Embolism spread in the primary xylem of Polystichum munitum: implications for water transport during seasonal drought.

Xylem network structure and function have been characterized for many woody plants, but less is known about fern xylem, particularly in species endemic to climates where water is a limiting resource for months at a time. We characterized seasonal variability in soil moisture and frond water status in a common perennial fern in the redwood understory of a costal California, and then investigated the consequences of drought-induced embolism on vascular function. Seasonal variability in air temperature and soil water content was minimal, and frond water potential declined slowly over the observational period. Our data show that Polystichum munitum was protected from significant drought-induced hydraulic dysfunction during this growing season because of a combination of cavitation resistant conduits (Air-seeding threshold (ASP) = -1.53 MPa; xylem pressure inducing 50% loss of hydraulic conductivity (P50 ) = -3.02 MPa) and a soil with low moisture variability. High resolution micro-computed tomography (MicroCT) imaging revealed patterns of embolism formation in vivo for the first time in ferns providing insight into the functional status of the xylem network under drought conditions. Together with stomatal conductance measurements, these data suggest that P. munitum is adapted to tolerate drier conditions than what was observed during the growing season.

Cavitation Resistance in Seedless Vascular Plants: The Structure and Function of Interconduit Pit Membranes.

Plant water transport occurs through interconnected xylem conduits that are separated by partially digested regions in the cell wall known as pit membranes. These structures have a dual function. Their porous construction facilitates water movement between conduits while limiting the spread of air that may enter the conduits and render them dysfunctional during a drought. Pit membranes have been well studied in woody plants, but very little is known about their function in more ancient lineages such as seedless vascular plants. Here, we examine the relationships between conduit air seeding, pit hydraulic resistance, and pit anatomy in 10 species of ferns (pteridophytes) and two lycophytes. Air seeding pressures ranged from 0.8 ± 0.15 MPa (mean ± sd) in the hydric fern Athyrium filix-femina to 4.9 ± 0.94 MPa in Psilotum nudum, an epiphytic species. Notably, a positive correlation was found between conduit pit area and vulnerability to air seeding, suggesting that the rare-pit hypothesis explains air seeding in early-diverging lineages much as it does in many angiosperms. Pit area resistance was variable but averaged 54.6 MPa s m-1 across all surveyed pteridophytes. End walls contributed 52% to the overall transport resistance, similar to the 56% in angiosperm vessels and 64% in conifer tracheids. Taken together, our data imply that, irrespective of phylogenetic placement, selection acted on transport efficiency in seedless vascular plants and woody plants in equal measure by compensating for shorter conduits in tracheid-bearing plants with more permeable pit membranes.

The effect of subambient to elevated atmospheric CO2 concentration on vascular function in Helianthus annuus: implications for plant response to climate change.

Plant gas exchange is regulated by stomata, which coordinate leaf-level water loss with xylem transport. Stomatal opening responds to internal concentrations of CO2 in the leaf, but changing CO2 can also lead to changes in stomatal density that influence transpiration. Given that stomatal conductance increases under subambient concentrations of CO2 and, conversely, that plants lose less water at elevated concentrations, can downstream effects of atmospheric CO2 be observed in xylem tissue? We approached this problem by evaluating leaf stomatal density, xylem transport, xylem anatomy and resistance to cavitation in Helianthus annuus plants grown under three CO2 regimes ranging from pre-industrial to elevated concentrations. Xylem transport, conduit size and stomatal density all increased at 290 ppm relative to ambient and elevated CO2 concentrations. The shoots of the 290-ppm-grown plants were most vulnerable to cavitation, whereas xylem cavitation resistance did not differ in 390- and 480-ppm-grown plants. Our data indicate that, even as an indirect driver of water loss, CO2 can affect xylem structure and water transport by coupling stomatal and xylem hydraulic functions during plant development. This plastic response has implications for plant water use under variable concentrations of CO2, as well as the evolution of efficient xylem transport.

Structure-function constraints of tracheid-based xylem: a comparison of conifers and ferns.

The ferns comprise one of the most ancient tracheophytic plant lineages, and occupy habitats ranging from tundra to deserts and the equatorial tropics. Like their nearest relatives the conifers, modern ferns possess tracheid-based xylem but the structure-function relationships of fern xylem are poorly understood. Here, we sampled the fronds (megaphylls) of 16 species across the fern phylogeny, and examined the relationships among hydraulic transport, drought-induced cavitation resistance, the xylem anatomy of the stipe, and the gas-exchange response of the pinnae. For comparison, the results are presented alongside a similar suite of conifer data. Fern xylem is as resistant to cavitation as conifer xylem, but exhibits none of the hydraulic or structural trade-offs associated with resistance to cavitation. On a conduit diameter basis, fern xylem can exhibit greater hydraulic efficiency than conifer and angiosperm xylem. In ferns, wide and long tracheids compensate in part for the lack of secondary xylem and allow ferns to exhibit transport rates on a par with those of conifers. We suspect that it is the arrangement of the primary xylem, in addition to the intrinsic traits of the conduits themselves, that may help explain the broad range of cavitation resistance in ferns.