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Testing Hypotheses That Link Wood Anatomy to Cavitation Resistance and Hydraulic Conductivity in the Genus Acer

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Testing Hypotheses That Link Wood Anatomy to Cavitation Resistance and Hydraulic Conductivity in the Genus Acer New Phytologist Research Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer Frederic Lens1,5, John S. Sperry2, Mairgareth A. Christman2, Brendan Choat3, David Rabaey1 and Steven Jansen4 1Laboratory of Plant Systematics, Institute of Botany and Microbiology, Kasteelpark Arenberg 31 Box 2437, K.U. Leuven, BE-3001 Leuven, Belgium; 2Biology Department, University of Utah, 257S 1400E Salt Lake City, UT 84112, USA; 3Plant Science Division, Research School of Biology, The Australian National University, Canberra, ACT, 0200, Australia; 4Institute for Systematic Botany and Ecology, Ulm University, Albert Einstein Allee 11, D-89081, Ulm, Germany; 5Present address: Netherlands Centre for Biodiversity Naturalis (section NHN), Leiden University, PO Box 9514, NL-2300 RA, Leiden, the Netherlands Summary Author for correspondence: • Vulnerability to cavitation and conductive efficiency depend on xylem anatomy. Frederic Lens We tested a large range of structure–function hypotheses, some for the first time, Tel: +32 16 32 86 37 within a single genus to minimize phylogenetic ‘noise’ and maximize detection of Email: [email protected] functionally relevant variation. Received: 19 August 2010 • This integrative study combined in-depth anatomical observations using light, Accepted: 17 September 2010 scanning and transmission electron microscopy of seven Acer taxa, and compared these observations with empirical measures of xylem hydraulics. New Phytologist (2010) • Our results reveal a 2 MPa range in species’ mean cavitation pressure (MCP). doi: 10.1111/j.1469-8137.2010.03518.x MCP was strongly correlated with intervessel pit structure (membrane thickness and porosity, chamber depth), weakly correlated with pit number per vessel, and not related to pit area per vessel. At the tissue level, there was a strong correlation Key words: Acer, cavitation resistance, hydraulic conductivity, pit structure, rare pit between MCP and mechanical strength parameters, and some of the first evidence hypothesis, vessel distribution, vessel wall is provided for the functional significance of vessel grouping and thickenings on thickenings, wood density. inner vessel walls. In addition, a strong trade-off was observed between xylem- specific conductivity and MCP. Vessel length and intervessel wall characteristics were implicated in this safety–efficiency trade-off. • Cavitation resistance and hydraulic conductivity in Acer appear to be controlled by a very complex interaction between tissue, vessel network and pit characteristics. Introduction (TEM), scanning electron microscope (SEM), and light microscope (LM) observations of seven Acer species with Xylem cavitation represents an important constraint on empirical measures of xylem hydraulics. By studying closely plant survival, and xylem hydraulic conductance potentially related species in a single genus, we reduced phylogenetic limits plant productivity (Rood et al., 2000; McDowell noise in anatomical traits. This facilitated the testing of a et al., 2008; Brodribb & Cochard, 2009). Numerous exper- wide range of structure–function hypotheses, some of which imental studies on xylem hydraulics in woody plants have have not been evaluated before. been published, and there is a rich literature on ecological The experimental literature implicates intervessel pitting wood anatomy that has fostered numerous hypothetical as a key structure determining both hydraulic conductivity correlations between wood structure and its hydraulic function. and cavitation resistance. The flow resistance through inter- However, the few integrative studies that have combined vessel pits accounts for > 50% of the total resistance of the anatomical and experimental approaches mostly lack in- vessel network (Wheeler et al., 2005; Choat et al., 2008). depth anatomical observations using electron microscopy Vulnerability to cavitation of air-seeding is determined by (Wheeler et al., 2005; Sperry et al., 2006; Cochard et al., the ability of the pitted intervessel walls to resist the passage 2008; but see Hacke & Jansen, 2009; Pittermann et al., through an air–water interface (Zimmermann, 1983). Since 2010). The present study bridges the structure–function air-seeding requires the failure of only one intervessel pit, all gap by combining transmission electron microscope else being equal, the more extensive the pitting, the greater Ó 2010 The Authors New Phytologist (2010) 1 New Phytologist Ó 2010 New Phytologist Trust www.newphytologist.com New 2 Research Phytologist should be the probability of one pit failing (‘rare pit’ (small conduits) and efficient xylem (large conduits). hypothesis; Wheeler et al., 2005; Christman et al., 2009). However, experimental support for such a safety vs effi- All else is not necessarily equal, however, and the seemingly ciency correlation is often equivocal and statistically noisy inevitable effect of pit quantity can be compensated for by for drought-induced cavitation (Wheeler et al., 2005; changes in pit structure (Sperry et al., 2007). Hacke et al., 2006). If drought-induced cavitation resist- Recently, a comparative study of three Acer species con- ance is influenced by the extent of intervessel pitting per cluded that the major determinant of cavitation resistance vessel, larger vessels would, on average, be more vulnerable was established by differences in pit structure rather than than smaller ones in the same vessel group. However, if pit quantity (Christman et al., 2009). However, this study cavitation is mostly influenced by intervessel pit structure, did not examine the ultrastructure of the intervessel pits, large vessels could be as safe from air-seeding as smaller ones and pit quantity was expressed as pit area per vessel (Ap) regardless of how much pitting is present. rather than pit number (Np). One of the hypotheses we Acer species have been regularly included in experimental tested in the present paper was to evaluate whether pit struc- studies; for example, some of the first experimental evidence ture (especially pit membrane thickness and porosity, and for air-seeding comes from Acer saccharum (Sperry & Tyree, pit chamber depth) is more crucial than pit quantity per 1988). Also the wood anatomy of Acer has been extensively vessel (whether measured as Ap or Np) for explaining differ- described (e.g. Yamauchi, 1962; Ogata, 1967), but integra- ences in cavitation resistance between Acer species. tive anatomical–physiological work is lacking. We com- Other hypotheses are related to the mechanical strength of bined detailed anatomical observations at the tissue level the vessel walls and surrounding fibres. Cavitation-resistant (i.e. the three-dimensional hydraulic network) and inter- xylem is likely to carry water under more negative pressures. vessel pit level with empirical measures on xylem hydraulics These stronger tensions put a greater mechanical load on for seven Acer species. Our major focus was to evaluate the vessel walls, which need to be well reinforced to avoid previously published anatomical hypotheses with respect to collapse (Hacke et al., 2001). The pressure at which implo- cavitation resistance and conducting efficiency, and to sion of the vessel occurs is a function of the ‘thickness- reveal traits implicated in any trade-off we might observe to-span’ ratio, that is, the double vessel wall thickness per between safety and efficiency within the genus. –1 lumen diameter (Tw Dv ). Wood density (WD) is also strongly influenced by thickness-to-span ratio of the imper- Materials and Methods forate tracheary elements (Hacke et al., 2001; Martı´nez- Cabrera et al., 2009). Because both T D –1 and WD w v Plant material increase with cavitation resistance in many broad-scale stud- ies (Hacke et al., 2001; Jacobsen et al., 2005, 2007; Chave Branches c. 1 m in length and 8–11 mm in diameter belong- et al., 2009; Onoda et al., 2009), we investigated whether ing to different parts of an individual’s crown were sampled these two mechanical parameters are also significant at the around midday for a total of seven Acer taxa during the genus level. months of May–June 2009. Stems were wrapped tightly in The ecological wood anatomical literature has produced plastic and stored in a cold room in the laboratory until use a number of correlational hypotheses between wood anat- (up to 1 wk). Acer pseudoplatanus L. and Acer platanoides omy and function, but many of these have not been well L. were irrigated street trees growing in Salt Lake City evaluated experimentally. More cavitation-resistant species (UT, USA, c. 40°45¢N 111°51¢W), A. saccharinum L. was are thought to possess shorter vessel elements (Le; Carlquist, collected along the Jordan River near Salt Lake City (UT, USA, 1966, 1975; Baas et al., 1983; Lens et al., 2003, 2004, c. 40°41¢27¢¢N 111°55 24¢¢W), and Acer glabrum Torr. var. 2009), lower vulnerability indices (VI = vessel diameter diffusum (Greene) Smiley was collected in a narrow, shaded divided by vessel frequency; Carlquist, 1975), lower meso- canyon in the arid House Range mountains (Sawtooth morphy indices (MI = VI · Le; Carlquist & DeBuhr, Canyon, UT, USA, c. 39°07¢N 113°23¢W). Stems of the 1977), and more pronounced thickenings on inner vessel three remaining taxa were recollected from the same popula- walls (Carlquist, 1966). In addition, when vessels are tions used by Christman et al. (2009). Voucher specimens embedded in a background of nonconductive fibres and not are housed in the University of Utah (Salt Lake City). surrounded
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