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Nanobubbles: a new paradigm for air-seeding in xylem H. Jochen Schenk1, Kathy Steppe2, and Steven Jansen3 1
Department of Biological Science, California State University Fullerton, PO Box 6850, Fullerton, CA 92834-6850, USA Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium 3 Institute for Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany 2
Long-distance water transport in plants relies on a system that typically operates under negative pressure and is prone to hydraulic failure due to gas bubble formation. One primary mechanism of bubble formation takes place at nanoporous pit membranes between neighboring conduits. We argue that this process is likely to snap off nanobubbles because the local increase in liquid pressure caused by entry of air-water menisci into the complex pit membrane pores would energetically favor nanobubble formation over instant cavitation. Nanobubbles would be stabilized by surfactants and by gas supersaturation of the sap, may dissolve, fragment into smaller bubbles, or create embolisms. The hypothesis that safe and stable nanobubbles occur in plants adds a new component supporting the cohesion-tension theory. A new twist on the cohesion-tension theory If every air bubble inside a functioning conduit prevented any further ascent of sap then it certainly would be ensured to keep these conduits entirely free of air. Then there would hardly exist a wood structure such as the one found in vascular plants (Eduard Strasburger 1893; translated from German) [1]. The stability of water in plants when it is transported under substantial negative pressure has been a question of central importance since the cohesion-tension theory was first proposed 120 years ago [2,3]. The theory posits that transpiring surfaces in leaves create sub-atmospheric or negative pressure that provides the driving force for water movement in hydraulic systems of plants. Hydraulic systems that are operated under negative pressure impose serious engineering design challenges because they are likely to form gas bubbles that can expand to block conduits, form embolisms, and disable the entire system [4]. It is well known that bubbles can penetrate into plant hydraulic systems, although there are open questions about whether this can occur daily and under mild drought stress, followed by refilling of conduits overnight [5,6], or whether embolisms are essentially permanent and form Corresponding author: Jansen, S. ([email protected]). Keywords: xylem embolisms; nanobubbles; surfactants; Blake threshold; cohesion tension theory. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.01.008
only under severe drought stress [7–9] or due to freezing. Answers to these questions will depend on understanding how the bubbles form initially and how they cause embolisms in the plant hydraulic system. In this Opinion paper we briefly review anatomical traits that affect bubble and embolism formation in flowering plants, discuss the physics that governs these processes, and propose a new component to the cohesion-tension theory to account for the stability of gas nanobubbles under negative pressure. The importance of pit membranes Water is transported in plants through xylem conduits, which are cells that are dead at maturity. Xylem conduits show a relatively wide lumen and provide a low-resistance pathway through the plant but, because they have a finite length, water is forced to move between neighboring conduits via bordered pits, which are narrow cavities in the secondary cell wall. Bordered pits (Figure 1) do not represent complete openings in the cell wall and retain a modified, nanoporous primary cell wall, the pit membrane, which functions as a hydraulic safety valve [10–12]. In flowering plants, this pit membrane ranges in thickness between 70 and 1200 nm and consists of non-interwoven layers of cellulose microfibrils with an average diameter around 20 nm [11], which translates into 3–60 microfibril layers per membrane. Most polysaccharides that interconnect microfibrils in primary cell walls are thought to be hydrolyzed in pit membranes and are therefore absent [13]. Pectins have been found embedded near the edge of pit membranes, the annulus, where they may play an important role when membranes are deflected and stretched under pressure [14–17]. Pit membranes in their natural state are often coated with an amorphous or globular layer of unknown chemistry [18–21], which is usually removed by routine ethanol treatments used for fixing specimens for microscopy [19–21]. In addition, some authors have postulated that cellulose microfibrils in pit membranes may be embedded in a matrix of pectin hydrogel [8,18,22]. This hypothesis was not supported by studies of pit membrane chemistry in several angiosperms [14,15,17], but more studies will be necessary to test a wider variety of species for different types of pectins. Nanobubble formation The process of gas bubble formation in xylem tissue of plants, which is frequently described as the air-seeding process [4], assumes that the entry of a new bubble into a Trends in Plant Science xx (2015) 1–7
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(A)
(B)
2RP
(D)
RB ϕ (C)
Air
H2O Surfactants
Pit membrane Pit border
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Pit chamber
20 nm
Microfibril TRENDS in Plant Science
Figure 1. Proposed model of nanobubble formation in an angiosperm pit membrane. (A) Typical angiosperm bordered pit with pit membrane and partially enclosed pit chamber. (B) Air–water meniscus moving through a cellulose nanofiber pore inside a pit membrane. The pressure difference between the gas and liquid phase required to force a meniscus of radius RB through the pore depends on the smallest radius RP of the largest pore, contact angle w, and surface tension g (see Box 1). (C) Entry of the meniscus through the pore constriction has caused an increase in liquid pressure in the pore, resulting in nanobubble snap-off. (D) Surfactants coating a nanobubble that emerges from a pit membrane pore.
xylem conducting cell under tension would cause immediate expansion of the bubble, followed by cavitation and embolism formation. However, gas bubbles below a critical radius are safe from expansion and cavitation, even under negative liquid pressure. This was first recognized in 1949 [23], and was later pointed out for conditions in the xylem [24], but has rarely been mentioned in the plant science literature since then. There are serious gaps in our mechanistic understanding of air-seeding in plants, largely because until recently it has been impossible to observe microscale processes under negative pressure [25–27]. In particular, we do not know at present how bubbles move through pit membranes between conduits, how large they are when they enter the liquid phase, and whether they dissolve, expand to form embolisms, or remain stable. The physics behind the movement of an air–water interface through a porous membrane and the resulting bubble formation is explained in Box 1. Because pore radii in pit membranes are variable in shape and size, ranging between 2 and 200 nm, and usually less than 100 nm [11,12,28], bubbles that move through these pores are nanobubbles. The pressure difference required to force a meniscus through a pore strongly depends on the geometry of the pore (Box 1), and pit membrane pores typically have far lower bubble point pressures than those expected from the widely used Laplace–Washburn equation (Box 1, Figure 2) [11,28]. How do nanobubbles form in a pit membrane? First, movement of a meniscus through a nanoporous constriction snaps off a nanobubble (Figure 1C) inside the membrane if the radius of the constriction is less than half the radii of that pore on either side of the constriction [29,30]. In geometrically complex pore spaces, the invasion of a non-wetting fluid, such as air invading a pit membrane wetted with water, occurs not as a simple wetting front, but instead in rapid snap-off events and so-called Haines jumps [31,32]. Second, a gas meniscus moving into a 2
Box 1. Theory of pressure-driven nanobubble movement through porous media Movement of a gas-liquid interface through an asymmetrical pore can be described by a modified version of the Young-Laplace equation [91]: 1 1 DP bp ¼ g T ; P l cos ’ [I] þ R1 R2 with DPbp = Pg Pl, where DPbp is the bubble point pressure difference [92], Pg and Pl are the gas (including water vapor) pressure and the liquid pressure, respectively, g(T,Pl) is the surface tension of the liquid at temperature T and liquid pressure Pl, w is the contact angle of the gas-liquid interface with the pore wall. R1 and R2 are the principal radii of curvature of the gas-liquid interface and are equal to the longest and shortest pore radii minus the thickness of the absorption film (between 0.5 and 2 nm thick [93]). Surface tension, g, of pure water decreases with increasing temperature by 0.12% 8C1 and increases with decreasing liquid pressure and decreasing meniscus radius, but the effect is small for relevant pore sizes in plants above 10 nm radius [94]. The contact angle w between nanocellulose and water has been found to be between 58 and 88 [95], but because the meniscus is effectively in contact with water absorbed in cellulose, the actual contact angle is expected to be zero [93]. The principal radii depend on the geometry of a pore, with R1 = R2 for a circular pore or R1 >> R2 for a slit-shaped pore. For perfectly cylindrical pore shapes, R1 = R2 = Rp and [II] DP bp ¼ 2gðT ; P l Þcosð’Þ=R p This approximation, known as the Laplace–Washburn equation, is almost universally cited in the plant hydraulics literature [4,11,12,28]. In reality, each pit membrane will have a range of characteristic pore shapes, based on the spatial arrangement of microfibrils, such that R1 and R2 cannot be determined and DPbp for the membrane may be expressed as a function of the smallest radius Rp of the largest pore as: DP bp ¼ k2gðT ; P l Þcosð’Þ=R p
[III]
[96,97], where k is a dimensionless shape correction factor that can range between 0 and 1. Because pit membrane pores consist of openings between cellulose microfibrils, pore shapes between microfibrils in the same plane are slit- or V-shaped rather than circular. In this case, R1 is >> R2 in Equation I and 1/R1 then approaches zero, which leads to a pore shape correction factor k in Equation II that approaches 0.5 [10].
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Pit membrane pore shape factor, κ
1.2 1.0 R2 = 0.7336
0.8 0.6 0.4 0.2 0.0
0
100
200
300
Pit membrane thickness (nm)
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Figure 2. Pore shape correction factors recalculated from single vessel air injection data and observations of maximum pit membrane pore sizes for seven tree species in Jansen et al. [11] in relation to pit membrane thickness. Pit membranes shown are the thinnest (Betula pendula Roth) and the thickest (Arbutus uva-ursii L.) in the study (1 mm scale bars; images from [11]). Pore shape corrections factors, k, were calculated from Equation III in Box 1, assuming w = 0 and surface tension of pure water. Species with smaller pores and thicker membranes had lower pore shape correction factors, while species with larger pores and thinner membranes had correction factors close to k = 1, thereby fitting Equation II in Box 1.
liquid-filled pore increases the local pressure in this partially confined space, and this stabilizes the meniscus and contributes to bubble snap-off at the pore constriction. Owing to the low compressibility of liquid water, the pressure release caused by bubble entry into water under negative pressure is substantial – a bubble that compresses water volume in the confined space of a pit membrane pore or within the partially confined pit chamber (0.5–10 mm3 [33]) by only 0.1% temporarily releases about 2 MPa of negative pressure [27,34]. Third, in liquid
that is under negative pressure, surface-area minimization leading to bubble formation is thermodynamically favored over rupture of hydrogen bonds between water molecules at the gas–water interface, which requires far more tensile energy density [35]. Therefore, air-seeding inside a porous membrane at the interface between air and water under negative pressure occurs by snapping off nanobubbles, not by creating a continuous stream of air or cavitation voids. This, however, does not necessarily imply that the nanobubbles remain stable (see below). Although it is not possible to study the air-seeding process directly in plants, it can be seen in artificial nanofluidic devices. In a recent study [25], rupture of a meniscus under negative pressure snapped off a nanobubble (Figure 3) that relieved the pressure in the nanochannel and thereby restored stability to the meniscus. Negative pressure in confined spaces within hydrogels also creates bubbles, not explosive cavitation voids [26,27]. The same should be true for plant xylem. A layer of surfactants on the cellulose microfibrils of the pit membrane would lower surface tension relative to water and decrease the pressure required to force nanobubbles through membrane pores (Box 1) [36,37]. Xylem sap includes a large variety of surfactant molecules, such as many different proteins [38] and arabinogalactan proteins [39], as well as phospholipids [40]. Surfactants in water form micelles, which would be transported in sap to pit membranes and be deposited there, and it therefore seems very possible that amorphous layers observed on pit membranes [18–21] consist of surfactants. When hydrated, the amorphous layer clearly shows a globular structure (Figure 4) [19] that is consistent with the idea that the layer is made up of micelles. Surfactants on nanoporous membranes would lower surface tension and cause smaller bubbles to emerge from the pit membrane pores [41], with charged surfactants creating the smallest bubbles [42]. Nanobubble stability Gas-filled nanobubbles forming in water under negative pressure will be stable provided that their sizes remain
(A)
Deformed meniscus
Entrance a
b
4 μm (B)
4 μm TRENDS in Plant Science
Figure 3. Top view microscope images of deformed menisci and nanobubble snap-off under negative pressure at a silica nanochannel entrance. Nanochannels are 4 mm wide and 58 nm in height. (A) A deformed meniscus at the entrance. The channel height difference at locations (a) and (b) results in different liquid pressure and meniscus deformation on the horizontal plane. (B) Three representative images showing the deformed meniscus, bubble snap-off, and bubble entrapment. Reproduced, with permission, from the appendix to Duan et al. [25].
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Box 2. Stability of gas nanobubbles as a function of size and surface tension Because of surface tension, nanobubbles filled only with water vapor are stable under negative water pressure provided that their size remains below a critical radius Rc,v [23,24]: R c;v ¼
2g ðP v P l Þ
[I]
where Pv is the saturation vapor pressure inside the gas bubble (a function of temperature), Pl is the liquid pressure, and g is the surface tension, which for surfactants is radius-dependent [57,60,61]. Watervapor bubbles do not result from air-seeding and are unlikely to form in xylem sap through homogeneous nucleation [4,98]. In addition to the variables in Equation I, the stability of gas nanobubbles forming in water under negative pressure is also affected by the pressure of the gas inside the bubble [24]. Taking this into account, the critical radius for gas bubbles is the so-called Blake threshold, Rc,v+g, which is calculated as: 4g 4g R c;vþg ¼ for R crit < 200 nm [II] 3P l 3 Pv Pl [23,43,60], where the saturation vapor pressure inside the gas bubble Pv becomes negligible at small nanobubble sizes below 200 nm radius.
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Figure 4. Atomic force microscopy height image of a Triadica sebifera Small (Euphorbiaceae) pit membrane surface, coated with a globular material that may consist of surfactant micelles. Reticulate interstitial coating material present in the lower half of the image. Scale bar, 258 nm. Slightly modified and reproduced, with permission, from Pesacreta et al. [19].
below the so-called Blake threshold or critical radius [23,43] (Box 2). Depending on the dissolved gas concentration in xylem sap, nanobubbles may either quickly dissolve or remain in the sap until cooling nocturnal temperatures increase gas solubility. According to the Young–Laplace equation (Box 1) and Henry’s law, the high internal gas pressure in small nanobubbles would drive the gas into solution [44–46], unless the xylem sap was supersaturated with gas. Gas supersaturation is likely to occur in xylem almost daily during periods of rising temperatures, which decrease gas solubility. Recent findings have shown that nanobubbles in bulk solution can be surprisingly stable. The reasons for this stability of nanobubbles are under very active investigation [44,47–50], and include stabilization by electrostatic double-layers at the air–water interface [49,51], involving OH ions [52] and electrolytes [53], diffusive shielding of bubble clusters in supersaturated water [54], and the presence of surfactant shells [46,55–57]. The stability of a nanobubble greatly depends on its size and surface tension. It is generally assumed that surfactants in xylem sap reduce surface tension and bubble stability, and thereby increase the vulnerability of sap to embolism formation under negative pressure [36,37,58]. 4
This was confirmed by experiments in which surfactants were added to water fed into detached stems of angiosperms [33,59]. However, natural surfactant concentrations in xylem sap are far lower than in these experiments. Moreover, the surface tension of surfactant-coated bubbles is radius-dependent, not constant, and can range from zero, when surfactant molecules are jammed together, to temporarily exceeding that of water in expanding bubbles, in which surfactant molecules stretch apart [57,60,61]. Because of radius-dependent surface tension, surfactantcoated nanobubbles are actually more stable under negative pressure than are bubbles in pure water [60]. Most importantly, surfactant-coated nanobubbles that form under a typical surface tension one third that of water will have only a third of the radius of a bubble in pure water, and therefore can safely expand to the Blake threshold radius of a surfactant-free bubble when the surfactant coat breaks apart. Nanobubbles could potentially coalesce into larger and less-stable bubbles. Coalescence could be affected greatly by the presence of surfactant shells and by the concentrations of electrolytes in xylem sap and/or by charges on the surface of the pit membrane [62]. Dissolved salts such as KCl, CaCl2, and MgCl2 are powerful bubble coalescence inhibitors [63,64]. Thus, ions in xylem sap may have a stabilizing effect on nanobubbles. The presence of such electrolytes in xylem sap is known to increase xylem hydraulic conductance [22,65,66], and this may be due to prevention of bubble coalescence in sap and pit membranes [67], especially if nanobubbles remained there after previous air-seeding events or became stuck when carried to pit membranes with the transpiration stream. Nanobubble breakup and cavitation When nanobubbles enlarge and become unstable under decreasing liquid pressure, or when a steady stream of nanobubbles from pit membrane pores produces a cluster of bubbles that coalesce into larger ones, then nanobubbles
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Opinion would expand beyond the Blake threshold (Box 2), become unstable, and possibly form embolisms. In a recent experiment it was found that embolisms could be created by slowly spinning stems of a long-vesseled plant species in a centrifuge for several hours [68]. One explanation for this finding would be that nanobubbles already present in vessels slowly migrated under centrifugal force towards the middle of the stem segment, where the centrifugal tension is highest. There, nanobubbles clustered, coalesced, and expanded to become emboli. Whether bubble expansion occurs immediately after bubble entry through a pit membrane or later, the most likely space by far for it to occur in is within the overhanging parts of the secondary wall, in other words the pit border (Figure 1), because nanobubbles would not move out of the chamber other than through Brownian motion. Because pit apertures represent a small (80% confined chamber. Bubble cavitation in confined spaces of approximately 50 000 mm3 volume, three orders of magnitude larger than a pit border, was found to produce oscillating pressure pulses of 10 to 50 MPa in a microfluidic synthetic tree [27]. Pressure travels at the speed of sound, far faster than water molecules could move through the aperture into the conduit, and therefore pressure waves in the pit chamber may fragment a cavitating bubble rather than allow its expansion into the conduit. In the process, the pressure oscillations in the surrounding cell wall could produce the acoustic emissions that are well known to be associated with bubble collapse during cavitation [35,69,70], and are equally well known to be associated with cavitation in plants [71–74]. The number of acoustic emission events in angiosperm xylem typically greatly exceeds the number of xylem embolisms formed [71,75], possibly due to cavitation in fibers [71] or xylem shrinkage [75]. Alternatively, cavitation events in pit chambers that do not result in embolism formation may cause these unexplained acoustic emissions. Surfactant shells would also affect nanobubble breakup and cavitation. First, breakup of a surfactant shell would expose the air–water interface of the bubble with its higher surface tension, which provides a second layer of protection to bubble stability. Second, under decreasing liquid pressure, expansion of surfactant-coated nanobubbles can disrupt the surfactant coat into islands of low surface tension, surrounded by areas with high pure-water surface tension [76–79]. Surfactant islands could bulge out to create buds and small bubble fragments, and this has been observed in response to pressure fluctuations created by ultrasound treatment of lipid-coated microbubbles [80]. Thus, a surfactant coat might allow a bubble to safely bud into smaller bubbles rather than cavitate under decreasing pressure. In turn, bubble shrinkage caused by increasing liquid pressure and/or bubble dissolution causes the surfactant layer to wrinkle and fold [76–79], and, upon further shrinkage, to crumble and eventually break off parts as micelles or sapfilled vesicles [56].
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Nanobubbles and the cohesion-tension theory What are the consequences of nanobubbles for understanding water transport in plants? Stable nanobubbles in xylem under negative pressure add a new component to the cohesion-tension theory and the well-supported air-seeding hypothesis [4]. Recognition that small bubbles are safe from cavitation enables a new appreciation of plant water transport under negative pressure because the system may not be as vulnerable as previously thought. The theory therefore fits in well with recent findings that suggest that the prevalence of xylem embolisms may have been overestimated [8,9]. The hypothesis that bordered pits may function to confine cavitation events to the largely enclosed pit chambers is another aspect of the theory that offers a new explanation for why all xylem conduits have bordered pits [12]. While only flowering plants are considered here (Figure 1), it can be suggested that the nanobubbles hypothesis also applies to ferns, while it is unclear whether nanobubbles would be formed in conifers, where torusmargo pits possess much larger pores and a valve-sealing mechanism that may prevent nanobubble formation [81]. One implication of the nanobubble theory is that the largest pore in inter-vessel pit membranes may not necessarily be the sole determinant of the resistance of a particular vessel to embolism formation – the ‘rare pit’ hypothesis [82,83] – because not every nanobubble would create an embolism. Embolisms instead might form when nanobubble concentration exceeds a critical threshold combined with bubble expansion under declining liquid pressure. This would be most likely to occur in vessels with larger pit pores, as predicted by the rare pit hypothesis, and in agreement with experimental findings [83]. Any new theory to explain a natural phenomenon has to fit all known facts and explain, or at least not contradict, all known observations. Particular strengths of the nanobubble theory include that it supports the cohesion-tension theory and that it also creates a framework that can explain embolism repair under tension. This is a subject that requires a thorough theoretical treatment beyond the scope of this paper. Briefly, pressure-driven movement of nanobubbles from an embolism into a sap-filled conduit could be a far more efficient way to remove the air than diffusion, which is a far slower process [84,85]. Non-destructive observations of vessel refilling show that, even in the absence of sap flow, air can be completely removed from vessels within 30 minutes to a few hours [6,86–88]. The other aspect of vessel refilling that the nanobubble theory could help to explain is the process of hydraulic reconnection between the refilled and functioning conduit, because this would seemingly require simultaneous reconnection of every single pit pore to avoid new bubble formation [89,90]. Reconnection would normally occur once water has entered all pit apertures and reached the surface of all pit membranes within a refilling conduit. At this point, the bubbles remaining in the pit membrane after hydraulic reconnection would be nanobubbles that could be stable under negative pressure and eventually dissolve. We conclude that the nanobubble theory is in agreement not only with the cohesion-tension theory but also with recent findings regarding ionic effects on xylem conductance, the relatively low prevalence of embolisms under 5
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Opinion natural conditions, and the existence of embolism repair under tension. It also could explain the otherwise puzzling presence of surfactants in xylem sap, the fact that real pit membrane pores are far more vulnerable to air-seeding than theoretical cylindrical pores, the function of bordered pits, and the patterns of acoustic emissions in droughtstressed xylem. The theory obviously is in need of testing for the presence of stable nanobubbles in xylem sap and especially in bordered pit chambers, by chemical analysis of xylem sap surfactants, and by further studies of pit membrane bubble point pressures in relation to pore geometries and surfactants. Acknowledgments Research that contributed to this paper was funded by the National Science Foundation (IOS-0943502 and IOS-1146993). The authors thank Susana Espino, Philippe Marmottant, Olivier Vincent, Chuanhua Duan, Emily Cranston, James Kwan, Thomas Pesacreta, and five anonymous reviewers for comments on earlier drafts.
References 1 Strasburger, E. (1893) Histologische Beitra¨ge, V. Ueber das Saftsteigen, Verlag von Gustaf Fischer 2 Dixon, H.H. and Joly, J. (1895) On the ascent of sap. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 186, 563–576 3 Askenasy, E. (1895) Ueber das Saftsteigen. Verh. Nat. Med. Ver. Heidelb. N. F. 5, 325–345 4 Tyree, M.T. and Zimmermann, M.H. (2002) Xylem Structure and the Ascent of Sap, Springer-Verlag 5 Brodersen, C.R. and McElrone, A.J. (2013) Maintenance of xylem network transport capacity: a review of embolism repair capacity in vascular plants. Front. Plant Sci. 4, 108 6 Brodersen, C.R. et al. (2010) The dynamics of embolism repair in xylem: in vivo visualizations using high resolution computed tomography. Plant Physiol. 154, 1088–1095 7 Cochard, H. and Delzon, S. (2013) Hydraulic failure and repair are not routine in trees. Ann. For. Sci. 70, 659–661 8 Rockwell, F.E. et al. (2014) Cavitation and its discontents: opportunities for resolving current controversies. Plant Physiol. 164, 1649–1660 9 Wheeler, J.K. et al. (2013) Cutting xylem under tension or supersaturated with gas can generate PLC and the appearance of rapid recovery from embolism. Plant Cell Environ. 36, 1938–1949 10 Meyra, A.G. et al. (2007) Geometrical and physicochemical considerations of the pit membrane in relation to air seeding: the pit membrane as a capillary valve. Tree Physiol. 27, 1401–1405 11 Jansen, S. et al. (2009) Morphological variation of intervessel pit membranes and implications to xylem function in angiosperms. Amer. J. Bot. 96, 409–419 12 Choat, B. et al. (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytol. 177, 608–626 13 Butterfield, B.G. and Meylan, B.A. (1982) Cell wall hydrolysis in the tracheary elements of the secondary xylem. In New Perspectives in Wood Anatomy (Baas, P., ed.), pp. 71–84, Nijhoff/W. Junk 14 Kim, J.S. and Daniel, G. (2013) Developmental localization of homogalacturonan and xyloglucan in pit membranes varies between pit types in two poplar species. IAWA J. 34, 245–262 15 Plavcova´, L. and Hacke, U.G. (2011) Heterogeneous distribution of pectin epitopes and calcium in different pit types of four angiosperm species. New Phytol. 192, 885–897 16 Dusotoit-Coucaud, A. et al. (2014) Hydrolase treatments help unravel the function of intervessel pits in xylem hydraulics. Physiol. Plant 150, 388–396 17 Herbette, S. et al. (2014) Immunolabelling of intervessel pits for polysaccharides and lignin helps in understanding their hydraulic properties in Populus tremula alba. Ann. Bot. Published online November 30, 2014. http://dx.doi.org/10.1093/aob/mcu232 18 Lee, J. et al. (2012) Ion induced changes in the structure of bordered pit membranes. Front. Plant Sci. 3, 55 6
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19 Pesacreta, T.C. et al. (2005) Atomic force microscopy of the intervessel pit membrane in the stem of Sapium sebiferum (Euphorbiaceae). IAWA J. 26, 397–426 20 Jansen, S. et al. (2008) The effect of preparation techniques on SEMimaging of pit membranes. IAWA J. 29, 161–178 21 Sano, Y. (2005) Inter- and intraspecific structural variations among intervascular pit membranes, as revealed by field-emission scanning electron microscopy. Amer. J. Bot. 92, 1077–1084 22 Zwieniecki, M.A. et al. (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059–1062 23 Blake, F.G. (1949) The Onset of Cavitation in Liquids. I: Cavitation Threshold Sound Pressures in Water as a Function of Temperature and Hydrostatic Pressure, Acoustics Research Laboratory, Department of Engineering Sciences and Applied Physics, Harvard University 24 Oertli, J.J. (1971) The stability of water under tension in the xylem. Z. Pflanzenphysiol. 65, 195–209 25 Duan, C. et al. (2012) Evaporation-induced cavitation in nanofluidic channels. Proc. Natl. Acad. Sci. U.S.A. 109, 3688–3693 26 Vincent, O. et al. (2014) The fast dynamics of cavitation bubbles within water confined in elastic solids. Soft Matter 10, 1455–1461 27 Vincent, O. et al. (2012) Birth and growth of cavitation bubbles within water under tension confined in a simple synthetic tree. Phys. Rev. Lett. 108, 184502 28 Lens, F. et al. (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol. 190, 709–723 29 Kovscek, A.R. and Radke, C.J. (1996) Gas bubble snap-off under pressure-driven flow in constricted noncircular capillaries. Colloid Surf. A 117, 55–76 30 Kovscek, A.R. et al. (2007) Verification of Roof snap off as a foamgeneration mechanism in porous media at steady state. Colloid Surf. A 302, 251–260 31 Berg, S. et al. (2013) Real-time 3D imaging of Haines jumps in porous media flow. Proc. Natl. Acad. Sci. U.S.A. 110, 3755–3759 32 Moebius, F. et al. (2012) Characteristics of acoustic emissions induced by fluid front displacement in porous media. Water Resour. Res. 48, W11507 33 Choat, B. et al. (2004) Changes in pit membrane porosity due to deflection and stretching: the role of vestured pits. J. Exp. Bot. 55, 1569–1575 34 Davitt, K. et al. (2010) Equation of state of water under negative pressure. J. Chem. Phys. 133, 174507 35 Brennen, C.E. (2014) Cavitation and Bubble Dynamics, Cambridge University Press 36 Christensen-Dalsgaard, K.K. et al. (2011) Surface tension phenomena in the xylem sap of three diffuse porous temperate tree species. Tree Physiol. 31, 361–368 37 Ho¨ltta¨, T. et al. (2012) Cavitation induced by a surfactant leads to a transient release of water stress and subsequent ‘run away’ embolism in Scots pine (Pinus sylvestris) seedlings. J. Exp. Bot. 63, 1057–1067 38 Buhtz, A. et al. (2004) Xylem sap protein composition is conserved among different plant species. Planta 219, 610–618 39 Iwai, H. et al. (2003) Analysis of sugars in squash xylem sap. Plant Cell Physiol. 44, 582–587 40 Gonorazky, G. et al. (2012) Phosphatidylinositol 4-phosphate is associated to extracellular lipoproteic fractions and is detected in tomato apoplastic fluids. Plant Biol. 14, 41–49 41 Kukizaki, M. and Goto, M. (2006) Size control of nanobubbles generated from Shirasu-porous-glass (SPG) membranes. J. Membr. Sci. 281, 386–396 42 Kukizaki, M. and Baba, Y. (2008) Effect of surfactant type on microbubble formation behavior using Shirasu porous glass (SPG) membranes. Colloid Surf. A 326, 129–137 43 Sa´nchez, J.M. and Sa´ Lo´pez, D. (2003) A micro mechanics model for cavitation. In Computational methods in engineering and science (Iu, V.P. et al., eds), pp. 719–726, Swets and Zeitlinger 44 Seddon, J.R.T. et al. (2012) A deliberation on nanobubbles at surfaces and in bulk. ChemPhysChem 13, 2179–2187 45 Epstein, P.S. and Plesset, M.S. (1950) On the stability of gas bubbles in liquid-gas solutions. J. Chem. Phys. 18, 1505–1509 46 Duncan, P.B. and Needham, D. (2004) Test of the Epstein–Plesset model for gas microparticle dissolution in aqueous media: effect of
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surface tension and gas undersaturation in solution. Langmuir 20, 2567–2578 Ushikubo, F.Y. et al. (2010) Evidence of the existence and the stability of nano-bubbles in water. Colloid Surf. A 361, 31–37 Ohgaki, K. et al. (2010) Physicochemical approach to nanobubble solutions. Chem. Eng. Sci. 65, 1296–1300 Jin, F. et al. (2007) Effects of pH and ionic strength on the stability of nanobubbles in aqueous solutions of a-cyclodextrin. J. Phys. Chem. B 111, 11745–11749 Jin, F. et al. (2007) Observation of kinetic and structural scalings during slow coalescence of nanobubbles in an aqueous solution. J. Phys. Chem. B 111, 13143–13146 Creux, P. et al. (2007) Specific cation effects at the hydroxide-charged air/water interface. J. Phys. Chem. C 111, 3753–3755 Liu, M.Y. et al. (2012) The surface relaxation of water. J. Phys. Chem. B. 116, 8981–8988 Browne, C. et al. (2011) Bubble coalescence during acoustic cavitation in aqueous electrolyte solutions. Langmuir 27, 12025–12032 Weijs, J.H. et al. (2012) Diffusive shielding stabilizes bulk nanobubble clusters. ChemPhysChem 13, 2197–2204 Longo, M.L. et al. (2009) Physical chemistry of experimental models for lipid shells of medical microbubbles. Bubble Sci. Eng. Technol. 1, 18–30 Kwan, J.J. and Borden, M.A. (2012) Lipid monolayer collapse and microbubble stability. Adv. Colloid Interface Sci. 183, 82–99 Kwan, J.J. and Borden, M.A. (2010) Microbubble dissolution in a multigas environment. Langmuir 26, 6542–6548 Domec, J.C. (2011) Let’s not forget the critical role of surface tension in xylem water relations. Tree Physiol. 31, 359–360 Sperry, J.S. and Tyree, M.T. (1988) Mechanism of water stress-induced xylem embolism. Plant Physiol. 88, 581–587 Atchley, A.A. (1989) The Blake threshold of a cavitation nucleus having a radius-dependent surface tension. J. Acoust. Soc. Am. 85, 152–157 Mørch, K.A. (2007) Reflections on cavitation nuclei in water. Phys. Fluids 19, 072104 van Doorn, W.G. et al. (2011) Hydrogel regulation of xylem water flow: an alternative hypothesis. Plant Physiol. 157, 1642–1649 Craig, V.S.J. (2004) Bubble coalescence and specific-ion effects. Curr. Opin. Colloid Interface Sci. 9, 178–184 Craig, V.S.J. et al. (1993) The effect of electrolytes on bubble coalescence in water. J. Phys. Chem. 97, 10192–10197 Jansen, S. et al. (2011) Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? New Phytol. 189, 218–228 Nardini, A. et al. (2011) More than just a vulnerable pipeline: xylem physiology in the light of ion-mediated regulation of plant water transport. J. Exp. Bot. 62, 4701–4718 Espino, S. and Schenk, H.J. (2011) Mind the bubbles: Achieving stable measurements of maximum hydraulic conductivity through woody plant samples. J. Exp. Bot. 62, 1119–1132 Wang, R. et al. (2014) Water relations of Robinia pseudoacacia L.: do vessels cavitate and refill diurnally or are R-shaped curves invalid in Robinia? Plant Cell Environ. 37, 2667–2678 Harrison, M. (1952) An experimental study of single bubble cavitation noise. J. Acoust. Soc. Am. 24, 776–782 Mellen, R.H. (1954) Ultrasonic spectrum of cavitation noise in water. J. Acoust. Soc. Am. 26, 356–360 Ritman, K.T. and Milburn, J.A. (1988) Acoustic emissions from plants: ultrasonic and audible compared. J. Exp. Bot. 39, 1237–1248 Rosner, S. and Kikuta, S.B. (2004) Ultrasonic acoustic detection of cavitation events in water conducting elements of Norway spruce wood. In 26th European Conference on Acoustic Emission Testing, September 15–17, 2004, Berlin, Germany (European Working Group on Acoustic Emission eds), pp. 155–165 German Society for None-Destructive Testing Johnson, D.M. et al. (2009) Leaf xylem embolism, detected acoustically and by cryo-SEM, corresponds to decreases in leaf hydraulic conductance in four evergreen species. Plant Cell Environ. 32, 828–836
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74 Ferna´ndez, E. et al. (2012) Natural and laser-induced cavitation in corn stems: On the mechanisms of acoustic emissions. Pap. Phys. 4, 040003 75 Vergeynst, L.L. et al. (2014) Cavitation: a blessing in disguise? New method to establish vulnerability curves and assess hydraulic capacitance of woody tissues. Tree Physiol. Published online July 15, 2014. http://dx.doi.org/10.1093/treephys/tpu1056 76 Pu, G. et al. (2006) Collapse and shedding transitions in binary lipid monolayers coating microbubbles. Langmuir 22, 2993–2999 77 Borden, M.A. and Longo, M.L. (2002) Dissolution behavior of lipid monolayer-coated, air-filled microbubbles: effect of lipid hydrophobic chain length. Langmuir 18, 9225–9233 78 Lozano, M.M. and Longo, M.L. (2009) Microbubbles coated with disaturated lipids and DSPE-PEG2000: phase behavior, collapse transitions, and permeability. Langmuir 25, 3705–3712 79 Borden, M. (2009) Nanostructural features on stable microbubbles. Soft Matter 5, 716–720 80 Cox, D.J. and Thomas, J.L. (2013) Rapid shrinkage of lipid-coated bubbles in pulsed ultrasound. Ultrasound Med. Biol. 39, 466–474 81 Pittermann, J. et al. (2005) Torus-margo pits help conifers compete with angiosperm. Science 310, 1924 82 Wheeler, J.K. et al. (2005) Inter-vessel pitting and cavitation in woody Rosaceae and other vesseled plants: a basis for a safety vs. efficiency trade-off in xylem transport. Plant Cell Environ. 28, 800–812 83 Plavcova´, L. et al. (2013) Nobody’s perfect: Can irregularities in pit structure influence vulnerability to cavitation? Front. Plant Sci. 4, 453 84 Tyree, M.T. and Yang, S. (1992) Hydraulic conductivity recovery versus water pressure in xylem of Acer saccharum. Plant Physiol. 100, 669–676 85 Yang, S. and Tyree, M.T. (1992) A theoretical-model of hydraulic conductivity recovery from embolism with comparison to experimental data on Acer saccharum. Plant Cell Environ. 15, 633–643 86 Zwieniecki, M.A. et al. (2013) Analysis of spatial and temporal dynamics of xylem refilling in Acer rubrum L. using magnetic resonance imaging (MRI). Front. Plant Sci. 4, 265 87 Scheenen, T.W.J. et al. (2007) Intact plant magnetic resonance imaging to study dynamics in long-distance sap flow and flow-conducting surface area. Plant Physiol. 144, 1157–1165 88 Holbrook, N.M. et al. (2001) In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiol. 126, 27–31 89 Holbrook, N.M. and Zwieniecki, M.A. (1999) Embolism repair and xylem tension: Do we need a miracle? Plant Physiol. 120, 7–10 90 Zwieniecki, M.A. and Holbrook, N.M. (2009) Confronting Maxwell’s demon: biophysics of xylem embolism repair. Trends Plant Sci. 14, 530–534 91 Zhang, C. et al. (2011) Liquid CO2 displacement of water in a dualpermeability pore network micromodel. Environ. Sci. Technol. 45, 7581–7588 92 Baker, R.W. (2004) Membrane Technology and Applications, John Wiley & Sons 93 Mercury, L. and Tardy, Y. (2004) Response to the comment by J. V. Walther on ‘negative pressure of stretched liquid water: Geochemistry of soil capillaries.’ (2001) Geochim. Cosmochim. Acta 65, 3391-3408; and ‘thermodynamic properties of solutions in metastable systems under negative or positive pressures.’ (2003) Geochim. Cosmochim. Acta 67, 1769–1785. Geochim. Cosmochim. Acta 68, 2775–2780 94 Mercury, L. and Tardy, Y. (2001) Negative pressure of stretched liquid water. Geochemistry of soil capillaries. Geochim. Cosmochim. Acta 65, 3391–3408 95 Dankovich, T.A. and Gray, D.G. (2011) Contact angle measurements on smooth nanocrystalline cellulose (I) thin films. J. Adhes. Sci. Technol. 25, 699–708 96 US EPA Office of Water (2005) Membrane Filtration Guidance Manual, US Environmental Protection Agency 97 Emory, S.F. (1989) Principles of integrity testing hydrophilic microporous membrane filters. Pharm. Technol. 13, 68,70,74,76,77 98 Pickard, W.F. (1981) The ascent of sap in plants. Prog. Biophys. Mol. Biol. 37, 181–229
7
Opinion
Nanobubbles: a new paradigm for air-seeding in xylem H. Jochen Schenk1, Kathy Steppe2, and Steven Jansen3 1
Department of Biological Science, California State University Fullerton, PO Box 6850, Fullerton, CA 92834-6850, USA Laboratory of Plant Ecology, Department of Applied Ecology and Environmental Biology, Faculty of Bioscience Engineering, Ghent University, Coupure Links 653, 9000 Ghent, Belgium 3 Institute for Systematic Botany and Ecology, Ulm University, Albert-Einstein-Allee 11, 89081 Ulm, Germany 2
Long-distance water transport in plants relies on a system that typically operates under negative pressure and is prone to hydraulic failure due to gas bubble formation. One primary mechanism of bubble formation takes place at nanoporous pit membranes between neighboring conduits. We argue that this process is likely to snap off nanobubbles because the local increase in liquid pressure caused by entry of air-water menisci into the complex pit membrane pores would energetically favor nanobubble formation over instant cavitation. Nanobubbles would be stabilized by surfactants and by gas supersaturation of the sap, may dissolve, fragment into smaller bubbles, or create embolisms. The hypothesis that safe and stable nanobubbles occur in plants adds a new component supporting the cohesion-tension theory. A new twist on the cohesion-tension theory If every air bubble inside a functioning conduit prevented any further ascent of sap then it certainly would be ensured to keep these conduits entirely free of air. Then there would hardly exist a wood structure such as the one found in vascular plants (Eduard Strasburger 1893; translated from German) [1]. The stability of water in plants when it is transported under substantial negative pressure has been a question of central importance since the cohesion-tension theory was first proposed 120 years ago [2,3]. The theory posits that transpiring surfaces in leaves create sub-atmospheric or negative pressure that provides the driving force for water movement in hydraulic systems of plants. Hydraulic systems that are operated under negative pressure impose serious engineering design challenges because they are likely to form gas bubbles that can expand to block conduits, form embolisms, and disable the entire system [4]. It is well known that bubbles can penetrate into plant hydraulic systems, although there are open questions about whether this can occur daily and under mild drought stress, followed by refilling of conduits overnight [5,6], or whether embolisms are essentially permanent and form Corresponding author: Jansen, S. ([email protected]). Keywords: xylem embolisms; nanobubbles; surfactants; Blake threshold; cohesion tension theory. 1360-1385/ ß 2015 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tplants.2015.01.008
only under severe drought stress [7–9] or due to freezing. Answers to these questions will depend on understanding how the bubbles form initially and how they cause embolisms in the plant hydraulic system. In this Opinion paper we briefly review anatomical traits that affect bubble and embolism formation in flowering plants, discuss the physics that governs these processes, and propose a new component to the cohesion-tension theory to account for the stability of gas nanobubbles under negative pressure. The importance of pit membranes Water is transported in plants through xylem conduits, which are cells that are dead at maturity. Xylem conduits show a relatively wide lumen and provide a low-resistance pathway through the plant but, because they have a finite length, water is forced to move between neighboring conduits via bordered pits, which are narrow cavities in the secondary cell wall. Bordered pits (Figure 1) do not represent complete openings in the cell wall and retain a modified, nanoporous primary cell wall, the pit membrane, which functions as a hydraulic safety valve [10–12]. In flowering plants, this pit membrane ranges in thickness between 70 and 1200 nm and consists of non-interwoven layers of cellulose microfibrils with an average diameter around 20 nm [11], which translates into 3–60 microfibril layers per membrane. Most polysaccharides that interconnect microfibrils in primary cell walls are thought to be hydrolyzed in pit membranes and are therefore absent [13]. Pectins have been found embedded near the edge of pit membranes, the annulus, where they may play an important role when membranes are deflected and stretched under pressure [14–17]. Pit membranes in their natural state are often coated with an amorphous or globular layer of unknown chemistry [18–21], which is usually removed by routine ethanol treatments used for fixing specimens for microscopy [19–21]. In addition, some authors have postulated that cellulose microfibrils in pit membranes may be embedded in a matrix of pectin hydrogel [8,18,22]. This hypothesis was not supported by studies of pit membrane chemistry in several angiosperms [14,15,17], but more studies will be necessary to test a wider variety of species for different types of pectins. Nanobubble formation The process of gas bubble formation in xylem tissue of plants, which is frequently described as the air-seeding process [4], assumes that the entry of a new bubble into a Trends in Plant Science xx (2015) 1–7
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(A)
(B)
2RP
(D)
RB ϕ (C)
Air
H2O Surfactants
Pit membrane Pit border
1 μm
Pit chamber
20 nm
Microfibril TRENDS in Plant Science
Figure 1. Proposed model of nanobubble formation in an angiosperm pit membrane. (A) Typical angiosperm bordered pit with pit membrane and partially enclosed pit chamber. (B) Air–water meniscus moving through a cellulose nanofiber pore inside a pit membrane. The pressure difference between the gas and liquid phase required to force a meniscus of radius RB through the pore depends on the smallest radius RP of the largest pore, contact angle w, and surface tension g (see Box 1). (C) Entry of the meniscus through the pore constriction has caused an increase in liquid pressure in the pore, resulting in nanobubble snap-off. (D) Surfactants coating a nanobubble that emerges from a pit membrane pore.
xylem conducting cell under tension would cause immediate expansion of the bubble, followed by cavitation and embolism formation. However, gas bubbles below a critical radius are safe from expansion and cavitation, even under negative liquid pressure. This was first recognized in 1949 [23], and was later pointed out for conditions in the xylem [24], but has rarely been mentioned in the plant science literature since then. There are serious gaps in our mechanistic understanding of air-seeding in plants, largely because until recently it has been impossible to observe microscale processes under negative pressure [25–27]. In particular, we do not know at present how bubbles move through pit membranes between conduits, how large they are when they enter the liquid phase, and whether they dissolve, expand to form embolisms, or remain stable. The physics behind the movement of an air–water interface through a porous membrane and the resulting bubble formation is explained in Box 1. Because pore radii in pit membranes are variable in shape and size, ranging between 2 and 200 nm, and usually less than 100 nm [11,12,28], bubbles that move through these pores are nanobubbles. The pressure difference required to force a meniscus through a pore strongly depends on the geometry of the pore (Box 1), and pit membrane pores typically have far lower bubble point pressures than those expected from the widely used Laplace–Washburn equation (Box 1, Figure 2) [11,28]. How do nanobubbles form in a pit membrane? First, movement of a meniscus through a nanoporous constriction snaps off a nanobubble (Figure 1C) inside the membrane if the radius of the constriction is less than half the radii of that pore on either side of the constriction [29,30]. In geometrically complex pore spaces, the invasion of a non-wetting fluid, such as air invading a pit membrane wetted with water, occurs not as a simple wetting front, but instead in rapid snap-off events and so-called Haines jumps [31,32]. Second, a gas meniscus moving into a 2
Box 1. Theory of pressure-driven nanobubble movement through porous media Movement of a gas-liquid interface through an asymmetrical pore can be described by a modified version of the Young-Laplace equation [91]: 1 1 DP bp ¼ g T ; P l cos ’ [I] þ R1 R2 with DPbp = Pg Pl, where DPbp is the bubble point pressure difference [92], Pg and Pl are the gas (including water vapor) pressure and the liquid pressure, respectively, g(T,Pl) is the surface tension of the liquid at temperature T and liquid pressure Pl, w is the contact angle of the gas-liquid interface with the pore wall. R1 and R2 are the principal radii of curvature of the gas-liquid interface and are equal to the longest and shortest pore radii minus the thickness of the absorption film (between 0.5 and 2 nm thick [93]). Surface tension, g, of pure water decreases with increasing temperature by 0.12% 8C1 and increases with decreasing liquid pressure and decreasing meniscus radius, but the effect is small for relevant pore sizes in plants above 10 nm radius [94]. The contact angle w between nanocellulose and water has been found to be between 58 and 88 [95], but because the meniscus is effectively in contact with water absorbed in cellulose, the actual contact angle is expected to be zero [93]. The principal radii depend on the geometry of a pore, with R1 = R2 for a circular pore or R1 >> R2 for a slit-shaped pore. For perfectly cylindrical pore shapes, R1 = R2 = Rp and [II] DP bp ¼ 2gðT ; P l Þcosð’Þ=R p This approximation, known as the Laplace–Washburn equation, is almost universally cited in the plant hydraulics literature [4,11,12,28]. In reality, each pit membrane will have a range of characteristic pore shapes, based on the spatial arrangement of microfibrils, such that R1 and R2 cannot be determined and DPbp for the membrane may be expressed as a function of the smallest radius Rp of the largest pore as: DP bp ¼ k2gðT ; P l Þcosð’Þ=R p
[III]
[96,97], where k is a dimensionless shape correction factor that can range between 0 and 1. Because pit membrane pores consist of openings between cellulose microfibrils, pore shapes between microfibrils in the same plane are slit- or V-shaped rather than circular. In this case, R1 is >> R2 in Equation I and 1/R1 then approaches zero, which leads to a pore shape correction factor k in Equation II that approaches 0.5 [10].
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Pit membrane pore shape factor, κ
1.2 1.0 R2 = 0.7336
0.8 0.6 0.4 0.2 0.0
0
100
200
300
Pit membrane thickness (nm)
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Figure 2. Pore shape correction factors recalculated from single vessel air injection data and observations of maximum pit membrane pore sizes for seven tree species in Jansen et al. [11] in relation to pit membrane thickness. Pit membranes shown are the thinnest (Betula pendula Roth) and the thickest (Arbutus uva-ursii L.) in the study (1 mm scale bars; images from [11]). Pore shape corrections factors, k, were calculated from Equation III in Box 1, assuming w = 0 and surface tension of pure water. Species with smaller pores and thicker membranes had lower pore shape correction factors, while species with larger pores and thinner membranes had correction factors close to k = 1, thereby fitting Equation II in Box 1.
liquid-filled pore increases the local pressure in this partially confined space, and this stabilizes the meniscus and contributes to bubble snap-off at the pore constriction. Owing to the low compressibility of liquid water, the pressure release caused by bubble entry into water under negative pressure is substantial – a bubble that compresses water volume in the confined space of a pit membrane pore or within the partially confined pit chamber (0.5–10 mm3 [33]) by only 0.1% temporarily releases about 2 MPa of negative pressure [27,34]. Third, in liquid
that is under negative pressure, surface-area minimization leading to bubble formation is thermodynamically favored over rupture of hydrogen bonds between water molecules at the gas–water interface, which requires far more tensile energy density [35]. Therefore, air-seeding inside a porous membrane at the interface between air and water under negative pressure occurs by snapping off nanobubbles, not by creating a continuous stream of air or cavitation voids. This, however, does not necessarily imply that the nanobubbles remain stable (see below). Although it is not possible to study the air-seeding process directly in plants, it can be seen in artificial nanofluidic devices. In a recent study [25], rupture of a meniscus under negative pressure snapped off a nanobubble (Figure 3) that relieved the pressure in the nanochannel and thereby restored stability to the meniscus. Negative pressure in confined spaces within hydrogels also creates bubbles, not explosive cavitation voids [26,27]. The same should be true for plant xylem. A layer of surfactants on the cellulose microfibrils of the pit membrane would lower surface tension relative to water and decrease the pressure required to force nanobubbles through membrane pores (Box 1) [36,37]. Xylem sap includes a large variety of surfactant molecules, such as many different proteins [38] and arabinogalactan proteins [39], as well as phospholipids [40]. Surfactants in water form micelles, which would be transported in sap to pit membranes and be deposited there, and it therefore seems very possible that amorphous layers observed on pit membranes [18–21] consist of surfactants. When hydrated, the amorphous layer clearly shows a globular structure (Figure 4) [19] that is consistent with the idea that the layer is made up of micelles. Surfactants on nanoporous membranes would lower surface tension and cause smaller bubbles to emerge from the pit membrane pores [41], with charged surfactants creating the smallest bubbles [42]. Nanobubble stability Gas-filled nanobubbles forming in water under negative pressure will be stable provided that their sizes remain
(A)
Deformed meniscus
Entrance a
b
4 μm (B)
4 μm TRENDS in Plant Science
Figure 3. Top view microscope images of deformed menisci and nanobubble snap-off under negative pressure at a silica nanochannel entrance. Nanochannels are 4 mm wide and 58 nm in height. (A) A deformed meniscus at the entrance. The channel height difference at locations (a) and (b) results in different liquid pressure and meniscus deformation on the horizontal plane. (B) Three representative images showing the deformed meniscus, bubble snap-off, and bubble entrapment. Reproduced, with permission, from the appendix to Duan et al. [25].
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Box 2. Stability of gas nanobubbles as a function of size and surface tension Because of surface tension, nanobubbles filled only with water vapor are stable under negative water pressure provided that their size remains below a critical radius Rc,v [23,24]: R c;v ¼
2g ðP v P l Þ
[I]
where Pv is the saturation vapor pressure inside the gas bubble (a function of temperature), Pl is the liquid pressure, and g is the surface tension, which for surfactants is radius-dependent [57,60,61]. Watervapor bubbles do not result from air-seeding and are unlikely to form in xylem sap through homogeneous nucleation [4,98]. In addition to the variables in Equation I, the stability of gas nanobubbles forming in water under negative pressure is also affected by the pressure of the gas inside the bubble [24]. Taking this into account, the critical radius for gas bubbles is the so-called Blake threshold, Rc,v+g, which is calculated as: 4g 4g R c;vþg ¼ for R crit < 200 nm [II] 3P l 3 Pv Pl [23,43,60], where the saturation vapor pressure inside the gas bubble Pv becomes negligible at small nanobubble sizes below 200 nm radius.
TRENDS in Plant Science
Figure 4. Atomic force microscopy height image of a Triadica sebifera Small (Euphorbiaceae) pit membrane surface, coated with a globular material that may consist of surfactant micelles. Reticulate interstitial coating material present in the lower half of the image. Scale bar, 258 nm. Slightly modified and reproduced, with permission, from Pesacreta et al. [19].
below the so-called Blake threshold or critical radius [23,43] (Box 2). Depending on the dissolved gas concentration in xylem sap, nanobubbles may either quickly dissolve or remain in the sap until cooling nocturnal temperatures increase gas solubility. According to the Young–Laplace equation (Box 1) and Henry’s law, the high internal gas pressure in small nanobubbles would drive the gas into solution [44–46], unless the xylem sap was supersaturated with gas. Gas supersaturation is likely to occur in xylem almost daily during periods of rising temperatures, which decrease gas solubility. Recent findings have shown that nanobubbles in bulk solution can be surprisingly stable. The reasons for this stability of nanobubbles are under very active investigation [44,47–50], and include stabilization by electrostatic double-layers at the air–water interface [49,51], involving OH ions [52] and electrolytes [53], diffusive shielding of bubble clusters in supersaturated water [54], and the presence of surfactant shells [46,55–57]. The stability of a nanobubble greatly depends on its size and surface tension. It is generally assumed that surfactants in xylem sap reduce surface tension and bubble stability, and thereby increase the vulnerability of sap to embolism formation under negative pressure [36,37,58]. 4
This was confirmed by experiments in which surfactants were added to water fed into detached stems of angiosperms [33,59]. However, natural surfactant concentrations in xylem sap are far lower than in these experiments. Moreover, the surface tension of surfactant-coated bubbles is radius-dependent, not constant, and can range from zero, when surfactant molecules are jammed together, to temporarily exceeding that of water in expanding bubbles, in which surfactant molecules stretch apart [57,60,61]. Because of radius-dependent surface tension, surfactantcoated nanobubbles are actually more stable under negative pressure than are bubbles in pure water [60]. Most importantly, surfactant-coated nanobubbles that form under a typical surface tension one third that of water will have only a third of the radius of a bubble in pure water, and therefore can safely expand to the Blake threshold radius of a surfactant-free bubble when the surfactant coat breaks apart. Nanobubbles could potentially coalesce into larger and less-stable bubbles. Coalescence could be affected greatly by the presence of surfactant shells and by the concentrations of electrolytes in xylem sap and/or by charges on the surface of the pit membrane [62]. Dissolved salts such as KCl, CaCl2, and MgCl2 are powerful bubble coalescence inhibitors [63,64]. Thus, ions in xylem sap may have a stabilizing effect on nanobubbles. The presence of such electrolytes in xylem sap is known to increase xylem hydraulic conductance [22,65,66], and this may be due to prevention of bubble coalescence in sap and pit membranes [67], especially if nanobubbles remained there after previous air-seeding events or became stuck when carried to pit membranes with the transpiration stream. Nanobubble breakup and cavitation When nanobubbles enlarge and become unstable under decreasing liquid pressure, or when a steady stream of nanobubbles from pit membrane pores produces a cluster of bubbles that coalesce into larger ones, then nanobubbles
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Opinion would expand beyond the Blake threshold (Box 2), become unstable, and possibly form embolisms. In a recent experiment it was found that embolisms could be created by slowly spinning stems of a long-vesseled plant species in a centrifuge for several hours [68]. One explanation for this finding would be that nanobubbles already present in vessels slowly migrated under centrifugal force towards the middle of the stem segment, where the centrifugal tension is highest. There, nanobubbles clustered, coalesced, and expanded to become emboli. Whether bubble expansion occurs immediately after bubble entry through a pit membrane or later, the most likely space by far for it to occur in is within the overhanging parts of the secondary wall, in other words the pit border (Figure 1), because nanobubbles would not move out of the chamber other than through Brownian motion. Because pit apertures represent a small (80% confined chamber. Bubble cavitation in confined spaces of approximately 50 000 mm3 volume, three orders of magnitude larger than a pit border, was found to produce oscillating pressure pulses of 10 to 50 MPa in a microfluidic synthetic tree [27]. Pressure travels at the speed of sound, far faster than water molecules could move through the aperture into the conduit, and therefore pressure waves in the pit chamber may fragment a cavitating bubble rather than allow its expansion into the conduit. In the process, the pressure oscillations in the surrounding cell wall could produce the acoustic emissions that are well known to be associated with bubble collapse during cavitation [35,69,70], and are equally well known to be associated with cavitation in plants [71–74]. The number of acoustic emission events in angiosperm xylem typically greatly exceeds the number of xylem embolisms formed [71,75], possibly due to cavitation in fibers [71] or xylem shrinkage [75]. Alternatively, cavitation events in pit chambers that do not result in embolism formation may cause these unexplained acoustic emissions. Surfactant shells would also affect nanobubble breakup and cavitation. First, breakup of a surfactant shell would expose the air–water interface of the bubble with its higher surface tension, which provides a second layer of protection to bubble stability. Second, under decreasing liquid pressure, expansion of surfactant-coated nanobubbles can disrupt the surfactant coat into islands of low surface tension, surrounded by areas with high pure-water surface tension [76–79]. Surfactant islands could bulge out to create buds and small bubble fragments, and this has been observed in response to pressure fluctuations created by ultrasound treatment of lipid-coated microbubbles [80]. Thus, a surfactant coat might allow a bubble to safely bud into smaller bubbles rather than cavitate under decreasing pressure. In turn, bubble shrinkage caused by increasing liquid pressure and/or bubble dissolution causes the surfactant layer to wrinkle and fold [76–79], and, upon further shrinkage, to crumble and eventually break off parts as micelles or sapfilled vesicles [56].
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Nanobubbles and the cohesion-tension theory What are the consequences of nanobubbles for understanding water transport in plants? Stable nanobubbles in xylem under negative pressure add a new component to the cohesion-tension theory and the well-supported air-seeding hypothesis [4]. Recognition that small bubbles are safe from cavitation enables a new appreciation of plant water transport under negative pressure because the system may not be as vulnerable as previously thought. The theory therefore fits in well with recent findings that suggest that the prevalence of xylem embolisms may have been overestimated [8,9]. The hypothesis that bordered pits may function to confine cavitation events to the largely enclosed pit chambers is another aspect of the theory that offers a new explanation for why all xylem conduits have bordered pits [12]. While only flowering plants are considered here (Figure 1), it can be suggested that the nanobubbles hypothesis also applies to ferns, while it is unclear whether nanobubbles would be formed in conifers, where torusmargo pits possess much larger pores and a valve-sealing mechanism that may prevent nanobubble formation [81]. One implication of the nanobubble theory is that the largest pore in inter-vessel pit membranes may not necessarily be the sole determinant of the resistance of a particular vessel to embolism formation – the ‘rare pit’ hypothesis [82,83] – because not every nanobubble would create an embolism. Embolisms instead might form when nanobubble concentration exceeds a critical threshold combined with bubble expansion under declining liquid pressure. This would be most likely to occur in vessels with larger pit pores, as predicted by the rare pit hypothesis, and in agreement with experimental findings [83]. Any new theory to explain a natural phenomenon has to fit all known facts and explain, or at least not contradict, all known observations. Particular strengths of the nanobubble theory include that it supports the cohesion-tension theory and that it also creates a framework that can explain embolism repair under tension. This is a subject that requires a thorough theoretical treatment beyond the scope of this paper. Briefly, pressure-driven movement of nanobubbles from an embolism into a sap-filled conduit could be a far more efficient way to remove the air than diffusion, which is a far slower process [84,85]. Non-destructive observations of vessel refilling show that, even in the absence of sap flow, air can be completely removed from vessels within 30 minutes to a few hours [6,86–88]. The other aspect of vessel refilling that the nanobubble theory could help to explain is the process of hydraulic reconnection between the refilled and functioning conduit, because this would seemingly require simultaneous reconnection of every single pit pore to avoid new bubble formation [89,90]. Reconnection would normally occur once water has entered all pit apertures and reached the surface of all pit membranes within a refilling conduit. At this point, the bubbles remaining in the pit membrane after hydraulic reconnection would be nanobubbles that could be stable under negative pressure and eventually dissolve. We conclude that the nanobubble theory is in agreement not only with the cohesion-tension theory but also with recent findings regarding ionic effects on xylem conductance, the relatively low prevalence of embolisms under 5
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Opinion natural conditions, and the existence of embolism repair under tension. It also could explain the otherwise puzzling presence of surfactants in xylem sap, the fact that real pit membrane pores are far more vulnerable to air-seeding than theoretical cylindrical pores, the function of bordered pits, and the patterns of acoustic emissions in droughtstressed xylem. The theory obviously is in need of testing for the presence of stable nanobubbles in xylem sap and especially in bordered pit chambers, by chemical analysis of xylem sap surfactants, and by further studies of pit membrane bubble point pressures in relation to pore geometries and surfactants. Acknowledgments Research that contributed to this paper was funded by the National Science Foundation (IOS-0943502 and IOS-1146993). The authors thank Susana Espino, Philippe Marmottant, Olivier Vincent, Chuanhua Duan, Emily Cranston, James Kwan, Thomas Pesacreta, and five anonymous reviewers for comments on earlier drafts.
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