Leaf Hydraulic Vulnerability Is Related to Conduit Dimensions and Drought Resistance Across a Diverse Range of Woody Angiosperms
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New Phytologist Research Leaf hydraulic vulnerability is related to conduit dimensions and drought resistance across a diverse range of woody angiosperms Christopher J. Blackman, Tim J. Brodribb and Gregory J. Jordan School of Plant Science, University of Tasmania, Private Bag 55, Hobart, Tas. 7001, Australia Summary Author for correspondence: • Hydraulic dysfunction in leaves determines key aspects of whole-plant responses Tim Brodribb to water stress; however, our understanding of the physiology of hydraulic dys- Tel: +61 3 62261707 function and its relationships to leaf structure and ecological strategy remains Email: [email protected] incomplete. Received: 23 May 2010 • Here, we studied a morphologically and ecologically diverse sample of angio- Accepted: 16 July 2010 sperms to test whether the water potential inducing a 50% loss in leaf hydraulic conductance (P50leaf) is predicted by properties of leaf xylem relating to water New Phytologist (2010) 188: 1113–1123 tension-induced conduit collapse. We also assessed the relationships between P50leaf doi: 10.1111/j.1469-8137.2010.03439.x and other traits considered to reflect drought resistance and ecological strategy. • Across species, P50leaf was strongly correlated with a theoretical predictor of vul- nerability to cell collapse in minor veins (the cubed ratio of the conduit wall thick- Key words: cavitation, cell collapse, drought resistance, functional traits, leaf hydraulics, ness to the conduit lumen breadth). P50leaf was also correlated with mesophyll pressure–volume, water stress, xylem traits known to be related to drought resistance, but unrelated to traits associated vulnerability. with carbon economy. • Our data indicate a link between the structural mechanics of leaf xylem and hydraulic function under water stress. Although it is possible that collapse may contribute directly to dysfunction, this relationship may also be a secondary product of vascular economics, suggesting that leaf xylem is dimensioned to avoid wall collapse. implications for plant function because photosynthesis and Introduction growth are dependent on the efficient supply of water to the The ability of plants to maintain hydraulic conductance sites of evaporation (Hubbard et al., 2001; Brodribb & under conditions of water stress is a central driver of species’ Holbrook, 2007). The vulnerability of the hydraulic path- distribution patterns (Engelbrecht et al., 2007). Because way to dysfunction is typically assessed as P50, or the physical tension increases in the xylem when leaf water tension required to cause a 50% decline in hydraulic con- potentials fall as a result of transpirational water loss, the ductance. In leaves, P50 has been linked to plant survival hydraulic pathway from the roots to the shoots is exposed (Blackman et al., 2009; Brodribb & Cochard, 2009), and to stresses that can compromise the capacity of plants to stem P50 has been shown to be adaptive across broad taxo- transport water. Although this tension-induced loss of nomic groups in relation to gradients in water availability hydraulic conductance is often attributed to cavitation (Brodribb & Hill, 1999; Pockman & Sperry, 2000; resulting from air bubbles entering the water column via pit Maherali et al., 2004). membranes (Zimmermann, 1983; Tyree & Sperry, 1989), Hydraulic vulnerability to dysfunction is a highly inte- it may also be a consequence of xylem wall implosion and grated component of a suite of physiological and anatomical cell collapse (Cochard et al., 2004; Brodribb & Holbrook, traits that reflect different patterns of hydraulic response to 2005) or increased extra-xylary resistance (Brodribb & drought. In dry climate environments, P50 in stems is Holbrook, 2004). Hydraulic dysfunction has serious correlated with the minimum seasonal water potential Ó The Authors (2010) New Phytologist (2010) 188: 1113–1123 1113 Journal compilation Ó New Phytologist Trust (2010) www.newphytologist.com New 1114 Research Phytologist experienced by species in the field (Pockman & Sperry, Materials and Methods 2000; Bhaskar et al., 2007; Jacobsen et al., 2007). Coordination between loss of leaf hydraulic conductance Plant species and habitat and the regulation of stomatal conductance also suggests that hydraulic vulnerability to dysfunction in leaves plays an We sampled 20 phylogenetically disparate woody angio- important role in plant responses to short-term water stress sperm species from montane rainforest (15 species) and dry (Brodribb et al., 2003). Others have demonstrated a strong sclerophyll forest (five species) on the island of Tasmania, in positive correlation between wood density (WD) and P50 cool temperate Australia (Table 1). Nineteen of these species in stems (Hacke et al., 2001) and have emphasized the were evergreen, but ranged in their degree of scleromorphy inherent costs of increased resistance to hydraulic dysfunc- (as reflected by leaf mass per unit area, LMA) from ) tion in terms of both xylem cell wall reinforcement and 137 g m 2 in the relatively broad leaves of the rainforest ) narrower xylem conduits that reduce hydraulic efficiency species Atherosperma moschatum to 772 g m 2 in the extre- (Hacke et al., 2006) and affect plant growth (Poorter et al., mely scleromorphic needles of Hakea lissosperma (Table 1). 2010). The sample group also included the winter deciduous spe- ) Most studies of the functional and ecological significance cies Nothofagus gunnii with LMA = 102 g m 2. One of the of hydraulic vulnerability have focused on stems (Hacke evergreen species, Tasmannia lanceolata, was vessel-less. et al., 2001, 2009; Maherali et al., 2004). However, water Climatic limits in terms of minimum water availability, as transport in leaves is functionally distinct from that in stems reflected by the fifth percentile of mean annual rainfall ) and, because of their relatively high hydraulic resistance across each species’ distribution, ranged from 351 mm yr 1 ) (Sack & Holbrook, 2006), leaves impose significant for the dry forest species Bursaria spinosa to 1268 mm yr 1 constraints on maximum stomatal conductance and photo- for the montane rainforest species Orites diversifolia (C. J. synthetic capacity (Brodribb et al., 2005). Compared with Blackman et al., unpublished). These species are known to stems, leaves are often more vulnerable to hydraulic dys- vary widely in leaf xylem vulnerability to hydraulic dysfunc- function (Salleo et al., 2000; Brodribb et al., 2003; Choat tion, which, in turn, is closely correlated with the estimates et al., 2005a; Hao et al., 2008). They also differ in xylem of climatic limits for water availability described above (C. structure. Unlike the xylem in stems (Wagner et al., 1998), J. Blackman et al., unpublished). much of the leaf xylem is not reinforced to withstand mechanical rupture under dynamic or static loads, and Vulnerability to hydraulic dysfunction therefore may be vulnerable to cell collapse under negative pressure. Cell collapse has been linked to leaf hydraulic dys- For each species, leaf hydraulic vulnerability curves were function in some conifers (Cochard et al., 2004; Brodribb constructed by measuring the percentage loss of leaf hydraulic & Holbrook, 2005), although cavitation in the petioles and conductance from maximum values (Kmax) in leaves rehy- midribs of a number of conifer and angiosperm species has drated from a range of leaf water potentials (Wleaf). For the also been reported (Nardini et al., 2001; Johnson et al., purposes of these curves, Kleaf was measured by assessing the 2009a). The large volumes of air inside these leaves create kinetics of Wleaf relaxation upon leaf rehydration (Brodribb maximum pressure differentials across xylem cell walls and & Holbrook, 2003). Briefly, hydrated branches from three create a substantial risk of xylem implosion in the leaf veins. individuals of each species were cut early in the morning and However, this phenomenon has not been observed in angio- immediately bagged to arrest water loss. Having transported sperms, and no studies have examined how leaf xylem them to the laboratory, the branches were allowed to desiccate anatomy may relate to drought resistance across different slowly at light intensities sufficient to ensure light-induced ) ) angiosperm species. hydraulic function (c.50lmol quanta m 2 s 1) over a Here, we examine how interspecific variation in the maximum of 48 h or until the percentage loss of Kleaf vulnerability of leaves to hydraulic dysfunction (P50leaf)is approached 100%. Initial Wleaf was determined by measuring related to a number of structural and functional traits in a leaves neighbouring the sample leaf in a Scholander pressure sample of woody temperate angiosperm species with a chamber (PMS, Albany, OR, USA). The sample leaf was broad range of leaf forms and rainfall preferences. then cut under water and allowed to rehydrate for a period Specifically, we tested whether structural properties of the of between 30 and 300 s depending on the initial Wleaf. leaf xylem were related to hydraulic vulnerability, on the Final Wleaf was measured with the pressure chamber, and basis that the wall thickness and lumen diameter of leaf Kleaf was calculated from the ratio of the initial to final Wleaf xylem conduits determine their capacity to resist implosion and the capacitance of the leaf: by water tension. We also tested for relationships between K ¼ C ln½W =W =T Eqn 1 leaf hydraulic vulnerability and other leaf structural and leaf leaf o f functional traits that are widely recognized to influence [Wo,