Peter J. Melcher

Vulnerability of Xylem Vessels to Cavitation in Sugar Maple. Scaling from Individual Vessels to Whole Branches

The relation between xylem vessel age and vulnerability to cavitation of sugar maple (Acer saccharum Marsh.) was quantified by measuring the pressure required to force air across bordered pit membranes separating individual xylem vessels. We found that the bordered pit membranes of vessels located in current year xylem could withstand greater applied gas pressures (3.8 MPa) compared with bordered pit membranes in vessels located in older annular rings (2.0 MPa). A longitudinal transect along 6-year-old branches indicated that the pressure required to push gas across bordered pit membranes of current year xylem did not vary with distance from the growing tip. To understand the contribution of age-related changes in vulnerability to the overall resistance to cavitation, we combined data on the pressure thresholds of individual xylem vessels with measurements of the relative flow rate through each annual ring. The annual ring of the current year contributed only 16% of the total flow measured on 10-cm-long segments cut from 6-year-old branches, but it contributed more than 70% of the total flow when measured through 6-year-old branches to the point of leaf attachment. The vulnerability curve calculated using relative flow rates measured on branch segments were similar to vulnerability curves measured on 6-year-old branches (pressure that reduces hydraulic conductance by 50% = 1.6–2.4 MPa), whereas the vulnerability curve calculated using relative flow rates measured on 6-year-old branches were similar to ones measured on the extension growth of the current year (pressure that reduces hydraulic conductance by 50% = 3.8 MPa). These data suggest that, in sugar maple, the xylem of the current year can withstand larger xylem tensions than older wood and dominates water delivery to leaves.

Analysis of spatial and temporal dynamics of xylem refilling in Acer rubrum L. using magnetic resonance imaging

We report results of an analysis of embolism formation and subsequent refilling observed in stems of Acer rubrum L. using magnetic resonance imaging (MRI). MRI is one of the very few techniques that can provide direct non-destructive observations of the water content within opaque biological materials at a micrometer resolution. Thus, it has been used to determine temporal dynamics and water distributions within xylem tissue. In this study, we found good agreement between MRI measures of pixel brightness to assess xylem liquid water content and the percent loss in hydraulic conductivity (PLC) in response to water stress (P50 values of 2.51 and 2.70 for MRI and PLC, respectively). These data provide strong support that pixel brightness is well correlated to PLC and can be used as a proxy of PLC even when single vessels cannot be resolved on the image. Pressure induced embolism in moderately stressed plants resulted in initial drop of pixel brightness. This drop was followed by brightness gain over 100 min following pressure application suggesting that plants can restore water content in stem after induced embolism. This recovery was limited only to current-year wood ring; older wood did not show signs of recovery within the length of experiment (16 h). In vivo MRI observations of the xylem of moderately stressed (~-0.5 MPa) A. rubrum stems revealed evidence of a spontaneous embolism formation followed by rapid refilling (~30 min). Spontaneous (not induced) embolism formation was observed only once, despite over 60 h of continuous MRI observations made on several plants. Thus this observation provide evidence for the presence of naturally occurring embolism-refilling cycle in A. rubrum, but it is impossible to infer any conclusions in relation to its frequency in nature.

Growth and Photosynthetic Responses of Scaevola sericea, A Hawaiian Coastal Shrub, to Substrate Salinity and Salt Spray

Growth patterns, water relations, and photosynthetic traits in Scaevola sericea plants grown under different levels of substrate salinity and salt spray were studied. Scaevola sericea is a dominant shrub species in coastal strand ecosystems throughout the tropical and subtropical Pacific and Indian Oceans. Seventy-two cuttings from two coastal sites on the island of Oahu (Hawaii) were grown in a greenhouse under six treatments that resulted from the combination of three levels of substrate salinity (0, 100, and 335 mOsm kg-1) and two levels of simulated salt spray (0 and 1200 mg salt m-2 d-1). Several characteristics of S. sericea were strongly affected by substrate salinity but only weakly affected by salt spray. New stem and leaf biomass per plant decreased by ca. 65% as substrate salinity increased from 0 to 335 mOsm kg-1; photosynthetic rates decreased by only 20% over the same salinity range. Leaf sap osmolarity increased 300 mOsm kg-1 as substrate salinity changed from 0 to 335 mOsm kg-1, allowing the maintenance of a constant soil-to-leaf osmotic potential gradient favorable for water uptake even at higher salinity levels. Carboxylation capacity, determined by the initial slope of net CO2 assimilation--intercellular CO2 concentration relationships, remained constant for plants grown under different levels of salinities. The δ13C of leaves increased from -29.2‰ to -26.3‰ with increasing salinity and was associated with lower stomatal conductances but nearly unchanged photosynthetic rates. Scaevola sericea is capable of substantial growth and physiological responses, which apparently are required to maintain a positive carbon balance in coastal habitats characterized by large temporal and spatial variations in substrate salinity and salt spray levels.

The Dynamics of "Dead Wood": Maintenance of Water Transport Through Plant Stems'

Abstract The lack of mobility in plants is often interpreted as a sign of their passivity in the face of environmental variation. This view is perhaps most firmly entrenched with regard to water transport through the xylem in which water flows through the lumen of cells that are “dead” (i.e., lack any cytoplasm or nucleus) at maturity. However, recent work demonstrates that a number of active, physiological processes may be involved in maintaining the transport capacity of this essential pathway. Here we review work relating to both embolism repair and the effect of ion concentrations on xylem hydraulic properties as examples of such dynamic processes.

SUPERCOOLING CAPACITY INCREASES FROM SEA LEVEL TO TREE LINE IN THE HAWAIIAN TREE SPECIES METROSIDEROS POLYMORPHA

Population‐specific differences in the freezing resistance of Metrosideros polymorpha leaves were studied along an elevational gradient from sea level to tree line (located at ca. 2500 m above sea level) on the east flank of the Mauna Loa volcano in Hawaii. In addition, we also studied 8‐yr‐old saplings grown in a common garden from seeds collected from the same field populations. Leaves of low‐elevation field plants exhibited damage at −2°C, before the onset of ice formation, which occurred at −5.7°C. Leaves of high‐elevation plants exhibited damage at ca. −8.5°C, concurrent with ice formation in the leaf tissue, which is typical of plants that avoid freezing in their natural environment by supercooling. Nuclear magnetic resonance studies revealed that water molecules of both extra‐ and intracellular leaf water fractions from high‐elevation plants had restricted mobility, which is consistent with their low water content and their high levels of osmotically active solutes. Decreased mobility of water molecules may delay ice nucleation and/or ice growth and may therefore enhance the ability of plant tissues to supercool. Leaf traits that correlated with specific differences in supercooling capacity were in part genetically determined and in part environmentally induced. Evidence indicated that lower apoplastic water content and smaller intercellular spaces were associated with the larger supercooling capacity of the plant’s foliage at tree line. The irreversible tissue‐damage temperature decreased by ca. 7°C from sea level to tree line in leaves of field populations. However, this decrease appears to be only large enough to allow M. polymorpha trees to avoid leaf tissue damage from freezing up to a level of ca. 2500 m elevation, which is also the current tree line location on the east flank of Mauna Loa. The limited freezing resistance of M. polymorpha leaves may be partially responsible for the occurrence of tree line at a relatively low elevation in Hawaii compared with continental tree lines, which can be up to 1500 m higher. If the elevation of tree line is influenced by the inability of M. polymorpha leaves to supercool to lower subzero temperatures, then it will be the first example that freezing damage resulting from limited supercooling capacity can be a factor in tree line formation.

Morphological and Physiological Responses of Hawaiian Hibiscus tiliaceus Populations to Light and Salinity

Hibiscus tiliaceus (Hau) is a pantropical mangrove associate that usually occurs in coastal ecosystems where substrate salinity is relatively high, but it also inhabits upland habitats in Hawaii. Cuttings from three populations on the island of Oahu, Hawaii, were collected and grown in the glasshouse under two levels of substrate salinity (0 and 335 mOsm kg−1) and three light treatments (0%, 50%, and 90% shade). Photosynthetic gas exchange, biomass allocation, and accumulation were studied in relation to salinity and light. Salinity reduced net CO2 assimilation in the upland population but had no effect or stimulated photosynthesis in the coastal populations, whereas increasing salinity decreased stomatal conductance in all populations and therefore increased water‐use efficiency. The degree to which photosynthesis was inhibited by salinity was inversely proportional to the salinity of the source population, indicating a loss of salinity tolerance in upland plants. Light had a stronger effect on leaf area ratio (LAR) and leaf mass per area (LMA), whereas salinity had a stronger effect on leaf water content, internode length, and plant biomass. Salinity reduced total new biomass by 58%, 50%, and 34% in full sun, 50% shade, and 90% shade, respectively, but this response did not differ between populations. Salinity reduced the photosynthesis, but not growth, of upland plants because increased allocation to photosynthetic tissue increased LAR to compensate for inhibition of photosynthesis by salinity.

Photosynthetic gas exchange and temperature-induced damage in seedlings of the tropical alpine species Argyroxiphium sandwicense

The capacity of Argyroxiphium sandwicense (silverword) seedlings to acclimate photosynthetic processes to different growing temperatures, as well as the tolerance of A. sandwicense to temperatures ranging from −15 to 60° C, were analyzed in a combination of field and laboratory studies. Altitudinal changes in temperature were also analyzed in order to explain the observed spatial distribution of A. sandwicense. A. sandwicense (Asteraceae) is a giant rosette plant that grows at high elevation on two Hawaiian volcanoes, where nocturnal subzero temperatures frequently occur. In addition, the soil temperatures at midday in the open alpine vegetation can exceed 60° C. In marked contrast to this large diurnal temperature variation, the seasonal variation in temperature is very small due to the tropical maritime location of the Hawaiian archipelago. Diurnal changes of soil and air temperature as well as photosynthetic photon flux density were measured on Haleakala volcano during four months. Seedlings were grown in the laboratory, from seeds collected in ten different A. sandwicense populations on Haleakala volcano, and maintained in growth chambers at 15/5, 25/15, and 30/25° C day/night temperatures. Irreversible tissue damage was determined by measuring electrolyte leakage of leaf samples. For seedlings maintained at each of the three different day/night temperatures, tissue damage occurred at −10° C due to freezing and at about 50° C due to high temperatures. Tissue damage occurred immediately after ice nucleation suggesting that A. sandwicense seedlings tend to avoid ice formation by permanent supercooling. Seedlings maintained at different day/night temperatures had similar maximum photosynthetic rates (5 μmol m−2 s−1) and similar optimum temperatures for photosynthesis (about 16° C). Leaf dark respiration rates compared at identical temperatures, however, were substantially higher for seedlings maintained at low temperatures, but almost perfect homeostasis is observed when compared at their respective growing conditions. The lack of acclimation in terms of frost resistance and tolerance to high temperatures, as well as in terms of the optimum temperature for photosynthesis, may contribute to the restricted altitudinal range of A. sandwicense. The small seasonal temperature variations in the tropical environment where this species grows may have prevented the development of mechanisms for acclimation to longterm temperature changes.

Determinants of thermal balance in the Hawaiian giant rosette plant, Argyroxiphium sandwicense

The effects of leaf pubescence and rosette geometry on thermal balance were studied in a subspecies of a Hawaiian giant rosette plant, Argyroxiphium sandwicense. This species, a member of the silversword alliance, grows above 2000 m elevation in the alpine zone of two Hawaiian volcanoes. Its highly pubescent leaves are very reflective (absorptance in the 400–700 nm waveband=0.44). Temperature of the expanded leaves was very similar to, or even lower than, air temperature during clear days, which was somewhat surprising given that solar radiation at the high elevation sites where this species grows can exceed 1100 W m−2. However, the temperature of the apical bud, which is located in the center of the parabolic rosette, was usually 25°C higher than air temperature at midday. Experimental manipulations in the field indicated that incoming solar radiation being focussed towards the center of the rosette resulted in higher temperatures of the apical bud. Attenuation of wind speed inside the rosette, which increased the thickness of the boundary layer surrounding the apical bud, also contributed to higher temperatures. The heating effect on the apical bud of the large parabolic rosette, which apparently enhances the rates of physiological processes in the developing leaves, may exclude the species from lower elevations by producing lethal tissue temperatures. Model simulations of apical bud temperatures at different elevations and laboratory estimates of the temperature threshold for permanent heat injury predicted that the lower altitude limit should be approximately 1900 m, which is reasonably close to the lower limit of distribution of A. sandwicense on Haleakala volcano.

Perspectives on the Biophysics of Xylem Transport

Publisher Summary This chapter provides a brief discussion on cohesion-tension theory. The chapter also focuses on factors that affect hydraulic resistance in plants. It addresses how sap is extruded into the empty tracheary element even though the free energy gradient from soil to xylem seems often to be in the wrong direction, how the element is hydraulically isolated during refilling to avoid its new contents being sucked away in the transpiration stream, and how a refilled vessel ultimately reestablishes hydraulic contact with neighboring conduits in such fashion as to become once again useful in water transport. For xylem sap to flow through the plant, the negative hydrostatic pressure gradient must be large enough to overcome the “resistive” force of sap viscosity and the force of gravity. Because the rate of xylem sap flow through plants is relatively slow, the laminar flow pattern within an individual vessel consists of layers of sap that flow past each other in a sheetlike fashion, with the result that neither eddies nor vortices occur and turbulence is absent. However, in both laminar and turbulent flow, viscosity leads to internal friction, which produces energy dissipation. The cohesion-tension theory still stands as the hegemonic model for understanding long-distance sap transport in plants, but a controversy related to it propelled the development of new ideas and possible alternative paradigms to replace the postulates of cohesion-tension theory.

Photosynthesis and Freezing Avoidance in Ohia (Metrosideros polymorpha) at Treeline in Hawaii

Metrosideros polymorpha (Ohia), the dominant tree species in Hawaiian forest ecosystems, grows from sea level to treeline (2500 m). Carboxylation efficiency and area-based leaf N content were substantially higher at treeline than at lower elevations while leaf size and instantaneous photosynthetic nitrogen-use efficiency (PNUE) were substantially lower at treeline. For example, PNUE decreased from 45 jimol CO2 mol N-1 at low elevation to 17.4 ,Imol CO2 mol N-1 at high elevation. In contrast, average net CO2 assimilation and integrated PNUE remained relatively constant along the elevation gradient despite suboptimal temperatures and decreased soil nitrogen availability at treeline. These and other homeostatic mechanisms allow M. polymorpha to maintain a relatively high level of growth-related activities at treeline despite frequent near- and below-freezing temperatures. High-elevation populations avoided freezing by supercooling apparently as a result of small leaves, reduced intercellular spaces, and low apoplastic water content in leaves. Ice nucleation temperatures were about -8.5?C for leaves of treeline populations, 3?C lower than those of low elevation populations. Irreversible tissue damage temperature decreased 7?C from sea level to treeline. However, the decrease appeared to be only large enough to allow M. polymorpha trees to avoid leaf tissue damage due to freezing up to the current location of treeline. All of the above leaf traits in high-elevation populations serve to promote carbon gain in a nutrient and temperature limited environment as well as to avoid freezing by supercooling.