Advertisement

Planta

, Volume 227, Issue 6, pp 1363–1375 | Cite as

Cortical microtubules mark the mucilage secretion domain of the plasma membrane in Arabidopsis seed coat cells

  • Heather E. McFarlane
  • Robin E. Young
  • Geoffrey O. Wasteneys
  • A. Lacey SamuelsEmail author
Original Article

Abstract

During their differentiation Arabidopsis thaliana seed coat cells undergo a brief but intense period of secretory activity that leads to dramatic morphological changes. Pectic mucilage is secreted to one domain of the plasma membrane and accumulates under the primary cell wall in a ring-shaped moat around an anticlinal cytoplasmic column. Using cryofixation/transmission electron microscopy and immunofluorescence, the cytoskeletal architecture of seed coat cells was explored, with emphasis on its organization, function and the large amount of pectin secretion at 7 days post-anthesis. The specific domain of the plasma membrane where mucilage secretion is targeted was lined by abundant cortical microtubules while the rest of the cortical cytoplasm contained few microtubules. Actin microfilaments, in contrast, were evenly distributed around the cell. Disruption of the microtubules in the temperature-sensitive mor1-1 mutant affected the eventual release of mucilage from mature seeds but did not appear to alter the targeted secretion of vesicles to the mucilage pocket, the shape of seed coat cells or their secondary cell wall deposition. The concentration of cortical microtubules at the site of high vesicle secretion in the seed coat may utilize the same mechanisms required for the formation of preprophase bands or the bands of microtubules associated with spiral secondary cell wall thickening during protoxylem development.

Keywords

Arabidopsis thaliana Cortical microtubules mor1-1 Pectin Secretion Seed coat 

Abbreviation

DPA

Days post-anthesis

Notes

Acknowledgments

The authors acknowledge the technical support of the UBC Bioimaging Facility, Eiko Kawamura and Miki Fujuta. CCRC-M36 antibodies were the kind gift of Michael Hahn at the Complex Carbohydrate Research Center, Athens, GA, USA. Tamara Western and Colin McLeod provided constructive comments on the manuscript. Funding, in the form of Canadian Natural Sciences and Engineering Research Council (NSERC) Discovery Grants to A.L. Samuels and G.O. Wasteneys and a summer NSERC USRA to H.E. McFarlane, is gratefully acknowledged.

References

  1. Asada T, Kuriyama R, Shibaoka H (1997) TKRP125, a kinesin-related protein involved in the centrosome-independent organization of the cytokinetic apparatus in tobacco BY-2 cells. J Cell Sci 110:179–189PubMedGoogle Scholar
  2. Boevink P, Oparka K, Santa Cruz S, Martin B, Betteridge A, Hawes C (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant J 15:441–447PubMedCrossRefGoogle Scholar
  3. Caspar T, Huber SC, Somerville C (1985) Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity. Plant Physiol 79:11–17PubMedGoogle Scholar
  4. Collings DW, Wasteneys GO (2005) Actin microfilament and microtubule distribution patterns in the expanding root of Arabidopsis thaliana. Can J Bot 83:579–590CrossRefGoogle Scholar
  5. Donohoe BS, Movelsvang S, Staehelin LA (2006) Electron tomography of ER, Golgi and related membrane systems. Methods 39:154–162PubMedCrossRefGoogle Scholar
  6. Fukuda H (1997) Tracheary element differentiation. Plant Cell 9:1147–1156PubMedCrossRefGoogle Scholar
  7. Kawamura E, Himmelspach R, Rashbrooke MC, Whittington AT, Gale KR, Collings DA, Wasteneys GO (2006) MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis Root. Plant Physiol 140:102–114PubMedCrossRefGoogle Scholar
  8. Hawes C, Saint-Jore C, Brandizzi F (2003) Endomembrane and cytoskeleton interrelationships in higher plants. In: Robinson D (ed) The Golgi apparatus and the plant secretory pathway. Blackwell Publishers, Oxford, pp 63–75Google Scholar
  9. Himmelspach R, Williamson RE, Wasteneys GO (2003) Cellulose microfibril alignment recovers from DCB-induced disruption despite microtubule disorganization. Plant J 36:565–575PubMedCrossRefGoogle Scholar
  10. Komis G, Apostolakos P, Galatis B (2001) Altered patterns of tubulin polymerization in dividing leaf cells of Chlorophyton comosum after a hyperosmotic treatment. New Phytol 149:193–205CrossRefGoogle Scholar
  11. Kremer JR, Mastronarde DN, McIntosh JR (1996) Computer visualization of three-dimensional image data using IMOD. J Struct Biol 116:71–76PubMedCrossRefGoogle Scholar
  12. Mastronarde DN (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120:343–352PubMedCrossRefGoogle Scholar
  13. McIntosh JR, Euteneuer U (1984) Tubulin hooks as probes for microtubule polarity: an analysis of the method and an evaluation of data on microtubule polarity in the mitotic spindle. J Cell Biol 98:525–533PubMedCrossRefGoogle Scholar
  14. Meagher RB, Williamson R (1994) The plant cytoskeleton. In: Meyerowitz E, Somerville CR (eds) Arabidopsis. Cold Spring Harbor Laboratory Press, Plainview, pp 1049–1084Google Scholar
  15. Mineyuki Y (1999) The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. Int Rev Cytol 187:1–49Google Scholar
  16. Moore PJ, Swords KM, Lynch MA, Staehelin LA (1991) Spatial organization of the assembly pathways of glycoproteins and complex polysaccharides in the Golgi apparatus of plants. J Cell Biol 112:589–602PubMedCrossRefGoogle Scholar
  17. Nebenfuhr A, Gallagher LA, Dunahay TG, Frohlick JA, Mazurkiewicz AM, Meehl JB, Staehelin LA (1999) Stop-and-go movements of plant golgi stacks are mediated by the acto-myosin system. Plant Physiol 121:1127–1142PubMedCrossRefGoogle Scholar
  18. Penfield S, Meissner RC, Shoue DA, Carpita NC, Bevan MW (2001) MYB61 is required for mucilage deposition and extrusion in the Arabidopsis seed coat. Plant Cell 13:2777–2791PubMedCrossRefGoogle Scholar
  19. Roberts AW, Frost AO, Roberts EM, Haigler CH (2004) Roles of microtubules and cellulose microfibril assembly in the localization of secondary-cell-wall deposition in developing tracheary elements. Protoplasma 224:217–229PubMedCrossRefGoogle Scholar
  20. Scheller HV, Jensen JK, Sorensen SO, Harholt J, Geshi N (2007) Biosynthesis of pectin. Physiol Plant 129:283–295CrossRefGoogle Scholar
  21. Shannon T, Steer MW (1984) The root cap as a test system for the evaluation of Golgi inhibitors. I. Structure and dynamics of the secretory system and response to solvents. J Exp Bot 35:1697–1707CrossRefGoogle Scholar
  22. Smith LG, Oppenheimer DG (2005) Spatial control of cell expansion by the plant cytoskeleton. Annu Rev Cell Dev Biol 21:271–295PubMedCrossRefGoogle Scholar
  23. Sugimoto K, Himmelspach R, Williamson RE, Wasteneys GO (2003) Mutation or drug-dependant microtubule disruption causes radial swelling without altering parallel cellulose microfibril deposition in Arabidopsis root cells. Plant Cell 15:1414–1429PubMedCrossRefGoogle Scholar
  24. Thiel G, Battey N (1998) Exocytosis in plants. Plant Mol Biol 38:111–125PubMedCrossRefGoogle Scholar
  25. Vaughan JG, Whitehouse JM (1971) Seed structure and taxonomy of the Cruciferae. Bot J Linn Soc 64:383–409CrossRefGoogle Scholar
  26. Wasteneys GO (2002) Microtubule organization in the green kingdom: chaos or self-order? J Cell Sci 115:1345–1354PubMedGoogle Scholar
  27. Wasteneys GO (2004) Progress in understanding the role of microtubules in plant cells. Curr Opin Plant Biol 7:651–660PubMedCrossRefGoogle Scholar
  28. Wasteneys G, Fujita M (2006) Establishing and maintaining axial growth: wall mechanical properties and the cytoskeleton. J Plant Res 119:5–10PubMedCrossRefGoogle Scholar
  29. Western TL (2006) Changing spaces: the Arabidopsis mucilage secretory cells as a novel system to dissect cell wall production in differentiating cells. Can J Bot 84:622–630CrossRefGoogle Scholar
  30. Western TL, Skinner DJ, Haughn GW (2000) Differentiation of mucilage secretory cells of the Arabidopsis seed coat. Plant Physiol 122:345–356PubMedCrossRefGoogle Scholar
  31. Western TL, Burn J, Tan WL, Skinner DJ, Martin-McCaffrey L, Moffatt BA, Haughn GW (2001) Isolation and characterization of mutants defective in seed coat mucilage secretory cell development in Arabidopsis. Plant Physiol 127:998–1011PubMedCrossRefGoogle Scholar
  32. Western TL, Young DS, Dean GH, Tan WL, Samuels AL, Haughn GW (2004) MUCILAGE-MODIFIED4 encodes a putative pectin biosynthetic enzyme developmentally regulated by APETALA2, TRANSPARENT TESTA GLABRA1, and GLABRA2 in the Arabidopsis seed coat. Plant Physiol 134:296–306PubMedCrossRefGoogle Scholar
  33. Whittington AT, Vugrek O, Wei KJ, Hasenbein NG, Sugimoto K, Rashbrooke MC, Wasteneys GO (2001) MOR1 is essential for organizing cortical microtubules in plants. Nature 411:610–613PubMedCrossRefGoogle Scholar
  34. Windsor JB, Symonds VV, Mendenhall J, Lloyd AM (2000) Arabidopsis seed coat development: morphology and differentiation of the outer integument. Plant J 22:483–493PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Heather E. McFarlane
    • 1
  • Robin E. Young
    • 1
  • Geoffrey O. Wasteneys
    • 1
  • A. Lacey Samuels
    • 1
    Email author
  1. 1.Department of BotanyUniversity of British ColumbiaVancouverCanada

Personalised recommendations