Hydraulic analysis of water flow through leaves of sugar maple and red oak

Leaves constitute a substantial fraction of the total resistance to water flow through plants. A key question is how hydraulic resistance within the leaf is distributed among petiole, major veins, minor veins, and the pathways downstream of the veins. We partitioned the leaf hydraulic resistance (R(leaf)) for sugar maple (Acer saccharum) and red oak (Quercus rubra) by measuring the resistance to water flow through leaves before and after cutting specific vein orders. Simulations using an electronic circuit analog with resistors arranged in a hierarchical reticulate network justified the partitioning of total R(leaf) into component additive resistances. On average 64% and 74% of the R(leaf) was situated within the leaf xylem for sugar maple and red oak, respectively. Substantial resistance-32% and 49%- was in the minor venation, 18% and 21% in the major venation, and 14% and 4% in the petiole. The large number of parallel paths (i.e. a large transfer surface) for water leaving the minor veins through the bundle sheath and out of the leaf resulted in the pathways outside the venation comprising only 36% and 26% of R(leaf). Changing leaf temperature during measurement of R(leaf) for intact leaves resulted in a temperature response beyond that expected from changes in viscosity. The extra response was not found for leaves with veins cut, indicating that water crosses cell membranes after it leaves the xylem. The large proportion of resistance in the venation can explain why stomata respond to leaf xylem damage and cavitation. The hydraulic importance of the leaf vein system suggests that the diversity of vein system architectures observed in angiosperms may reflect variation in whole-leaf hydraulic capacity.     

STUDIES ON THE LEAF OF POPULUS DELTOIDES (SALICACEAE): MORPHOLOGY AND ANATOMY

Mature field- and growth-chamber-grown leaves of Populus deltoides Bartr. ex Marsh. were examined with light and scanning electron microscopes to determine their vasculature and the spatial relationships of the various orders of vascular bundles to the mesophyll. Three leaf traces, one median and two lateral, enter the petiole at the node. Progressing acropetally in the petiole these bundles are rearranged and gradually form as many as 13 tiers of vascular tissue in the petiole at the base of the lamina. (Most leaves contained seven vertically stacked tiers.) During their course through the midrib the tiers “unstack” and portions diverge outward and continue as secondary veins toward the margin on either side of the lamina. As the midvein approaches the leaf tip it is represented by a single vascular bundle which is a continuation of the original median bundle. Tertiary veins arise from the secondary veins or the midvein, and minor veins commonly arise from all orders of veins. All major veins–primaries, secondaries, intersecondaries, and tertiaries–are associated with rib tissue, while minor veins are completely surrounded by a parenchymatous bundle sheath. The bundle sheaths of tertiary, quaternary, and portions of quinternary veins are associated with bundle-sheath extensions. Minor veins are closely associated spatially with both ad- and abaxial palisade parenchyma of the isolateral leaf and also with one or two layers of paraveinal mesophyll that extend horizontally between the veins. The leaves of growth-chamber-grown plants had thinner blades, a higher proportion of air space, and greater interveinal distances than those of field-grown plants.     

Leaf hydraulic capacity in ferns, conifers and angiosperms: impacts on photosynthetic maxima

* The hydraulic plumbing of vascular plant leaves varies considerably between major plant groups both in the spatial organization of veins, as well as their anatomical structure. * Five conifers, three ferns and 12 angiosperm trees were selected from tropical and temperate forests to investigate whether the profound differences in foliar morphology of these groups lead to correspondingly profound differences in leaf hydraulic efficiency. * We found that angiosperm leaves spanned a range of leaf hydraulic conductance from 3.9 to 36 mmol m2 s-1 MPa-1, whereas ferns (5.9-11.4 mmol m-2 s-1 MPa-1) and conifers (1.6-9.0 mmol m-2 s-1 MPa-1) were uniformly less conductive to liquid water. Leaf hydraulic conductance (Kleaf) correlated strongly with stomatal conductance indicating an internal leaf-level regulation of liquid and vapour conductances. Photosynthetic capacity also increased with Kleaf, however, it became saturated at values of Kleaf over 20 mmol m-2 s-1 MPa-1. * The data suggest that vessels in the leaves of the angiosperms studied provide them with the flexibility to produce highly conductive leaves with correspondingly high photosynthetic capacities relative to tracheid-bearing species.     

The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods

A comparison was made of three methods for measuring the leaf lamina hydraulic conductance (K(lamina)) for detached mature leaves of six woody temperate angiosperm species. The high-pressure method, the evaporative flux method and the vacuum pump method involve, respectively, pushing, evaporating and pulling water out of the lamina while determining the flow rate into the petiole and the water potential drop across the leaf. Tests were made of whether the high-pressure method and vacuum pump method measurements of K(lamina) on single leaves were affected by irradiance. In Quercus rubra, the high pressure method was sensitive to irradiance; K(lamina) measured under high irradiance (>1200 micro mol m(-2) s(-1 )photosynthetically active radiation) was 4.6-8.8 times larger than under ambient laboratory lighting (approximately 6 micro mol m(-2) s(-1 )photosynthetically active radiation). By constrast, the vacuum pump method was theoretically expected to be insensitive to irradiance, and this expectation was confirmed in experiments on Hedera helix. When used in the ways recommended here, the three methods produced measurements that agreed typically within 10%. There were significant differences in species' K(lamina); values ranged from 1.24x10(-4) kg s(-1) m(-2) MPa(-1) for Acer saccharum to 2.89x10(-4) kg s(-1) m(-2) MPa(-1) for Vitis labrusca. Accurate, rapid determination of K(lamina) will allow testing of the links between K(lamina), water-use, drought tolerance, and the enormous diversity of leaf form, structure and composition.     

Dehydration tolerance of leaf tissues of six woody angiosperm species

Electrolyte leakage from leaf discs (measured as an index of dehydration tolerance) increased as water potentials of excised leaves declined for field-grown saplings of six woody species. Until late in the growing season (mid-August), leaves of Cornus florida L. exhibited greater leakage than those of other species; however, in August and September leakage in this species was much reduced, indicating apparent hardening in response to mid-season drought. Leaves of Quercus alba L., Q. rubra L. and Q. velutina Lam. generally exhibited less electrolyte leakage than did those of Acer saccharum Marsh, and Juglans nigra L. over the season. Moreover, leaves of Quercus species showed a reduction in electrolyte leakage late in the season similar to (but less accentuated than) that of C. florida . Saplings of A. saccharum and J. nigra showed little and no drought-hardening response, respectively. The responses shown by the studied species suggest that dehydration tolerance plays a role in plant distribution and that environmentally induced shifts in this tolerance are a significant phenomenon in natural plant communities.     

Comparative sectoriality in temperate hardwoods: hydraulics and xylem anatomy

In wood, lateral transport of water and minerals occurs readily in 'integrated' trees but is more restricted in 'sectored species'. Dye distribution and a novel hydraulic technique are used to quantify species-specific differences in sectoriality in three temperate hardwoods, Betula papyrifera , Acer saccharum and Quercus rubra. Sectoriality was related to key elements of xylem structure: intervascular pitting, vessel diameter and vessel grouping. Perfusion of 0.5% safranin through isolated roots showed root-to-branch dye transport was most extensive in B. papyrifera and least extensive in Q. rubra . To test sectorialty using hydraulics, 20 m m KCl solution was pushed at 0.1 MPa through 5-cm wood segments, before and after occluding the direct axial outlet with glue, with flow rate measured in grams of solution expelled over time. Direct (axial) conductance (g MPa⁻¹ s⁻¹) through unglued outlets was compared with indirect (tangential) conductance around occluded outlets. Species with high indirect/direct conductance ratios (Integration Index) are the most integrated. Integration Index ranged from 0.26 in B. papyrifera to 0.02 in Q. rubra . Macerates showed that B. papyrifera has much greater percentage of cell wall area covered with intervascular pits than does A. saccharum or Q. rubra . Vessel grouping was closest in B. papyrifera and vessels were most isolated in Q. rubra . Widest diameter vessels occurred in Q. rubra , where they concentrated in springwood. Intervascular pitting, vessel diameter and grouping are wood traits that contribute to the continuum of sectoriality in trees, and may influence the ability of tree species to dominate in homogeneous or in patchy environments.  © 2006 The Linnean Society of London, Botanical Journal of the Linnean Society , 2006, 150 , 61–71.     

Hydraulic architecture of leaf venation in Laurus nobilis L.

Veins are the main irrigation system of the leaf lamina and an understanding of the hydraulic architecture of the vein networks is essential for understanding leaf function. However, determination of leaf hydraulic parameters is challenging, because for most leaves the vein system is reticulate, contains a hierarchy of different vein sizes, and consists of leaky conduits. We present a new approach that allows for measurements of pressure differences between the petiole and any vein within the leaf. Measurements of Laurus nobilis leaves indicate that first‐ and second‐order veins have high axial conductance and relatively small radial permeability, thus allowing water to reach distal areas of the leaf with only a small loss of water potential. Higher order veins tend to be more hydraulically resistant and permit greater radial leakage. This design allows for a relatively equitable distribution of water potential and thus reflects the capacity of the venation to provide a relatively homogeneous water supply across the leaf lamina, with only the leaf margins being hydraulically disadvantaged relative to the rest of the leaf.     

The pathways of water movement in leaves modified into tents by bats

A number of species of bats modify leaves into tents, which they use as roost-sites. Through this process, some areas of the leaf lamina are damaged or become detached from the midrib. Such injuries do not cause death of the leaf or the detached areas, indicating that water supply to these areas must be maintained. We examined the anatomy of the vascular systems and water transport in the leaves of three species of plants: Heliconia pogonantha L., Manicaria plukenetii Griseb. & H. Wendl., and Cryosophila warcsewiczii (H. Wend.) Bartlett. In altered leaves of all three species, detached areas of the laminae were supplied with water by minor transverse veins branching from the first major parallel vein that remained intact next to the cut. These transverse veins conducted water through single xylem elements of narrow diameter (approximately 10 urn) previously thought to supply water only to mesophyll cells in their immediate vicinity. The short lengths of these veins compensates their high resistance to water flow (a consequence of their small diameter xylem elements), indicating that small transverse veins have a large capacity for water transport. Water typically flowed through transverse veins into detached major and minor parallel veins, filled these parallel veins in both directions (i.e. toward the midrib and the leaf edge), and continued on into subsequent transverse and parallel veins, thereby supplying water to the entire leaf. Water conduction through these small transverse veins could support large areas of leaf lamina, keeping the leaf-tent alive for at least several months. The maintenance of the flow of water and nutrients to areas of leaves detached by bats during the tent-making process increases the longevity and decreases the conspicuousness of leaf-tents, and is likely a key factor in the success of this roosting strategy.     

Physiological and morphological acclimation of shade-grown tree seedlings to late-season canopy gap formation

Because acclimation to canopy gaps may involve coordination of new leaf production with morphological or physiological changes in existing, shade-developed leaves, we examined both new leaf production and photosynthesis of existing leaves on shade-grown seedlings after exposure to a late-season canopy gap. Midway through the summer, we transferred potted, shade-grown seedlings of four co-occurring temperate deciduous tree species representing a range of shade-tolerance categories and leaf production strategies to gaps. Shade-tolerant Acer saccharum was the least responsive to gap conditions. It produced few new, high-light acclimated leaves and increases in photosynthetic rates of shade-developed leaves appeared stomatally limited. Intermediately shade-tolerant Fraxinus americana and Quercus rubra responded most, by producing new leaves and increasing photosynthetic rates of existing shade-developed leaves to levels not significantly different from gap-grown controls within four weeks of gap exposure. Shade-intolerant Liriodendron tulipifera was intermediate in response. In these species, the degree of shoot-level morphological acclimation (new leaf production) and leaf-level physiological acclimation (photosynthetic increases in existing leaves) appear coupled. Mechanisms of acclimation also appear related to intrinsic patterns of nitrogen use and mobilization, the ability to adjust stomatal conductance, and shade tolerance.     

Massive release of volatile organic compounds due to leaf midrib wounding in <Emphasis Type="Italic">Populus tremula</Emphasis>

We investigated the rapid initial response to wounding damage generated by straight cuts to the leaf lamina and midrib transversal cuts in mature aspen (Populus tremula) leaves that can occur upon herbivore feeding. Wound-induced volatile emission time-courses of 24 compounds were continuously monitored by a proton-transfer-reaction time-of-flight mass spectrometer (PTR-TOF-MS). After the mechanical wounding, an emission cascade was rapidly elicited, resulting in emissions of key stress volatiles methanol, acetaldehyde and volatiles of the lipoxygenase pathway, collectively constituting ca. 99% of the total emission. For the same wounding magnitude, midrib cuts lead to six-fold greater emissions of volatiles per mm² of surface cut than lamina cuts during the first emission burst (shorter than 7 min), and exhibited a particularly high methanol emission compared to the emissions of other volatiles. This evidence suggests that feeding by herbivores capable of consuming the leaf midrib can result in disproportionally greater volatile release than feeding by smaller herbivores incapable of biting through the major veins.     

白蜡虫7种寄主植物叶片解剖结构与寄主选择性的关系

用石蜡切片法在显微镜下观察白蜡虫[Ericerus pela(Chavannes)]7种寄主植物叶的解剖结构。结果表明,寄主植物的叶脉、表皮、栅栏组织、海绵组织、维管束解剖结构及数量性状特征在属、种间存在显著差异。7种寄主植物中,华南小蜡(Ligustrum calleryanum Decne.)和白蜡树(Fraxinus chinensis Roxb.)表皮被毛,华南小蜡表皮毛浓密,白蜡树表皮毛稀疏,其它寄主植物表皮无毛;女贞树(Ligustrum lucidum Ait.)栅栏组织、海绵组织和叶脉的厚度最厚、维管束直径最大,其它寄主植物相对较小。因此,叶片表面光滑、叶脉发达、叶片肥厚是白蜡虫优良寄主植物的重要解剖学特征。7种寄主植物中脉和侧脉发达,近轴面凹陷,远轴面突起,肉脉包埋在叶肉中,推测叶脉突起和凹槽可能是白蜡虫固定位点选择的关键线索。     

Evidence for xylem embolism as a primary factor in dehydration-induced declines in leaf hydraulic conductance

Hydraulic conductance of leaves (K(leaf)) typically decreases with increasing water stress and recent studies have proposed different mechanisms responsible for decreasing K(leaf) . We measured K(leaf) concurrently with ultrasonic acoustic emissions (UAEs) in dehydrating leaves of several species to determine whether declining K(leaf) was associated with xylem embolism. In addition, we performed experiments in which the surface tension of water in the leaf xylem was reduced by using a surfactant solution. Finally, we compared the hydraulic vulnerability of entire leaves with the leaf lamina in three species. Leaf hydraulic vulnerability based on rehydration kinetics and UAE was very similar, except in Quercus garryana. However, water potentials corresponding to the initial decline in K(leaf) and the onset of UAE in Q. garryana were similar. In all species tested, reducing the surface tension of water caused K(leaf) to decline at less negative water potentials compared with leaves supplied with water. Microscopy revealed that as the fraction of embolized xylem increased, K(leaf) declined sharply in Q. garryana. Measurements on leaf discs revealed that reductions in lamina hydraulic conductance with dehydration were not as great as those observed in intact leaves, suggesting that embolism was the primary mechanism for reductions in K(leaf) during dehydration.     

Coppicing alters ecophysiology of Quercus rubrasaplings in Wisconsin forest openings

In the spring of 1987, entire shoots were removed from Quercus rubra L. saplings in two southwestern Wisconsin forest openings. Shoots possessed newly expanding leaves at the time of coppicing. All coppiced individuals sprouted from dormant stem buds near the root collar. Leaf gas exchange and water potential were monitored on these sprouts and on untreated (control) Q. rubra saplings throughout several clear warm days during the 1987 growing season. Daily maxima and averages for sprout leaf photosynthesis and stomatal conductance generally exceeded those of controls. On average, treatment differences in daily maximum photosynthetic rate were modest (11–14%) and were attributed primarily to a 30–38% enhancement of sprout leaf stomatal conductance. Relative differences in daily average photosynthetic rate (29–39%) were substantially larger than those in daily maximum photosynthesis, owing to the fact that sprouts and controls exhibited distinct diurnal gas exchange patterns. Photosynthetic rate and stomatal conductance of control leaves typically declined during the day following a mid-morning maximum. Sprout leaves, on the other hand, tended to maintain gas exchange rates nearer to their morning maxima throughout the day. This difference in diurnal gas exchange pattern was associated with an apparent differential leaf sensitivity to leaf-to-air vapor pressure gradient (VPG). The relative decline in sprout leaf gas exchange rates with increasing VPG was less than that of controls. Treatment differences in gas exchange did not appear to be related to leaf water potential or tissue water relations, but sprouts had a higher soil-to-leaf hydraulic conductivity than controls.     

Diurnal and seasonal changes of leaf lamina hydraulic conductance in bur oak (Quercus macrocarpa) and trembling aspen (Populus tremuloides)

The aim of this study was to examine the diurnal and seasonal variations in the sensitivity of leaf lamina (K _lam) hydraulic conductance to irradiance in bur oak (Quercus macrocarpa Michx.) and trembling aspen (Populus tremuloides Michx.), which vary in their responses of K _lam to irradiance. K _lam was determined using the high-pressure method and the measurements were carried out in June, August and September. The irradiance response of K _lam in bur oak was present throughout the day and declined in senescing leaves. In trembling aspen, K _lam declined from morning to late afternoon and drastically decreased before the onset of leaf senescence, but it was not sensitive to irradiance. In both tree species, the capacity of the petioles to supply water to leaf lamina changed during the day in accordance with the ability of the leaf lamina to transport water. Petiole hydraulic conductivity (K _pet) declined during the season in bur oak leaves, while it tended to increase in trembling aspen leaves. There was no correlation between the K _lam values and air temperature or light intensity at the time of leaf collection. For trembling aspen, K _pet was negatively correlated with the air temperature suggesting sensitivity to drought. We conclude that the water transport properties of petioles and leaf lamina in the two studied tree species reflect their ecological adaptations. Trembling aspen leaves have high hydraulic conductivity and high stomatal conductance regardless of the irradiance level, consistent with the rapid growth and high demand for water. In contrast, the increased lamina hydraulic conductivity and stomatal conductance under high irradiance in bur oak trees reflect a water conservation strategy.     

Water Transport in Impaired Leaf Vein Systems

Abstract: The subject of our investigation was the water regime of broad bean leaves ( Vicia faba L.), especially after having mechanically severed parts of the leaf blade and the leaf venation. Under moderate conditions, 18 - 22 °C temperature and 50 - 70 % relative humidity, the leaves remained viable even after extensive damage. Only if more than 90 % of the xylem cross sectional area of a leaf was severed, the leaf wilted. Lesser damage to the xylem cross-sectional area only resulted in a reduced rate of transpiration and assimilation, compared to intact leaves. The cuts in larger veins were bypassed into small or even very small veins, as shown by xylem transport of dyes. In intact leaves, small veins have a negligible task in long-distance transport. Here, however, transport velocity in small veins was severalfold increased compared to the measurement of transport velocity in veins of the same size in intact leaves. Thereby, water transport to leaf areas distal from the cut was ensured.     

Hydathodal leaf teeth of Chloranthus japonicus (Chloranthaceae) prevent guttation-induced flooding of the mesophyll

Why the leaves of cold temperate deciduous and moisture-loving angiosperms are so often toothed has long puzzled biologists because the functional consequences of teeth remain poorly understood. Here we provide functional and structural evidence that marginal leaf teeth of Chloranthus japonicus, an understory herb, enable the release of guttation sap during root pressure. When guttation from teeth hydathodes was experimentally blocked, we found that the leaf intercellular airspaces became flooded. Measurements of chlorophyll a fluorescence revealed that internal flooding resulted in an inhibition of photosynthesis, most likely through the formation of a film of water within the leaf that reduced CO₂ diffusion. Comparing a developmental series of leaves with and without teeth experimentally covered with wax, we found that teeth did not affect overall leaf stomatal conductance and CO₂ uptake. However, maximal and effective light-saturation PSII quantum yields of teeth were found to be lower or equal to the surrounding lamina throughout leaf ontogeny. Collectively, our results suggest hydathodes and their development on teeth apices enable the avoidance of mesophyll flooding by root pressure. We discuss how these new findings bear on the potential physiological interpretations of models that apply leaf marginal traits to infer ancient climates.     

Behavioral Sabotage of Plant Defense: Do Vein Cuts and Trenches Reduce Insect Exposure to Exudate?

Many insect folivores sever veins or cut trenches before feeding on leaves that emit fluid from latex, resin, or phloem canals. The behaviors reportedly function to reduce the insect's exposure to exudate. This hypothesis was tested with three species that sever leaf midribs and two species that trench. In each case, the insect's cuts reduced exudation at the distal feeding site by at least 94% relative to an adjacent control leaf. However, most of the insects contacted exudate during the vein-cutting/trenching operation, which could potentially negate any benefits received during feeding. To estimate how much exudate red milkweed beetles (Tetraopes tetrophthalmus) ingest, I weighed beetles before and after vein cutting, and simulated beetle feeding on leaves with and without vein cuts. By severing veins, the beetles decreased their total ingestion of exudate by at least 92%.     

HETEROPHYLLIC DEVELOPMENT IN MUEHLENBECKIA (POLYGONACEAE)

Flowering shoots of Muehlenbeckia platyclados Meisn. bear only reduced scale leaves which resemble the membranous sheath portion (ochrea) of leaves of other members of the Polygonaceae. Shoots propagated from cuttings bear enlarged foliage leaves with distinct lamina, petiole, and ochrea zones. The developmental basis for this heterophylly is explored in order to determine whether scale leaves resemble foliage leaves in their pattern of ontogeny or are developmentally unique. SEM and histological analyses have shown that scale leaves and foliage leaves are distinctive from inception. The scale leaf arises as a collarlike growth and extends over the shoot apex as a hooded sheath without evidence of blade initiation. By contrast, the first stage of foliage-leaf ontogeny is the differentiation of the distal lamina from the future leaf base. As the foliage-leaf ochrea encircles the stem axis, the lamina grows erect and projects from the abaxial surface of the sheath. Lamina reduction coupled with ochrea elaboration in intermediate leaf types indicate a homology between the entire scale leaf and foliage-leaf ochrea. Despite this homology, the production of the bladeless scale leaf does not involve a mere suppression of the foliage-leaf lamina. Erect growth of the saccate ochrea of the foliage leaf contrasts with the hooded expansion of the scale. Early histological differences, including contrasting rates of cell differentiation, also distinguish the two organs. This disparity in modes of growth and differentiation from inception results from separate, predetermined courses of ontogeny. Unlike other plants studied, leaf size and degree of leaf elaboration decrease with shoot meristem enlargement in Muehlenbeckia. Leaf packing does increase with shoot development and may contribute to variations in leaf morphology. It is concluded that the peculiarities of the heterophyllic leaf sequence in Muehlenbeckia are a property of the shoot system as a whole.     

MORPHOLOGY AND VASCULATURE OF THE LEAF OF POTATO (SOLANUM TUBEROSUM)

The leaf and stem of the potato plant (Solanum tuberosum L. cv. Russet Burbank) were studied by light microscopy to determine their morphology and vasculature; scanning electron microscopy provided supplemental information on the leaf's morphology. The morphology of the basal leaves of the potato shoot is quite variable, ranging from simple to pinnately compound. The upper leaves of the shoot are more uniform, being odd pinnate with three major pairs of lateral leaflets and a number of folioles. The primary vascular system of the stem is comprised of six bundles, three large and three small ones. The three large bundles form a highly interconnected system through a repeated series of branchings and arch-producing mergers. Two of the three large bundles give rise to short, lateral leaf traces at each node. Each of the small bundles in the stem is actually a median leaf trace which extends three internodes before diverging into a leaf. The three leaf traces enter the petiole through a single gap; thus the nodel anatomy is three-trace unilacunar. Upon entering the petiole, each of the laterals splits into an upper and a lower lateral. Whereas the upper laterals diverge entirely into the first pair of leaflets, the lower laterals feed all of the lateral leaflets through a series of bifurcations. Prior to their entering the terminal leaflet, the lower laterals converge on the median bundle to form a single vascular crescent which progresses acropetally into the terminal leaflet as the midvein, or primary vein. In the midrib, portions of the midvein diverge outward and continue as secondaries to the margin on either side of the lamina. Near the tip of the terminal leaflet, the midvein consists of a single vascular bundle which is a continuation of the median bundle. Six to seven orders of veins occur in the terminal leaflet.