Summary
The dynamics of actin distribution during stomatal complex formation in leaves of winter rye was examined by means of immunofluorescence microscopy of epidermal sheets. This method results in actin localization patterns that are the same as those seen with rhodamine-phalloidin staining, but are more stable. During stomatal development MFs are extensively rearranged, and most of the time the orientation or placement of MFs is distinctly different from that of MTs, the exception being co-localization of MTs and MFs in phragmoplasts. Although MFs show an orientation similar to that of MTs in interphase guard mother cells, no banding of MFs into anything resembling the interphase MT band is observed. From prophase to telophase, a distinct, dense concentration of MFs is found in subsidiary cell mother cells (SMCs) between the nucleus and the region of the cell cortex facing the guard mother cell. Cytochalasin B treatment causes incorrect positioning of the SMC nucleus/daughter nuclei and abarrent placement and orientation of the new cell wall that forms the boundary of the subsidiary cell at cytokinesis. These results suggest that MFs are involved in maintaining the SMC nucleus in its correct position and the SMC spindle in the correct orientation relative to the division site previously delineated by the preprophase band. Because these MFs thus appear to assure that the SMC phragmoplast begins to form in the correct orientation near the division site to which it needs to grow, we suggest that MFs are involved in control of correct placement and orientation of the new cell wall of the subsidiary cell.
Similar content being viewed by others
Abbreviations
- CB:
-
cytochalasin B
- DIC:
-
differential interference contrast
- DMSO:
-
dimethylsulfoxide
- MBS:
-
m-maleimidobenzoyl-N-hydroxylsuccinimide ester
- MF:
-
microfilament
- MT:
-
microtubule
- PBS:
-
phosphate buffered saline
- SMC:
-
subsidiary cell mother cell
References
Busby CH, Gunning BES (1980) Observations on preprophase bands of micro tubules in uniseriated hairs, stomatal complexes of sugar cane, andCyperus root meristems. Eur J Cell Biol 21: 214–223
Cho S-O, Wick SM (1989) Microtubule orientation during stomatal differentiation in grasses. J Cell Sci 92: 581–594
Cleary AL, Hardham AR (1989) Microtubule organization during development of stomatal complexes inLolium rigidum. Protoplasma 149: 67–81
Galatis B, Apostolakos P, Katsaros C (1983) Synchronous organization of two preprophase microtubule bands and final cell plate arrangement in subsidiary cell mother cells of someTriticum species. Protoplasma 117: 24–39
— — — (1984 a) Experimental studies on the function of the cortical cytoplasmic zone of the preprophase microtubule band. Protoplasma 122: 11–26
— — — (1984 b) Positional inconsistency between preprophase microtubule band and final cell plate arrangement during triangular subsidiary cell and atypical hair cell formation in twoTriticum species. Can J Bot 62: 343–359
Gunning BES, Wick SM (1985) Preprophase bands, phragmoplasts, and spatial control of cytokinesis. J Cell Sci [Suppl] 2: 157–179
Hensel W (1985) Cytochalasin B affects the structural polarity of statocytes from cress roots (Lepidium sativum L.). Protoplasma 129: 178–187
Hepler PK (1981) Morphogenesis of tracheary elements and guard cells. In: Kiermayer O (ed) Cytomorphogenesis in plants. Springer, Wien New York, pp 327–347 [Alfert M et al (eds) Cell biology monographs, vol 8]
Heslop-Harrison J, Heslop-Harrison Y (1989 a) Conformation and movement of the vegetative nucleus of the angiosperm pollen tube: association with the actin cytoskeleton. J Cell Sci 93: 299–308
— — (1989 b) Cytochalasin effects on structure and movement in the pollen tube ofIris. Sex Plant Reprod 2: 27–37
Kakimoto T, Shibaoka H (1987) Actin filaments and microtubules in the preprophase band and phragmoplast of tobacco cells. Protoplasma 140: 151–156
Katsuta J, Shibaoka H (1988) The roles of the cytoskeleton and the cell wall in nuclear positioning in tobacco BY-2 cells. Plant Cell Physiol 29: 403–413
Kobayashi H, Fukuda H, Shibaoka H (1988) Interrelation between the spatial disposition of actin filaments and microtubules during the differentiation of tracheary elements in culturedZinnia cells. Protoplasma 143: 29–37
Lancelle SA, Hepler PK (1988) Cytochalasin-induced ultrastructural alterations inNicotiana pollen tubes. Protoplasma [Suppl] 2: 65–75
Lessard JL (1988) Two monoclonal antibodies to actin: one muscle selective and one generally reactive. Cell Motil Cytoskeleton 10: 349–362
Lloyd CW (1986) Microtubules and the cellular morphogenesis of plants. In: Browder LW (ed) The cellular basis of morphogenesis. Plenum, New York, pp 31–57 (Developmental biology: a comprehensive synthesis, vol 2)
—, Pearce KJ, Rawlins DJ, Ridge RW, Shaw PJ (1987) Endoplasmic microtubules connect the advancing nucleus to the tip of legume root hairs, but F-actin is involved in basipetal migration. Cell Motil Cytoskeleton 8: 27–36
—, Traas JA (1988) The role of F-actin in determining the division plane of carrot suspension cells. Drug studies. Development 102: 211–221
McCurdy DW, Sammut M, Gunning BES (1988) Immunofluorescent visualization of arrays of transverse cortical actin microfilaments in wheat root-tip cells. Protoplasma 147: 204–206
Mullinax JB, Palevitz BA (1989) Microtubule reorganization accompanying preprophase band formation in guard mother cells ofAvena saliva L. Protoplasma 149: 89–94
Ôta T (1961) The role of cytoplasm in cytokinesis of plant cells. Cytologia 26: 428–447
Palevitz BA (1980) Comparative effects of phalloidin and cytochalasin B on motility and morphogenesis inAllium. Can J Bot 58: 773–785
— (1982) The stomatal complex as a model of cytoskeletal participation in cell differentiation. In: Lloyd CW (ed) The cytoskeleton in plant growth and development. Academic Press, London, pp 346–376
— (1986) Division plane determination in guard mother cells ofAllium: video time-lapse analysis of nuclear movements and phragmoplast rotation in the cortex. Dev Biol 117: 644–654
— (1988) Cytochalasin-induced reorganization of actin inAllium root cells. Cell Motil Cytoskeleton 9: 283–298
—, Hepler PK (1974) The control of the plane of division during stomatal differentiation inAllium. Chromosoma 46: 327–341
—, Mullinax JB (1989) Developmental changes in the arrangement of cortical microtubules in stomatal cells of oat (Avena sativa L.). Cell Motil Cytoskeleton 13: 170–180
Parthasarathy MV, Perdue TD, Witzum A, Alvernaz J (1985) Actin network as a normal component of the Cytoskeleton in many vascular plant cells. Amer J Bot 72: 1318–1323
Pesacreta TC, Carley WW, Webb WW, Parthasarathy MV (1982) F-actin in conifer roots. Proc Natl Acad Sci USA 79: 2898–2901
Pickett-Heaps JD (1969) Preprophase microtubules and stomatal differentiation; some effects of centrifugation on symmetrical and asymmetrical cell division. J Ultrastruct Res 27: 24–44
Schnepf E (1982) Morphogenesis in moss protonemata. In: Lloyd CW (ed) The Cytoskeleton in plant growth and development. Academic Press, London, pp 321–344
—, Quader H (1987) Functions of microtubules in plant cells. Fortsch Zool 34: 115–124
Seagull RW (1989) The plant Cytoskeleton. CRC Crit Rev Biol 8: 131–167
—, Falconer MM, Weerdenburg CA (1987) Microfilaments: dynamic arays in higher plant cells. J Cell Biol 104: 995–1004
Sonobe S, Shibaoka H (1989) Cortical fine actin filaments in higher plant cells visualized by rhodamine-phalloidin after pretreatment withm-maleimidobenzoyl N-hydroxysuccinimide ester. Protoplasma 148: 80–86
Staiger CJ, Schliwa M (1987) Actin localization and function in higher plants. Protoplasma 141: 1–12
Tang X, Lancelle SA, Hepler PK (1989) Fluorescence microscopic localization of actin in pollen tubes: comparison of actin antibody and phalloidin staining. Cell Motil Cytoskeleton 12: 216–224
Thomas DDS, Dunn DM, Seagull RW (1977) Rapid cytoplasmic responses of oat coleoptiles to cytochalasin B, auxin, and colchicine. Can J Bot 55: 1797–1800
Traas JA, Doonan JH, Rawlins DJ, Shaw PJ, Watts J, Lloyd CW (1987) An actin network is present in the cytoplasm throughout the cell cycle of carrot cells and associates with the dividing nucleus. J Cell Biol 105: 387–395
Author information
Authors and Affiliations
Additional information
Dedicated to the memory of Professor Oswald Kiermayer
Rights and permissions
About this article
Cite this article
Cho, SO., Wick, S.M. Distribution and function of actin in the developing stomatal complex of winter rye (Secale cereale cv. Puma). Protoplasma 157, 154–164 (1990). https://doi.org/10.1007/BF01322648
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01322648