Cell Wall Yield Properties of Growing Tissue

Abstract

Growing pea stem tissue, when isolated from an external supply of water, undegoes stress relaxation because of continued loosening of the cell wall. A theoretical analysis is presented to show that such stress relaxation should result in an exponential decrease in turgor pressure down to the yield threshold (Y), with a rate constant given by 4e where 0 is the metabolically maintained irreversible extensibility of the cell wall and e is the volumetric elastic modulus of the cell. This theory represents a new method to determine 0 in growing tissues. Stress relaxation was measured in pea (Pisum satinis L.) stem segments using the pressure microprobe technique. From the rate of stress relaxation,# of segments pretreated with water was calculated to be 0.08 per megapascal per hour while that of auxin-pretreated tissue was 0.24 per megapascal per hour. These values agreed closely with estimates of * made by a steady-state technique. The yield threshold (0.29 megapas-cal) was not affected by auxin. Technical difficulties with measuring 0 by stress relaxation may arise due to an internal water reserve or due to changes in # subsequent to excision. These difficulties are discussed and evaluated. A theoretical analysis is also presented to show that the tissue hydraulic conductance may be estimated from the TV, of tissue swelling. Experimentafly, pea stems had a swelling Ty,of 2.0 minutes, corresponding to a relative hydraulic conductance of about 2.0 per megapascal per hour. This value is at least 8 times larger than 0. From these data and from computer modeling, it appears that the radial gradient in water potential which sustains water uptake in growing pea segments is small (0.04 megapascal). This means that hydraulic conductance does not substantially restrict growth. The results also demonstrate that the stimulation of growth by auxin can be entirely accounted for by the change in #. Irreversible cell enlargement is the primary means by which plants increase in size and surface area during growth. Such cell enlargement requires simultaneous water absorption to increase cell volume and irreversible expansion of the cell wall to accommodate the water influx and to generate new surface area. It is the relative values of the coefficients governing these two physically distinct but coupled processes that determine whether water transport or wall yielding limits growth (7, 18, 26). Water absorption occurs in response to a gradient in water potential (A4,) between the growing cells and the water source. For growth studies, it is frequently convenient to define growth in terms of relative, rather than absolute, change in cell volume. Using this convention, the relative rate of water absorption (dV/ Vdt) is governed by a transport coefficient (a relative hydraulic conductance, L; see Table I for units), such that: 1 dV= L (AO) Under steady conditions, the quantity dV/Vdt equals the relative growth rate. The water potential gradient A4' is established and maintained by 'loosening' ofthe cell wall; such loosening permits a turgor-driven yielding of the wall and consequent decrease in the turgor pressure and water potential ofthe growing cell (7, 18, 26). To assess whether water transport (that is, L) restricts the growth rate of plant tissues, most recent studies have attempted to estimate the A4. needed to sustain the water flux associated with growth. This gradient is negligible in tissues with very high hydraulic conductance, but may be sizeable in tissues with low hydraulic conductance (18, 22). Most studies have concluded that the water potentials of growing tissues are from 0.15 to 0.4 MPa (1.5-4 bar) lower than that expected ofwell-hydrated tissues (2, 3, 21, 22; see 28 for a critique of earlier work). In these studies, it was generally assumed that such disequilib-rium in water potential was due to low tissue hydraulic conduct-ance. By this interpretation, plant growth appeared to be limited by water entry into the growing tissue. However, recent work (8) with growing pea, cucumber, and soybean stems has suggested an alternative interpretation, that the apoplasts of these tissues contain a substantial concentration of solutes-high enough to account for the low 4A. Moreover, Cosgrove and Cleland (9) observed that turgor pressure (P) and 4y in pea stems changed very little when growth rates were altered over a 20-fold range by various treatments. This result suggested that the hydraulic conductance was sufficiently large that it did not impede the rate of water entry into the growing tissue, and that growth was controlled primarily by the yielding properties of the cell wall. These wall yielding properties, however, were not measured. The rate of wall yielding has been shown in a number of studies to depend on the turgor pressure (P) in excess ofa critical turgor (the 'yield threshold', Y) according to the approximate relation (5, 11, 14): 1 dV _(P-Y), for P> y V dt (2) The parameter X is a coefficient relating the growth rate to the turgor in excess of Y. Current evidence indicates that 4 comprises two distinct phenomena: the rate of 'loosening' of the wall to enable it to yield to the wall stress generated by turgor, and the potential amount of turgor-dependent extension which results from each 'loosening event' (5, 6, 26). The first phenomenon is coupled to metabolic processes, is thought to be mediated by 347 (1)