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

McClendon, John H.

doi:10.1104/pp.99.4.1677

Cited by 39 publications

(33 citation statements)

References 6 publications

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“…However, according to McClendon (1992), the occurrence of prominent BSEs is more frequent in trees than in herbaceous plants. It has been also proposed that Mediterranean-climate sclerophylls exhibit low photosynthetic capacities compared with many mesomorphic species (Ehleringer and Mooney, 1983;Turner, 1994a;Larcher, 1995).…”

Section: Relationship Between a P Spatial Characteristics And Photosymentioning

confidence: 99%

“…Heterobaric leaves are characterized by the occurrence of transparent regions in the leaf blade that are easily seen as a network of bright lines on a dark green background under low magnification with transmitted light (McClendon, 1992). These transparent areas are created because the bundle sheaths of these leaves extend to the epidermis on both sides of the leaf, forming bundle sheath extensions (BSEs), which project as ribs on both surfaces of the lamina (Wylie, 1952;Esau, 1977;Fahn, 1990).…”

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The Relationship between Anatomy and Photosynthetic Performance of Heterobaric Leaves

et al. 2002

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Heterobaric leaves show heterogeneous pigmentation due to the occurrence of a network of transparent areas that are created from the bundle sheaths extensions (BSEs). Image analysis showed that the percentage of photosynthetically active leaf area (A p ) of the heterobaric leaves of 31 plant species was species dependent, ranging from 91% in Malva sylvestris to only 48% in Gynerium sp. Although a significant portion of the leaf surface does not correspond to photosynthetic tissue, the photosynthetic capacity of these leaves, expressed per unit of projected area (P max ), was not considerably affected by the size of their transparent leaf area (A t ). This means that the photosynthetic capacity expressed per A p (P* max ) should increase with A t . Moreover, the expression of P* max could be allowing the interpretation of the photosynthetic performance in relation to some critical anatomical traits. The P* max , irrespective of plant species, correlated with the specific leaf transparent volume ( t ), as well as with the transparent leaf area complexity factor ( CF A t ), parameters indicating the volume per unit leaf area and length/density of the transparent tissues, respectively. Moreover, both parameters increased exponentially with leaf thickness, suggesting an essential functional role of BSEs mainly in thick leaves. The results of the present study suggest that although the A p of an heterobaric leaf is reduced, the photosynthetic performance of each areole is increased, possibly due to the light transferring capacity of BSEs. This mechanism may allow a significant increase in leaf thickness and a consequent increase of the photosynthetic capacity per unit (projected) area, offering adaptive advantages in xerothermic environments.

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Section: Relationship Between a P Spatial Characteristics And Photosymentioning

confidence: 99%

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confidence: 99%

The Relationship between Anatomy and Photosynthetic Performance of Heterobaric Leaves

et al. 2002

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“…Below the dotted line, \5% of the extravascular resistance remains. another or flow largely through the bundle sheath extensions in species that possess them (Armacost, 1944;Wylie, 1946;McClendon, 1992) to the epidermis. Finally, evaporation might occur only near the stomata (Wylie, 1943(Wylie, , 1946Tyree and Yianoulis, 1980;Shackel and Brinckmann, 1985) or, alternatively, take place throughout the spongy mesophyll (Davies, 1986;Nonami and Schulze, 1989;Nonami et al, 1991).…”

Section: Partitioning Of Leaf Hydraulic Resistance: Water Flow Througmentioning

confidence: 99%

Hydraulic Analysis of Water Flow through Leaves of Sugar Maple and Red Oak

2004

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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.Water flow through the leaf is one of the most important but least understood components of the whole-plant hydraulic system. The leaf hydraulic resistance (R leaf ) constitutes a significant hydraulic bottleneck, correlates with leaf structure, and apparently constrains gas exchange (Tyree and Zimmermann, 2002;Sack et al., 2003b;Sack and Tyree, 2004). R leaf is an aggregate measure; once past the petiole, water flows through a reticulate network of veins, across the bundle sheath cells, and through or around mesophyll cells before evaporation and diffusion from the stomata (Esau, 1965). Recent work has focused primarily on measurement of R leaf and its functional correlates. Few studies have attempted to determine quantitatively how the various components of the water flow pathway through the leaf contribute to its total resistance.Partitioning of R leaf is a crucial step for understanding leaf hydraulic design. Cavitation in the leaf vein xylem can substantially increase R leaf , as can physical damage to major veins; both drive reductions of leaf water potential and gas exchange Nardini et al., 2001Cochard et al., 2002;Huve et al., 2002;Sack et al., 2003a). These observations suggest that a large proportion of R leaf is situated in the veins. However, a number of studies have reported that most of the leaf resista...

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“…The permeability depends on leaf anatomy, particularly mesophyll cell size and shape, packing density, and the vascular anatomy (Pieruschka et al, 2005;Morison and Lawson, 2007). Many species have bundle sheath extensions (BSE) consisting of achlorophyllous parenchyma cells (Wylie, 1952;McClendon, 1992) that appear to provide a better supply of water to the epidermis (Kenzo et al, 2007) and may also allow local penetration of light into leaves (Vogelmann, 1989;Karabourniotis et al, 2000). In some species, these BSE can divide the mesophyll into discrete compartments or areoles leading to heterogeneous photosynthesis (Terashima, 1992;Morison and Lawson, 2007).…”

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Lateral CO2 Diffusion inside Dicotyledonous Leaves Can Be Substantial: Quantification in Different Light Intensities

2007

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Substantial lateral CO 2 diffusion rates into leaf areas where stomata were blocked by grease patches were quantified by gas exchange and chlorophyll a fluorescence imaging in different species across the full range of photosynthetic photon flux densities (PPFD). The lateral CO 2 flux rate over short distances was substantial and very similar in five dicotyledonous species with different vascular anatomies (two species with bundle sheath extensions, sunflower [Helianthus annuus] and dwarf bean [Phaseolus vulgaris]; and three species without bundle sheath extensions, faba bean [Vicia faba], petunia [Petunia hybrida], and tobacco [Nicotiana tabacum]). Only in the monocot maize (Zea mays) was there little or no evident lateral CO 2 flux. Lateral diffusion rates were low when PPFD ,300 mmol m 22 s 21 but approached saturation in moderate PPFD (300 mmol m 22 s 21 ) when lateral CO 2 diffusion represented 15% to 24% of the normal CO 2 assimilation rate. Smaller patches and higher ambient CO 2 concentration increased lateral CO 2 diffusion rates. Calculations with a two-dimensional diffusion model supported these observations that lateral CO 2 diffusion over short distances inside dicotyledonous leaves can be important to photosynthesis. The results emphasize that supply of CO 2 from nearby stomata usually dominates assimilation, but that lateral supply over distances up to approximately 1 mm can be important if stomata are blocked, particularly when assimilation rate is low.

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

Cited by 39 publications

References 6 publications

The Relationship between Anatomy and Photosynthetic Performance of Heterobaric Leaves

The Relationship between Anatomy and Photosynthetic Performance of Heterobaric Leaves

Hydraulic Analysis of Water Flow through Leaves of Sugar Maple and Red Oak

Lateral CO2 Diffusion inside Dicotyledonous Leaves Can Be Substantial: Quantification in Different Light Intensities

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