PAN1 to polarize asymmetric cell division in maize. Plant Cell 23:2273–84
    [Google Scholar]
  65. Hung TJ, Kemphues KJ. 1999. PAR-6 is a conserved PDZ domain–containing protein that colocalizes with PAR-3 in Caenorhabditis elegans embryos. Development 126:127–35
    [Google Scholar]
  66. Hwang JU, Vernoud V, Szumlanski A, Nielsen E, Yang Z 2008. A tip-localized RhoGAP controls cell polarity by globally inhibiting Rho GTPase at the cell apex. Curr. Biol. 18:1907–16
    [Google Scholar]
  67. Hwang JU, Wu G, Yan A, Lee YJ, Grierson CS, Yang Z 2010. Pollen-tube tip growth requires a balance of lateral propagation and global inhibition of Rho-family GTPase activity. J. Cell Sci. 123:340–50
    [Google Scholar]
  68. Ischebeck T, Werner S, Krishnamoorthy P, Lerche J, Meijon M et al. 2013. Phosphatidylinositol 4,5-bisphosphate influences PIN polarization by controlling clathrin-mediated membrane trafficking in Arabidopsis. Plant Cell 25:4894–911
    [Google Scholar]
  69. Jilkine A, Edelstein-Keshet L. 2011. A comparison of mathematical models for polarization of single eukaryotic cells in response to guided cues. PLOS Comput. Biol. 7:e1001121
    [Google Scholar]
  70. Kasai K, Takano J, Miwa K, Toyoda A, Fujiwara T 2011. High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J. Biol. Chem 286:6175–83
    [Google Scholar]
  71. Kiba T, Feria-Bourrellier AB, Lafouge F, Lezhneva L, Boutet-Mercey S et al. 2012. The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24:245–58
    [Google Scholar]
  72. Kim TW, Michniewicz M, Bergmann DC, Wang ZY 2012. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482:419–22
    [Google Scholar]
  73. Kitakura S, Vanneste S, Robert S, Lofke C, Teichmann T et al. 2011. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis. Plant Cell 23:1920–31
    [Google Scholar]
  74. Klahre U, Becker C, Schmitt AC, Kost B 2006. Nt-RhoGDI2 regulates Rac/Rop signaling and polar cell growth in tobacco pollen tubes. Plant J 46:1018–31
    [Google Scholar]
  75. Klahre U, Kost B. 2006. Tobacco RhoGTPase ACTIVATING PROTEIN1 spatially restricts signaling of RAC/Rop to the apex of pollen tubes. Plant Cell 18:3033–46
    [Google Scholar]
  76. Kleine-Vehn J, Dhonukshe P, Sauer M, Brewer PB, Wisniewska J et al. 2008a. ARF GEF–dependent transcytosis and polar delivery of PIN auxin carriers in Arabidopsis. Curr. Biol 18:526–31
    [Google Scholar]
  77. Kleine-Vehn J, Dhonukshe P, Swarup R, Bennett M, Friml J 2006. Subcellular trafficking of the Arabidopsis auxin influx carrier AUX1 uses a novel pathway distinct from PIN1. Plant Cell 18:3171–81
    [Google Scholar]
  78. Kleine-Vehn J, Ding Z, Jones AR, Tasaka M, Morita MT, Friml J 2010. Gravity-induced PIN transcytosis for polarization of auxin fluxes in gravity-sensing root cells. PNAS 107:22344–49
    [Google Scholar]
  79. Kleine-Vehn J, Langowski L, Wisniewska J, Dhonukshe P, Brewer PB, Friml J 2008b. Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol. Plant 1:1056–66
    [Google Scholar]
  80. Kleine-Vehn J, Wabnik K, Martiniere A, Langowski L, Willig K et al. 2011. Recycling, clustering, and endocytosis jointly maintain PIN auxin carrier polarity at the plasma membrane. Mol. Syst. Biol. 7:540
    [Google Scholar]
  81. Kozubowski L, Saito K, Johnson JM, Howell AS, Zyla TR, Lew DJ 2008. Symmetry-breaking polarization driven by a Cdc42p GEF-PAK complex. Curr. Biol. 18:1719–26
    [Google Scholar]
  82. Kuchen EE, Fox S, de Reuille PB, Kennaway R, Bensmihen S et al. 2012. Generation of leaf shape through early patterns of growth and tissue polarity. Science 335:1092–96
    [Google Scholar]
  83. Lampard GR, Macalister CA, Bergmann DC 2008. Arabidopsis stomatal initiation is controlled by MAPK-mediated regulation of the bHLH SPEECHLESS. Science 322:1113–16
    [Google Scholar]
  84. Langowski L, Ruzicka K, Naramoto S, Kleine-Vehn J, Friml J 2010. Trafficking to the outer polar domain defines the root-soil interface. Curr. Biol. 20:904–8
    [Google Scholar]
  85. Lau OS, Song Z, Zhou Z, Davies KA, Chang J et al. 2018. Direct control of SPEECHLESS by PIF4 in the high-temperature response of stomatal development. Curr. Biol. 28:1273–80.e3
    [Google Scholar]
  86. Li H, Wu G, Ware D, Davis KR, Yang Z 1998. Arabidopsis Rho-related GTPases: differential gene expression in pollen and polar localization in fission yeast. Plant Physiol 118:407–17
    [Google Scholar]
  87. Li H, Lin Y, Heath RM, Zhu MX, Yang Z 1999. Control of pollen tube tip growth by a Rop GTPase–dependent pathway that leads to tip-localized calcium influx. Plant Cell 11:1731–42
    [Google Scholar]
  88. Liao CY, Smet W, Brunoud G, Yoshida S, Vernoux T, Weijers D 2015. Reporters for sensitive and quantitative measurement of auxin response. Nat. Methods 12:207–10
    [Google Scholar]
  89. Lin D, Nagawa S, Chen J, Cao L, Chen X et al. 2012. A ROP GTPase–dependent auxin signaling pathway regulates the subcellular distribution of PIN2 in Arabidopsis roots. Curr. Biol. 22:1319–25
    [Google Scholar]
  90. Lin Y, Wang Y, Zhu JK, Yang Z 1996. Localization of a Rho GTPase implies a role in tip growth and movement of the generative cell in pollen tubes. Plant Cell 8:293–303
    [Google Scholar]
  91. Liu SH, Marks MS, Brodsky FM 1998. A dominant-negative clathrin mutant differentially affects trafficking of molecules with distinct sorting motifs in the class II major histocompatibility complex (MHC) pathway. J. Cell Biol. 140:1023–37
    [Google Scholar]
  92. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S et al. 2006. A silicon transporter in rice. Nature 440:688–91
    [Google Scholar]
  93. Ma JF, Yamaji N, Mitani N, Tamai K, Konishi S et al. 2007. An efflux transporter of silicon in rice. Nature 448:209–12
    [Google Scholar]
  94. MacAlister CA, Ohashi-Ito K, Bergmann DC 2007. Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–40
    [Google Scholar]
  95. Mansfield C, Newman JL, Olsson TSG, Hartley M, Chan J, Coen E 2018. Ectopic BASL reveals tissue cell polarity throughout leaf development in Arabidopsis thaliana. Curr. Biol 28:2638–46.e4
    [Google Scholar]
  96. Marchant A, Kargul J, May ST, Muller P, Delbarre A et al. 1999. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J 18:2066–73
    [Google Scholar]
  97. Marhava P, Bassukas AEL, Zourelidou M, Kolb M, Moret B et al. 2018. A molecular rheostat adjusts auxin flux to promote root protophloem differentiation. Nature 558:297–300
    [Google Scholar]
  98. Marhavy P, Duclercq J, Weller B, Feraru E, Bielach A et al. 2014. Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Curr. Biol. 24:1031–37
    [Google Scholar]
  99. Martiniere A, Lavagi I, Nageswaran G, Rolfe DJ, Maneta-Peyret L et al. 2012. Cell wall constrains lateral diffusion of plant plasma-membrane proteins. PNAS 109:12805–10
    [Google Scholar]
  100. Martins S, Montiel-Jorda A, Cayrel A, Huguet S, Roux CP et al. 2017. Brassinosteroid signaling–dependent root responses to prolonged elevated ambient temperature. Nat. Commun. 8:309
    [Google Scholar]
  101. Men S, Boutte Y, Ikeda Y, Li X, Palme K et al. 2008. Sterol-dependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 10:237–44
    [Google Scholar]
  102. Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A et al. 2007. Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130:1044–56
    [Google Scholar]
  103. Miwa K, Takano J, Omori H, Seki M, Shinozaki K, Fujiwara T 2007. Plants tolerant of high boron levels. Science 318:1417
    [Google Scholar]
  104. Miwa K, Wakuta S, Takada S, Ide K, Takano J et al. 2013. Roles of BOR2, a boron exporter, in cross linking of rhamnogalacturonan II and root elongation under boron limitation in Arabidopsis. Plant Physiol 1631699–709
    [Google Scholar]
  105. Molendijk AJ, Bischoff F, Rajendrakumar CS, Friml J, Braun M et al. 2001. Arabidopsis thaliana Rop GTPases are localized to tips of root hairs and control polar growth. EMBO J 20:2779–88
    [Google Scholar]
  106. Mouchel CF, Osmont KS, Hardtke CS 2006. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature 443:458–61
    [Google Scholar]
  107. Mravec J, Petrasek J, Li N, Boeren S, Karlova R et al. 2011. Cell plate restricted association of DRP1A and PIN proteins is required for cell polarity establishment in Arabidopsis. Nat. Plants 21:1055–60
    [Google Scholar]
  108. Muller A, Guan C, Galweiler L, Tanzler P, Huijser P et al. 1998. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 17:6903–11
    [Google Scholar]
  109. Nadeau JA, Sack FD. 2002. Control of stomatal distribution on the Arabidopsis leaf surface. Science 296:1697–700
    [Google Scholar]
  110. Nagashima Y, Tsugawa S, Mochizuki A, Sasaki T, Fukuda H, Oda Y 2018. A Rho-based reaction-diffusion system governs cell wall patterning in metaxylem vessels. Sci. Rep. 8:11542
    [Google Scholar]
  111. Nagawa S, Xu T, Lin D, Dhonukshe P, Zhang X et al. 2012. ROP GTPase–dependent actin microfilaments promote PIN1 polarization by localized inhibition of clathrin-dependent endocytosis. PLOS Biol 10:e1001299
    [Google Scholar]
  112. Nance J, Zallen JA. 2011. Elaborating polarity: PAR proteins and the cytoskeleton. Development 138:799–809
    [Google Scholar]
  113. Naseer S, Lee Y, Lapierre C, Franke R, Nawrath C, Geldner N 2012. Casparian strip diffusion barrier in Arabidopsis is made of a lignin polymer without suberin. PNAS 109:10101–6
    [Google Scholar]
  114. O'Connor DL, Runions A, Sluis A, Bragg J, Vogel JP et al. 2014. A division in PIN-mediated auxin patterning during organ initiation in grasses. PLOS Comput. Biol. 10:e1003447
    [Google Scholar]
  115. Oda Y, Fukuda H. 2012. Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337:1333–36
    [Google Scholar]
  116. Oda Y, Fukuda H. 2013. Rho of plant GTPase signaling regulates the behavior of Arabidopsis kinesin-13A to establish secondary cell wall patterns. Plant Cell 25:4439–50
    [Google Scholar]
  117. Paciorek T, Zažímalová E, Ruthhardt N, Petrášek J, Stierhof Y-D 2005. Auxin inhibits endocytosis and promotes its own efflux from cells. Nature 435:1251–56
    [Google Scholar]
  118. Peret B, Swarup K, Ferguson A, Seth M, Yang Y et al. 2012. AUX/LAX genes encode a family of auxin influx transporters that perform distinct functions during Arabidopsis development. Plant Cell 24:2874–85
    [Google Scholar]
  119. Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M et al. 2006. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312:914–18
    [Google Scholar]
  120. Pillitteri LJ, Peterson KM, Horst RJ, Torii KU 2011. Molecular profiling of stomatal meristemoids reveals new component of asymmetric cell division and commonalities among stem cell populations in Arabidopsis. Plant Cell 23:3260–75
    [Google Scholar]
  121. Platre MP, Bayle V, Armengot L, Bareille J, Marques-Bueno MDM et al. 2019. Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine. Science 364:57–62
    [Google Scholar]
  122. Rakusova H, Abbas M, Han H, Song S, Robert HS, Friml J 2016. Termination of shoot gravitropic responses by auxin feedback on PIN3 polarity. Curr. Biol. 26:3026–32
    [Google Scholar]
  123. Robert HS, Grunewald W, Sauer M, Cannoot B, Soriano M et al. 2015. Plant embryogenesis requires AUX/LAX-mediated auxin influx. Development 142:702–11
    [Google Scholar]
  124. Rowe MH, Dong J, Weimer AK, Bergmann DC 2019. A plant-specific polarity module establishes cell fate asymmetry in the Arabidopsis stomatal lineage. bioRxiv 614636. https://doi.org/10.1101/614636
    [Crossref] [Google Scholar]
  125. Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T et al. 1999. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99:463–72
    [Google Scholar]
  126. Sasaki A, Yamaji N, Yokosho K, Ma JF 2012. Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24:2155–67
    [Google Scholar]
  127. Sasaki T, Fukuda H, Oda Y 2017. CORTICAL MICROTUBULE DISORDERING1 is required for secondary cell wall patterning in xylem vessels. Plant Cell 29:3123–39
    [Google Scholar]
  128. Sauer M, Balla J, Luschnig C, Wisniewska J, Reinohl V et al. 2006. Canalization of auxin flow by Aux/IAA-ARF-dependent feedback regulation of PIN polarity. Genes Dev 20:2902–11
    [Google Scholar]
  129. Schlereth A, Moller B, Liu W, Kientz M, Flipse J et al. 2010. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 464:913–16
    [Google Scholar]
  130. Skirycz A, Claeys H, De Bodt S, Oikawa A, Shinoda S et al. 2011. Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23:1876–88
    [Google Scholar]
  131. Sorefan K, Girin T, Liljegren SJ, Ljung K, Robles P et al. 2009. A regulated auxin minimum is required for seed dispersal in Arabidopsis. Nature 459:583–86
    [Google Scholar]
  132. Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL et al. 1999. Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286:316–18
    [Google Scholar]
  133. Sugiyama Y, Wakazaki M, Toyooka K, Fukuda H, Oda Y 2017. A novel plasma membrane–anchored protein regulates xylem cell-wall deposition through microtubule-dependent lateral inhibition of Rho GTPase domains. Curr. Biol. 27:2522–28.e4
    [Google Scholar]
  134. Sukumar P, Edwards KS, Rahman A, Delong A, Muday GK 2009. PINOID kinase regulates root gravitropism through modulation of PIN2-dependent basipetal auxin transport in Arabidopsis. Plant Physiol 150:722–35
    [Google Scholar]
  135. Sun H, Basu S, Brady SR, Luciano RL, Muday GK 2004. Interactions between auxin transport and the actin cytoskeleton in developmental polarity of Fucus distichus embryos in response to light and gravity. Plant Physiol 135:266–78
    [Google Scholar]
  136. Swarup R, Friml J, Marchant A, Ljung K, Sandberg G et al. 2001. Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes Dev 15:2648–53
    [Google Scholar]
  137. Swarup R, Kramer EM, Perry P, Knox K, Leyser HM et al. 2005. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7:1057–65
    [Google Scholar]
  138. Takano J, Miwa K, Yuan L, von Wiren N, Fujiwara T 2005. Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. PNAS 102:12276–81
    [Google Scholar]
  139. Takano J, Tanaka M, Toyoda A, Miwa K, Kasai K et al. 2010. Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. PNAS 107:5220–25
    [Google Scholar]
  140. Tanaka M, Sotta N, Yamazumi Y, Yamashita Y, Miwa K et al. 2016. The minimum open reading frame, AUG-stop, induces boron-dependent ribosome stalling and mRNA degradation. Plant Cell 28:2830–49
    [Google Scholar]
  141. Tanaka M, Takano J, Chiba Y, Lombardo F, Ogasawara Y et al. 2011. Boron-dependent degradation of NIP5;1 mRNA for acclimation to excess boron conditions in Arabidopsis. Plant Cell 23:3547–59
    [Google Scholar]
  142. 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 26:2114–28
    [Google Scholar]
  143. Tominaga M, Ito K. 2015. The molecular mechanism and physiological role of cytoplasmic streaming. Curr. Opin. Plant Biol. 27:104–10
    [Google Scholar]
  144. Truernit E, Bauby H, Belcram K, Barthelemy J, Palauqui JC 2012. OCTOPUS, a polarly localised membrane-associated protein, regulates phloem differentiation entry in Arabidopsis thaliana. Development 139:1306–15
    [Google Scholar]
  145. Uchida N, Takahashi K, Iwasaki R, Yamada R, Yoshimura M et al. 2018. Chemical hijacking of auxin signaling with an engineered auxin-TIR1 pair. Nat. Chem. Biol. 14:299–305
    [Google Scholar]
  146. Ueno D, Sasaki A, Yamaji N, Miyaji T, Fujii Y et al. 2015. A polarly localized transporter for efficient manganese uptake in rice. Nat. Plants 1:15170
    [Google Scholar]
  147. Valdez-Taubas J, Pelham HR. 2003. Slow diffusion of proteins in the yeast plasma membrane allows polarity to be maintained by endocytic cycling. Curr. Biol. 13:1636–40
    [Google Scholar]
  148. Vaten A, Soyars CL, Tarr PT, Nimchuk ZL, Bergmann DC 2018. Modulation of asymmetric division diversity through cytokinin and SPEECHLESS regulatory interactions in the Arabidopsis stomatal lineage. Dev. Cell 47:53–66.e5
    [Google Scholar]
  149. Vernoux T, Besnard F, Traas J 2010. Auxin at the shoot apical meristem. Cold Spring Harb. Perspect. Biol. 2:a001487
    [Google Scholar]
  150. Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H et al. 2011. The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7:508
    [Google Scholar]
  151. Wakuta S, Mineta K, Amano T, Toyoda A, Fujiwara T et al. 2015. Evolutionary divergence of plant borate exporters and critical amino acid residues for the polar localization and boron-dependent vacuolar sorting of AtBOR1. Plant Cell Physiol 56:852–62
    [Google Scholar]
  152. Wang S, Yoshinari A, Shimada T, Hara-Nishimura I, Mitani-Ueno N et al. 2017. Polar localization of the NIP5;1 boric acid channel is maintained by endocytosis and facilitates boron transport in Arabidopsis roots. Plant Cell 29:824–42
    [Google Scholar]
  153. Weller B, Zourelidou M, Frank L, Barbosa IC, Fastner A et al. 2017. Dynamic PIN-FORMED auxin efflux carrier phosphorylation at the plasma membrane controls auxin efflux–dependent growth. PNAS 114:E887–96
    [Google Scholar]
  154. Willemsen V, Friml J, Grebe M, van den Toorn A, Palme K, Scheres B 2003. Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Sci. Rep. 15:612–25
    [Google Scholar]
  155. Willige BC, Ahlers S, Zourelidou M, Barbosa IC, Demarsy E et al. 2013. D6PK AGCVIII kinases are required for auxin transport and phototropic hypocotyl bending in Arabidopsis. Plant Cell 25:1674–88
    [Google Scholar]
  156. Winge P, Brembu T, Bones AM 1997. Cloning and characterization of rac-like cDNAs from Arabidopsis thaliana. Plant Mol. Biol 35:483–95
    [Google Scholar]
  157. Wisniewska J, Xu J, Seifertova D, Brewer PB, Ruzicka K et al. 2006. Polar PIN localization directs auxin flow in plants. Science 312:883
    [Google Scholar]
  158. Woods B, Lai H, Wu CF, Zyla TR, Savage NS, Lew DJ 2016. Parallel actin-independent recycling pathways polarize Cdc42 in budding yeast. Curr. Biol. 26:2114–26
    [Google Scholar]
  159. Wu CF, Chiou JG, Minakova M, Woods B, Tsygankov D et al. 2015. Role of competition between polarity sites in establishing a unique front. eLife 4:e11611
    [Google Scholar]
  160. Wu G, Li H, Yang Z 2000. Arabidopsis RopGAPs are a novel family of Rho GTPase–activating proteins that require the Cdc42/Rac-interactive binding motif for Rop-specific GTPase stimulation. Plant Physiol 124:1625–36
    [Google Scholar]
  161. Yamaji N, Ma JF. 2007. Spatial distribution and temporal variation of the rice silicon transporter Lsi1. Plant Physiol 143:1306–13
    [Google Scholar]
  162. Yanagisawa M, Alonso JM, Szymanski DB 2018. Microtubule-dependent confinement of a cell signaling and actin polymerization control module regulates polarized cell growth. Curr. Biol. 28:2459–66.e4
    [Google Scholar]
  163. Yang Y, Hammes UZ, Taylor CG, Schachtman DP, Nielsen E 2006. High-affinity auxin transport by the AUX1 influx carrier protein. Curr. Biol. 16:1123–27
    [Google Scholar]
  164. Yang Z, Watson JC. 1993. Molecular cloning and characterization of rho, a ras-related small GTP-binding protein from the garden pea. PNAS 90:8732–36
    [Google Scholar]
  165. Ye J, Zheng Y, Yan A, Chen N, Wang Z et al. 2009. Arabidopsis formin3 directs the formation of actin cables and polarized growth in pollen tubes. Plant Cell 21:3868–84
    [Google Scholar]
  166. Yoshida S, van der Schuren A, van Dop M, van Galen L, Saiga S et al. 2019. A SOSEKI-based coordinate system interprets global polarity cues in Arabidopsis. Nat. Plants 5:160–66
    [Google Scholar]
  167. Yoshinari A, Fujimoto M, Ueda T, Inada N, Naito S, Takano J 2016. DRP1-dependent endocytosis is essential for polar localization and boron-induced degradation of the borate transporter BOR1 in Arabidopsis thaliana. Plant Cell Physiol 57:1985–2000
    [Google Scholar]
  168. Yoshinari A, Kasai K, Fujiwara T, Naito S, Takano J 2012. Polar localization and endocytic degradation of a boron transporter, BOR1, is dependent on specific tyrosine residues. Plant Signal. Behav. 7:46–49
    [Google Scholar]
  169. Zhang J, Nodzynski T, Pencik A, Rolcik J, Friml J 2010. PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. PNAS 107:918–22
    [Google Scholar]
  170. Zhang X, Facette M, Humphries JA, Shen Z, Park Y et al. 2012. Identification of PAN2 by quantitative proteomics as a leucine-rich repeat-receptor–like kinase acting upstream of PAN1 to polarize cell division in maize. Plant Cell 24:4577–89
    [Google Scholar]
  171. Zhang Y, Guo X, Dong J 2016. Phosphorylation of the polarity protein BASL differentiates asymmetric cell fate through MAPKs and SPCH. Curr. Biol. 26:2957–65
    [Google Scholar]
  172. Zhang Y, McCormick S. 2007. A distinct mechanism regulating a pollen-specific guanine nucleotide exchange factor for the small GTPase Rop in Arabidopsis thaliana. PNAS 104:18830–35
    [Google Scholar]
  173. Zhang Y, Wang P, Shao W, Zhu JK, Dong J 2015. The BASL polarity protein controls a MAPK signaling feedback loop in asymmetric cell division. Dev. Cell 33:136–49
    [Google Scholar]
  174. Zonies S, Motegi F, Hao Y, Seydoux G 2010. Symmetry breaking and polarization of the C. elegans zygote by the polarity protein PAR-2. Development 137:1669–77
    [Google Scholar]
  175. Zourelidou M, Absmanner B, Weller B, Barbosa IC, Willige BC et al. 2014. Auxin efflux by PIN-FORMED proteins is activated by two different protein kinases, D6 PROTEIN KINASE and PINOID. eLife 3:e02860
    [Google Scholar]
  176. Zourelidou M, Muller I, Willige BC, Nill C, Jikumaru Y et al. 2009. The polarly localized D6 PROTEIN KINASE is required for efficient auxin transport in Arabidopsis thaliana. Development 136:627–36
    [Google Scholar]
/content/journals/10.1146/annurev-cellbio-100818-125211
Loading
/content/journals/10.1146/annurev-cellbio-100818-125211
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