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Cell wall accumulation of fluorescent proteins derived from a trans-Golgi cisternal membrane marker and paramural bodies in interdigitated Arabidopsis leaf epidermal cells

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Abstract

In most dicotyledonous plants, leaf epidermal pavement cells develop jigsaw puzzle-like shapes during cell expansion. The rapid growth and complicated cell shape of pavement cells is suggested to be achieved by targeted exocytosis that is coordinated with cytoskeletal rearrangement to provide plasma membrane and/or cell wall materials for lobe development during their morphogenesis. Therefore, visualization of membrane trafficking in leaf pavement cells should contribute an understanding of the mechanism of plant cell morphogenesis. To reveal membrane trafficking in pavement cells, we observed monomeric red fluorescent protein-tagged rat sialyl transferases, which are markers of trans-Golgi cisternal membranes, in the leaf epidermis of Arabidopsis thaliana. Quantitative fluorescence imaging techniques and immunoelectron microscopic observations revealed that accumulation of the red fluorescent protein occurred mostly in the curved regions of pavement cell borders and guard cell ends during leaf expansion. Transmission electron microscopy observations revealed that apoplastic vesicular membrane structures called paramural bodies were more frequent beneath the curved cell wall regions of interdigitated pavement cells and guard cell ends in young leaf epidermis. In addition, pharmacological studies showed that perturbations in membrane trafficking resulted in simple cell shapes. These results suggested possible heterogeneity of the curved regions of plasma membranes, implying a relationship with pavement cell morphogenesis.

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References

  • Abramoff MD, Magelhaes PJ, Ram SJ (2004) Image processing with ImageJ. Biophoton Int 11:36–42

    Google Scholar 

  • Akita K, Higaki T, Kutsuna N, Hasezawa S (2015) Quantitative analysis of microtubule orientation in interdigitated leaf pavement cells. Plant Signal Behav 10, e1024396

    Article  PubMed  PubMed Central  Google Scholar 

  • Ambrose C, DeBono A, Wasteneys G (2013) Cell geometry guides the dynamic targeting of apoplastic GPI-linked lipid transfer protein to cell wall elements and cell borders in Arabidopsis thaliana. PLoS One 8, e81215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • An Q, Ehlers K, Kogel KH, van Bel AJE, Hückelhoven R (2006a) Multivesicular compartments proliferate in susceptible and resistant MLA12-barley leaves in response to infection by the biotrophic powdery mildew fungus. New Phytol 172:563–576

    Article  CAS  PubMed  Google Scholar 

  • An Q, Hückelhoven R, Kogel KH, van Bel AJE (2006b) Multivesicular bodies participate in a cell wall associated defense response in barley leaves attacked by the pathogenic powdery mildew fungus. Cell Microbiol 8:1009–1019

    Article  CAS  PubMed  Google Scholar 

  • Armour WJ, Barton DA, Law AM, Overall RL (2015) Differential growth in periclinal and anticlinal walls during lobe formation in Arabidopsis cotyledon pavement cells. Plant Cell 27:2484–2500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boevink P, Oparka K, Cruz SS, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447

    Article  CAS  PubMed  Google Scholar 

  • Chardin P, McCormick F (1999) Brefeldin A: the advantage of being uncompetitive. Cell 97:153–155

    Article  CAS  PubMed  Google Scholar 

  • Chen J, Wang F, Zheng S, Xu T, Yang Z (2015) Pavement cells: a model for non-transcriptional auxin signaling and crosstalks. J Exp Bot 66:4957–4970

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Denzer K, Kleijmeer MJ, Heijnen HFG, Stoorvogel W, Geuze HJ (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113:3365–3374

    CAS  PubMed  Google Scholar 

  • Elsner J, Michalski M, Kwiatkowska D (2012) Spatiotemporal variation of leaf epidermal cell growth: a quantitative analysis of Arabidopsis thaliana wild-type and triple cyclinD3 mutant plants. Ann Bot 109:897–910

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Falbel TG, Koch LM, Nadeau JA, Segui-Simarro JM, Sack FD, Bednarek SY (2003) SCD1 is required for cell cytokinesis and polarized cell expansion in Arabidopsis thaliana. Development 130:4011–4024

    Article  CAS  PubMed  Google Scholar 

  • 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 12:849–853

    Article  CAS  PubMed  Google Scholar 

  • 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 130:753–762

    Article  CAS  PubMed  Google Scholar 

  • 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 14:777–794

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Xu T, Zhu L, Wen M, Yang Z (2009) A ROP GTPase signaling pathway controls cortical microtubule ordering and cell expansion in Arabidopsis. Curr Biol 19:1827–1832

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geitmann A, Ortega JK (2009) Mechanics and modeling of plant cell growth. Trends Plant Sci 14:467–478

    Article  CAS  PubMed  Google Scholar 

  • Grebe M, Xu J, Möbius W, Ueda T, Nakano A, Geuze HJ, Rook MB, Scheres B (2003) Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr Biol 13:1378–1387

    Article  CAS  PubMed  Google Scholar 

  • Hardham AR, Takemoto D, White RG (2008) Rapid and dynamic subcellular reorganization following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biol 8:63

    Article  PubMed  PubMed Central  Google Scholar 

  • Harding C, Heuser J, Stahl P (1983) Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 97:329–339

    Article  CAS  PubMed  Google Scholar 

  • Higaki T, Sano T, Hasezawa S (2007) Actin microfilament dynamics and actin side-binding proteins in plants. Curr Opin Plant Biol 10:549–556

    Article  CAS  PubMed  Google Scholar 

  • Higaki T, Kutsuna N, Hosokawa Y, Akita K, Ebine K, Ueda T, Kondo N, Hasezawa S (2012) Statistical organelle dissection of Arabidopsis guard cells using image database LIPS. Sci Rep 2:405

    Article  PubMed  PubMed Central  Google Scholar 

  • Higaki T, Kutsuna N, Hasezawa S (2013) LIPS database with LIPService: a microscopic image database of intracellular structures in Arabidopsis guard cells. BMC Plant Biol 13:81

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito E, Fujimoto M, Ebine K, Uemura T, Ueda T, Nakano A (2012a) Dynamic behavior of clathrin in Arabidopsis thaliana unveiled by live imaging. Plant J 69:204–216

    Article  CAS  PubMed  Google Scholar 

  • Ito Y, Uemura T, Shoda K, Fujimoto M, Ueda T, Nakano A (2012b) cis-Golgi proteins accumulate near the ER exit sites and act as the scaffold for Golgi regeneration after brefeldin A treatment in tobacco BY-2 cells. Mol Biol Cell 23:3203–3214

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacques E, Verbelen JP, Vissenberg K (2014) Review on shape formation in epidermal pavement cells of the Arabidopsis leaf. Funct Plant Biol 41:914–921

    Article  Google Scholar 

  • Jaillais Y, Fobis-Loisy I, Miège C, Gaude T (2008) Evidence for a sorting endosome in Arabidopsis root cells. Plant J 53:237–247

    Article  CAS  PubMed  Google Scholar 

  • Jones MA, Shen JJ, Fu Y, Li H, Yang Z, Grierson CS (2002) The Arabidopsis Rop2 GTPase is a positive regulator of both root hair initiation and tip growth. Plant Cell 14:763–776

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jung JY, Kim YW, Kwak JM, Hwang JU, Young J, Schroeder JI, Hwang I, Lee Y (2002) Phosphatidylinositol 3- and 4-phosphate are required for normal stomatal movements. Plant Cell 14:2399–2412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lancelle SA, Hepler PH (1992) Ultrastructure of freeze-substituted pollen tubes of Lilium longiflorum. Protoplasma 167:215–230

    Article  Google Scholar 

  • Latijnhouwers M, Hawes C, Carvalho C, Oparka K, Gillingham AK, Boevink P (2005) An Arabidopsis GRIP domain protein locates to the trans-Golgi and binds the small GTPase ARL1. Plant J 44:459–470

    Article  CAS  PubMed  Google Scholar 

  • 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 11:1731–1742

    CAS  PubMed  PubMed Central  Google Scholar 

  • Marchant R, Peat A, Banbury GH (1967) The ultrastructural basis of hyphal growth. New Phytol 66:623–629

    Article  Google Scholar 

  • McCloud TG, Burns MP, Majadly FD, Muschik GM, Miller DA, Poole KK, Roach JM, Ross JT, Lebherz WB 3rd (1995) Production of brefeldin-A. J Ind Microbiol 15:5–9

    Article  CAS  PubMed  Google Scholar 

  • McMichael CM, Reynolds GD, Koch LM, Wang C, Jiang N, Nadeau J, Sack FD, Gelderman MB, Pan J, Bednarek SY (2013) Mediation of clathrin-dependent trafficking during cytokinesis and cell expansion by Arabidopsis stomatal cytokinesis defective proteins. Plant Cell 25:3910–3925

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Naito S, Hirai MY, Chino M, Komeda Y (1994) Expression of a soybean (Glycine max [L.] Merr.) seed storage protein gene in transgenic Arabidopsis thaliana and its response to nutritional stress and to abscisic acid mutations. Plant Physiol 104:497–503

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Negi J, Moriwaki K, Konishi M, Yokoyama R, Nakano T, Kusumi K, Hashimoto-Sugimoto M, Schroeder JI, Nishitani K, Yanagisawa S, Iba K (2013) A Dof transcription factor, SCAP1, is essential for the development of functional stomata in Arabidopsis. Curr Biol 23:479–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishitani K, Tominaga R (1991) In vitro molecular weight increase in xyloglucans by an apoplastic enzyme preparation from epicotyls of Vigna angularis. Physiol Plant 82:490–497

    Article  CAS  Google Scholar 

  • Panteris E, Galatis B (2005) The morphogenesis of lobed plant cells in the mesophyll and epidermis: organization and distinct roles of cortical microtubules and actin filaments. New Phytol 167:721–732

    Article  CAS  PubMed  Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1993) Microtubules and morphogenesis in ordinary epidermal cells of Vigna sinensis leaves. Protoplasma 174:91–100

    Article  Google Scholar 

  • Panteris E, Apostolakos P, Galatis B (1994) Sinuous ordinary epidermal cells: behind several patterns of waviness, a common morphogenetic mechanism. New Phytol 127:771–780

    Article  Google Scholar 

  • Parton RM, Fischer-Parton S, Watahiki MK, Trewavas AJ (2001) Dynamics of the apical vesicle accumulation and the rate of growth are related in individual pollen tubes. J Cell Sci 114:2685–2695

    CAS  PubMed  Google Scholar 

  • Parton RM, Fischer-Parton S, Trewavas AJ, Watahiki MK (2003) Pollen tubes exhibit regular periodic membrane trafficking events in the absence of apical extension. J Cell Sci 116:2707–2719

    Article  CAS  PubMed  Google Scholar 

  • Qiu JL, Jilk R, Marks MD, Szymanski DB (2002) The Arabidopsis SPIKE1 gene is required for normal cell shape control and tissue development. Plant Cell 14:101–118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robards AW, Kidwai P (1969) Vesicular involvement in differentiating plant vascular cells. New Phytol 68:343–349

    Article  Google Scholar 

  • Robatzek S, Chinchilla D, Boller T (2006) Ligand-induced endocytosis of the pattern recognition receptor FLS2 in Arabidopsis. Genes Dev 20:537–542

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sampathkumar A, Krupinski P, Wightman R, Milani P, Berquand A, Boudaoud A, Hamant O, Jönsson H, Meyerowitz EM (2014) Subcellular and supracellular mechanical stress prescribes cytoskeleton behavior in Arabidopsis cotyledon pavement cells. eLife 3, e01967

    Article  PubMed  PubMed Central  Google Scholar 

  • Samuels AL, Giddings TH Jr, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 130:1345–1357

    Article  CAS  PubMed  Google Scholar 

  • Séveno M, Bardor M, Paccalet T, Gomord V, Lerouge P, Faye L (2004) Glycoprotein sialylation in plants? Nat Biotechnol 22:1351–1352

    Article  PubMed  Google Scholar 

  • Shah MM, Fujiyama K, Flynn CR, Joshi L (2003) Sialylated endogenous glycoconjugates in plant cells. Nat Biotechnol 21:1470–1471

    Article  CAS  PubMed  Google Scholar 

  • Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol 21:271–295

    Article  CAS  PubMed  Google Scholar 

  • Stefano G, Renna L, Moss T, McNew JA, Brandizzi F (2012) In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C-terminal domain of RHD3, a non-essential GTPase. Plant J 69:957–966

    Article  CAS  PubMed  Google Scholar 

  • Tanchak MA, Griffing LR, Mersey BG, Fowke LC (1984) Endocytosis of cationized ferritin by coated vesicles of soybean protoplasts. Planta 162:481–486

    Article  CAS  PubMed  Google Scholar 

  • Toyooka K, Sato M, Kutsuna N, Higaki T, Sawaki F, Wakazaki M, Goto Y, Hasezawa S, Nagata N, Matsuoka K (2014) Wide-range high-resolution transmission electron microscopy reveals morphological and distributional changes of endomembrane compartments during log to stationary transition of growth phase in tobacco BY-2 cells. Plant Cell Physiol 55:1544–1555

    Article  CAS  PubMed  Google Scholar 

  • Tse YC, Mo B, Hillmer S, Zhao M, Lo SW, Robinson DG, Jiang L (2004) Identification of multivesicular bodies as prevacuolar compartments in Nicotiana tabacum BY-2 cells. Plant Cell 16:672–693

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tse YC, Lo SW, Hillmer S, Dupree P, Jiang L (2006) Dynamic response of prevacuolar compartments to brefeldin A in plant cells. Plant Physiol 142:1442–1459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Uemura T, Kim H, Saito C, Ebine K, Ueda T, Schulze-Lefert P, Nakano A (2012) Qa-SNAREs localized to the trans-Golgi network regulate multiple transport pathways and extracellular disease resistance in plants. Proc Natl Acad Sci U S A 109:1784–1789

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang F, Shang Y, Fan B, Yu JQ, Chen Z (2014) Arabidopsis LIP5, a positive regulator of multivesicular body biogenesis, is a critical target of pathogen-responsive MAPK cascade in plant basal defense. PLoS Pathog 10, e1004243

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu T, Wen M, Nagawa S, Fu Y, Chen JG, Wu MJ, Perrot-Rechenmann C, Friml J, Jones AM, Yang Z (2010) Cell surface- and rho GTPase-based auxin signaling controls cellular interdigitation in Arabidopsis. Cell 143:99–110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang C, Halsey LE, Szymanski DB (2011) The development and geometry of shape change in Arabidopsis thaliana cotyledon pavement cells. BMC Plant Biol 11:27

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhao L, Sack FD (1999) Ultrastructure of stomatal development in Arabidopsis (Brassicaceae) leaves. Am J Bot 86:929–939

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank Dr. Mamiko Sato of the Japan Women’s University and Ms. Mayumi Wakazaki of the RIKEN Center for Sustainable Resource Sciences for microscopic observation. We thank Dr. Haruko Ueda and Prof. Ikuko Hara-Nishimura of Kyoto University for kind comments. This work was supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI to K.A. (26891006), N.K. (24770038), T.U. (24114003), K.T. (24687007 and 23657051), N.N. (23120526), S.H. (24114007 and 25291056), and T.H. (25711017).

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  1. Takashi Ueda

    Present address: Division of Cellular Dynamics, National Institute for Basic Biology, Nishigonaka 38, Myodaiji, Okazaki, Aichi, 444-8585, Japan

Authors and Affiliations

  1. Department of Integrated Biosciences, Graduate School of Frontier Sciences, The University of Tokyo, Kashiwanoha, Kashiwa, Chiba, 277-8562, Japan

    Kae Akita, Natsumaro Kutsuna, Seiichiro Hasezawa & Takumi Higaki

  2. Faculty of Science, Japan Women’s University, Mejirodai, Bunkyo-ku, Tokyo, 112-8681, Japan

    Megumi Kobayashi & Noriko Nagata

  3. RIKEN Center for Sustainable Resource Sciences, 1-7-22, Suehiro-cho, Tsurumi-ku, Yokohama, Kanagawa, 230-0045, Japan

    Mayuko Sato & Kiminori Toyooka

  4. Research and Development Division, LPixel Inc., Bunkyo-ku, Tokyo, 150-0002, Japan

    Natsumaro Kutsuna

  5. Department of Biological Sciences, Graduate School of Science, The University of Tokyo, Bunkyo-ku, Tokyo, 113-0033, Japan

    Takashi Ueda

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  1. Kae Akita
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  2. Megumi Kobayashi
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Correspondence to Kae Akita.

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Akita, K., Kobayashi, M., Sato, M. et al. Cell wall accumulation of fluorescent proteins derived from a trans-Golgi cisternal membrane marker and paramural bodies in interdigitated Arabidopsis leaf epidermal cells. Protoplasma 254, 367–377 (2017). https://doi.org/10.1007/s00709-016-0955-1

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