Developmentally based scaling of leaf venation architecture explains global ecological patterns

Sack, Lawren; Scoffoni, Christine; McKown, Athena D.; Frole, Kristen; Rawls, Michael; Havran, J. C.; Tran, Huy; Tran, Thusuong

doi:10.1038/ncomms1835

Cited by 284 publications

(395 citation statements)

References 56 publications

(98 reference statements)

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“…Briefly, minor veins of fully hydrated leaves were cut under water over a light bench to ensure that no major veins were severed. Cuts were made between about 95% of tertiary veins, yielding 5 to 33 cuts mm 22 depending on sample size (larger leaves have their major veins spaced farther apart, so that fewer but longer cuts were made; Sack et al, 2012;. These cuts were enough for water to move directly out of minor veins and not through outside-xylem pathways (Sack et al, 2004;Nardini et al, 2005).…”

Section: Empirical Measurements Of K Oxmentioning

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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Section: Empirical Measurements Of K Oxmentioning

confidence: 99%

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

et al. 2015

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“…Lobed leaves are generally associated with adaptation to shade [45]; however, in very small leaves lobes are associated with high density of major veins that maintain equable water potential across the leaf under bright conditions [46,47]. Small dissected leaves also enable rapid convective cooling, protecting the leaves from overheating in high light and still air [46,[48][49][50]. Furthermore, the relatively low inferred LMA of Fairlingtonia (electronic supplementary material, S1) is a value typical of herbaceous plants in riparian habitats [34].…”

Section: (B) Ecological Implicationsmentioning

confidence: 99%

Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous

Jud¹

2015

Proc. R. Soc. B.

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Eudicot flowering plants comprise roughly 70% of land plant species diversity today, but their early evolution is not well understood. Fossil evidence has been largely restricted to their distinctive tricolpate pollen grains and this has limited our understanding of the ecological strategies that characterized their primary radiation. I describe megafossils of an Early Cretaceous eudicot from the Potomac Group in Maryland and Virginia, USA that are complete enough to allow reconstruction of important life-history traits. I draw on quantitative and qualitative analysis of functional traits, phylogenetic analysis and sedimentological evidence to reconstruct the biology of this extinct species. These plants were small and locally rare but widespread, fast-growing herbs. They had complex leaves and they were colonizers of bright, wet, disturbance-prone habitats. Other early eudicot megafossils appear to be herbaceous rather than woody, suggesting that this habit was characteristic of their primary radiation. A mostly herbaceous initial diversification of eudicots could simultaneously explain the heretofore sparse megafossil record as well as their rapid diversification during the Early Cretaceous because the angiosperm capacity for fast reproduction and fast evolution is best expressed in herbs.

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“…Previous studies have shown that the pattern of leaf veins and xylem morphology allow a broad range of leaf hydraulic differentiations between species or during development (Sack and Holbrook, 2006;Sack et al, 2012). In addition, living tissues and associated membrane water transport can provide rapid and reversible regulation of leaf water transport capacity (hydraulic conductance) by environmental or physiological cues.…”

Section: Introductionmentioning

confidence: 99%

Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins

et al. 2013

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The water status of plant leaves depends on the efficiency of the water supply, from the vasculature to inner tissues. This process is under hormonal and environmental regulation and involves aquaporin water channels. In Arabidopsis thaliana, the rosette hydraulic conductivity (K ros ) is higher in darkness than it is during the day. Knockout plants showed that three plasma membrane intrinsic proteins (PIPs) sharing expression in veins (PIP1;2, PIP2;1, and PIP2;6) contribute to rosette water transport, and PIP2;1 can fully account for K ros responsiveness to darkness. Directed expression of PIP2;1 in veins of a pip2;1 mutant was sufficient to restore K ros . In addition, a positive correlation, in both wild-type and PIP2;1-overexpressing plants, was found between K ros and the osmotic water permeability of protoplasts from the veins but not from the mesophyll. Thus, living cells in veins form a major hydraulic resistance in leaves. Quantitative proteomic analyses showed that light-dependent regulation of K ros is linked to diphosphorylation of PIP2;1 at Ser-280 and Ser-283. Expression in pip2;1 of phosphomimetic and phosphorylation-deficient forms of PIP2;1 demonstrated that phosphorylation at these two sites is necessary for K ros enhancement under darkness. These findings establish how regulation of a single aquaporin isoform in leaf veins critically determines leaf hydraulics.

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Developmentally based scaling of leaf venation architecture explains global ecological patterns

Cited by 284 publications

References 56 publications

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

How Does Leaf Anatomy Influence Water Transport outside the Xylem?

Fossil evidence for a herbaceous diversification of early eudicot angiosperms during the Early Cretaceous

Regulation of Arabidopsis Leaf Hydraulics Involves Light-Dependent Phosphorylation of Aquaporins in Veins

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