The Bundle Sheath Extension in Leaves of Dicotyledons

Wylie, Robert B.

doi:10.1002/j.1537-2197.1952.tb13080.x

Cited by 78 publications

(69 citation statements)

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“…This suggests the BSEs are in the hydraulic pathway and can provide additional flow paths that may reduce r leaf in heterobaric leaves relative to homobaric leaves. Thus, as Wylie (1952) hypothesized based on their anatomy, BSEs may contribute significantly to water flow in heterobaric leaves by facilitating water transport to the epidermis. It is surprising that the role of BSEs in stomatal control has received so little attention.…”

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confidence: 87%

“…The latter possess bundle sheath extensions (BSEs) that connect the epidermis and vascular bundles (Wylie, 1952). BSEs can help distribute light through thicker leaves, enhancing photosynthesis (Nikolopoulos et al, 2002), and they may limit lateral CO 2 diffusion within the leaf (Terashima, 1992;Morison et al, 2007).…”

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confidence: 99%

“…BSEs can help distribute light through thicker leaves, enhancing photosynthesis (Nikolopoulos et al, 2002), and they may limit lateral CO 2 diffusion within the leaf (Terashima, 1992;Morison et al, 2007). BSEs are more common in xeric, high-light species and upper canopy trees (Kenzo et al, 2007) and in deciduous woody species than in herbs (Wylie, 1952;McClendon, 1992). Scoffoni et al (2008) found that the reduction of r leaf by light was much stronger in heterobaric than homobaric species (averaging 58% versus 20%, respectively).…”

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The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

2011

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Bundle sheath extensions (BSEs) are key features of leaf structure with currently little-understood functions. To test the hypothesis that BSEs reduce the hydraulic resistance from the bundle sheath to the epidermis (r be ) and thereby accelerate hydropassive stomatal movements, we compared stomatal responses with reduced humidity and leaf excision among 20 species with heterobaric or homobaric leaves and herbaceous or woody life forms. We hypothesized that low r be due to the presence of BSEs would increase the rate of stomatal opening (V) during transient wrong-way responses, but more so during wrong-way responses to excision (V e ) than humidity (V h ), thus increasing the ratio of V e to V h . We predicted the same trends for herbaceous relative to woody species given greater hydraulic resistance in woody species. We found that V e , V h , and their ratio were 2.3 to 4.4 times greater in heterobaric than homobaric leaves and 2.0 to 3.1 times greater in herbaceous than woody species. To assess possible causes for these differences, we simulated these experiments in a dynamic compartment/resistance model, which predicted larger V e and V e /V h in leaves with smaller r be . These results support the hypothesis that BSEs reduce r be . Comparison of our data and simulations suggested that r be is approximately 4 to 16 times larger in homobaric than heterobaric leaves. Our study provides new evidence that variations in the distribution of hydraulic resistance within the leaf and plant are central to understanding dynamic stomatal responses to water status and their ecological correlates and that BSEs play several key roles in the functional ecology of heterobaric leaves.

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The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

2011

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“…Previous studies that inferred the effect of BSEs on K leaf from anatomy, simpler hydraulic models, K leaf responses to light, and stomatal responses to evaporative demand in heterobaric versus homobaric species have hypothesized that BSEs are a major route for water flow from the veins to the epidermis to the stomata (Wylie, 1952;Scoffoni et al, 2008;Buckley et al, 2011;Sommerville et al, 2012;Zsögön et al, 2015). MOFLO allowed us to directly quantify the effect of BSEs on K ox by replacing BSEs with mesophyll tissue in the model.…”

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confidence: 99%

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

et al. 2015

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Leaves are arguably the most complex and important physicobiological systems in the ecosphere. Yet, water transport outside the leaf xylem remains poorly understood, despite its impacts on stomatal function and photosynthesis. We applied anatomical measurements from 14 diverse species to a novel model of water flow in an areole (the smallest region bounded by minor veins) to predict the impact of anatomical variation across species on outside-xylem hydraulic conductance (K ox ). Several predictions verified previous correlational studies: (1) vein length per unit area is the strongest anatomical determinant of K ox , due to effects on hydraulic pathlength and bundle sheath (BS) surface area; (2) palisade mesophyll remains well hydrated in hypostomatous species, which may benefit photosynthesis, (3) BS extensions enhance K ox ; and (4) the upper and lower epidermis are hydraulically sequestered from one another despite their proximity. Our findings also provided novel insights: (5) the BS contributes a minority of outside-xylem resistance; (6) vapor transport contributes up to two-thirds of K ox ; (7) K ox is strongly enhanced by the proximity of veins to lower epidermis; and (8) K ox is strongly influenced by spongy mesophyll anatomy, decreasing with protoplast size and increasing with airspace fraction and cell wall thickness. Correlations between anatomy and K ox across species sometimes diverged from predicted causal effects, demonstrating the need for integrative models to resolve causation. For example, (9) K ox was enhanced far more in heterobaric species than predicted by their having BS extensions. Our approach provides detailed insights into the role of anatomical variation in leaf function.

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“…Wylie (4)(5)(6)(7)(8) and Armacost (1) reported that the BSE are particularly common in the leaves of deciduous woody plants and that they are importance as conduits of water between the vascular tissue and the mesophyll via the epidermis. In addition, Meidner (2) and Terashima et al (3) showed that these plates are barriers to the lateral movement of air within the leaf blade.…”

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Photographic Survey of the Occurrence of Bundle-Sheath Extensions in Deciduous Dicots

McClendon¹

1992

Plant Physiol.

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MATERIALS AND METHODSIn a survey of over 300 nonevergreen dicots in 69 families, many species were found to have translucent patterns attributed to the presence of bundle-sheath extensions (BSE) on the small and ultimate veinlets. The BSE have been shown by others to inhibit transverse air movement within leaves, and it has been suggested that they are important passageways between vascular tissue and the palisade. The only characteristic found to be associated with prominent BSE is that more trees have such features than herbaceous plants. However, many important herbs have them also, including soybeans and sunflowers. Fresh leaves were photographed in transmitted light with a 35-mm single-lens reflex camera attached to a 19-cm bellows extension with a 20-mm, f/3.5 lens, giving about 13X magnification at the film. The leaf sample was pressed against a hole in a metal plate by a microscope slide held in place by clips. The upper (adaxial) surface of the leaf faced the lens.All leaves were from dicots, and were selected from broadleaf, deciduous trees, shrubs, or vines, or from annual or perennial herbs or vines. A few leaves had dark veins instead of bright ones (Amaranthus sp., Gomphrena sp.), which are presumed to be C-4 leaves. Sampling was of native, cultivated and weedy plants, mostly in southeast Nebraska.Two different methods were used to classify the contact prints. For the first, two lines were placed across the photograph (i.e. 48 mm on the film, or about 3.7 mm of the leaf) and the number of sharply visible veins that touched the lines were counted. For convenience in tabulation, these numbers were pooled into six 'vein density' groups that had the following designations and ranges: A (28-22 veins/3.7 mm), B (21-16), C (15-12), D (11-8), E (7-4), F (3-0).The second measure was a subjective assessment ('visual index,' ranging from 4 to 0) of the optical importance of the visible veins. This attempted to give credit to the optical contrast between the veins and leaf mesophyll, as well as to the extent of the network. The two measures were highly correlated (r = 0.85). RESULTS AND DISCUSSIONFigures 1 through 4 show representative photographs of the range of leaf pattems found. Wylie (7)

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The Bundle Sheath Extension in Leaves of Dicotyledons

Cited by 78 publications

References 2 publications

The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

The Role of Bundle Sheath Extensions and Life Form in Stomatal Responses to Leaf Water Status

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

Photographic Survey of the Occurrence of Bundle-Sheath Extensions in Deciduous Dicots

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