Summary
Cytoplasmic structure and rates of cyclosis in trichomes from chilling-sensitive watermelon (Citrullus vulgaris L.), tomato (Lycopersicon esculentum Mill.) andEpiscia reptans plants and from chilling-resistant foxglove (Digitalis purpurea) andVeronica persica were examined with differential interference contrast optics (DIC) as the temperature of the microscope stage was lowered. Below the chilling threshold, the rate of streaming in chilling-sensitive species fell markedly. At chilling temperatures the complex network of transvacuolar strands in the cytoplasm disappeared and the cytoplasm became vesiculated. During rewarming of the chilled cells, the vesicles fused into pleiomorphic blebs, which gradually stretched out into fully functional strands. These events were not seen during the chilling and rewarming of chilling-resistant plant cells.
Similar inhibition of cyclosis and changes in cytoplasmic structure were observed in cells from all species studied when they were treated with the actin inhibitor, cytochalasin B, or with uncoupling agents. Phalloidin had no detectable effect. Cyclosis in colchicine-, nocodazole-, trifluralin- and IPC-treated cells was not affected for many hours and did not cause the structural changes seen with chilling. The possible role of actin in these low-temperature effects on cytoplasmic structure and function is discussed.
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References
Allen, N. S., Allen, R. D., 1978 a: Cytoplasmic streaming in green plants. Ann. Rev. Biophys. Bioeng.7, 497–526.
— —, 1978 b: Cytoplasmic streaming in amoeboid movement. Ann. Rev. Biophys. Bioeng.7, 469–495.
Bartels, P. G., Hilton, J. L., 1973: Comparison of trifluralin, oryzalin, promamide, prophan and colchicine on microtubules. Pest. Bioch. Physiol.3, 462–472.
Breidenbach, R. W., Waring, A. J., 1977: Response to chilling of tomato seedlings and cells in suspension cultures. Plant Physiol.60, 190–192.
Brown, S. S., Spudich, J. A., 1981: Mechanism of action of cytochalasin B: evidence that it binds to actin filament ends. J. Cell Biol.88, 487–491.
—,Yamamoto, K., Spudich, J. A., 1982: A 40,000 d-protein fromDictyostelium discoideum affects assembly properties of actin in a Ca+-dependent manner. J. Cell Biol.93, 203–210.
Condeelis, J., 1981: Microfilament-membrane interaction in cell shape and surface architecture. Int. Cell Biol. (Schweiger, H., ed.), pp. 306–320. Berlin-Heidelberg-New York: Springer.
Condeelis, J. S., 1974: The identification of F-actin in the pollen tube and protoplast ofAmaryllis belladonna. Expt. Cell Res.88, 435–439.
Danker, P., Low, I., 1979: Complex influence of cytochalasin B on actin polymerization. Z. Naturforsch.34, 555–557.
Das, T. M., Hildebrandt, A. C., Riker, A. J., 1966: Cinephotomicrography of low temperature effects on cytoplasmic streaming, nucleolar activity and mitosis in single tobacco cells in microculture. Amer. J. Bot.53, 253–259.
Fulton, A. C., 1982: The crowded cytoplasm. Cell30, 345–347.
Gotz von Olenhusen, K.,Wohlfarth-Botterman, K. E., Evidence for actin transformation during the contraction/relaxation cycle cytoplasmic actomyosin: cycle blockade by phalloidin injection. Cell Tiss. Res.196, 455–470.
Graham, D., Patterson, B. D., 1982: Responses of plants to low, non-freezing temperatures: proteins, metabolism and acclimation. Ann. Rev. Plant Physiol.33, 347–372.
Hasegawa, T., Takahashi, S., Hayashi, H., Hatano, S., 1980: Ca++-sensitive regulatory factor on the formation of actin filaments. Biochem.19, 2677–2683.
Hepler, P. K., Palevitz, B. A., 1974: Microtubules and microfilaments. Ann. Rev. Plant Physiol.25, 309–362.
Hinssen, J., 1981 a: An actin modulating protein inPhysarum polycephalum. I. Isolation and purification. Eur. J. Cell Biol.23, 225–233.
—, 1981 b: An actin modulating protein ofPhysarum polycephalum. II. Ca++-dependence and other properties. Eur. J. Cell Biol.23, 234–240.
Ilker, R. A., Breidenbach, R. W., Murphy, T. M., 1979: Partial purification of actin from wheatgerm. Phytochem.18, 1781–1783.
Kamiya, N., 1981: Physical and chemical basis of cytoplasmic streaming. Ann. Rev. Plant Physiol.32, 205–236.
—,Yoshimoto, Y., Matsumura, F., 1981: Physiological aspects of actomyosin based cell motility. Int. Cell Biol. 1980/81 (Schweiger, H. G., ed.), pp. 346–358. Berlin-Heidelberg-New York: Springer.
Lee, J. C., Field, D. J., Lee, L. L. Y., 1980: Effect of nocodazole on structures of calf brain tubulin. Biochem.19, 6209–6215.
Lewis, D. A., 1956: Protoplasmic streaming in plants sensitive and insensitive to chilling temperatures. Sci.124, 75–76.
Lyons, J. M., 1973: Chilling injury in plants. Ann. Rev. Plant Physiol.24, 455–466.
—,Graham, D., Raison, J. K., 1979: Low temperature stress in crop plants: the role of the membrane, 565 pp. London-New York: Academic Press.
Mersey, B., McCully, M. E., 1978: Monitoring the course of fixation of plant cells. J. Microscopy114, 49–76.
Palevitz, B. A., 1980: Comparative effects of phalloidin and cytochalasin B on motility and morphology inAllium. Can. J. Bot.58, 773–785.
—,Hepler, P. K., 1975: Identification of actinin situ at the ectoplasm/endoplasm interface ofNitella. J. Cell Biol.65, 29–38.
Patterson, B. D., Graham, D., 1977: Effect of chilling temperatures on the protoplasmic streaming of plants from different climates. J. exp. Bot.28, 736–743.
— —,Paull, R., 1979: Adaptation to chilling: survival, germination, respiration and protoplasmic streaming. In: Low temperature stress in crop plants (Lyons, J. M., Graham, D., Raison, J. K., eds.), pp. 25–35. London: Academic Press.
Sachs, J. von, 1864: Über die obere Temperaturgrenze der Vegetation. Flora47, 65–75.
Scarpa, A.,Carafoli, E., 1978: Calcium transport and cell function. N. Y. Acad. Sci.307, 655 pp.
Schliwa, M., 1982: Action of cytochalasin D on cytoskeletal networks. J. Cell Biol.92, 79–91.
Stebbins, H.,Hyams, J. S., 1979: Cell motility, 192pp. Longman.
Taylor, D. L., Condeelis, J. S., Moore, P. L., Allen, R. D., 1973: The contractile basis of amoeboid movement. I. The chemical control of motility in isolated cytoplasm. J. Cell Biol.59, 378–394.
— —, 1979: Cytoplasmic structure and contraction in amoeboid cells. Int. Rev. Cytol.56, 57–144.
Vahey, M., Scordelis, S. P., 1980: Contractile proteins from tomato. Can. J. Bot.58, 797–801.
Wessels, N. K., Spooner, B. S., Bradley, M. O., Luduena, M. A., Taylor, E. L., Wrenn, J. T., Yamada, K. M., 1971: Microfilaments in cellular and developmental processes. Sci.171, 135–140.
Wieland, T., 1977: Modification of actin by phallotoxins. Naturwissenschaften64, 303–309.
Williamson, R. E., 1980: Actin in motile and other processes in plant cells. Can. J. Bot.58, 766–772.
Wolosewick, J. J., Porter, K. R., 1979: Microtrabecular lattice of the cytoplasmic ground substance. J. Cell Biol.82, 114–139.
Yin, H. L., Strossel, T. P., 1979: Control of cytoplasmic actin gelsol transformation by gelsolin, a Ca++-dependent regulatory protein. Nat.281, 583–586.
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Woods, C.M., Reid, M.S. & Patterson, B.D. Response to chilling stress in plant cells I. Changes in cyclosis and cytoplasmic structure. Protoplasma 121, 8–16 (1984). https://doi.org/10.1007/BF01279747
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DOI: https://doi.org/10.1007/BF01279747