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Microtubule organization in the differentiating transfer cells of the placenta inLilium spp.

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Summary

Placental cells in the ovarian transmitting tissue ofLilium spp. are organized as transfer cells with inbuddings facing the ovarian locule. A detailed analysis of microtubule (MT) organization during development of these polarized cells is reported here. Formation of wall projections occurs at the apical part of the cell starting on the day of anthesis, and a fully mature secretion zone is found four days after anthesis. MTs are organized into distinct cortical and central arrays. The cortical array undergoes a unique transition at anthesis. MTs in the basal half of the cell remain in longitudinal bundles while in the apical half of the cell their longitudinal orientation is replaced by a transverse alignment. One day after anthesis, these transverse bundles become a meshwork of short, randomly organized MTs, while MTs in the basal half of the cell retain their longitudinal alignment. The realignment of MTs in the apical half of the cell coincides with the deposition of the secondary cell wall. The central array is composed of short, randomly arranged strands of MTs in the cytoplasm between the nucleus and the apical and basal periclinal walls of the cell. This array first appears as solitary strands in the apical part of the cell one day before anthesis. The central array extends during development and is eventually seen in the basal half of the cell. We propose that MTs in the cortical region near the apical wall act as templates for the deposition of cellulose microfibrils in the secondary cell wall. MTs in the central array in these transfer cells may be involved in the trafficking of vesicles and/or positioning of organelles near the secretion zone.

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Abbreviations

MT:

microtubule

daa:

day after anthesis

dba:

day before anthesis

References

  • Briggs CL (1995) The initiation, development and removal of embryo sac wall ingrowths in the developing seeds ofSolanum nigrum L.: an ultrastructural study. Ann Bot 76: 429–439

    Google Scholar 

  • Bulbert MW, Offler CE, McCurdy DW (1998) Polarized microtubule deposition coincides with wall ingrowth formation in transfer cells ofVicia faba L. cotyledons. Protoplasma 201: 8–16

    Google Scholar 

  • Cass DD, Karas I (1974) Ultrastructural organization of the egg ofPlumbago zeylanica. Protoplasma 81: 49–62

    Google Scholar 

  • Cleary AL, Hardman AR (1989) Microtubule organization during development of stomatal complexes inLolium rigidum. Protoplasma 149: 67–81

    Google Scholar 

  • —, Gunning BES, Wasteneys GO, Hepler PK (1992) Microtubule and F-actin dynamics at the division site in livingTradescantia stamen hair cells. J Cell Sci 103: 977–988

    Google Scholar 

  • Cyr RJ (1994) Microtubules in plant morphogenesis: role of the cortical array. Annu Rev Cell Biol 10: 153–180

    Google Scholar 

  • Dashek WV, Thomas HR, Rosen WG (1971) Secretory cells of lily pistils II: electron microscope cytochemistry of canal cells. Am J Bot 58: 909–920

    Google Scholar 

  • Emons AMC, Kieft H (1994) Winding threads around plant cells: applications of the geometrical model for microfibril deposition. Protoplasma 180: 59–69

    Google Scholar 

  • —, Derkens J, Sassen MMA (1992) Do microtubules orient plant cell microfibrils? Physiol Plant 84: 486–493

    Google Scholar 

  • Falconer MM, Seagull RW (1986) Xylogenesis in tissue culture II: microtubules, cell shape and secondary wall patterns. Protoplasma 133: 140–148

    Google Scholar 

  • Fisher DD, Cyr RJ (1998) Extending the microtubule/microfibril paradigm: cellulose synthesis is required for normal cortical microtubule alignment in elongating cells. Plant Physiol 116: 1043–1051

    Google Scholar 

  • Fosket DE, Morejohn LC (1992) Structural and functional organization of tubulin. Annu Rev Plant Physiol Plant Mol Biol 43: 201–240

    Google Scholar 

  • Funada R, Abe H, Furusawa O, Imaizumi H, Fukazawa K, Ohtani J (1997) The orientation and localization of cortical microtubules in differentiating conifer tracheids during cell expansion. Plant Cell Physiol 38: 210–212

    Google Scholar 

  • Giddings TH, Staehelin LA (1988) Spatial relationship between microtubules and plasma membrane rosettes during the deposition of primary wall microfibrils inClosterium sp. Planta 173: 22–30

    Google Scholar 

  • Gunning BES, Hardham AR (1982) Microtubules. Annu Rev Plant Physiol 33: 651–698

    Google Scholar 

  • —, Pate JS (1969) “Transfer cells”: plant cells with wall ingrowths, specialization in relation to short distance transport of solutes - their occurrence, structure and development. Protoplasma 68: 107–133

    Google Scholar 

  • Hepler PK, Hush JM (1996) Behavior of microtubules in living plant cells. Plant Physiol 112: 455–461

    Google Scholar 

  • Hogetsu T (1991) Mechanism for formation of the secondary wall thickening in tracheary elements: microtubules and microfibrils of tracheary elements ofPisum sativum L. andCommelina communis and the effects of amiprophosmethyl. Planta 185: 190–200

    Google Scholar 

  • Huang B-Q, Russel SD (1994) Fertilization inNicotiana tabacum: cytoskeletal modifications in the embryo sac during synergid degeneration: a hypothesis for short-distance transport of sperm cells prior to gamete fusion. Planta 194: 200–214

    Google Scholar 

  • Janson J, Reinders MC, Valkering AGM, Van Tuly JM, Keijzer CJ (1994) Pistil exudate production and pollen tube growth inLilium longiflorum Thunb. Ann Bot 73: 437–446

    Google Scholar 

  • — —, Van Tuly JM, Keijzer CJ (1993) Pollen tube growth inLilium longiflorum following different pollination techniques and flower manipulation. Acta Bot Neerl 42: 461–472

    Google Scholar 

  • Kronestedt E, Walles B, Alkemar I (1986) Structural studies of pollen tube growth in the pistil ofStrelitzia reginae. Protoplasma 131: 224–232

    Google Scholar 

  • Li Y-Q, Moscatelli A, Cai G, Cresti M (1997) Functional interactions among cytoskeleton, membranes and cell wall in the pollen tube of flowering plants. Int Rev Cytol 176: 133–199

    Google Scholar 

  • Marc J, Mineyuki Y, Palevitz BA (1989) The generation and consolidation of a radial array of cortical microtubules in developing guard cells ofAllium cepa L. Planta 179: 516–529

    Google Scholar 

  • Mc Donald AR, Liu B, Joshi HC, Palevitz BA (1993) γ-Tubulin is associated with a cortical-microtubule-organizing zone in the developing guard cells ofAllium cepa L. Planta 191: 357–361

    Google Scholar 

  • Rosen WG, Thomas HR (1970) Secretory cells of lily pistils I: fine structure and function. Am J Bot 57: 1108–1114

    Google Scholar 

  • Singh S, Walles B (1992) The ovarian transmitting tissue inLilium regale. Int J Plant Sci 153: 205–211

    Google Scholar 

  • — — (1995) Ultrastructural differentiation of the ovarian transmitting tissue inLilium regale. Ann Bot 75: 455–462

    Google Scholar 

  • Tilton VR, Horner HT Jr (1980) Stigma, style and obturator ofOmithogalum caudatum (Liliaceae) and their function in the reproductive process. Am J Bot 67: 1113–1131

    Google Scholar 

  • Van Roggen PM, Keijzer CJ, Wilms HJ, Van Tuly JM, Stals AWDT (1988) An SEM study of pollen tube growth in intra- and interspecific crosses betweenLilium species. Bot Gaz 149: 365–369

    Google Scholar 

  • Welk M, Millington WF, Rosen WG (1965) Chemotropic activity and the pathway of the pollen in lily. Am J Bot 52: 774–781

    Google Scholar 

  • Williamson RE (1991) Orientation of cortical microtubules in inter-phase plant cells. Int Rev Cytol 129: 135–206

    Google Scholar 

  • — (1993) Organelle movements. Annu Rev Plant Physiol Plant Mol Biol 44: 181–202

    Google Scholar 

  • Wymer CL, Lloyd C (1996) Dynamic microtubules: implications for cell wall pattern. Trends Plant Sci 1: 222–228

    Google Scholar 

  • —, Fisher DD, Moore RC, Cyr RJ (1996) Elucidating the mechanism of cortical microtubule reorientation in plant cells. Cell Motil Cytoskeleton 35: 162–173

    Google Scholar 

  • Ye Xiu-Lin, Edward Y, Xu Shi-Xiong, Zee SY, Tong Sui-Hai, Tung Shiu-Hoi (1996) Confocal microscopic observations on microtubular cytoskeleton changes during megasporogenesis inPhaius tankervilliae (Alton) Bl. Acta Bot Sin 38: 667–685

    Google Scholar 

  • Yuan M, Warn RM, Shaw PJ, Lloyd CW (1995) Dynamic microtubules under the radial and outer tangential walls of microinjected pea epidermal cells observed by computer reconstruction. Plant J 7: 17–23

    Google Scholar 

  • Zhang DH, Wadsworth P, Hepler PK (1993) Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living, dividing plant cells. Cell Motil Cytoskeleton 24: 151–155

    Google Scholar 

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Correspondence to B. Walles.

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Singh, S., Lazzaro, M.D. & Walles, B. Microtubule organization in the differentiating transfer cells of the placenta inLilium spp.. Protoplasma 207, 75–83 (1999). https://doi.org/10.1007/BF01294715

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