In Situ Visualization of the Dynamics in Xylem Embolism Formation and Removal in the Absence of Root Pressure: A Study on Excised Grapevine Stems

Knipfer, Thorsten; Cuneo, Italo F.; Brodersen, Craig R.; McElrone, Andrew J.

doi:10.1104/pp.16.00136

Cited by 88 publications

(88 citation statements)

References 53 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…This result implies that the lumen surface is neither completely hydrophilic (i.e., zero contact angle) nor completely hydrophobic (contact angle >90°). Previous observation of contact angles between water and lumen surfaces of xylem conduits range from 40 to 90° with the most commonly observed values between 40 and 55° (Schneider et al, 2000;Zwieniecki and Holbrook, 2000;van Ieperen et al, 2001;Brodersen et al, 2010;Kim and Lee, 2010;Lee et al, 2013;McCully et al, 2014;Knipfer et al, 2016). Purified lignin has a contact angle somewhere between 46 and 56° (Notley and Norgren, 2010).…”

Section: Possible Functional Implications Of the Findingsmentioning

confidence: 98%

“…In recent years, a growing number of studies have found that xylem surfaces tend to be somewhere between hydrophilic and hydrophobic, with observed aqueous contact angles ranging from about 40° to a little more than 90° (Schneider et al, 2000;Zwieniecki and Holbrook, 2000;van Ieperen et al, 2001;Shen et al, 2008;Kohonen and Helland, 2009;Brodersen et al, 2010;Kim and Lee, 2010;Lee et al, 2013;McCully et al, 2014;Knipfer et al, 2016), where a contact angle of 0° denotes a completely hydrophilic surface and contact angles above 90° a hydrophobic one. Other recent studies have shown that xylem surfaces, at least in angiosperms, feature a complex spatial arrangement of surfaces with hydrophilic and hydrophobic properties (McCully et al, 2014;Schenk et al, 2017), including coatings consisting at least in part of amphiphilic lipids (Schenk et al, 2017).…”

Section: Invited Special Articlementioning

confidence: 99%

“…Purified lignin has a contact angle somewhere between 46 and 56° (Notley and Norgren, 2010). Some have reported a pronounced variability of wetting angles either spatially or depending on whether the water was advancing on the surface or receding (Brodersen et al, 2010;Kim and Lee, 2010;Lee et al, 2013;McCully et al, 2014;Knipfer et al, 2016), which may have been caused by the presence of surfactants on the lumen surfaces (McCully et al, 2014). Contact angles matter for xylem refilling after embolism (Zwieniecki and Holbrook, 2000;Rolland et al, 2015), but in functional xylem, contact angle also affects heterogeneous gas bubble nucleation on surfaces (Schenk et al, 2017).…”

Section: Possible Functional Implications Of the Findingsmentioning

confidence: 99%

See 2 more Smart Citations

From the sap's perspective: The nature of vessel surfaces in angiosperm xylem

Schenk

Espino

Rich‐Cavazos

et al. 2018

American J of Botany

View full text Add to dashboard Cite

Plant xylem is a unique evolutionary invention: It functions as a negative pressure hydraulic system that can move vast quantities of water and solutes over distances longer than 100 m. No other kind of organism transports liquids under negative pressure, and the most successful attempts to build an artificial negative pressure hydraulic system succeeded only to move a small amount of water over a few centimeters in a single microchannel (Wheeler and Stroock, 2008). That experiment proved that it is possible to move water under negative pressure, but it left the question unanswered how plants can do this so effectively and over such long distances. Somehow plants manage to move large volumes of water in heterogeneous channels that range in diameter from nanometers to a few hundred micrometers, that is, in nanofluidic and microfluidic systems where water moves very close to surfaces of other phases, both solid and gas (Eijkel and van den Berg, 2005;Squires and Quake, 2005). Plants move all this water efficiently along these phase surfaces without constantly creating gas bubbles in the system . What do we actually know about these surfaces in xylem conduits (i.e., vessels and tracheids)? INVITED SPECIAL ARTICLE PREMISE OF THE STUDY:Xylem sap in angiosperms moves under negative pressure in conduits and cell wall pores that are nanometers to micrometers in diameter, so sap is always very close to surfaces. Surfaces matter for water transport because hydrophobic ones favor nucleation of bubbles, and surface chemistry can have strong effects on flow. Vessel walls contain cellulose, hemicellulose, lignin, pectins, proteins, and possibly lipids, but what is the nature of the inner, lumen-facing surface that is in contact with sap?METHODS: Vessel lumen surfaces of five angiosperms from different lineages were examined via transmission electron microscopy and confocal and fluorescence microscopy, using fluorophores and autofluorescence to detect cell wall components. Elemental composition was studied by energy-dispersive X-ray spectroscopy, and treatments with phospholipase C (PLC) were used to test for phospholipids.KEY RESULTS: Vessel surfaces consisted mainly of lignin, with strong cellulose signals confined to pit membranes. Proteins were found mainly in inter-vessel pits and pectins only on outer rims of pit membranes and in vessel-parenchyma pits. Continuous layers of lipids were detected on most vessel surfaces and on most pit membranes and were shown by PLC treatment to consist at least partly of phospholipids. CONCLUSIONS:Vessel surfaces appear to be wettable because lignin is not strongly hydrophobic and a coating with amphiphilic lipids would render any surface hydrophilic. New questions arise about these lipids and their possible origins from living xylem cells, especially about their effects on surface tension, surface bubble nucleation, and pit membrane function.

show abstract

Section: Possible Functional Implications Of the Findingsmentioning

confidence: 98%

Section: Invited Special Articlementioning

confidence: 99%

Section: Possible Functional Implications Of the Findingsmentioning

confidence: 99%

See 1 more Smart Citation

From the sap's perspective: The nature of vessel surfaces in angiosperm xylem

Schenk

Espino

Rich‐Cavazos

et al. 2018

American J of Botany

View full text Add to dashboard Cite

show abstract

“…However, cavitation reversal, when it occurs at all, requires that xylem water potentials relax to at least a few bars below zero over a time scale of hours (Hochberg et al, 2016;Knipfer et al, 2016), conditions that may not be met diurnally. Reversible collapse would be as effective as cavitation in increasing the gain of an abscisic acid (ABA) signal mediated by mesophyll turgor (or cell volume) during a transient increase in E (Zabadal, 1974;Pierce and Raschke, 1980;McAdam and Brodribb, 2016), even as it protected upstream xylem.…”

Section: Sensitivity Of the Modelmentioning

confidence: 99%

Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation

et al. 2016

View full text Add to dashboard Cite

We report a novel form of xylem dysfunction in angiosperms: reversible collapse of the xylem conduits of the smallest vein orders that demarcate and intrusively irrigate the areoles of red oak (Quercus rubra) leaves. Cryo-scanning electron microscopy revealed gradual increases in collapse from approximately 22 MPa down to 23 MPa, saturating thereafter (to 24 MPa). Over this range, cavitation remained negligible in these veins. Imaging of rehydration experiments showed spatially variable recovery from collapse within 20 s and complete recovery after 2 min. More broadly, the patterns of deformation induced by desiccation in both mesophyll and xylem suggest that cell wall collapse is unlikely to depend solely on individual wall properties, as mechanical constraints imposed by neighbors appear to be important. From the perspective of equilibrium leaf water potentials, petioles, whose vessels extend into the major veins, showed a vulnerability to cavitation that overlapped in the water potential domain with both minor vein collapse and buckling (turgor loss) of the living cells. However, models of transpiration transients showed that minor vein collapse and mesophyll capacitance could effectively buffer major veins from cavitation over time scales relevant to the rectification of stomatal wrong-way responses. We suggest that, for angiosperms, whose subsidiary cells give up large volumes to allow large stomatal apertures at the cost of potentially large wrong-way responses, vein collapse could make an important contribution to these plants' ability to transpire near the brink of cavitation-inducing water potentials.Terrestrial photosynthesis is inextricably linked with water loss. Plants expose hydrated cells to the atmosphere to obtain CO 2 , with evaporation an inevitable consequence. Vascular plants meet this challenge by replacing water lost via transpiration with water pulled from the soil. What allows this is the xylem: a system of stiff-walled conduits capable of remaining water filled at negative pressures low enough to extract water from micrometer-to nanometer-scale soil capillaries and to drive flow through the 10-to 100-mm-diameter xylem conduits that extend from the roots to the leaves (Tyree and Zimmermann, 2002). To deliver water at rates equal to transpiration, the pressure in the xylem must fall far below the vapor pressure of water, such that water transport through the xylem occurs in a metastable state (i.e. at kinetic, but not thermodynamic, equilibrium) and thus at risk of cavitation (Stroock et al., 2014). How many plants seemingly operate with little to no safety margin against cavitation Brodribb and Holbrook, 2004;Meinzer et al., 2009;Choat et al., 2012) remains an important and unsolved question.Cavitation occurs when metastable liquid water is replaced by water vapor due to the expansion of a gas bubble nucleus, forming an embolism or air blockage: embolism disrupts water transport because tensions cannot be transmitted through gas. The most probable origin of such nuclei is thought to be g...

show abstract

“…Living cells are required for making new wood (in this issue : Jacobsen et al, 2018;Johnson et al, 2018), but they also play important roles in maintaining and repairing the water transport system by refilling embolized conduits (Knipfer et al, 2016) and possibly by ionic control of hydraulic conductance through wood (Nardini et al, 2011). Both these functions in angiosperms are provided by living cells that are in contact with vessels, sometimes surrounding them completely.…”

mentioning

confidence: 99%

Wood: Biology of a living tissue

Schenk

2018

American J of Botany

View full text Add to dashboard Cite

In Situ Visualization of the Dynamics in Xylem Embolism Formation and Removal in the Absence of Root Pressure: A Study on Excised Grapevine Stems

Cited by 88 publications

References 53 publications

From the sap's perspective: The nature of vessel surfaces in angiosperm xylem

From the sap's perspective: The nature of vessel surfaces in angiosperm xylem

Reversible Leaf Xylem Collapse: A Potential “Circuit Breaker” against Cavitation

Wood: Biology of a living tissue

Contact Info

Product

Resources

About