Endomembrane trafficking driven by microtubule growth regulates stomatal movement in Arabidopsis.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
11 Sep 2024
11 Sep 2024
Historique:
received:
04
09
2021
accepted:
31
08
2024
medline:
12
9
2024
pubmed:
12
9
2024
entrez:
11
9
2024
Statut:
epublish
Résumé
Microtubule-based vesicle trafficking usually relies upon kinesin and dynein motors and few reports describe microtubule polymerisation driving directional vesicle trafficking. Here we show that Arabidopsis END BINDING1b (EB1b), a microtubule plus-end binding protein, directly interacts with SYP121, a SNARE protein that mediates the trafficking of the K
Identifiants
pubmed: 39261498
doi: 10.1038/s41467-024-52338-x
pii: 10.1038/s41467-024-52338-x
doi:
Substances chimiques
Arabidopsis Proteins
0
Microtubule-Associated Proteins
0
AT1G12360 protein, Arabidopsis
0
Katanin
EC 5.6.1.1
Cell Cycle Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
7967Subventions
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32230030
Organisme : National Natural Science Foundation of China (National Science Foundation of China)
ID : 32061143018
Informations de copyright
© 2024. The Author(s).
Références
Schliwa, M. & Woehlke, G. Molecular motors. Nature 422, 759–765 (2003).
pubmed: 12700770
doi: 10.1038/nature01601
Vale, R. D. The molecular motor toolbox for intracellular transport. Cell 112, 467–480 (2003).
pubmed: 12600311
doi: 10.1016/S0092-8674(03)00111-9
Hirokawa, N., Noda, Y., Tanaka, Y. & Niwa, S. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 10, 682–696 (2009).
pubmed: 19773780
doi: 10.1038/nrm2774
Buchnik, L., Abu-Abied, M. & Sadot, E. Role of plant myosins in motile organelles: is a direct interaction required? J. Int. Plant Biol. 57, 23–30 (2015).
doi: 10.1111/jipb.12282
Perico, C. & Sparkes, I. Plant organelle dynamics: cytoskeletal control and membrane contact sites. N. Phytol. 220, 381–394 (2018).
doi: 10.1111/nph.15365
Foissner, I., Menzel, D. & Wasteneys, G. O. Microtubule-dependent motility and orientation of the cortical endoplasmic reticulum in elongating characean internodal cells. Cell Motil. Cytoskeleton 66, 142–155 (2009).
pubmed: 19137584
doi: 10.1002/cm.20337
Crowell, E. F. et al. Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell 21, 1141–1154 (2009).
pubmed: 19376932
pmcid: 2685615
doi: 10.1105/tpc.108.065334
Gutierrez, R., Lindeboom, J. J., Paredez, A. R., Emons, A. M. & Ehrhardt, D. W. Arabidopsis cortical microtubules position cellulose synthase delivery to the plasma membrane and interact with cellulose synthase trafficking compartments. Nat. Cell Biol. 11, 797–806 (2009).
pubmed: 19525940
doi: 10.1038/ncb1886
Ambrose, C. et al. CLASP interacts with sorting nexin 1 to link microtubules and auxin transport via PIN2 recycling in Arabidopsis thaliana. Dev. Cell 24, 649–659 (2013).
pubmed: 23477787
doi: 10.1016/j.devcel.2013.02.007
Brandizzi, F. & Wasteneys, G. O. Cytoskeleton-dependent endomembrane organization in plant cells: an emerging role for microtubules. Plant J. 75, 339–349 (2013).
pubmed: 23647215
doi: 10.1111/tpj.12227
Acharya, B. R. & Assmann, S. M. Hormone interactions in stomatal function. Plant Mol. Biol. 69, 451–462 (2009).
pubmed: 19031047
doi: 10.1007/s11103-008-9427-0
Hubbard, K. E., Siegel, R. S., Valerio, G., Brandt, B. & Schroeder, J. I. Abscisic acid and CO
pubmed: 21994053
doi: 10.1093/aob/mcr252
Kim, T. H., Bohmer, M., Hu, H., Nishimura, N. & Schroeder, J. I. Guard cell signal transduction network: advances in understanding abscisic acid, CO
pubmed: 20192751
pmcid: 3056615
doi: 10.1146/annurev-arplant-042809-112226
Shimazaki, K., Doi, M., Assmann, S. M. & Kinoshita, T. Light regulation of stomatal movement. Annu. Rev. Plant Biol. 58, 219–247 (2007).
pubmed: 17209798
doi: 10.1146/annurev.arplant.57.032905.105434
Yang, J., Li, C. L., Kong, D. X., Guo, F. Y. & Wei, H. B. Light-mediated signaling and metabolic changes coordinate stomatal opening and closure. Front. Plant Sci. 11, 601478 (2020).
pubmed: 33343603
pmcid: 7746640
doi: 10.3389/fpls.2020.601478
Kollist, H., Nuhkat, M. & Roelfsema, M. R. Closing gaps: linking elements that control stomatal movement. N. Phytol. 203, 44–62 (2014).
doi: 10.1111/nph.12832
Lawson, T. & Blatt, M. R. Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency. Plant Physiol. 164, 1556–1570 (2014).
pubmed: 24578506
pmcid: 3982722
doi: 10.1104/pp.114.237107
Hedrich, R. Ion channels in plants. Physiol. Rev. 92, 1777–1811 (2012).
pubmed: 23073631
doi: 10.1152/physrev.00038.2011
Sutter, J. U., Campanoni, P., Tyrrell, M. & Blatt, M. R. Selective mobility and sensitivity to SNAREs is exhibited by the Arabidopsis KAT1 K
pubmed: 16531497
pmcid: 1425843
doi: 10.1105/tpc.105.038950
Sutter, J. U. et al. Abscisic acid triggers the endocytosis of the Arabidopsis KAT1 K
pubmed: 17683934
doi: 10.1016/j.cub.2007.07.020
Lefoulon, C., Waghmare, S., Karnik, R. & Blatt, M. R. Gating control and K
pubmed: 29940699
pmcid: 6220998
doi: 10.1111/pce.13392
Kim, M., Hepler, P. K., Eun, S. O., Ha, K. S. & Lee, Y. Actin filaments in mature guard cells are radially distributed and involved in stomatal movement. Plant Physiol. 109, 1077–1084 (1995).
pubmed: 12228654
pmcid: 161411
doi: 10.1104/pp.109.3.1077
Eun, S. O. & Lee, Y. Actin filaments of guard cells are reorganized in response to light and abscisic acid. Plant Physiol. 115, 1491–1498 (1997).
pubmed: 9414559
pmcid: 158614
doi: 10.1104/pp.115.4.1491
Couot-Gastelier, L. & Louguet, P. Effet de la colchicine sur les mouvements des stomates et l’ultrastructure des cellules stomatiques deTradescantia virginiana. Bull. Soc. Bot. Fr. Lett. Bot. 139, 345–356 (1992).
Jiang, C. J., Nakajim, N. & Kondo, N. Disruption of microtubules by abscisic acid in guard cells of Vicia faba L. Plant Cell Physiol. 37, 697–701 (1996).
doi: 10.1093/oxfordjournals.pcp.a029001
Assmann, S. M. & Baskin, T. I. The function of guard cells does not require an intact array of cortical microtubules. J. Exp. Bot. 49, 163–170 (1998).
doi: 10.1093/jxb/49.319.163
Marcus, A. I., Moore, R. C. & Cyr, R. J. The role of microtubules in guard cell function. Plant Physiol. 125, 387–395 (2001).
pubmed: 11154346
pmcid: 61019
doi: 10.1104/pp.125.1.387
Moore, R. C. & Cyr, R. J. Association btween elongation factor-1alpha and microtubules in vivo is domain dependent and conditional. Cell Motil. Cytoskeleton 45, 279–292 (2000).
pubmed: 10744861
doi: 10.1002/(SICI)1097-0169(200004)45:4<279::AID-CM4>3.0.CO;2-4
Gardiner, J. & Marc, J. Arabidopsis thaliana, a plant model organism for the neuronal microtubule cytoskeleton? J. Exp. Bot. 62, 89–97 (2011).
pubmed: 20813785
doi: 10.1093/jxb/erq278
Eisinger, W., Ehrhardt, D. & Briggs, W. Microtubules are essential for guard-cell function in Vicia and Arabidopsis. Mol. Plant 5, 601–610 (2012).
pubmed: 22402260
doi: 10.1093/mp/sss002
Eisinger, W. R., Kirik, V., Lewis, C., Ehrhardt, D. W. & Briggs, W. R. Quantitative changes in microtubule distribution correlate with guard cell function in Arabidopsis. Mol. Plant 5, 716–725 (2012).
pubmed: 22492121
doi: 10.1093/mp/sss033
Galatis, B. & Apostolakos, P. The role of the cytoskeleton in the morphogenesis and function of stomatal complexes. N. Phytol. 161, 613–639 (2004).
doi: 10.1046/j.1469-8137.2003.00986.x
Nehlig, A., Molina, A., Rodrigues‑Ferreira, S., Honoré, S. & Nahmias, C. Regulation of end-binding protein EB1 in the control of microtubule dynamics. Cell Mol. Life Sci. 74, 2381–2393 (2017).
pubmed: 28204846
pmcid: 11107513
doi: 10.1007/s00018-017-2476-2
Akhmanova, A. & Steinmetz, M. O. Tracking the ends: a dynamic protein network controls the fate of microtubule tips. Nat. Rev. Mol. Cell Biol. 9, 309–322 (2008).
pubmed: 18322465
doi: 10.1038/nrm2369
Komaki, S. et al. Nuclear-localized subtype of end-binding 1 protein regulates spindle organization in Arabidopsis. J. Cell Sci. 123, 451–459 (2010).
pubmed: 20067996
doi: 10.1242/jcs.062703
Bisgrove, S. R., Lee, Y. R., Liu, B., Peters, N. T. & Kropf, D. L. The microtubule plus-end binding protein EB1 functions in root responses to touch and gravity signals in Arabidopsis. Plant Cell 20, 396–410 (2008).
pubmed: 18281505
pmcid: 2276450
doi: 10.1105/tpc.107.056846
Galva, C. et al. The microtubule plus-end tracking proteins SPR1 and EB1b interact to maintain polar cell elongation and directional organ growth in Arabidopsis. Plant Cell 26, 4409–4425 (2014).
pubmed: 25415978
pmcid: 4277225
doi: 10.1105/tpc.114.131482
Lindeboom, J. J. et al. CLASP stabilization of plus ends created by severing promotes microtubule creation and reorientation. J. Cell Biol. 218, 190–205 (2019).
pubmed: 30377221
pmcid: 6314540
doi: 10.1083/jcb.201805047
Zheng, W. N. et al. AP3M harbors actin filament binding activity that is crucial for vacuole morphology and stomatal closure in Arabidopsis. Proc. Natl Acad. Sci. USA 116, 18132–18141 (2019).
pubmed: 31431522
pmcid: 6731635
doi: 10.1073/pnas.1901431116
Negi, J. et al. A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Curr. Biol. 23, 479–484 (2013).
pubmed: 23453954
pmcid: 4039172
doi: 10.1016/j.cub.2013.02.001
Chan, J., Calder, G. M., Doonan, J. H. & Lloyd, C. W. EB1 reveals mobile microtubule nucleation sites in Arabidopsis. Nat. Cell Biol. 5, 967–971 (2003).
pubmed: 14557818
doi: 10.1038/ncb1057
Higaki, T., Kutsuna, N., Sano, T., Kondo, N. & Hasezawa, S. Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J. 61, 156–165 (2010).
pubmed: 20092030
doi: 10.1111/j.1365-313X.2009.04032.x
Fukuda, M., Hasezawa, S., Asai, N., Nakajima, N. & Kondo, N. Dynamic organization of microtubules in guard cells of Vicia faba L. with diunral cycle. Plant Cell Physiol. 39, 80–86 (1998).
pubmed: 9517004
doi: 10.1093/oxfordjournals.pcp.a029293
Dou, L., He, K., Peng, J., Wang, X. & Mao, T. The E3 ligase MREL57 modulates microtubule stability and stomatal closure in response to ABA. Nat. Commun. 12, 2181 (2021).
pubmed: 33846350
pmcid: 8041845
doi: 10.1038/s41467-021-22455-y
Murphy, A. S., Bandyopadhyay, A., Holstein, S. E. & Peer, W. A. Endocytotic cycling of PM proteins. Annu. Rev. Plant Biol. 56, 221–251 (2005).
pubmed: 15862095
doi: 10.1146/annurev.arplant.56.032604.144150
Peer, W. A. Plasma membrane protein trafficking. In The Plant Plasma Membrane, Plant Cell Monographs (Springer, Berlin). 19, 31–56 (2011).
Philippar, K. et al. Auxin activates KAT1 and KAT2, two K
pubmed: 14996216
doi: 10.1111/j.1365-313X.2003.02006.x
Eisenach, C., Chen, Z. H., Grefen, C. & Blatt, M. R. The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K
pubmed: 21914010
doi: 10.1111/j.1365-313X.2011.04786.x
Meckel, T., Hurst, A. C., Thiel, G. & Homann, U. Endocytosis against high turgor: intact guard cells of Vicia faba constitutively endocytose fluorescently labelled plasma membrane and GFP-tagged K-channel KAT1. Plant J. 39, 182–193 (2004).
pubmed: 15225284
doi: 10.1111/j.1365-313X.2004.02119.x
Wang, F. L. et al. A potassium-sensing niche in Arabidopsis roots orchestrates signaling and adaptation responses to maintain nutrient homeostasis. Dev. Cell 56, 781–794 (2021).
pubmed: 33756120
doi: 10.1016/j.devcel.2021.02.027
Nielsen, M. E. & Thordal-Christensen, H. Recycling of Arabidopsis plasma membrane PEN1 syntaxin. Plant Signal Behav. 7, 1541–1543 (2012).
pubmed: 23073012
pmcid: 3578888
doi: 10.4161/psb.22304
Karnik, R. et al. Arabidopsis Sec1/Munc18 protein SEC11 is a competitive and dynamic modulator of SNARE binding and SYP121-dependent vesicle traffic. Plant Cell 25, 1368–1382 (2013).
pubmed: 23572542
pmcid: 3663274
doi: 10.1105/tpc.112.108506
Wan, Y. L. et al. Variable-angle total internal reflection fluorescence microscopy of intact cells of Arabidopsis thaliana. Plant Methods 7, 27 (2011).
pubmed: 21943324
pmcid: 3219692
doi: 10.1186/1746-4811-7-27
Fendrych, M. et al. Visualization of the exocyst complex dynamics at the plasma membrane of Arabidopsis thaliana. Mol. Biol. Cell 24, 510–520 (2013).
pubmed: 23283982
pmcid: 3571873
doi: 10.1091/mbc.e12-06-0492
Zhang, W. W., Huang, L., Zhang, C. H. & Staiger, C. J. Arabidopsis myosin XIK interacts with the exocyst complex to facilitate vesicle tethering during exocytosis. Plant Cell 33, 2454–2478 (2021).
pubmed: 33871640
pmcid: 8364239
doi: 10.1093/plcell/koab116
Cui, X. K. et al. Arabidopsis SYP121 acts as an ROP2 effector in the regulation of root hair tip growth. Mol. Plant 15, 1008–1023 (2022).
pubmed: 35488430
doi: 10.1016/j.molp.2022.04.008
Roelfsema, M. R., Steinmeyer, R., Staal, M. & Hedrich, R. Single guard cell recordings in intact plants: light-induced hyperpolarization of the plasma membrane. Plant J. 26, 1–13 (2001).
pubmed: 11359605
doi: 10.1046/j.1365-313x.2001.01000.x
Szyroki, A. et al. KAT1 is not essential for stomatal opening. Proc. Natl Acad. Sci. USA 98, 2917–2921 (2001).
pubmed: 11226341
pmcid: 30240
doi: 10.1073/pnas.051616698
Laloux, T., Matyjaszczyk, I., Beaudelot, S., Hachez, C. & Chaumont, F. Interaction between the SNARE SYP121 and the plasma membrane aquaporin PIP2;7 involves different protein domains. Front. Plant Sci. 11, 631643 (2021).
pubmed: 33537055
pmcid: 7847993
doi: 10.3389/fpls.2020.631643
Hachez et al. Arabidopsis SNAREs SYP61 and SYP121 coordinate the trafficking of plasma membrane aquaporin PIP2;7 to modulate the cell membrane water permeability. Plant Cell 26, 3132–3147 (2014).
pubmed: 25082856
pmcid: 4145137
doi: 10.1105/tpc.114.127159
Cheerambathur, D. K. & Desai, A. Linked in: formation and regulation of microtubule attachments during chromosome segregation. Curr. Opin. Cell Biol. 26, 113–122 (2014).
pubmed: 24529253
doi: 10.1016/j.ceb.2013.12.005
Liu, Z. Y., Persson, S. & Zhang, Y. The connection of cytoskeletal network with plasma membrane and the cell wall. J. Integr. Plant Biol. 57, 330–340 (2015).
pubmed: 25693826
pmcid: 4405036
doi: 10.1111/jipb.12342
Zheng, J. M., Han, S. W., Rodriguez-Welsh, M. F. & Rojas-Pierce, M. Homotypic vacuole fusion requires VTI11 and is regulated by phosphoinositides. Mol. Plant 7, 1026–1040 (2014).
pubmed: 24569132
doi: 10.1093/mp/ssu019
Galjart, N. Plus-end-tracking proteins and their interactions at microtubule ends. Curr. Biol. 20, R528–R537 (2010).
pubmed: 20620909
doi: 10.1016/j.cub.2010.05.022
Molines, A. T. et al. EB1 contributes to microtubule bundling and organization, along with root growth, in Arabidopsis thaliana. Biol. Open 7, bio030510 (2018).
pubmed: 29945874
pmcid: 6124560
doi: 10.1242/bio.030510
Silva, P. A., Ul-Rehman, R., Rato, C., Sansebastiano, G. P. D. & Malho, R. Asymmetric localization of Arabidopsis SYP124 syntaxin at the pollen tube apical and sub-apical zones is involved in tip growth. BMC Plant Biol. 10, 179 (2010).
pubmed: 20718953
pmcid: 3095309
doi: 10.1186/1471-2229-10-179
Ichikawa et al. Syntaxin of plant proteins SYP123 and SYP132 mediate root hair tip growth in Arabidopsis thaliana. Plant Cell Physiol. 55, 790–800 (2014).
pubmed: 24642714
doi: 10.1093/pcp/pcu048
Ichikawa, M., Iwano, M. & Sato, M. H. Nuclear membrane localization during pollen development and apex-focused polarity establishment of SYP124/125 during pollen germination in Arabidopsis thaliana. Plant Reprod. 28, 143–151 (2015).
pubmed: 26111864
doi: 10.1007/s00497-015-0265-3
Alberico, E. O. et al. Interactions between the microtubule binding protein EB1 and F-Actin. J. Mol. Biol. 428, 1304–1314 (2016).
pubmed: 26854759
pmcid: 4834876
doi: 10.1016/j.jmb.2016.01.032
Henty-Ridilla, J. L., Rankova, A., Eskin, J. A., Kenny, K. & Goode, B. L. Accelerated actin filament polymerization from microtubule plus ends. Science 352, 1004–1009 (2016).
pubmed: 27199431
pmcid: 5179141
doi: 10.1126/science.aaf1709
Dixit, R., Chang, E. & Cyr, R. Establishment of polarity during organization of the acentrosomal plant cortical microtubule array. Mol. Biol. Cell 17, 1298–1305 (2006).
pubmed: 16381813
pmcid: 1382318
doi: 10.1091/mbc.e05-09-0864
Novak, D. et al. Analysis of formin functions during cytokinesis using specific inhibitor SMIFH2. Plant Physiol. 186, 945–963 (2021).
pubmed: 33620500
pmcid: 8195507
doi: 10.1093/plphys/kiab085
Zhang, L. N. et al. Analysis of formin functions during cytokinesis using specific inhibitor SMIFH2. Plant Physiol. 186, 945–963 (2021).
pubmed: 33620500
pmcid: 8195507
doi: 10.1093/plphys/kiab085
Ho, C. M. et al. Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65-3 in Arabidopsis. Plant Cell 23, 2909–2923 (2011).
pubmed: 21873565
pmcid: 3180800
doi: 10.1105/tpc.110.078204
Rogers, S. L., Wiedemann, U., Hacker, U., Turck, C. & Vale, R. D. Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr. Biol. 14, 1827–1833 (2004).
pubmed: 15498490
doi: 10.1016/j.cub.2004.09.078
Barth, A. I., Caro-Gonzalez, H. Y. & Nelson, W. J. Role of adenomatous polyposis coli (APC) and microtubules in directional cell migration and neuronal polarization. Semin. Cell Dev. Biol. 19, 245–251 (2008).
pubmed: 18387324
pmcid: 2673958
doi: 10.1016/j.semcdb.2008.02.003
Gu, C. et al. The microtubule plus-end tracking protein EB1 is required for Kv1 voltage-gated K
pubmed: 17145502
doi: 10.1016/j.neuron.2006.10.022
Waadt, R. et al. Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56, 505–516 (2008).
pubmed: 18643980
doi: 10.1111/j.1365-313X.2008.03612.x
Chang, M. & Huang, S. J. Arabidopsis ACT11 modifies actin turnover to promote pollen germination and maintain the normal rate of tube growth. Plant J. 83, 515–527 (2015).
pubmed: 26096143
doi: 10.1111/tpj.12910
Xu, T. D. et al. Cell surface ABP1-TMK auxin-sensing complex activates ROPGTPase signaling. Science 343, 1025–1028 (2014).
pubmed: 24578577
pmcid: 4166562
doi: 10.1126/science.1245125
Baster, P. et al. SCF(TIR1/AFB)-auxin signalling regulates PIN vacuolar trafficking and auxin fluxes during root gravitropism. EMBO J. 32, 260–274 (2013).
pubmed: 23211744
doi: 10.1038/emboj.2012.310
Liu, L. et al. Actomyosin and CSI1/POM2 cooperate to deliver cellulose synthase from Golgi to cortical microtubules in Arabidopsis. Nat. Commun. 14, 7442 (2023).
pubmed: 37978293
pmcid: 10656550
doi: 10.1038/s41467-023-43325-9