Declining Hydraulic Efficiency As Transpiring Leaves Desiccate
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T. J. Brodribb & N. M. Holbrook Plant, Cell and Environment (2006) 29, 2205–2215 doi: 10.1111/j.1365-3040.2006.01594.x Declining hydraulic efficiency as transpiring leaves desiccate: two types of response* TIM J. BRODRIBB1,2 & N. MICHELE HOLBROOK2 1Department of Plant Science, University of Tasmania, PO Box 252-55, TAS, Australia 7001, and 2Department of Organismic and Evolutionary Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA, USA ABSTRACT between sites of water delivery and water loss while not interfering with light harvesting or the CO2 diffusion path- The conductance of transpiring leaves to liquid water (K ) leaf way. In most plants, these demands are met by a hierarchi- was measured across a range of steady-state leaf water cal branching network of veins that terminate in extremely potentials ( ). Manipulating the transpiration rate in Yleaf small xylem conduits, tens to hundreds of microns from the excised leaves enabled us to vary in the range 0.1 MPa Yleaf - sub-stomatal cavities where the bulk of evaporation takes to less than 1.5 MPa while using a flowmeter to monitor - place (Wylie 1943; Roth-Nebelsick et al. 2001). Current the transpiration stream. Employing this technique to mea- research suggests that this vascular arrangement generates sure how desiccation affects K in 19 species, including leaf a large resistance to water flow through leaves, representing lycophytes, ferns, gymnosperms and angiosperms, we found between 30 and 90% of the hydraulic resistance of the two characteristic responses. Three of the six angiosperm whole plant (Salleo, Nardini & Lo Gullo 1997; Nardini, species sampled maintained a steady maximum K while leaf Tyree & Salleo 2001; Sack et al. 2002). One important con- remained above 1.2 MPa, although desiccation of Yleaf - sequence of this is that even in plants with good access to leaves beyond this point resulted in a rapid decline in K . leaf soil water and high stem water potential, stomatal closure In all other species measured, declining led to a pro- Yleaf could be induced during the day due to water potential portional decrease in K , such that midday of leaf Yleaf gradients generated in the hydraulic passage from petiole unstressed plants in the field was sufficient to depress K leaf to sub-stomatal cavities. It follows therefore, that the effi- by an average of 37%. It was found that maximum K was leaf ciency of leaf water transport plays a governing role in strongly correlated with maximum CO assimilation rate, 2 processes linked to leaf water status, most importantly, sto- while K = 0 occurred at a slightly less negative than leaf Yleaf matal behaviour and photosynthetic gas exchange. at leaf turgor loss. A strong linear correlation across species The efficiency of water transport within leaves, or leaf between Yleaf at turgor loss and Yleaf at Kleaf = 0 raises the hydraulic conductance (Kleaf), has been demonstrated to was related to declining cell possibility that declining Kleaf vary enormously between species (Tyree et al. 1999; Bro- turgor in the leaf prior to the onset of vein cavitation. The dribb et al. 2005), ecological niches (Nardini & Salleo 2005; vulnerability of leaves rehydrating after desiccation was Sack, Tyree & Holbrook 2005) and seasons (Salleo et al. compared with vulnerability of leaves during steady-state 2002; Brodribb & Holbrook 2003a). Among this variation, evaporation, and differences between methods suggest perhaps the best physiological correlate with Kleaf is sto- that in many cases vein cavitation occurs only as Kleaf matal conductance (Brodribb & Holbrook 2004b; Brodribb approaches zero. et al. 2005; Nardini, Salleo & Andri 2005). Considering that these parameters represent liquid and gas phase con- INTRODUCTION ductances of water moving in a serial pathway through the leaf, this correlation, and similar relationships between Most of the water transported in vascular plants is destined stem hydraulic conductance and gs (Nardini & Salleo 2000; to replace leaf water sacrificed during the diffusive uptake Meinzer 2002) indicate that water potential gradients in of atmospheric CO2 for photosynthetic carbon fixation. non-stressed plants are relatively conservative. That is, dur- Irrigation of the leaf mesophyll thus represents the crux ing evolution plants appear to increase the conductance of of a plant’s vascular function. Leaves make complicated the vascular system in order to accommodate increased demands of the vascular system, requiring close proximity transpirational demand rather than operating at increased water potential gradients. Photosynthetic performance has Correspondence: T. J. Brodribb. Fax: 61 362 262698; e-mail: also been linked with Kleaf over a diverse selection of plants, [email protected] although the nature of the relationship is unclear in tropical angiosperms, where values of K appear to be higher than *This work was supported by an Australian Research Council leaf Fellowship (TJB), National Science Foundation (grant no. IBN in other species, but diurnally variable (Brodribb et al. 0212792) and by the National Geographic Society (grant no. 2005). Emerging relationships between Kleaf and anatomical 7475-03). characters that limit leaf gas exchange such as stomatal © 2006 The Authors Journal compilation © 2006 Blackwell Publishing Ltd 2205 2206 T. J. Brodribb & N. M. Holbrook pore area index and palisade thickness (Aasamaa, Sober & examine the relationship between Kleaf and Ψleaf in plants Rahi 2001; Sack et al. 2003; Sack & Frole 2006) indicate that spanning a large range of morphological and anatomical hydraulic efficiency in the leaf vascular system is highly complexity, from lycopod to angiosperm. We investigate adaptive. Kleaf under conditions that closely replicate those experi- While there is an ever-expanding library of data for Kleaf enced by leaves in situ by measuring Ψleaf under known variation between species, data describing the vulnerability conditions of leaf transpiration (Tyree et al. 1999). In a of the whole-leaf hydraulic pathway to dysfunction under novel application of this technique, we were able to create water stress remains sparse. Extensive work on stems has a large range of transpiration (E) in each species by using shown that the conductivity of the xylem is critically depen- a variable fan to force water loss, thus giving a measure of dent on water potential (Ψ), usually declining rapidly as Ψ Kleaf at a range of Ψleaf. Data from this steady-state tech- inside the xylem apoplast falls below a threshold value nique are compared with Kleaf vulnerability to dehydration (Sperry & Tyree 1988). Leaves are clearly sensitive to water determined by the non-steady-state pressure relaxation stress-induced depression of hydraulic conductance (Lin- technique (Brodribb & Holbrook 2003b), to indicate the ton & Nobel 2001; Cochard 2002; Brodribb & Holbrook processes responsible for impeding water flow at low water 2003b; Lo Gullo et al. 2003; Brodribb & Holbrook 2004a), potential. and due to the disproportionately large contribution leaves make to whole-plant hydraulic resistance, leaf vulnerability has the potential to dictate how plants respond to short- MATERIALS AND METHODS term water stress. This has been borne out by recent studies Plant material demonstrating a good correspondence between turgor loss, stomatal closure and leaf hydraulic dysfunction (Brodribb A list of 19 species, designed to span a large climatic as well & Holbrook 2003b). However, the exact nature of the as morphological and phylogenetic range, was sampled in temperate forest in Hobart, Australia, and Harvard Forest, decline in Kleaf with leaf water potential, remains poorly understood, hampered by a lack of techniques for probing USA and tropical forest at Santa Rosa National Park, Costa Rica; Lake Eacham, Australia; and Mt. Dzumac, Kleaf while leaves are simultaneously exposed to significant negative water potentials. To date, the only methods used New Caledonia. Among this selection were six lycophytes, two ferns, five gymnosperms (including a cycad) and six to examine the impact of water stress on Kleaf have used the angiosperms (see Table 1). All gymnosperm and angio- kinetics of Ψleaf relaxation (Brodribb & Holbrook 2003b), or measured infiltration rates of droughted leaves exposed sperm leaves were collected from small trees (< 4 m) in full to sub-atmospheric pressures (Trifilò et al. 2003). While sun, while only two of the fern species were collected in the both these techniques have successfully shown responses of sun and the other six collected in forest understorey. Only healthy mature leaves of a similar age were used in each Kleaf to drought, the conditions under which leaves are mea- sured in both cases are rather distant from those experi- species sample so as to minimize within species variation to a minimum. enced by leaves in the field. In the case of Ψleaf relaxation, leaves are measured during a rapid collapse of the water potential gradient, while leaves exposed to vacuum infiltra- K determined by evapotranspiration tion are measured with intercellular spaces flooded and leaf Ψ virtually no gradient in leaf. If we are to determine whether This method calculates Kleaf of a leaf transpiring at a known reductions in Kleaf in the field are likely to be rare events steady-state as the ratio of transpiration flux over the associated with significant plant stress, or common events pressure differential between water entering the leaf and that limit photosynthesis on a diurnal basis, it is desirable steady-state Ψleaf