Pit Membrane Porosity and Water Stress-Induced Cavitation in Four Co-Existing Dry Rainforest Tree Species

Abstract

Aspects of xylem anatomy and vulnerability to water stress-induced embolism were examined in stems of two droughtdeciduous species, Brachychiton australis (Schott and Endl.) A. Terracc. and Cochlospermum gillivraei Benth., and two evergreen species, Alphitonia excelsa (Fenzal) Benth. and Austromyrtus bidwillii (Benth.) Burret., growing in a seasonally dry rainforest. The deciduous species were more vulnerable to water stress-induced xylem embolism. B. australis and C. gillivraei reached a 50% loss of hydraulic conductivity at Ϫ3.17 MPa and Ϫ1.44 MPa, respectively; a 50% loss of hydraulic conductivity occurred at Ϫ5.56 MPa in A. excelsa and Ϫ5.12 MPa in A. bidwillii. To determine whether pit membrane porosity was responsible for greater vulnerability to embolism (air seeding hypothesis), pit membrane structure was examined. Expected pore sizes were calculated from vulnerability curves; however, the predicted inter-specific variation in pore sizes was not detected using scanning electron microscopy (pores were not visible to a resolution of 20 nm). Suspensions of colloidal gold particles were then perfused through branch sections. These experiments indicated that pit membrane pores were between 5 and 20 nm in diameter in all four species. The results may be explained by three possibilities: (a) the pores of the expected size range were not present, (b) larger pores, within the size range to cause air seeding, were present but were rare enough to avoid detection, or (c) pore sizes in the expected range only develop while the membrane is under mechanical stress (during air seeding) due to stretching/flexing.Xylem cavitation and embolism are recognized as major constraints affecting plants regularly exposed to water stress (Tyree and Sperry, 1989;Milburn, 1993). Water in the xylem is under negative pressure, or tension, i.e. it is held in a metastable state, below its vapor pressure, a condition that increases the likelihood of cavitation occurring (Oertli, 1971;Pickard, 1981). Cavitation is the process whereby a vapor phase is introduced to the xylem water column, creating an embolism. Embolisms are gas bubbles consisting initially of water vapor and later air, which become trapped within xylem conduits. Because of its inability to transmit tension, the vapor phase limits the volume flow of water through the conduit, reducing the plant's capacity to deliver water to the canopy (Meinzer et al., 2001). Plants must minimize this disruption to water transport to avoid effects on leaf water status that may result in limitations on stomatal conductance and photosynthesis.The structure of xylem vessels is seen as an important factor in determining the occurrence of water stress-induced cavitation (Zimmermann, 1983). Xylem vessels are bounded by pit membranes, through which water must pass to move from one vessel to the next. Pit membranes are the degraded primary cell walls and middle lamella of the vessels and are composed of tightly inter-woven cellulose microfibrils in a matrix of hemicellulose and pectin polysaccharide...

Hydraulic architecture of lianas in a semiarid climate: efficiency or safety?

“…On one hand, the increase of N pit may imply a lower cavitation resistance because the occurrence and size of large pit membrane pores is thought to increase with the total pit membrane area per vessel (Wheeler et al 2005). On the other hand, membrane pores often have similar sizes among species, and the rare largest membrane pore per vessel determines the level of safety against cavitation (Choat et al 2003). Thus, the smaller surface area of intervessel pits that we found may limit the area of the pit membrane and decrease the chance of occurrence of large pores in the membrane.…”

Management of crop water under drought: a review

“…Species differences in cavitation vulnerability may be related to the degree of stomata control, i.e. iso-versus anisohydric species (Tardieu and Simonneau 1998), differences in xylem structure (Sperry 2003;Choat et al 2003) and xylem embolism repair mechanisms (Zwieniecki and Holbrook 2009).…”

A physiologically explicit morphospace for tracheid-based water transport in modern and extinct seed plants

“…Tracheids with more or larger pits are rare in living plants but widespread in extinct groups, including Lyginopteris, Medullosa, Callistophyton, Cordaites, early conifers (Philippe and Bamford 2008), tgigantopterids (Li and Taylor 1998), and the Mesozoic seed plant Pentoxylon (Taylor and Taylor 1993). The drawbacks to increased pit area may have included decreased structural support from thinner cell walls (Hacke et al 2001a, Pittermann et al 2006b) and an increased probability that embolisms would spread because of microfibril failure, leaving large pores in pit membranes (Choat et al 2003). …”

“…Pit membrane porosity is based on values estimated from direct measurement or inferred from whole-plant measurements (Choat et al 2003, Choat et al 2006, Choat et al 2004). …”