Zwieniecki, Maciej A.

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Zwieniecki, Maciej A.

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Zwieniecki

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Maciej A.

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Zwieniecki, Maciej A.

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Stomatal plugs of Drimys winteri (Winteraceae) protect leaves from mist but not drought
(Proceedings of the National Academy of Sciences, 1998) Feild, T. S.; Zwieniecki, Maciej A.; Donoghue, Margaret Jane; Holbrook, Noel
Two outstanding features of the flowering plant family Winteraceae are the occlusion of their stomatal pores by cutin plugs and the absence of water-conducting xylem vessels. An adaptive relationship between these two unusual features has been suggested whereby stomatal plugs restrict gas exchange to compensate for the presumed poor conductivity of their vesselless wood. This hypothesized connection fueled evolutionary arguments that the vesselless condition is ancestral in angiosperms. Here we show that in Drimys winteri, a tree common to wet forests, these stomatal occlusions pose only a small fixed resistance to water loss. In addition, they modify the humidity response of guard cells such that under high evaporative demand, leaves with plugs lose water at a faster rate than leaves from which the plugs have been experimentally removed. Instead of being adaptations for drought, we present evidence that these cuticular structures function to maintain photosynthetic activity under conditions of excess water on the leaf surface. Stomatal plugs decrease leaf wettability by preventing the formation of a continuous water film that would impede diffusion of CO2 into the leaf. Misting of leaves had no effect on photosynthetic rate of leaves with plugs, but resulted in a marked decrease (-40%) in leaves from which the plugs had been removed. These findings do not support a functional association between stomatal plugs and hydraulic competence and provide a new perspective on debates surrounding the evolution of vessels in angiosperms.
Optimal vein density in artificial and real leaves
(Proceedings of the National Academy of Sciences, 2008) Noblin, X.; Mahadevan, Lakshminarayanan; Coomaraswamy, I. A.; Weitz, David; Holbrook, Noel; Zwieniecki, Maciej A.
The long evolution of vascular plants has resulted in a tremendous variety of natural networks responsible for the evaporatively driven transport of water. Nevertheless, little is known about the physical principles that constrain vascular architecture. Inspired by plant leaves, we used microfluidic devices consisting of simple parallel channel networks in a polymeric material layer, permeable to water, to study the mechanisms of and the limits to evaporation-driven flow. We show that the flow rate through our biomimetic leaves increases linearly with channel density (1/d) until the distance between channels (d) is comparable with the thickness of the polymer layer (δ), above which the flow rate saturates. A comparison with the plant vascular networks shows that the same optimization criterion can be used to describe the placement of veins in leaves. These scaling relations for evaporatively driven flow through simple networks reveal basic design principles for the engineering of evaporation–permeation-driven devices, and highlight the role of physical constraints on the biological design of leaves.
Confronting Maxwell's demon: biophysics of xylem embolism repair
(Elsevier BV, 2009) Zwieniecki, Maciej A.; Holbrook, Noel
Embolism results in a dramatic loss of xylem hydraulic transport capacity that can lead to decreased plant productivity and even death. The ability to refill embolized conduits despite the presence of tension in the xylem seems to be widespread, but how this occurs is not known. To promote discussion and future research on this topic, we describe how we believe refilling under tension might take place. Our scenario includes: (i) an osmotic role for low-molecular weight sugars; (ii) an apoplastic sugar-sensing mechanism to activate refilling; (iii) the contribution of vapor transport in both the influx of water and removal of entrapped gases; and (iv) the need for a mechanism that can synchronize reconnection to the transpiration stream through multiple bordered pits.
Quantifying Green Life: Grand Challenges in Plant Biophysics and Modeling
(Frontiers Research Foundation, 2011) Zwieniecki, Maciej A.; Dumais, J
Ion Induced Changes in the Structure of Bordered Pit Membranes
(Frontiers Research Foundation, 2012) Lee, Jinkee; Holbrook, Noel; Zwieniecki, Maciej A.
Ion-mediated changes in xylem hydraulic resistance are hypothesized to result from hydrogel like properties of pectins located in the bordered pit membranes separating adjacent xylem vessels. Although the kinetics of the ion-mediated changes in hydraulic resistance are consistent with the swelling/deswelling behavior of pectins, there is no direct evidence of this activity. In this report we use atomic force microscopy (AFM) to investigate structural changes in bordered pit membranes associated with changes in the ionic concentration of the surrounding solution. When submerged in de-ionized water, AFM revealed bordered pit membranes as relatively smooth, soft, and lacking any sharp edges surface, in contrast to pictures from scanning electron microscope (SEM) or AFM performed on air-dry material. Exposure of the bordered pit membranes to 50 mM KCl solution resulted in significant changes in both surface physical properties and elevation features. Specifically, bordered pit membranes became harder and the fiber edges were clearly visible. In addition, the membrane contracted and appeared much rougher due to exposed microfibers. In neither solution was there any evidence of discrete pores through the membrane whose dimensions were altered in response to the ionic composition of the surrounding solution. Instead the variable hydraulic resistance appears to involve changes in the both the permeability and the thickness of the pit membrane.
Understanding the Hydraulics of Porous Pipes: Tradeoffs Between Water Uptake and Root Length Utilization
(Springer Verlag, 2003) Zwieniecki, Maciej A.; Thompson, Matthew; Holbrook, Noel
The water uptake region in roots is several hundred times longer than the root diameter. The distributed nature of the uptake zone requires that the hydraulic design of roots be understood by analogy to flow through a "porous pipe." Here we present results of an analytical and experimental investigation that allowed an in-depth analysis of root hydraulic properties. Measurements on nodal maize roots confirm the nonlinear distribution of water uptake predicted by the porous pipe model. The major design parameter governing the distribution of water uptake along a porous pipe is the ratio between its axial and radial hydraulic resistance. However, total flow is proportional to the pipe's overall resistance. These results suggest the existence of a tradeoff between the effective utilization of root length and the total capacity for water uptake.
Tensioning the Helix: A Mechanism for Force Generation in Twining Plants
(Royal Society, The, 2009) Isnard, Sandrine; Cobb, Alexander R.; Holbrook, Noel; Zwieniecki, Maciej A.; Dumais, J
Twining plants use their helical stems to clasp supports and to generate a squeezing force, providing stability against gravity. To elucidate the mechanism that allows force generation, we measured the squeezing forces exerted by the twiner Dioscorea bulbifera while following its growth using time-lapse photography. We show that the development of the squeezing force is accompanied by stiffening of the stem and the expansion of stipules at the leaf base. We use a simple thin rod model to show that despite their small size and sparse distribution, stipules impose a stem deformation sufficient to account for the measured squeezing force. We further demonstrate that tensioning of the stem helix, although counter-intuitive, is the most effective mechanism for generating large squeezing forces in twining plants. Our observations and model point to a general mechanism for the generation of the twining force: a modest radial stem expansion during primary growth, or the growth of lateral structures such as leaf bases, causes a delayed stem tensioning that creates the squeezing forces necessary for twining plants to ascend their supports. Our study thus provides the long-sought answer to the question of how twining plants ascend smooth supports without the use of adhesive or hook-like structures.