The growth rate of any multilayered plant organ is limited by the cell layer with the least extensibility. The dicot leaf blade has two epidermal layers covering the mesophyll layers, in which the vascular network is embedded. There has been a lingering uncertainty about which layer limits the rate of blade expansion in dicot leaves. The current study made use of leaf strips cut from the <i> argenteum </i> variety of <i> Pisum sativum </i> L., in which the epidermal layers can easily be removed with minimal damage. After this procedure, the mesophyll showed accelerated growth in short-term and long-term experiments and light and darkness. Extension of both layers is strongly promoted by acidic solutions. Isolated mesophyll layers expand in response to light. This effect depends on turgor pressure, photosynthesis, and the plasma membrane H+-ATPase. The data allow concluding that expanding leaf blades share with axial stem organs a similar arrangement of tissue tension: an expanding core tissue pushing against a restrictive epidermal envelope. In complete leaves, partial removal of the epidermis from only one side of the blade causes a strong epinastic or hyponastic response. Removal of matching epidermis strips from both sides of complete blades causes the exposed mesophyll strip to elongate in excess of the neighboring tissue: it buckles.
Cosgrove, D.J. (1993) How Do Plant Cells Expand? Plant Physiology, 102, 1-6. http://dx.doi.org/10.1104/pp.102.1.1
Diehl, J.M., Gorter, C.J., van Iterson, G. and Kleinhoonte, A. (1939) The Influence of Growth Hormone on Hypocotyls of Helianthus and the Structure of Their Cell Walls. Recueil des Travaux Botanique Neerlandais, 36, 709-796.
Peters, W.S. and Tomos, A.D. (1996) The History of Tissue Tensions. Annals of Botany, 77, 657-665. http://dx.doi.org/10.1093/aob/77.6.657
Peters, W.S. and Tomos, A.D. (1996) Is the Epidermis Still in Control? Botanica Acta, 109, 264-267. http://dx.doi.org/10.1111/j.1438-8677.1996.tb00572.x
Dale, J.E. (1988) The Control of Leaf Expansion. Annual Review Plant Physiology and Plant Molecular Biology, 39, 267-295. http://dx.doi.org/10.1146/annurev.pp.39.060188.001411
Hall, L.N. and Langdale, J.A. (1996) Molecular Genetics of Cellular Differentiation in Leaves. New Phytologist, 132, 533-553. http://dx.doi.org/10.1146/annurev.pp.39.060188.001411
Avery, G.S. (1933) Structure and Development of the Tobacco Leaf. American Journal of Botany, 20, 565-592. http://dx.doi.org/10.2307/2436259
Dengler, N.G., Mackay, L.B. and Gregory, L.M. (1975) Cell Enlargement during Leaf Expansion in Beech, Fagus grandifolia. Canadian Journal Botany, 53, 2846-2865. http://dx.doi.org/10.1139/b75-313
Jeffree, C.E., Dale, J.E. and Fry, S.C. (1986) The Genesis of Intercellular Spaces in Developing Leaves of Phaseolus vulgaris. Protoplasma, 132, 90-98. http://dx.doi.org/10.1007/BF01275795
Maksymowytch, R. (1973) Analysis of Leaf Development. Cambridge University Press, Cambridge.
Elzenga, J.T.M., Staal, M. and Prins, H.B.A. (1997) Calcium-Calmodulin Signaling Is Involved in Light-Induced Acidification by Epidermal Leaf Cells of Pea Pisum sativum L. Journal Experimental Botany, 48, 2055-2060. http://dx.doi.org/10.1093/jexbot/48.317.2055
Elzenga, J.T.M., Staal, M. and Prins, H.B.A. (2000) Red Light-Induced Acidification by Pea Leaf Epidermal Cells Is Regulated by More than One Phytochrome. Phyton, 40, 35-44.
Horiguchi, G.A., Ferjani, U., Fujikura, U. and Tsukaya, H. (2006) Coordination of Cell Proliferation and Cell Expansion in the Control of Leaf Size in Arabidopsis thaliana. Journal of Plant Research, 119, 37-42. http://dx.doi.org/10.1007/s10265-005-0232-4
Marcotrigano, M. (2010) A Role for Leaf Epidermis in the Control of Leaf Size and the Rate and Extent of Mesophyll Cell Division. American Journal of Botany, 97, 224-233. http://dx.doi.org/10.3732/ajb.0900102
Stewart, R.N., Meyer, F.G. and Dermen, H. (1972) Camillia + “Daisy Eagleson”, a Graft Chimera of Camellia sasanqua and C. japonica. American Journal of Botany, 59, 515-524. http://dx.doi.org/10.2307/2441534
Kaddoura, R.L. and Mantell, S.H. (1991) Synthesis and Characterization of Nicotiana-Solanum Graft Chimeras. Annals of Botany, 68, 547-555.
Savaldi-Goldstein, S., Peto, C. and Chory, J. (2007) The Epidermis Both Drives and Restricts Plant Shoot Growth. Nature, 446, 199-202. http://dx.doi.org/10.1038/nature05618
Bemis, S.M. and Torii, K.U. (2007) Autonomy of Cell Proliferation and Developmental Programs during Arabidopsis aboveground Organ Morphogenesis. Developmental Biology, 304, 367-381. http://dx.doi.org/10.1016/j.ydbio.2006.12.049
Hoch, H.C., Pratt, C. and Marx, G.A. (1980) Subepidermal Air Spaces: Basis for the Phenotypic Expression of the Argenteum Mutant of Pisum. American Journal of Botany, 67, 905-911. http://dx.doi.org/10.2307/2442431
Hrazdina, G., Marx, G.A. and Hoch, H.C. (1982) Distribution of Secondary Plant Metabolites and Their Biosynthetic Enzymes in Pea (Pisum sativum L.) Leaves. Plant Physiology, 70, 745-748. http://dx.doi.org/10.1104/pp.70.3.745
Staal, M., Elzenga, J.T.M., van Elk, A.G., Prins, H.B.A. and Van Volkenburgh, E. (1994) Red and Blue Light-Stimulated Proton Efflux by Epidermal Leaf Cells of the Argenteum Mutant of Pisum sativum. Journal of Experimental Botany, 45, 1213-1218. http://dx.doi.org/10.1093/jxb/45.9.1213
Wilson, M.K.P. and Bruck, D.K. (1999) Lack of Influence of the Epidermis on Underlying Cell Development in Leaflets of Pisum sativum var. argenteum (Fabaceae). Annals of Botany, 83, 1-10. http://dx.doi.org/10.1006/anbo.1998.0773
Jewer, P.C., Incoll, L.D. and Shaw, J. (1982) Stomatal Responses of Argenteum—A Mutant of Pisum sativum L. with Readily Detachable Leaf Epidermis. Planta, 155, 146-153. http://dx.doi.org/10.1007/BF00392545
Aked, J. and Hall, J.L. (1992) The Uptake of Glucose, Fructose and Sucrose into the Lower Epidermis of Leaf Discs of Pea (Pisum sativum L cv. Argenteum). New Phytologist, 123, 271-278. http://dx.doi.org/10.1111/j.1469-8137.1993.tb03735.x
Stahlberg, R. and Van Volkenburgh, E. (1999) The Effect of Light on Membrane Potential, Apoplastic pH and Cell Expansion in Leaves of Pisum sativum L. var. argenteum. Planta, 208, 188-195. http://dx.doi.org/10.1007/s004250050549
Harris, N. and Oparka, K.J. (1994) Plant Cell Biology: A Practical Approach. Oxford University Press, Oxford.
Lamprecht, H. (1958) Gekräuselte Blättchen bei Pisum und ihre Vererbung. Agricultural and Horticultural Genetics, 16, 1-8.
Van Volkenburgh, E. (1999) Leaf Expansion—An Integrating Plant Behavior. Plant & Cell Physiology, 22, 1463-1473. http://dx.doi.org/10.1046/j.1365-3040.1999.00514.x
Niklas, K.J. and Paolillo, D.J. (1997) The Role of the Epidermis as a Stiffening Agent in Tulipa (Liliaceae) Stems. American Journal of Botany, 84, 735-744. http://dx.doi.org/10.2307/2445809
Hejnowicz, Z. and Sievers, A. (1995) Tissue Stresses in Organs of Herbaceous Plants (Parts I and II). Journal of Experimental Botany, 46, 1035-1053. http://dx.doi.org/10.1093/jxb/46.8.1035
Kutschera, U. and Nicklas, K.J. (2007) The Epidermal-Growth-Control Theory of Stem Elongation: An Old and a New Perspective. Journal of Plant Physiology, 164, 1395-1409. http://dx.doi.org/10.1016/j.jplph.2007.08.002