Regulation of developmental and environmental signaling by interaction between microtubules and membranes in plant cells

Abstract

Cell division and expansion require the ordered arrangement of microtubules, which are subject to spatial and temporal modifications by developmental and environmental factors. Understanding how signals translate to changes in cortical microtubule organization is of fundamental importance. A defining feature of the cortical microtubule array is its association with the plasma membrane; modules of the plasma membrane are thought to play important roles in the mediation of microtubule organization. In this review, we highlight advances in research on the regulation of cortical microtubule organization by membrane-associated and membrane-tethered proteins and lipids in response to phytohormones and stress. The transmembrane kinase receptor Rho-like guanosine triphosphatase, phospholipase D, phosphatidic acid, and phosphoinositides are discussed with a focus on their roles in microtubule organization.

Key words： abiotic stresses; cortical microtubule; lipids; plasma membrane

References

1 Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

2 Adamowski M, Friml J (2015) PIN-dependent auxin transport: action, regulation, and evolution. Plant Cell 27:20–32

3 Ambrose JC, Wasteneys GO (2008) CLASP modulates microtubulecortex interaction during self-organization of acentrosomal microtubules. Mol Biol Cell 19:4730–4737

4 Ambrose C, Ruan Y, Gardiner J, Tamblyn LM, Catching A, Kirik V,Marc J, Overall R, Wasteneys GO (2013) CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev Cell 24:649–659

5 Barton DA, Vantard M, Overall RL (2008) Analysis of cortical arrays from Tradescantia virginiana at high resolution reveals discrete microtubule subpopulations and demonstrates that confocal images of arrays can be misleading. Plant Cell 20:982–994

6 Baster P, Robert S, Kleine-Vehn J, Vanneste S, Kania U, Grunewald W, De Rybel B, Beeckman T, Friml J (2013) SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J 32:260–274

7 Beck M, Komis G, Ziemann A, Menzel D, Samaj J (2011) Mitogenactivated protein kinase 4 is involved in the regulation of mitoticand cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytol 189:1069–1083

8 Boutte Y, Crosnier MT, Carraro N, Traas J, Satiat-Jeunemaitre B(2006) The plasma membrane recycling pathway and cell polarityin plants: studies on PIN proteins. J Cell Sci 119:1255–1265

9 Brandizzi F, Wasteneys GO (2013) Cytoskeleton-dependent endomembrane organization in plant cells: an emerging role for microtubules. Plant J 75:339–349

10 Cao L, Wang L, Zheng M, Cao H, Ding L, Zhang X, Fu Y (2013) Arabidopsis AUGMIN subunit8 is a microtubule plus-end binding protein that promotes microtubule reorientation in hypocotyls. Plant Cell 25:2187–2201

11 Chen X, Grandont L, Li H, Hauschild R, Paque S, Abuzeineh A, Rakusova H, Benkova E, Perrot-Rechenmann C, Friml J (2014) Inhibition of cell expansion by rapid ABP1-mediated auxin effect on microtubules. Nature 516:90–93

12 Deeks MJ, Fendrych M, Smertenko A, Bell KS, Oparka K, Cvrckova F, Zarsky V,Hussey PJ (2010) The plant formin AtFH4 interacts with both actin and microtubules, and contains a newly identified microtubule-binding domain. J Cell Sci 123:1209–1215

13 Dhonukshe P, Laxalt AM, Goedhart J, Gadella TW, Munnik T (2003) Phospholipase D activation correlates with microtubule reorganization in living plant cells. Plant Cell 15:2666–2679

14 Dixit R, Cyr R (2004) The cortical microtubule array: from dynamics to organization. Plant Cell 16:2546–2552

15 Effendi Y, Jones AM, Scherer GF (2013) AUXIN-BINDING-PROTEIN1(ABP1) in phytochrome-B-controlled responses. J Exp Bot 64:5065–5074

16 Ehrhardt DW, Shaw SL (2006) Microtubule dynamics and organizationin the plant cortical array. Annu Rev Plant Biol 57:859–875

17 Eisinger W, Ehrhardt D, Briggs W (2012a) Microtubules are essential for guard-cell function in Vicia and Arabidopsis. Mol Plant 5:601–610

18 Eisinger WR, Kirik V, Lewis C, Ehrhardt DW, Briggs WR (2012b) Quantitative changes in microtubule distribution correlate with guard cell function in Arabidopsis. Mol Plant 5:716–725

19 Enders TA, Oh S, Yang Z, Montgomery BL, Strader LC (2015) Genome sequencing of Arabidopsis abp1-5 reveals second-site mutations that may affect phenotypes. Plant Cell 27:1820–1826

20 Galatis B, Apostolakos P (2004) The role of the cytoskeleton in the morphogenesis and function of stomatal complexes. New Phytol 161:613–639

21 Gao Y, Zhang Y, Zhang D, Dai X, Estelle M, Zhao Y (2015) Auxin binding protein 1 (ABP1) is not required for either auxin signaling or Arabidopsis development. Proc Natl Acad Sci U S A 112:2275–2280

22 Gardiner JC, Harper JD, Weerakoon ND, Collings DA, Ritchie S, Gilroy S, Cyr RJ, Marc J(2001) A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell 13:2143–2158

23 Geldner N, Friml J, Stierhof YD, Jurgens G, Palme K(2001) Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413:425–428

24 Gu Y, Deng Z, Paredez AR, DeBolt S, Wang ZY, Somerville C (2008) Prefoldin 6 is required for normal microtubule dynamics and organization in Arabidopsis. Proc Natl Acad Sci USA 105:18064–18069

25 Gudesblat GE, Russinova E (2011) Plants grow on brassinosteroids. Curr Opin Plant Biol 14:530–537

26 Hamada T (2014) Microtubule organization and microtubule-associated proteins in plant cells. Int Rev Cell Mol Biol 312:1–52

27 Hashimoto T (2015) Microtubules in plants. Arabidopsis Book 13:e0179

28 Heisler MG, Hamant O, Krupinski P, Uyttewaal M, Ohno C, Jönsson H, Traas J, Meyerowitz EM (2010) Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxint ransport. PLoS Biol 8:e1000516

29 Ho AY, Day DA, Brown MH, Marc J (2009) Arabidopsis phospho lipaseD δ as an initiator of cytoskeleton-mediated signalling to fundamental cellular processes. Funct Plant Biol 36:190–198

30 Huang S, Blanchoin L, Kovar DR, Staiger CJ (2003) Arabidopsis capping protein (AtCP) is a heterodimer that regulates assembly at the barbed ends of actin filaments. J Biol Chem 278:44832–44842

31 Huang S, Gao L, Blanchoin L, Staiger CJ (2006) Heterodimeric capping protein from Arabidopsis is regulated by phosphatidic acid. Mol Biol Cell 17:1946–1958

32 Jiang Y, Wu K, Lin F, Qu Y, Liu X, Zhang Q (2014) Phosphatidic acid integrates calcium signaling and microtubule dynamics into regulating ABA-induced stomatal closure in Arabidopsis. Planta 239:565–575

33 Kato M, Nagasaki-Takeuchi N, Ide Y, Maeshima M (2010) An Arabidopsis hydrophilic Ca2+ -binding protein with a PEVK-rich domain, PCaP2, is associated with the plasma membrane and interacts with calmodulin and phosphatidylinositol phosphates. Plant Cell Physiol 51:366–379

34 Keerthisinghe S, Nadeau JA, Lucas JR, Nakagawa T, Sack FD (2015) The Arabidopsis leucine-rich repeat receptor-like kinase MUSTACHES enforces stomatal bilateral symmetry in Arabidopsis. Plant J 81:684–694

35 Kendrick MD, Chang C (2008) Ethylene signaling: new levels of complexity and regulation. Curr Opin Plant Biol 11:479–485

36 Khanna R, Li J, Tseng TS, Schroeder JI, Ehrhardt DW, Briggs WR (2014) COP1 jointly modulates cytoskeletal processes and electrophysiological responses required for stomatal closure. Mol Plant 7:1441–1454

37 Kleine-Vehn J, Langowski L, Wisniewska J, Dhonukshe P, Brewer PB, Friml J (2008) Cellular and molecular requirements for polar PIN targeting and transcytosis in plants. Mol Plant 1:1056–1066

38 Li J (2010) Regulation of the nuclear activities of brassinosteroid signaling. Curr Opin Plant Biol 13:540–547

39 Li J, Wang X, Qin T, Zhang Y, Liu X, Sun J, Zhou Y, Zhu L, Zhang Z, Yuan M, Mao T (2011) MDP25, a novel calcium regulatory protein, mediates hypocotyl cell elongation by destabilizing cortical microtubules in Arabidopsis. Plant Cell 23:4411–4427

40 Li J, Henty-Ridilla JL, Huang S, Wang X, Blanchoin L, Staiger CJ (2012) Capping protein modulates the dynamic behavior of actin filaments in response to phosphatidic acid in Arabidopsis. Plant Cell 24:3742–3754

41 Lin D, Cao L, Zhou Z, Zhu L, Ehrhardt D, Yang Z, Fu Y (2013) Rho GTPase signaling activates microtubule severing to promote microtubule ordering in Arabidopsis. Curr Biol 23:290–297

42 Lin F, Qu Y, Zhang Q (2014) Phospholipids: molecules regulating cytoskeletal organization in plant abiotic stress tolerance. Plant Signal Behav 9:e28337

43 Lindeboom JJ, Nakamura M, Hibbel A, Shundyak K, Gutierrez R,Ketelaar T, Emons AM, Mulder BM, Kirik V, Ehrhardt DW (2013) A mechanism for reorientation of cortical microtubule arrays driven by microtubule severing. Science 342:1245533

44 Liu CM (2015) AUXIN BINDING PROTEIN 1 (ABP1): a matter of fact. J Integr Plant Biol 57:234–235

45 Liu X, Qin T, Ma Q, Sun J, Liu Z, Yuan M, Mao T (2013) Lightregulated hypocotyl elongation involves proteasome-dependent degradation of the microtubule regulatory protein WDL3 in Arabidopsis. Plant Cell 25:1740–1755

46 Lloyd C, Chan J (2004) Microtubules and the shape of plants to come. Nat Rev Mol Cell Biol 5:13–22

47 Locascio A, Blazquez MA, Alabadi D (2013) Dynamic regulation of cortical microtubule organization through prefoldin-DELLA interaction. Curr Biol 23:804–809

48 Lucas J, Shaw SL (2008) Cortical microtubule arrays in the Arabidopsis seedling. Curr Opin Plant Biol 11:94–98

49 Lucas JR, Nadeau JA, Sack FD (2006) Microtubule arrays and Arabidopsis stomatal development. J Exp Bot 57:71–79

50 Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) From The Cover:A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci U S A 102:12270–12275

51 Marcus AI, Moore RC, Cyr RJ (2001) The role of microtubules in guard cell function. Plant Physiol 125:387–395

52 Mollinari C, Kleman JP, Jiang W, Schoehn G, Hunter T, Margolis RL (2002) PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J Cell Biol 157:1175–1186

53 Muller M, Munne-Bosch S (2015) Ethylene response fekerehub in hormone and stress signaling. Plant Physiol 169:32–41

54 Nagasaki N, Tomioka R, Maeshima M (2008) A hydrophilic cationbinding protein of Arabidopsis thaliana, AtPCaP1, is localized to plasma membrane via N-myristoylation and interacts with calmodulin and the phosphatidylinositol phosphates PtdIns (3,4,5) P3 and PtdIns (3,5) P2. FEBS J 275:2267–2282

55 Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T (2004) SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16:1178–1190

56 Oda Y, Fukuda H (2012) Initiation of cell wall pattern by a Rho- and microtubule-driven symmetry breaking. Science 337:1333–1336

57 Oda Y, Fukuda H (2013) The dynamic interplay of plasma membrane domains and cortical microtubules in secondary cell wall patterning. Front Plant Sci 4:1–6

58 Paque S, Mouille G, Grandont L, Alabadi D, Gaertner C, Goyallon A, Muller P, Primard-Brisset C, Sormani R, Blazquez MA, Perrot-Rechenmann C (2014) AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in Arabidopsis. Plant Cell 26:280–295

59 Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F et al (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

60 Pleskot R, Potocky M, Pejchar P, Linek J, Bezvoda R, Martinec J, Valentova O, Novotna Z,Zarsky V (2010) Mutual regulation of plant phospholipase D and the actin cytoskeleton. Plant J 62:494–507

61 Pleskot R, Li J, Zarsky V, Potocky M, Staiger CJ (2013) Regulation of cytoskeletal dynamics by phospholipase D and phosphatidic acid. Trends Plant Sci 18:496–504

62 Pleskot R, Pejchar P, Staiger CJ, Potocky M (2014) When fat is not bad: the regulation of actin dynamics by phospholipid signaling molecules. Front Plant Sci 5:1–6

63 Polko JK, van Zanten M, van Rooij JA, Maree AF, Voesenek LA, Peeters AJ, Pierik R (2012) Ethylene-induced differential petiole growth in Arabidopsis thaliana involves local microtubule reorientation and cell expansion. New Phytol 193:339–348

64 Robert S, Kleine-Vehn J, Barbez E, Sauer M, Paciorek T, Baster P, Vanneste S, Zhang J, Simon S, Covanova M, Hayashi K,Dhonukshe P, Yang Z, Bednarek SY, Jones AM, Luschnig C,Aniento F, Zazimalova E, Friml J (2010) ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis. Cell 143:111–121

65 Rodriguez-Milla MA, Salinas J (2009) Prefoldins 3 and 5 play an essential role in Arabidopsis tolerance to salt stress. Mol Plant 2:526–534

66 Ruan Y, Wasteneys GO (2014) CLASP: a microtubule-based integrator of the hormone-mediated transitions from cell division to elongation. Curr Opin Plant Biol 22:149–158

67 Sambade A, Pratap A, Buschmann H, Morris RJ, Lloyd C (2012) The influence of light on microtubule dynamics and alignment in the Arabidopsis hypocotyl. Plant Cell 24:192–201

68 Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H, Itoh TJ, Hidaka M, Machida Y (2006) Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 20:1004–1014

69 Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR (2004) The Arabidopsis sku6/spiral1 gene encodes a plus endlocalized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16:1506–1520

70 Shoji T, Suzuki K, Abe T, Kaneko Y, Shi H, Zhu JK, Rus A, Hasegawa PM, Hashimoto T (2006) Salt stress affects cortical microtubule organization and helical growth in Arabidopsis. Plant Cell Physiol 47:1158–1168

71 Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M, Bogre L, Hussey PJ (2006) Control of the AtMAP65-1 interaction with microtubules through the cell cycle. J Cell Sci 119:3227–3237

72 Stace CL, Ktistakis NT (2006) Phosphatidic acid- and phosphatidylserine-binding proteins. Biochim Biophys Acta 1761:913–926

73 Sun J, Ma Q, Mao T (2015) Ethylene regulates Arabidopsis microtubule-associated protein WDL5 in etiolated hypocotyl elongation. Plant Physiol 169:325–337

74 Takahashi H, Kawahara A, Inoue Y (2003) Ethylene promotes the induction by auxin of the cortical microtubule randomization required for low-pH-induced root hair initiation in lettuce (Lactuca sativa L.) seedlings. Plant Cell Physiol 44:932–940

75 Wang C, Li J, Yuan M (2007) Salt tolerance requires cortical microtubule reorganization in Arabidopsis. Plant Cell Physiol 48:1534–1547

76 Wang S, Kurepa J, Hashimoto T, Smalle JA (2011) Salt stressinduced disassembly of Arabidopsis cortical microtubule arrays involves 26S proteasome-dependent degradation of SPIRAL1. Plant Cell 23:3412–3427

77 Wang X, Zhang J, Yuan M, Ehrhardt DW, Wang Z, Mao T (2012) Arabidopsis microtubule destabilizing protein 40 is involved in brassinosteroid regulation of hypocotyl elongation. Plant Cell 24:4012–4025

78 Wang X, Guo L, Wang G, Li M (2014) PLD: phospholipase Ds in plant signaling. Springer, Berlin, pp 3–26

79 Xu T, Dai N, Chen J, Nagawa S, Cao M, Li H, Zhou Z, Chen X, De Rycke R, Rakusová H (2014) Cell surface ABP1-TMK auxinsensing complex activates ROP GTPase signaling. Science 343:1025–1028

80 Ye J, Zhang W, Guo Y (2013) Arabidopsis SOS3 plays an important role in salt tolerance by mediating calcium-dependent microfilament reorganization. Plant Cell Rep 32:139–148

81 Yu L, Nie J, Cao C, Jin Y, Yan M, Wang F, Liu J,Xiao Y, Liang Y, Zhang W (2010) Phosphatidic acid mediates salt stress response by regulation of MPK6 in Arabidopsis thaliana. New Phytol 188:762–773

82 Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X(2009) Phospholipase Dalpha1 and phosphatidic acid regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377

83 Zhang Q, Lin F, Mao T, Nie J, Yan M, Yuan M, Zhang W (2012) Phosphatidic acid regulates microtubule organization by interacting with MAP65-1 in response to salt stress in Arabidopsis. Plant Cell 24:4555–4576

84 Zhang C, Raikhel NV, Hicks GR (2013) CLASPing microtubules and auxin transport. Dev Cell 24:569–571