Drought‐induced xylem pit membrane damage in aspen and balsam poplar

Abstract

Drought induces an increase in a tree's vulnerability to a loss of its hydraulic conductivity in many tree species, including two common in western Canada, trembling aspen (Populus tremuloides) and balsam poplar (Populus balsamifera). Termed 'cavitation fatigue' or 'air-seeding fatigue', the mechanism of this phenomenon is not well understood, but hypothesized to be a result of damage to xylem pit membranes. To examine the validity of this hypothesis, the effect of drought on the porosity of pit membranes in aspen and balsam poplar was investigated. Controlled drought and bench dehydration treatments were used to induce fatigue and scanning electron microscopy (SEM) was used to image pit membranes for relative porosity evaluations from air-dried samples after ethanol dehydration. A significant increase in the diameter of the largest pore was found in the drought and dehydration treatments of aspen, while an increase in the percentage of porous pit membranes was found in the dehydration treatments of both species. Additionally, the location of the largest pore per pit membrane was observed to tend toward the periphery of the membrane.

High porosity with tiny pore constrictions and unbending pathways characterize the 3D structure of intervessel pit membranes in angiosperm xylem

“…Constriction size diameters in intact, hydrated pit membranes are well below 50 nm, and typically below 20 nm. These values are in general agreement with earlier gold perfusion experiments (Choat et al, ; Choat et al, ; Zhang et al, ), and suggest that much larger pores (> 100 nm) based on SEM are likely preparation artefacts that do not occur in intact, hydrated pit membranes of angiosperms (Hillabrand et al, ; Jansen et al, ; Sano, ). Two additional, novel findings concern estimations of porous medium characteristics, and preliminary evidence that pore constriction sizes might be related to pit membrane thickness.…”

“…Our finding of reduced pore constriction sizes in dried, shrunken pit membranes suggests that pit membrane dehydration after embolism should make pit membranes less prone to air seeding, not more, as predicted based on air‐seeding fatigue (i.e. cavitation fatigue), where embolism increases the chance of subsequent embolism formation (Hacke, Stiller, Sperry, Pittermann, & McCulloh, ) in Aesculus hippocastanum , Helianthus annuus , Populus angustifolia and P. tremuloides (Hacke et al, ; Hillabrand et al, ; Stiller & Sperry, ). The thin and flimsy pit membranes of Aesculus hippocastanum and Populus (Jansen et al, ) may be more prone to developing larger pores after dehydration than species with thicker pit membranes, which might hold up capillary water for a longer time after embolism, although this requires further testing.…”

“…On the other hand, rearrangement of microfibril aggregates during dehydration is likely to create a few large openings if the pit membrane consists of a few layers only. In fact, large pores in dried pit membranes have especially been observed with SEM in species with thin pit membranes, such as Populus tremuloides , P. balsamifera , Salix alba , Aesculus hippocastanum and some vesselless angiosperms (Table ; Hillabrand et al, ; Jansen et al, ; Sperry, Perry, & Sullivan, ; Zhang et al, ). The effect of pit membrane thickness on pore constriction sizes in SEM is also clear when a few microfibril layers have been peeled off during sample preparation (e.g.…”

“…Large pores up to 700 nm (Table ) in SEM images of pit membranes could be formed because of the rearrangement of microfibril aggregates during sample preparation (Jansen et al, ; Sano, ; Shane, McCully, & Canny, ). This dehydration artefact may explain the very large variation in pit membrane pore constrictions as observed under SEM (Harvey & van den Driessche, ; Hillabrand et al, ; Jansen et al, ; Sano, ). A large variation in pore constriction sizes (82–200 nm) based on air injection was also suggested for Rhododendron ponticum (Crombie et al, ).…”

“…This view, however, requires a 3D view of pit membrane pores with multiple constrictions, which is fundamentally different from the oversimplified 2D view of pit membrane pores, with air‐seeding occurring through the single, largest pore (Jansen et al, ). Moreover, dehydration of a pit membrane can change the density and arrangement of its microfibril aggregates and may cause irreversible shrinkage (Hillabrand, Hacke, & Lieffers, ; Li et al, ; Zhang, Klepsch, & Jansen, ; Kotowska et al, 2019). Pit membranes were reported to shrink by 28% when comparing fresh samples (i.e.…”