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Planta

, Volume 218, Issue 2, pp 204–216 | Cite as

The association of peroxisomes with the developing cell plate in dividing onion root cells depends on actin microfilaments and myosin

  • David A. CollingsEmail author
  • John D. I. Harper
  • Kevin C. Vaughn
Original Article

Abstract

We have investigated changes in the distribution of peroxisomes through the cell cycle in onion (Allium cepa L.) root meristem cells with immunofluorescence and electron microscopy, and in leek (Allium porrum L.) epidermal cells with immunofluorescence and peroxisomal-targeted green fluorescent protein. During interphase and mitosis, peroxisomes distribute randomly throughout the cytoplasm, but beginning late in anaphase, they accumulate at the division plane. Initially, peroxisomes occur within the microtubule phragmoplast in two zones on either side of the developing cell plate. However, as the phragmoplast expands outwards to form an annulus, peroxisomes redistribute into a ring immediately inside the location of the microtubules. Peroxisome aggregation depends on actin microfilaments and myosin. Peroxisomes first accumulate in the division plane prior to the formation of the microtubule phragmoplast, and throughout cytokinesis, always co-localise with microfilaments. Microfilament-disrupting drugs (cytochalasin and latrunculin), and a putative inhibitor of myosin (2,3-butanedione monoxime), inhibit aggregation. We propose that aggregated peroxisomes function in the formation of the cell plate, either by regulating hydrogen peroxide production within the developing cell plate, or by their involvement in recycling of excess membranes from secretory vesicles via the β-oxidation pathway. Differences in aggregation, a phenomenon which occurs in onion, some other monocots and to a lesser extent in tobacco BY-2 suspension cells, but which is not obvious in the roots of Arabidopsis thaliana (L.) Heynh., may reflect differences within the primary cell walls of these plants.

Keywords

Actin microfilaments Allium Microtubule Cell plate Peroxisome Phragmoplast 

Abbreviations

BDM

2,3-butanedione monoxime

DAPI

4′,6-diamidino-2-phenylindole

ER

endoplasmic reticulum

GFP

green fluorescent protein

Notes

Acknowledgements

We thank the following people for discussions and encouragement: Brian Gunning and Geoff Wasteneys (ANU), Peter Ryan and Rosemary White (CSIRO Division of Plant Industry), Robert Mullen (University of Guelph), Dick Trelease (Arizona State University) and Robyn Overall and Jan Marc (Sydney University). We also wish to thank Spencer Whitney and Grant Pearce (ANU) for assistance with the particle bombardment gun, Lynn Libous-Bailey for technical assistance, and Ellie Kable (Electron Microscopy Unit, Sydney University) and Daryl Webb (ANU) for assistance with confocal and two-photon microscopy. D.A.C. acknowledges the receipt of an ARC (Australian Research Council) Research Fellowship and Discovery Grant DP0208806, while J.D.I.H. acknowledges funding from the Farrer Centre at Charles Sturt University. Mention of a trademark, proprietary product or vendor does not constitute an endorsement by the USDA.

References

  1. 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 15:441–447PubMedGoogle Scholar
  2. Brown RC, Lemmon BE (1985) Preprophasic establishment of division polarity in monoplastid mitosis of hornworts. Protoplasma 124:175–183Google Scholar
  3. Brown RC, Lemmon BE (1990) Monoplastidic cell division in lower land plants. Am J Bot 77:559–571Google Scholar
  4. Brownleader MD, Hopkins J, Mobasheri A, Dey PM, Jackson P, Trevan M (2000) Role of extensin peroxidase in tomato (Lycopersicon esculentum Mill.) seedling growth. Planta 210:668–676PubMedGoogle Scholar
  5. Busby CH, Gunning BES (1988) Establishment of plastid-based quadripolarity in spore mother cells of the moss Funaria hygrometrica. J Cell Sci 91:117–126Google Scholar
  6. Collings DA, Asada T, Allen NS, Shibaoka H (1998) Plasma membrane-associated actin in Bright Yellow 2 tobacco cells: evidence for interaction with microtubules. Plant Physiol 118:917–928PubMedGoogle Scholar
  7. Collings DA, Harper JDI, Marc J, Overall RL, Mullen RT (2002) Life in the fast lane: actin-based motility of plant peroxisomes. Can J Bot 80:430–441Google Scholar
  8. Cooper JB, Varner JE (1984) Crosslinking of soluble extensin in isolated cell walls. Plant Physiol 76:414–417Google Scholar
  9. Cutler SR, Ehrhardt DW, Griffitts JS, Somerville CR (2000) Random GFP::cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97:3718–3723PubMedGoogle Scholar
  10. Gerhardt B (1986) Basic metabolic function of the higher plant peroxisome. Physiol Veg 24:397–410Google Scholar
  11. Gerhardt B (1992) Fatty acid degradation in plants. Prog Lipid Res 31:417–446PubMedGoogle Scholar
  12. Giménez-Abián MI, Utrilla L, Cánovas JL, Giménez-Martin G, Navarrete MH, De La Torre C (1998) The positional control of mitosis and cytokinesis in higher-plant cells. Planta 204:37–43PubMedGoogle Scholar
  13. Hanzely L, Vigil EL (1975) Fine structural and cytochemical analysis of phragmosomes (microbodies) during cytokinesis in Allium root tip cells. Protoplasma 86:269–277Google Scholar
  14. Hu J, Aguirre M, Peot C, Alonso J, Ecker J, Chory J (2002) A role for peroxisomes in photomorphogenesis and development of Arabidopsis. Science 297:405–409PubMedGoogle Scholar
  15. Huang AHC, Trelease RN, Moore TS Jr (1983) Plant peroxisomes. Academic Press, New YorkGoogle Scholar
  16. Jedd G, Chua N-H (2002) Visualization of peroxisomes in living plant cells reveals acto-myosin-dependent cytoplasmic streaming and peroxisome budding. Plant Cell Physiol 43:384–392PubMedGoogle Scholar
  17. Kakimoto T, Shibaoka H (1988) Cytoskeletal ultrastructure of phragmoplast-nuclei complexes isolated from cultured tobacco cells. Protoplasma [Suppl] 2:95–103Google Scholar
  18. Liu B, Palevitz BA (1992) Organization of cortical microfilaments in dividing root cells. Cell Motil Cytoskel 23:252–264Google Scholar
  19. Mano S, Nakamori C, Hayashi M, Kato A, Kondo M, Nishimura M (2002) Distribution and characterization of peroxisomes in Arabidopsis by visualization with GFP: dynamic morphology and actin-dependent movement. Plant Cell Physiol 43:331–341PubMedGoogle Scholar
  20. Mathur J, Mathur N, Hülskamp M (2002) Simultaneous visualization of peroxisomes and cytoskeletal elements reveals actin and not microtubule-based peroxisome motility in plants. Plant Physiol 128:1031–1045PubMedGoogle Scholar
  21. McCurdy DW, Palevitz BA, Gunning BES (1991) Effect of cytochalasins on actin in dividing root tip cells of Allium and Triticum: a comparative immunocytochemical study. Cell Motil Cytoskel 18:107–112Google Scholar
  22. Miyagishima S, Takahara M, Kuroiwa T (2001) Novel filaments 5 nm in diameter constitute the cytosolic ring of the plastid division apparatus. Plant Cell 13:707–721PubMedGoogle Scholar
  23. Molchan TM, Valster AH, Hepler PK (2002) Actomyosin promotes cell plate alignment and late lateral expansion in Tradescantia stamen hair cells. Planta 214:683–693PubMedGoogle Scholar
  24. Mullen RT, Flynn CR, Trelease RN (2001) How are peroxisomes formed? The role of the endoplasmic reticulum and peroxins. Trends Plant Sci 6:256–261PubMedGoogle Scholar
  25. Nebenführ A, Frohlick JA, Staehelin LA (2000) Redistribution of Golgi stacks and other organelles during mitosis and cytokinesis in plant cells. Plant Physiol 124:135–151PubMedGoogle Scholar
  26. Ostap EM (2002) 2,3-butanedione monoxime (BDM) as a myosin inhibitor. J Musc Res Cell Motil 23:305–308Google Scholar
  27. Otegui M, Staehelin LA (2000) Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 3:493–502Google Scholar
  28. Otegui MS, Mastronarde DN, Kang B-H, Bednarek SY, Staehelin LA (2001) Three-dimensional analysis of syncitial-type cell plates during endosperm cellularization visualized by high resolution electron tomography. Plant Cell 13:2033–2051PubMedGoogle Scholar
  29. Palevitz BA, Hepler PK (1974) The control of the plane of division during stomatal differentiation in Allium. Chromosoma 46:327–341Google Scholar
  30. Parke J, Miller C, Anderton BH (1986) Higher plant myosin heavy-chain identified using a monoclonal antibody. Eur J Cell Biol 41:9–13Google Scholar
  31. Pickett-Heaps JD (1972) Cell division in Klebsormidium subtilissimum (formerly Ulothrix subtilissima), and its possible phylogenetic significance. Cytobios 6:167–183PubMedGoogle Scholar
  32. Porter KR, Machado RD (1960) Studies on the endoplasmic reticulum. IV. Its form and distribution during mitosis in cells of onion root tips. J Biophys Biochem Cytol 7:167–180Google Scholar
  33. Potikha TS, Collins CC, Johnson DI, Delmer DP, Levine A (1999) The involvement of hydrogen peroxide in the differentiation of secondary walls in cotton fibers. Plant Physiol 119:849–858PubMedGoogle Scholar
  34. Reumann S (2002) The photorespiratory pathway of leaf peroxisomes. In: Baker A, Graham IA (eds) Plant peroxisomes. Biochemistry, cell biology and biotechnology applications. Kluwer, Dordrecht, pp 141–189Google Scholar
  35. Samuels AL, Giddings TH Jr, Staehelin LA (1995) Cytokinesis in tobacco BY-2 and root tip cells: new model of cell plate formation in higher plant cells. J Cell Biol 130:1345–1347PubMedGoogle Scholar
  36. Schmit A-C (2000) Actin during mitosis and cytokinesis. In: Staiger CJ, Baluška F, Volkmann D, Barlow PW (eds) Actin: a dynamic framework for multiple plant cell functions. Kluwer, Dordrecht, pp 437–456Google Scholar
  37. Schopfer P (1996) Hydrogen peroxide-mediated cell-wall stiffening in vitro in maize coleoptiles. Planta 199:43–49Google Scholar
  38. Valster AH, Hepler PK (1997) Caffeine inhibition of cytokinesis: effect on the phragmoplast cytoskeleton in living Tradescantia stamen hair cells. Protoplasma 196:155–166Google Scholar
  39. van Breusegem F, Vranová E, Dat JF, Inzé D (2001) The role of reactive oxygen species in plant signal transduction. Plant Sci 161:405–414CrossRefGoogle Scholar
  40. Vaughn KC, Hoffman JC, Hahn MG, Staehelin LA (1996) The herbicide dichlobenil disrupts cell plate formation: immunogold characterization. Protoplasma 194:117–132Google Scholar
  41. Warren G, Wickner W (1996) Organelle inheritance. Cell 84:395–400PubMedGoogle Scholar
  42. Yamamoto K, Hamada S, Kashiyama T (1999) Myosins from plants. Cell Mol Life Sci 56:227–232PubMedGoogle Scholar
  43. Yasuhara H, Shibaoka H (2000) Inhibition of cell-plate formation by brefeldin A inhibited the depolymerization of microtubules in the central region of the phragmoplast. Plant Cell Physiol 41:300–310PubMedGoogle Scholar
  44. Zhang D, Wadsworth P, Hepler PK (1993) Dynamics of microfilaments are similar, but distinct from microtubules during cytokinesis in living, dividing plant cells. Cell Motil Cytoskel 24:151–155Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • David A. Collings
    • 1
    • 2
    Email author
  • John D. I. Harper
    • 3
  • Kevin C. Vaughn
    • 4
  1. 1.Plant Cell Biology Group, Research School of Biological SciencesAustralian National UniversityCanberraAustralia
  2. 2.School of Biological SciencesSydney UniversityAustralia
  3. 3.Farrer Centre, School of AgricultureCharles Sturt UniversityWagga WaggaAustralia
  4. 4.Southern Weed Science Research UnitUSDA–ARSStonevilleUSA

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