Abstract
Normally growing lily (Lilium longiflorum Thunb.) pollen tubes cultured in standard sucrose medium display a relatively steady tip-growth pattern and a rather even pectin sheath in the cell wall. In an attempt to better understand pulsatory growth, observed in some species, e.g., Petunia, and its possible role in causing the formation of thickened cell wall rings, we have imposed marked fluctuations in the growth-rate of lily pollen tubes. The appropriate growth-perturbing conditions were achieved by modulating the medium osmolarity or by applying caffeine, a non-turgor inhibitor, in a specially designed incubation chamber with a controlled medium flow. The relatively non-esterified pectin deposition in the wall of the growth-interrupted pollen tubes was detected by immunofluorescence microscopy using a monoclonal antibody, JIM 5. The observations show that the periods of slow or inhibited growth correspond to the times when the thickened walls are deposited. Since the growth fluctuations were induced by both turgor- and non-turgor-related means, the proposed endogenous regulatory role of turgor pressure is questioned. Other factors, such as the tip-focused Ca2+ gradient which was demonstrated by ratiometric ion imaging, and the alteration in the extensibility of the cell wall, which correlated with pectin esterification/de-esterification, emerge as candidates for the regulation of growth fluctuations.
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Abbreviations
- MAb:
-
monoclonal antibody
References
Battey NH, Blackbourn HD (1993) The control of exocytosis in plant cells. New Phytol 125: 307–338
Carpita NC, Gibeaut DM (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the walls during growth. Plant J 31: 1–30
Cosgrove DJ (1993a) Wall extensibility: its nature, measurement and relationship to plant cell growth. New Phytol 124: 1–23
Cosgrove DJ (1993b) How do plant cell walls extend? Plant Physiol 102: 1–6
Cresti M, Pacini E, Ciampolini F, Sarfatti G (1977) Germination and early tube development in vitro of Lycopersicum peruvianum pollen: Ultrastructural feature. Planta 136: 239–247
Derksen J, Rutten T, Van Amstel T, De Win A, Doris F, Steer M (1995) Regulation of pollen tube growth. Acta Bot Neerl 44: 93–119
Dickinson DB (1968) Rapid starch synthesis with increased respiration in germinating lily pollen. Plant Physiol 43: 1–8
Feijò JA, Malhò R, Obermeyer G (1995) Ion dynamics and its possible role during in vitro pollen germination and tube growth. Protoplasma 187: 155–167
Geitmann A, Li YQ, Cresti M (1995) Ultrastructural immunolocalization of periodic pectin deposition in the cell wall of Nicotiana tabacum pollen tubes. Protoplasma 187: 172–181
Hepler PK, Miller DD, Pierson ES, Callaham DA (1994) Calcium and pollen tube growth. In: Stephenson AG, Kao D-H (eds) Pollen-pistil interaction and pollen tube growth. American Society of Plant Physiologists, Rockville-Maryland, pp 111–123
Herth W, Reiss H-D, Hartmann E (1990) Role of calcium ions in tip growth of pollen tubes and moss protonema cells. In: Heath IB (ed.) Tip growth in plant and fungal cells. Academic Press, New York, pp 91–118
Heslop-Harrison J (1987) Pollen germination and pollen tube growth. Int Rev Cytol 107: 1–78
Jaffe LA, Weisenssel MH, Jaffe LF (1975) Calcium accumulations within the growing tips of pollen tubes. J Cell Biol 67: 488–492
Kim JB, Carpita NC (1992) Changes in esterification of the uronic acid groups of the cell wall polysaccharides during elongation of maize coleoptiles. Plant Physiol 98: 646–653
Knox JP, Linstead PJ, King J, Cooper C, Roberts K (1990) Pectin esterification is spatially regulated both within cell walls and between developing tissues of roots apices. Planta 20: 825–833
Kroh M, Kruiman B, Kudlicka K (1983) Effects of reduced turgor pressure on tobacco pollen tubes. In: Erdelskà O, Ciamporovà M, Lux A, Pretovà A, Tupy J (eds) Fertilization and embryogenesis in ovulated plants. Proceedings of the VII International Cytoembryological Symposium, Bratislava, pp 121–124
Li YQ, Croes AF, Linskens HF (1983) Cell-wall proteins in pollen and roots of Lilium longiflorum: extraction and partial characterization. Planta 158: 422–427
Li YQ, Bruun L, Pierson ES, Cresti M (1992) Periodic deposition of arabinogalactan epitopes in the cell wall of pollen tubes of Nicotiana tabacum L. Planta 188: 532–538
Li YQ, Chen F, Linskens HF, Cresti M (1994) Distribution of unesterified and esterified pectins in cell walls of pollen tubes of flowering plants. Sex Plant Reprod 7: 145–152
Li YQ, Chen F, Faleri C, Ciampolini F, Linskens HF, Cresti M (1995a) Presumed phylogenetic basis of the correlation of pectin deposition pattern in pollen tube walls and the stylar structure of angiosperms. Proc Kon Ned Akad Wet Amsterdam 98: 39–44
Li YQ, Faleri C, Geitmann A, Cresti M (1995b) Immunogold localization of arabinogalactan proteins, unesterified and esterified pectins in pollen grains and pollen tubes of Nicotiana tabacum L. Protoplasma 189: 26–36
Linskens HF, Kroh M (1970) Regulation of pollen tube growth. Current Topics Devel Biol 5: 89–113
Lòpez-Franco R, Bartnicki-Garcia S, Bracker CE (1994) pulsed growth of fungal hyphal tips. Proc Natl Acad Sci USA 91: 12228–122232
Malhò R, Read ND, Trewavas AJ, Salomè Pais M (1995) Calcium channel activity during pollen tube growth and reorientation. Plant Cell 7: 1173–1184
Mascarenhas JP (1993) Molecular mechanism of pollen tube growth and differentiation. Plant Cell 5: 1303–1314
McCann MC, Roberts K (1994) Changes in cell wall architecture during cell elongation. J Exp Bot 45: 1683–169
McCann MC, Stacey NJ, Wilson R, Roberts K (1993) Orientation of macromolecules in the walls of elongating carrot cells. J Cell Sci 106: 1347–1356
McCann MC, Shi J, Roberts K, Carpita NC (1994) Changes in pectin structure and localization during the growth of unadapted and NaCl-adapted tobacco cells. Plant J 5: 773–785
Miller DD, Callaham DA, Gross DJ, Hepler PK (1992) Free Ca2+ gradient in growing pollen tubes of Lilium. J Cell Sci 101: 7–12
Mulcahy DL, Mulcahy GB (1987) The effects of pollen competition. Am Sci 75: 44–50
Picton JM, Steer MW (1981) Determination of secretory vesicles production rate by dictyosomes in pollen tubes of Tradescantia using cytochalasin D. J Cell Sci 40: 261–272
Pierson ES, Lichtscheidl IK, Derksen J (1990) Structure and behaviour of organelles in living pollen tubes of Lilium longiflorum. J Exp Bot 41: 1461–1468
Pierson ES, Miller DD, Callaham DA, Shipley AM, Rivers BA, Cresti M, Hepler PK (1994) Pollen tube growth is coupled to the extracellular calcium ion flux and the intracellular calcium gradient: effect of BAPTA-type buffer and hypertonic media. Plant Cell 6: 1815–1828
Pierson ES, Li YQ, Zhang HQ, Willemse MTM, Linskens HF, Cresti M (1995) Pulsatory growth of pollen tubes: investigation of a possible relationship with the periodic distribution of cell wall components. Acta Bot Neerl 44: 121–128
Pierson ES, Miller DD, Callaham DA, Van Aken J, Hackett G, Hepler PK (1996) Tip-localized calcium entry fluctuates during pollen tube growth. Devel Biol 174: 160–173
Plyushch TA, Willemse MTM, Franssen-Verheijen MAW, Reinders MC (1995) Structural aspects of pollen tube growth and micropylar penetration in vitro in Gasteria verrucosa (Mill) H. Duval and Lilium longiflorum Thunb. Protoplasma 187: 13–21
Powell DA, Morris ER, Gidley MJ, Rees DA (1982) Conformation and function of pectins: II. Influence on chain association in calcium pectate gels. J Mol Biol 155: 517–521
Schaumann A, Bruyant-Vannier MP, Goubet F, Morvan C (1993) Pectic metabolism in suspension-cultured cells of flax, Linum usitatissimum. Plant Cell Physiol 34: 891–897
Schröter K, Sievers A (1971) Wirkung der Turgorreduktion auf den Golgi-Apparat und die Bildung der Zellwand bei Wurzelhaaren. Protoplasma 72: 203–211
Sievers A, Schnepf E (1981) Morphogenesis and polarity of tubular cells with tip growth. In: Kiermayer O (ed.) Cytomorphogenesis in plants. Springer-Verlag, Wien New York, pp 265–299
Steer MW, Steer JM (1989) Pollen tube tip growth. New Phytol 111: 323–358
Tang XW, Liu GQ, Yang Y, Zheng WL, Wu BC, Nie DT (1992) Quantitative measurement of pollen tube growth and particles movement. Acta Bot Sin 34: 893–898
Van Aelst AC (1983) Experimental pollen germination and pollen tube growth in vitro. In: Erdelskà O, Ciamporovà M, Lux A, Pretovà A, Tupy J (eds) Fertilization and embryogenesis in ovulated plants Proceedings of the VII International Cytoembryological Symposium, Bratislava, pp 117–124
Van Aelst AC, Van Went JL (1992) Effects of sucrose concentration on in-vitro pollen tube growth and tube morphology of Impatiens walleriana. Plant Physiol (Life Sci Adv) 11: 51–57
Walsh NE, Charlesworth D (1992) Evolutionary interpretations of differences in pollen tube growth rates. Quat Rev Bot 67: 19–37
Zhang HQ, Croes AF (1982) A new medium for pollen germination in vitro. Acta Bot Neerl 31: 113–119
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We sincerely thank Prof. C. Mariani and Dr. J. Derksen (Department of Experimental Botany, University of Nijimegen, The Netherlands) for critical reading of the manuscript, Dr. G. Cai, Dr. A. Moscatelli and A. Geitmann (Department of Environmental Biology, Univeristy of Siena, Italy) for kind support in setting up the incubation system and helpful discussion, Mr. G. Hackett (Department of Biology, University of Massachusetts, USA) for technical assitance in Ca2+ ratiometric analysis, and Dr. J. Van Tuyl (CPROSLO, Wageningen, The Netherlands) for providing lily bulbs. The research was supported by a grant from the Ministry of Foreign Affairs of Italy to Y.Q.L., the National Programme of MURST (Italy) to M.C., and National Science Foundation (USA) Grant No. MCB-9304953 to P.K.H.
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Li, YQ., Zhang, HQ., Pierson, E.S. et al. Enforced growth-rate fluctuation causes pectin ring formation in the cell wall of Lilium longiflorum pollen tubes. Planta 200, 41–49 (1996). https://doi.org/10.1007/BF00196647
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DOI: https://doi.org/10.1007/BF00196647