Abstract
Fifty years ago, an important paper appeared in Botanical Magazine Tokyo. Kamiya and Kuroda proposed a sliding theory for the mechanism of cytoplasmic streaming. This pioneering study laid the basis for elucidation of the molecular mechanism of cytoplasmic streaming—the motive force is generated by the sliding of myosin XI associated with organelles along actin filaments, using the hydrolysis energy of ATP. The role of the actin–myosin system in various plant cell functions is becoming evident. The present article reviews progress in studies on cytoplasmic streaming over the past 50 years.
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References
Adams RJ, Pollard TD (1986) Nature 322:754–756
Albanesi JP, Fujisaki H, Hammer III JA, Korn ED, Jones R, Sheetz MP (1985) J Biol Chem 260:8649–8652
Allwood EG, Anthony RG, Smertenko AP, Reichelt S, Drobak BK Doonan JH, Weeds AG Hussey PJ (2002) Plant Cell 14:2915–2927
Awata J, Saitoh K, Shimada K, Kasiyama T, Yamamoto K (2001) Plant Cell Physiol 42:828–834
Awata J, Kashiyama T, Ito K, Yamamoto K (2003) J Mol Biol 326:659–663
Barry WH (1968) J Cell Physiol 72:153–160
Bradley MO (1973) J Cell Sci 12:327–343
Brewbaker JL, Kwack BH (1963) Am J Bot 50:859–868
Chen JCW, Kamiya N (1975) Cell Struct Funct 1:1–9
Chen JCW, Kamiya N (1981) Cell Struct Funct 6:201–207
Chen CY, Wong EI, Vidali L, Estavillo A, Hepler PK Wu H-M, Cheung AY (2002) Plant Cell 14:2175–2190
Chen CY-H, Cheung AY, Wu H-M (2003) Plant Cell 15:237–249
Collings DA, Wasteneys GO, Williamson RE (1996) Protoplasma 191:178–190
Corti B (1774) Osservazioni microscopiche sulla tremella e sulla circolazione del fluido in una pianta acquajuola. Lucca
Dong X-J, Nagai R, Takagi S (1998) Plant Cell Physiol 39:1299–1306
Doree M, Picard A (1980) Experientia 36:1291–1292
Ewart AJ (1903) On the physics and physiology of protoplasmic streaming in plants. Oxford
Fan X, Hou J, Chen X, Chaudhry F, Stainger CJ, Ren H (2004) Plant Physiol 136:3979–3989
Fehrenbacher KL, Boldogh IR, Pon LA (2003) Trends Cell Biol 13:472–477
Franke WW, Herth W, van der Woude WJ, Morre DJ (1972) Planta 105:317–341
Funaki K, Nagata A, Akimoto Y, Shimada K, Ito K, Yamamoto K (2004) Plant Cell Physiol 45:1342–1345
Gross P, Julius D, Schmelzer E, Hahlbrock K (1993) EMBO J 12:1735–1744
Gu Y, Vernoud V, Fu Y Yang Z (2003) J Exp Bot 54:93–101
Hamada S, Sekimoto H, Tanabe Y, Tsuchikane Y, Ito M (2006) J Plant Res 119:105–113
Harada A, Okazaki Y, Takagi S (2002a) Planta 214:863–869
Harada A, Fukuhara, Takagi S (2002b) Planta 214:870–876
Hashimoto K, Igarashi H, Mano S, Nishimura M, Shimmen T, Yokota E (2005) Plant Cell Physiol 46:782–789
Haupt W (1982) Ann Rev Plant Physiol 33:205–233
Hayama T, Shimmen T, Tazawa M (1979) Protoplasma 99:305–321
Hayama T, Tazawa M (1980) Protoplasma 102:1–9
Hayashi T, Harada A, Sakai T, Takagi S (2006) Plant Cell Environ 29:661–672
Hayashi T, Takagi S (2003) Plant Cell Physiol 44:1027–1036
Herth W (1978) Protoplasma 96:275–282
Hill SE (1941) Biol Bull 81:296
Holweg C, Nick P (2004) Proc Natl Acad Sci USA 101:10488–10493
Huang S, Blanchoin L, Chaudhry F, Franklin-Tong VE, Staiger CJ (2004) J Biol Chem 279:23364–23375
Huxley AF, Niedergerke R (1954) Nature 173:971–973
Huxley HE, Hanson J (1954) Nature 173:973–976
Ishigami M, Nagai R (1980) Cell Struct Funct 5:13–20
Ito K, Kashiyama T, Shimada K, Yamaguchi A, Awata J, Hachikubu Y, Manstein DJ, Yamamoto K (2003) Biochem Biophys Res Commun 312:958–964
Jedd G, Chua NH (2002) Plant Cell Physiol 43:384–392
Kachar B, Reese TS (1988) J Cell Biol 106:1545–1552
Kadota A, Sato Y, Wada M (2000) Planta 210:932–937
Kamitsubo E (1966) Proc Jpn Acad 42:640–643
Kamitsubo E (1972) Exp Cell Res 74:613–616
Kamitsubo E (1981) Protoplasma 109:3–12
Kamiya N, Kuroda K (1956) Bot Mag Tokyo 69:544–554
Karcher RL, Deacon SW, Gelfand VI (2002) Trends Cell Biol 12:21–27
Kashiyama T, Kimura N, Mimura T, Yamamoto K (2000) J Biochem 127:1065–1070
Kashiyama T, Ito K, Yamamoto K (2001) J Mol Biol 311:461–466
Kasahara M, Kagawa T, Sato Y, Kiyosue TD, Wada M. (2004) Plant Physiol 135:1388–1397
Kawai H, Kanegae T, Christensen S, Kiyosue T, Sato Y, Imaizumi T, Kadota, Wada M (2003) Nature 421:287–290
Kersey YM, Wessells NK (1976) J Cell Biol 68:264–275
Kersey YM, Hepler PK, Palevitz BA, Wessells NK (1976) Proc Natl Acad Sci USA 73:165–167
Kikuyama M, Tazawa M (1982) Protoplasma 113:241–243
Kikuyama M, Shimada K, Hiramoto Y (1993) Protoplasma 174:142–146
Kimura Y, Toyoshima N, Hirakawa N, Okamoto K, Ishijima A (2003) J Mol Biol 328:939–950
Kishimoto U, Akabori H (1959) J Gen Physiol 42:1167–1183
Kobayashi Y, Kobayashi I, Funaki Y, Fujimoto S, Takemoto T, Kuhoh H (1997a) Plant J 11:525–537
Kobayashi Y, Yamada M, Kobayshi I, Kunoh H (1997b) Plant Cell Physiol 38:725–733
Kohno T, Okagaki T, Kohama K, Shimmen T (1991) Protoplasma 161:75–77
Kohno T, Ishikawa R, Nagata T, Kohama K, Shimmen T (1992) Protoplasma 170:77–85
Kohama K, Shimmen T (1985) Protoplasma 129:88–91
Kohno T, Shimmen T (1988a) J Cell Biol 106:1539–1543
Kohno T, Shimmen T (1988b) J Cell Sci 91:501–509
Koop H-U, Kiermayer O (1980) Protoplasma 102:295–306
Kron SJ, Spudich JA (1986) Proc Natl Acad Sci USA 83:6272–6276
Kunoh H, Aist JR, Hayashimoto A (1985) Physiol Plant Pathol 26:199–207
Kuroda K (1983) Proc Jpn Acad 59 ser B:126–130
Kuroda K, Kamiya N (1975) Proc Jpn Acad 51 ser B:774–777
Kuroda K, Manabe E (1983) Proc Jpn Acad 59 ser B:131–134
Lancelle SA, Hepler PK (1992) Protoplasma 167:215–230
Lancelle SA, Cresti M, Hepler PK (1987) Protoplasma 140:141–150
Lancelle SA. Cresti M, Heper PK (1997) Protoplasma 196:21–33
Maekawa T, Tsutsui I, Nagai R (1986) Plant Cell Physiol 27:837–851
Makita N, Shihira-Ishikawa I (1997) Protoplasma 197:86–95
Maruta H, Korn ED (1977) J Biol Chem 252:6501–6509
Mascarenhas JP, Lafountain J (1972) Tissue Cell 4:11–14
Masuda Y, Takagi S, Nagai R (1991) Protoplasma 162:151–159
McCurdy DW, Harmon AC (1992a) Planta 188:54–61
McCurdy DW, Harmon AC (1992b) Protoplasma 171:85–88
McKenna ST, Vidali L, Hepler PK (2004) Planta 218:906–915
Meagher RB, McKinny EC, Vitale AV (1999) Trends Genet 15:278–284
Menzel D, Elsner-Menzel C (1989) Bot Acta 102:241–248
Miller AJ, Sanders D (1987) Nature 326:397–399
Miller DD, Callaham DA, Gross DJ, Hepler P (1992) J Cell Sci 101:7–12
Miller DD, Lancelle SA, Hepler PK (1996) Protoplasma 195:123–132
Mizukami M, Wada S (1983) Protoplasma 114:154–162
Morimatsu M, Nakamura A, Sumiyoshi H, Sakabe N, Taniguchi H, Kohama K, Higashi-Fujime S (2000) Biochem Biophys Res Commun 270:147–152
Morimatsu M, Hasegawa S, Higashi-Fujime S (2002) Cell Motil Cytoskel 53:66–76
Nagai R, Hayama T (1979) J Cell Sci 36:121–136
Nagai R, Rebhun LI (1966) J Ultrastruct Res 14:571–589
Nakayasu T, Yokota E, Shimmen T (1998) Biochem Biophys Res Commun 249:61–65
Nishimura T, Yokota E, Wada T, Shimmen T, Okada K. (2003) Plant Cell Physiol 44:1131–1140
Nobling R, Reiss H-D (1987) Protoplasma 139:20–24
Okazaki Y, Tazawa M (1986) Plant Cell Environ 9:491–494
Okazaki Y, Shimmen T, Tazawa M (1984) Plant Cell Physiol 25:573–581
Okazaki Y, Yoshimoto Y, Hiramoto Y, Tazawa M (1987) Protoplasma 140:67–71
Palevitz BA, Hepler PK (1975) J Cell Biol 65:29–38
Palevitz BA, Ash JF, Hepler PK (1974) Proc Natl Acad Sci USA 71:363–366
Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK (1994) Plant Cell 6:1815–1828
Pierson ES, Miller DD, Callaham DA, van Aken J, Hackett G, Hepler PK (1996) Dev Biol 174:160–173
Plieth C, Hansen U-P (1992) Planta 188:332–339
Pollard TD, Korn ED (1973a) J Biol Chem 248:4682–4690
Pollard TD, Korn ED (1973b) J Biol Chem 248:4691–4697
Reichelt S, Kendrick-Jones J (2000) In actin: dynamic framework for multiple plant cell functions. Staiger CJ, Balujska F, Volkman D, Barlow PW (eds) Kluwer, Dordrecht, pp 29–44
Reiss H-D, Nobling R (1986) Protoplasma 131:244–246
Romagnoli S, Cai G, Cresti M (2003) Plant Cell 15:251–269
Ryu J-H, Takagi S, Nagai R (1995) J Cell Sci 108:1531–1539
Sato Y, Kadota A, Wada M (1999) Plant Physiol 121:37–44
Sato Y, Wada M, Kadota A (2000) J Cell Sci 114:269–279
Sato Y, Wada M, Kadota A (2001) Plant Physiol 127:497–504
Sato Y, Wada M, Kadota A (2003) Planta 216:772–777
Seitz K (1967) Z Pflanzenphysiol 6:246–261
Seki M, Awata J, Shimada K, Kashiyama T, Ito K, Yamamoto K (2003) Plant Cell Physiol 44:201–205
Seki M, Kashiyama T, Hachikubu Y, Ito K, Yamamoto K (2004) J Mol Biol 344:311–315
Sellers JR (2000) Biochim Biophys Acta 1496:3–22
Sellers JR, Spudich JA, Sheetz MP (1985) J Cell Biol 101:1897–1902
Sheetz MP, Spudich JA (1983) Nature 303:31–35
Shimmen T (1978) Cell Struct Funct 3:113–121
Shimmen T (1988a) Protoplasma suppl 1:3–9
Shimmen T (1988b) Bot Mag Tokyo 101:533–544
Shimmen T (1996) Plant Cell Physiol 37:591–597
Shimmen T, Tazawa M (1982) Protoplasma 113:127–131
Shimmen T, Tazawa M (1983) Protoplasma 115:18–24
Shimmen T, Yano M (1984) Protoplasma 121:132–137
Shimmen T, Yano M (1986) Protoplasma 132:129–136
Shimmen T, Yokota (2004) Curr Opinion Cell Biol 16:159–167
Shimmen T, Mimura T, Kikuyama M, Tazawa M (1994) Cell Struct Funct 19:263–278
Shimmen T, Xu Y-L, Kohno T (1990) Protoplasma 158:39–44
Sibaoka T, Oda K (1956) Sci Rep Tohoku Univ IV Biol 22:157–166
Staiger CJ, Schliwa M (1987) Protoplasma 141:1–12
Straight AF, Cheung A, Limouze J, Chen I, Westwood NJ, Sellers JR, Michison TJ (2003) Science 299:1743–1747
Takagi S, Nagai R (1983) J Cell Sci 62:385–405
Takagi S, Nagai R (1985) Plant Cell Physiol 26:941–951
Takagi S, Nagai R (1986) Plant Cell Physiol 27:953–959
Takagi S, Nagai R (1988) Plant Physiol 88:228–232
Takagi S, Yamamoto K, Furuya M, Nagai R (1990) Plant Physiol 94:1702–1708
Takagi S, Yokota E, Shimmen T, Nagai R (1995) Plant Cell Physiol 36 (suppl. s132)
Takemoto D, Jones DA, Hardham AR (2003) Plant J 33:775–792
Tazawa M (1964) Plant Cell Physiol 5:33–43
Tazawa M, Kishimoto U (1968) Plant Cell Physiol 9:361–368
Tazawa M, Shimmen T (2001) Aust J Plant Physiol 28:523–539
Tazawa M, Kikuyama M, Shimmen T (1976) Cell Struct Funct 1:165–176
Tiwari SC, Polito VS (1988) Protoplasma 147:100–112
Tlalka M, Gabrys H (1993) Planta 189:491–498
Tominaga Y, Tazawa M (1981) Protoplasma 109:103–111
Tominaga Y, Shimmen T, Tazawa M (1983) Protoplasma 116:75–77
Tominaga Y, Wayne R, Tung HYL, Tazawa M (1987) Protoplasma 136:161–169
Tominaga M, Morita K, Sonobe S, Yokota E, Shimmen T (1997) Protoplasma 199:83–92
Tominaga M, Yokota E, Sonobe S, Shimmen T (2000) Protoplasama 213:46–54
Tominaga M, Kojima H, Yokota E, Orii H, Nakamori R, Katayama E, Anson M, Shimmen T, Oiwa K (2003) EMBO J 22:1263–1272
Vale RD, Szent-Gyorgyi AG, Sheetz MP (1984) Proc Natl Acad Sci USA 81:6775–6778
Vidali L, Yokota E, Cheung AY, Shimmen T, Hepler PK (1999) Protoplasma 209:283–291
Williamson RE (1972) J Cell Sci 10:811–819
Williamson RE (1974) Nature 248:801–802
Williamson RE (1975) J Cell Sci 17:655–668
Williamson RE, Ashley CC (1982) Nature 296:647–651
Woods CM, Polito VS, Reid MS (1984) Protoplasma 121:17–24
Yamamoto K, Kikuyama M, Sutoh-Yamamoto N, Kamitsubo E (1994) Proc Jpn Acad 70 Ser. B:175–180
Yamamoto K, Kikuyama M, Sutoh-Yamamoto N, Kamitsubo E, Katayama E (1995) J Mol Biol 254:109–112
Yamamoto K, Shimada K, Ito K, Hamada S, Ishijima A, Tsuchiya T, Tazawa M (2006) Plant Cell Physiol 47:1427–1431
Yanagida T, Nakase M, Nishiyama K, Oosawa F (1984) Nature 307:58–60
Yatsuhashi H, Kadota A, Wada M (1985) Planta 165:43–50
Yokota E, Shimmen T (1994) Protoplasma 177:153–162
Yokota E, McDonald AR, Liu B, Shimmen T, Palevitz BA (1995a) Protoplasma 185:178–187
Yokota E, Mimura T, Shimmen T (1995b) Plant Cell Physiol 36:1541–1547
Yokota E, Takahara K, Shimmen T (1998) Plant Physiol 116:1421–1429
Yokota E, Muto S, Shimmen T. (1999a) Plant Physiol 119:231–239
Yokota E, Yukawa C, Muto S, Sonobe S, Shimmen T (1999b) Plant Physiol 121:525–534
Yokota E, Muto S, Shimmen T (2000) Plant Physiol 123:645–654
Yokota E, Vidali L, Tominaga M, Tahara H, Orii H, Morizane Y, Hepler PK, Shimmen T (2003) Plant Cell Physiol 44:1088–1099
Yokota E, Tominaga M, Mabuchi I, Tsuji Y. Staiger CJ, Oiwa K, Shimmen T (2005) Plant Cell Physiol 46:1690–1703
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Shimmen, T. The sliding theory of cytoplasmic streaming: fifty years of progress. J Plant Res 120, 31–43 (2007). https://doi.org/10.1007/s10265-006-0061-0
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DOI: https://doi.org/10.1007/s10265-006-0061-0