Abstract
The function of the epidermis in auxinmediated elongation growth of maize (Zea mays L.) coleoptile segments was investigated. The following results were obtained: i) In the intact organ, there is a strong tissue tension produced by the expanding force of the inner tissues which is balanced by the contracting force of the outer epidermal wall. The compression imposed by the stretched outer epidermal wall upon the inner tissues gives rise to a wall-pressure difference which can be transformed into a water-potential difference between inner tissues and external medium (water) by removal of the outer epidermal wall. ii) Peeled segments fail to respond to auxin with normal growth. The plastic extensibility of the inner-tissue cell walls (measured with a constant-load extensiometer using living segments) is not influenced by auxin (or abscisic acid) in peeled or nonpeeled segments. It is concluded that auxin induces (and abscisic acid inhibits) elongation of the intact segment by increasing (decreasing) the extensibility specifically in the outer epidermal wall. In addition, tissue tension (and therewith the pressure acting on the outer epidermal wall) is maintained at a constant level over several hours of auxin-mediated growth, indicating that the inner cells also contribute actively to organ elongation. However, this contribution does not involve an increase of cell-wall extensibility, but a continuous shifting of the potential extension threshold (i.e., the length to which the inner tissues would extend by water uptake after peeling) ahead of the actual segment length. Thus, steady growth involves the coordinated action of wall loosening in the epidermis and regeneration of tissue tension by the inner tissues. iii) Electron micrographs show the accumulation of striking osmiophilic material (particles of approx. 0.3 μm diameter) specifically at the plasma membrane/cell-wall interface of the outer epidermal wall of auxin-treated segments. iv) Peeled segments fail to respond to auxin with proton excretion. This is in contrast to fusicoccin-induced proton excretion and growth which can also be readily demonstrated in the absence of the epidermis. However, peeled and nonpeeled segments show the same sensitivity to protons with regard to the induction of acid-mediated in-vivo elongation and cell-wall extensibility. The observed threshold at pH 4.5–5.0 is too low to be compatible with a ‘second messenger’ function of protons also in the growth response of the inner tissues. Organ growth is described in terms of a physical model which takes into account tissue tension and extensibility of the outer epidermal wall as the decisive growth parameters. This model states that the wall pressure increment, produced by tissue tension in the outer epidermal wall, rather than the pressure acting on the inner-tissue walls, is the driving force of growth.
Similar content being viewed by others
Abbreviations
- E el, E pl :
-
elastic and plastic in-vitro cell-wall extensibility, respectively
- E tot :
-
E el+E pl
- FC:
-
fusicoccin
- IAA:
-
indole-3-acetic acid
- IT:
-
inner tissue
- ITW:
-
inner-tissue walls
- OEW:
-
outer epidermal wall
- π:
-
osmotic pressure
- P :
-
wall pressure
- Ψ:
-
water potential
References
Ballio, A., Federico, R., Scalorbi, D. (1981) Fusicoccin structure-activity relationships: in vitro binding to microsomal preparations of maize coleoptiles. Physiol. Plant. 52, 476–481
Boyer, J.S. (1985) Water transport. Annu. Rev. Plant Physiol. 36, 473–516
Brummell, D.A., Hall, J.L. (1980) The role of the epidermis in auxin-induced and fusicoccin-induced elongation of Pisum sativum stem segments. Planta 150, 371–379
Brummell, D.A., Hall, J.L. (1981) Medium acidification by auxin- and fusicoccin-treated peeled stem segments from etiolated seedlings of Pisum sativum. J. Exp. Bot. 32, 635–642
Burström, H.G., Uhrström, L., Wurscher, R. (1967) Growth, turgor, water potential and Joung's modulus in pea internodes. Physiol. Plant. 20, 213–231
Cleland, R.E. (1975) Auxin-induced hydrogen ion excretion: correlation with growth, and control by external pH and water stress. Planta 127, 233–242
Cleland, R.E. (1980) Auxin and H+-excretion: the state of our knowledge. In: Plant growth substances 1979, pp. 71–78, Skoog, F., ed. Springer, Berlin Heidelberg New York
Cosgrove, D. (1985) Cell wall yield properties of growing tissue. Evaluation by in vivo stress relaxation. Plant Physiol. 78, 347–356
Cunninghame, M.E., Hall, J.L. (1985) A quantitative stereological analysis of the effect of indoleacetic acid on the dictyosomes in pea stem epidermal cells. Protoplasma 125, 230–234
Darville, A.G., Smith, C.J., Hall, M.A. (1978) Cell wall structure and elongation growth in Zea mays coleoptile tissue. New Phytol. 80, 503–516
Diehl, J.M., gorter, C.J., Van Iterson, G., Kleinhoonte, A. (1939) The influence of growth hormone on hypocotyls of Helianthus and the structure of their cell walls. Rec. Trav. Bot. Neerl. 36, 709–798
Dohrmann, U., Pesci, P., Cocucci, S.M., Marrè, E. (1977) Stimulating effect of fusicoccin on K+-activated ATPase in plasmalemma preparations from higher plant tissues. Plant Sci. Lett. 8, 91–98
Durand, H., Rayle, D.L. (1973) Physiological evidence for auxin-induced hydrogen-ion secretion and the epidermal paradox. Planta 114, 185–193
Evans, M.L., Vesper, M.J. (1980) An improved method for detecting auxin-induced hydrogen ion efflux from corn coleoptile segments. Plant Physiol. 66, 561–565
Firn, R., Digby, J. (1977) The role of the peripheral cell layers in the geotropic curvature of sunflower hypocotyls: a new model of shoot geotropism. Aust. J. Plant. Physiol. 4, 337–347
Green, P.B. (1980) Organogenesis — a biophysical view. Annu. Rev. Plant Physiol. 31, 51–82
Kutschera, U., Schopfer, P. (1985a) Evidence against the acid-growth theory of auxin action. Planta 163, 483–493
Kutschera, U., Schopfer, P. (1985b) Evidence for the acid-growth theory of fusicoccin action. Planta 163, 494–499
Kutschera, U., Schopfer, P. (1986a) Effect of auxin and abscisic acid on cell wall extensibility in maize coleoptiles. Planta 167, 527–535
Kutschera, U., Schopfer, P. (1986b) In-vivo measurement of cell-wall extensibility in maize coleoptiles. Effects of auxin and abscisic acid. Planta 169, 437–442
Löbler, M., Klämbt, D. (1985) Auxin-binding protein from coleoptile membranes of corn (Zea mays L.) II. Localization of a putative auxin receptor. J. Biol. Chem. 260, 9854–9859
Masuda, Y., Yamamoto, R. (1972) Control of auxin-induced stem elongation by the epidermis. Physiol. Plant. 27, 109–115
Mentze, J., Raymond, B., Cohen, J.D., Rayle, D.L. (1977) Auxin-induced H+-secretion in Helianthus and its implications. Plant Physiol. 60, 509–512
Olesen, P. (1980) The visualization of wall-associated granules in thin sections of higher plant cells: occurrence, distribution, morphology and possible role in cell wall biogenesis. Z. Pflanzenphysiol. 96, 35–48
Pearce, D., Penny, D. (1983) Tissue interactions in indoleacetic acid-induced rapid elongation of lupin hypocotyls. Plant Sci. Lett. 30, 347–353
Penny, D., Miller, K.F., Penny, P. (1972) Studies on the mechanism of cell elongation of lupin hypocotyl segments. N.Z. J. Bot. 10, 97–111
Pesacreta, T.C., Lucas, W.J. (1984) Plasma membrane coat and a coated vesicle-associated reticulum of membranes: their structure and possible interrelationship in Chara corallina. J. Cell Biol. 98, 1537–1545
Pope, D.G. (1982) Effect of peeling on IAA-induced growth in Avena coleoptiles. Ann. Bot. 49, 493–501
Prat, R., Roland, J.-C. (1980) Croissance différentielle des tissues et texture des parvis. Physiol. Vég. 18, 241–257
Quaite, E., Parker, R.E., Steer, M.W. (1983) Plant cell extension: structural implications for the origin of the plasma membrane. Plant Cell Environ. 6, 429–432
Rayle, D.L. (1973) Auxin-induced hydrogen-ion secretion in Avena coleoptiles and its implications. Planta 144, 63–73
Rayle, D.L., Cleland, R. (1977) Control of plant cell enlargement by hydrogen ions. Curr. Top. Dev. Biol. 11, 187–214
Reynolds, E.S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 218–212
Robards, A.W. (1969) Particles associated with developing plant cell walls. Planta 88, 376–379
Rubinstein, B., Stein, O.L. (1980) Effects of peeling on the surface structure of the Avena coleoptile: implications for hormone research. Planta 150, 385–391
Sachs, J. (1865) Handbuch der Experimentalphysiologie der Pflanzen. Engelmann, Leipzig
Steudle, E. (1985) Water transport as limiting factor in extension growth. In: Control of leaf growth, pp. 35–55, Baker, N.R., Davis, W.J., Ong, C.K., eds. Cambridge University Press, Cambridge, UK
Tanimoto, E., Masuda, Y. (1971) Role of the epidermis in auxin-induced elongation of light-grown pea stem segments. Plant Cell Physiol. 12, 663–673
Taylor, J.A., West, D.W. (1980) The use of Evan's Blue stain to test the survival of plant cells after exposure to high salt and high osmotic pressure. J. Exp. Bot. 31, 571–576
Tepfer, M., Cleland, R.E. (1979) A comparison of acid-induced cell wall loosening in Valonia ventricosa and in oat coleoptiles. Plant Physiol. 63, 898–902
Thimann, K.V., Schneider, C.L. (1938) Differential growth in plant tissues. Am. J. Bot. 25, 627–641
Van Overbeek, J., Went, F.W. (1937) Mechanism and quantitative application of the pea test. Bot. Gaz. 99, 22–41
Vesper, M.J. (1985) Use of a pH-response curve for growth to predict apparent wall pH in elongating segments of maize coleoptiles and sunflower hypocotyls. Planta 166, 96–104
Went, F.W., Thimann, K.V. (1937) Phytohormones. Macmillan, New York
Yamagata, Y., Masuda, Y. (1975) Comparative studies on auxin and fusicoccin actions on plant growth. Plant Cell Physiol. 16, 41–52
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Kutschera, U., Bergfeld, R. & Schopfer, P. Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170, 168–180 (1987). https://doi.org/10.1007/BF00397885
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00397885