Abstract
The cell wall is one of the structural key players regulating pollen tube growth, since plant cell expansion depends on an interplay between intracellular driving forces and the controlled yielding of the cell wall. Pectin is the main cell wall component at the growing pollen tube apex. We therefore assessed its role in pollen tube growth and cytomechanics using the enzymes pectinase and pectin methyl esterase (PME). Pectinase activity was able to stimulate pollen germination and tube growth at moderate concentrations whereas higher concentrations caused apical swelling or bursting in Solanum chacoense Bitt. pollen tubes. This is consistent with a modification of the physical properties of the cell wall affecting its extensibility and thus the growth rate, as well as its capacity to withstand turgor. To prove that the enzyme-induced effects were due to the altered cell wall mechanics, we subjected pollen tubes to micro-indentation experiments. We observed that cellular stiffness was reduced and visco-elasticity increased in the presence of pectinase. These are the first mechanical data that confirm the influence of the amount of pectins in the pollen tube cell wall on the physical parameters characterizing overall cellular architecture. Cytomechanical data were also obtained to analyze the role of the degree of pectin methyl-esterification, which is known to exhibit a gradient along the pollen tube axis. This feature has frequently been suggested to result in a gradient of the physical properties characterizing the cell wall and our data provide, for the first time, mechanical support for this concept. The gradient in cell wall composition from apical esterified to distal de-esterified pectins seems to be correlated with an increase in the degree of cell wall rigidity and a decrease of visco-elasticity. Our mechanical approach provides new insights concerning the mechanics of pollen tube growth and the architecture of living plant cells.
Similar content being viewed by others
Abbreviations
- PME :
-
Pectin methyl esterase
References
Aouali N, Laporte P, Clement C (2001) Pectin secretion and distribution in the anther during pollen development in Lilium. Planta 213:71–79
Brewbaker J, Kwack B (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865
Brewbaker J, Kwack B (1964) The calcium ion and substances influencing pollen growth. In: Linskens HF (ed) Pollen physiology and fertilization. Elsevier, North-Holland, Amsterdam, pp 145–151
Carpita N, Gibeaut D (1993) Structural models of primary cell walls in flowering plants: consistency of molecular structure with the physical properties of the wall during growth. Plant J 3:1–30
Chanliaud E, Burrows KM, Jeronimidis G, Gidley MJ (2002) Mechanical properties of primary plant cell wall analogues. Planta 215:989–996
Chanliaud E, De Silva J, Strongitharm B, Jeronimidis G, Gidley MJ (2004) Mechanical effects of plant cell wall enzymes on cellulose/xyloglucan composites. Plant J 38:27–37
Cormack RGH (1956) A further study of the growth of Brassica roots in solutions of pectic enzymes. Can J Bot 34:983–987
Cosgrove DJ (1986) Biophysical control of plant cell growth. Annu Rev Plant Physiol 37:377–405
Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Devel Biol 13:171–201
Darley CP, Forrester AM, McQueen-Mason SJ (2001) The molecular basis of plant cell wall extension. Plant Mol Biol 47:179–195
Davies GC, Hiller S, Bruce DM (1998) A membrane model for elastic deflexion of individual plant cell walls. J Texture Stud 29:645–667
Dearnaley JDW, Daggard GA (2001) Expression of a polygalacturonase enzyme in germinating pollen of Brassica napus. Sex Plant Reprod 13:265–271
Derksen J (1996) Pollen tubes: a model system for plant cell growth. Bot Acta 109:341–345
Derksen J, Rutten T, Lichtscheidl I, de Win A, Pierson E, Rongen G (1995) Quantitative analysis of the distribution of organelles in tobacco pollen tubes: implications for exocytosis and endocytosis. Protoplasma 188:267–276
Ekdahl I (1957) On the growth mechanism of roots hairs. Physiol Plant 10:798
Elson EL, Daily BB, McConnaughey WB, Pasternak C, Petersen NO (1983) Measurement of forces which determine the shapes of adherent cells in culture. In: Liu T-Y, Sakakibara S, Schechter A, Yagi K, Yajima H, Yasunobu KT (eds) Frontiers in biochemical and biophysical studies of proteins and membranes. Elsevier, New York, pp 399–411
Franklin-Tong VE (1999) Signaling and the modulation of the pollen tube growth. Plant Cell 11:727–738
Geitmann A (1997) Growth and formation of the cell wall in pollen tubes of Nicotiana tabacum and Petunia hybrida. Egelsbach, Hänsel-Hohenhausen
Geitmann A (1999) The rheological properties of the pollen tube cell wall. In: Cresti M, Cai G, Moscatelli A (eds) Fertilization in higher plants. Springer, Berlin Heidelberg New York, pp 283–297
Geitmann A, Cresti M (1998) Ca2+ channels control the rapid expansions in pulsating growth of Petunia hybrida pollen tubes. J Plant Physiol 152:439–447
Geitmann A, Parre E (2004) The local cytomechanical properties of growing pollen tubes correspond to the axial distribution of structural cellular elements. Sex Plant Reprod 17:9–16
Geitmann A, Hudak J, Vennigerholz F, Walles B (1995) Immunogold localization of pectin and callose in pollen grains and pollen tubes of Brugmansia suaveolens—implication for the self-incompatibility reaction. J Plant Physiol 147:225–235
Green PB (1962) Mechanism for plant cellular morphogenesis. Science 138:1404–1405
Green PB (1969) Cell morphogenesis. Annu Rev Plant Physiol 20:365–394
Hasegawa Y, Nakamura S, Kakizoe S, Sato M, Nakamura N (1998) Immunocytochemical and chemical analyses of golgi vesicles isolated from the germinated pollen of Camellia japonica. J Plant Res 111:421–429
Hepler PK, Vidali L, Cheung AY (2001) Polarized cell growth in higher plants. Annu Rev Cell Devel Biol 17:159–87
Heslop-Harrison J (1987) Pollen germination and pollen-tube growth. Int Rev Cytol 107:1–78
Heslop-Harrison Y, Heslop-Harrison J (1992) Germination of monocolpate angiosperm pollen: evolution of actin cytoskeleton and wall during hydration, activation and tube emergence. Ann Bot 69:385–394
Hiller S, Bruce DM, Jeronimidis G (1996) A micro-penetration technique for mechanical testing of plant cell walls. J Texture Stud 27:559–587
Holdaway-Clarke TL, Hepler PK (2003) Control of pollen tube growth: role of ion gradients and fluxes. New Phytol 159:539–563
Jackson WMT (1959) Effect of pectinase and cellulase preparations on the growth and development of root hairs. Physiol Plant 12:502–510
Jarvis MC (1984) Structure and properties of pectin gels in plant cell walls. Plant Cell Environ 7:153–164
Jauh GY, Lord EM (1996) Localization of pectins and arabinogalactan-protein in lily (Lilium longiflorum L.) pollen tube and style, and their possible roles in pollination. Planta 199:251–261
Kauss H, Hassid WZ (1967) Enzymic introduction of the methyl ester groups of pectins. J Biol Chem 242:3449–3453
Kim J-B, Carpita NC (1992) Changes in esterification of the uronic acid groups of 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 esterifications spatially regulated both within cell walls and between developing tissues of root apices. Planta 181:512–521
Lennon KA, Lord EM (2000) In vivo pollen tube cell of Arabidopsis thaliana. Tube cell cytoplasm and wall. Protoplasma 214:45–56
Levy S, Staehelin LA (1992) Synthesis, assembly and function of plant cell wall macromolecules. Curr Opin Cell Biol 4:856–862
Li YQ, Chen F, Linskens H, 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 (1995) Presumed phylogenetic basis of the correlation of pectin deposition pattern in pollen tube walls and the stylar structure of angiosperms. Proc K Ned Akad Wet 98:39–44
Li YQ, Moscatelli A, Cai G, Cresti M (1997) Functional interactions among cytoskeleton membranes and cell wall in pollen tube of flowering plants. Int Rev Cytol 176:133–199
Li YQ, Mareck A, Faleri C, Moscatelli A, Liu Q, Cresti M (2002) Detection and localization of pectin methylesterase isoforms in pollen tubes of Nicotiana tabacum L. Planta 214:734–740
Lockhart JA (1965) An analysis of irreversible plant cell elongation. J Theor Biol 8:264–75
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
McNeil M, Darvill AG, Fry SC, Albersheim P (1984) Structure and function of the primary cell walls of plants. Ann Rev Biochem 53:625–63
Money NP, Harold FM (1992) Extension growth of the water mold Achlya: interplay of turgor and wall strength. Cell Biol 89:4245–4249
Money NP, Hill TW (1997) Correlation between endoglucanase secretion and cell wall strength in oomycete hyphae: implications for growth and morphogenesis. Mycologia 89:777–785
Morris ER, Powell DA, Gidley MJ, Rees DA (1982) Conformations and interactions of pectins. I. Polymorphism between gel and solid states of calcium polygalacturonate. J Mol Biol 155:507–16
Mu JH, Stains JP, Kao TH (1994) Characterization of a pollen-expressed gene encoding a putative pectin esterase of Petunia inflata. Plant Mol Biol 25:539–544
Ortega JKE (1985) Augmented equation for cell wall expansion. Plant Physiol 79:318–320
Petersen NO, McConnaughey WB, Elson EL (1982) Dependence of locally measured cellular deformability on position on the cell, temperature, and cytochalasin B. Proc Nat Acad Sci USA79:5327–5331
Roggen HPJR, Stanley RG (1969) Cell wall hydrolysing enzymes in wall formation as measured by pollen tube extension. Planta 84:295–303
Steer MW, Steer JM (1989) Pollen tube tip growth. New Phytol 111:323–358
Suarez-Cervera M, Arcalis E, Le Thomas A, Seoane-Camba JA (2002) Pectin distribution pattern in the apertural intine of Euphorbia peplus L. (Euphorbiaceae) pollen. Sex Plant Reprod 14:291–298
Taiz L (1984) Plant cell expansion: regulation of cell wall mechanical properties. Annu Rev Plant Physiol 35:585–657
Taylor LP (1997) Pollen germination and tube growth. Annu Rev Plant Physiol Plant Mol Biol 48:461–491
VandenBosch KA, Bradley DJ, Knox JP, Perotto S, Butcher GW, Brewin NJ (1989) Common components of the infection thread matrix and the intercellular space identified by immunocytochemical analysis of pea nodules and uninfected roots. EMBO J 8:335–342
Acknowledgements
This research was supported by grants from the Natural Sciences and Engineering Research Council of Canada (NSERC), the Canadian Foundation for Innovation (CFI), and the Fonds Québecois de la Recherche sur la Nature et les Technologies (FQRNT) to A. Geitmann. The generous gifts of monoclonal antibodies JIM5 and JIM7 from Keith Roberts, John Innes Centre, Norwich, UK, and from Paul Knox, Leeds University, UK, are gratefully acknowledged. We also thank William B. McConnaughey, Washington University, St. Louis, Missouri, for assistance with the micro-indentation setup.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Parre, E., Geitmann, A. Pectin and the role of the physical properties of the cell wall in pollen tube growth of Solanum chacoense. Planta 220, 582–592 (2005). https://doi.org/10.1007/s00425-004-1368-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00425-004-1368-5