Does turgor limit growth in tall trees

The gravitational component of water potential contributes a standing 0.01 MPa m 1 to the xylem tension gradient in plants. In tall trees, this contribution can significantly reduce the water potential near the tree tops. The turgor of cells in buds and leaves is expected to decrease in direct proportion with leaf water potential along a height gradient unless osmotic adjustment occurs. The pressure–volume technique was used to characterize height-dependent variation in leaf tissue water relations and shoot growth characteristics in young and old Douglas-fir trees to determine the extent to which growth limitation with increasing height may be linked to the influence of the gravitational water potential gradient on leaf turgor. Values of leaf water potential ( Y l ), bulk osmotic potential at full and zero turgor, and other key tissue water relations characteristics were estimated on foliage obtained at 13.5 m near the tops of young (approximately 25-year-old) trees and at 34.7, 44.2 and 55.6 m in the crowns of old-growth (approximately 450year-old) trees during portions of three consecutive growing seasons. The sampling periods coincided with bud swelling, expansion and maturation of new foliage. Vertical gradients of Y l and pressure–volume analyses indicated that turgor decreased with increasing height, particularly during the late spring when vegetative buds began to swell. Vertical trends in branch elongation, leaf dimensions and leaf mass per area were consistent with increasing turgor limitation on shoot growth with increasing height. During the late spring (May), no osmotic adjustment to compensate for the gravitational gradient of Y l was observed. By July, osmotic adjustment had occurred, but it was not sufficient to fully compensate for the vertical gradient of Y l . In tall trees, the gravitational component of Y l is superimposed on phenologically driven changes in leaf water relations characteristics, imposing potential constraints on turgor that may be indistinguishable from those associated with soil water deficits. Key-words : Pseudotsuga menziesii ; Douglas-fir; gravitational component of water potential; height growth; osmotic adjustment; pressure–volume curve; turgor maintenance. INTRODUCTION A great deal of attention has recently been focused on the mechanisms responsible for reduced growth in trees as they age and increase in height (Friend 1993; Yoder et al . 1994; Ryan & Yoder 1997; Magnani, Mencuccini & Grace 2000; McDowell et al . 2002). Much of this research has addressed the hydraulic limitation hypothesis, which proposes that reduced growth in ageing and tall trees may be linked to reductions in leaf-specific hydraulic conductance, which in turn lead to reductions in stomatal conductance and therefore photosynthesis (Ryan & Yoder 1997). In addition to strictly hydraulic constraints that may require stomatal limitation of transpiration to regulate leaf water potential ( Y l ) within a relatively narrow range, the gravitational component of Y influences Y l whether or not transpiration is occurring. In the absence of transpiration, the gravitational component of water potential should result in a standing xylem tension gradient of 0.01 MPa per metre increase in height (Scholander et al . 1965; Hellkvist, Richards & Jarvis 1974; Zimmermann 1983; Bauerle et al . 1999). Thus, at the top of a non-transpiring 60-m-tall tree, leaf water potential should be at least 0.6 MPa more negative than foliage at ground level. When transpiration occurs, frictional resistance will lower leaf water potential even further (Hellkvist et al . 1974; Connor, Legge & Turner 1977; Bauerle et al . 1999). The turgor of cells in leaves and buds is expected to decrease in direct proportion with the leaf water potential if the osmotic potential of these cells remains constant. A variety of growth-related processes, including cell formation, expansion and metabolism are dependent on turgor pressure and cell volume (Boyer 1968; Hsiao et al . 1976; Gould & Measures 1977; Ray 1987). However, osmotic adjustment, the active accumulation of symplastic solutes, could maintain turgor and cell volume and may serve to sustain growth and photosynthetic gas exchange with increasing tree height. Nevertheless, compensatory osmotic adjustment may only partially offset reductions in growth with increasing height if it results in a substantial amount of resources being diverted from leaf expansion towards production and accumulation of osmolytes for turgor and volume maintenance. Osmotic adjustment has been well documented as an adaptation to drought and salinity stress (Hsiao et al . 1976; Osonubi & Davies 1978; Turner & Jones 1980; Morgan 1984; McNulty 1985; Heuer & Plaut 1989; Pereira & Pallardy 1989; Ranney, Bassuk & Whitlow 1991; Rieger 1995). 230 D. R. Woodruff et al . © 2004 Blackwell Publishing Ltd, Plant, Cell and Environment, 27, 229–236 However, we know of no studies that have attempted to evaluate the effects of the gravitational component of water potential on the osmotic, morphological and growth characteristics of foliage along a height gradient in tall trees. The objective of this study therefore was to characterize height-dependent variation in leaf tissue water relations and morphological characteristics in young and old Douglas-fir trees to determine the extent to which shoot growth limitation with increasing height may be linked to the influence of the gravitational water potential gradient on leaf turgor. The pressure–volume technique was employed at various phenological stages during three consecutive growing seasons to assess water relations characteristics of foliage sampled along a height gradient from approximately 14 to 57 m. MATERIALS AND METHODS