Cavitation and Its Discontents: Opportunities for Resolving Current Controversies  

Abstract

Cavitation has long been recognized as a key constraint on the structure and functional integrity of the xylem. Yet, recent results call into question how well we understand cavitation in plants. Here, we consider embolism formation in angiosperms at two scales. The first focuses on how air-seeding occurs at the level of pit membranes, raising the question of whether capillary failure is an appropriate physical model. The second addresses methodological uncertainties that affect our ability to infer the formation of embolism and its reversal in plant stems. Overall, our goal is to open up fresh perspectives on the structure-function relationships of xylem.A central question in the biology of vascular plants is under what conditions the continuity of the liquid phase, essential for the transport of water from soil to leaves, is lost (Tyree and Zimmerman, 2002). Without the highconductance pathway for water movement through the xylem, vascular plants could not sustain the water loss associated with the diffusional uptake of CO 2 from a subsaturated atmosphere. As a result, substantial effort in the field of xylem transport focuses on quantifying vulnerability to cavitation and its impact. Yet, a number of recent studies raise questions regarding how well we understand cavitation in plant stems, pointing to apparently anomalous or inconsistent experimental results that suggest methodological artifacts Ennajeh et al., 2011;Wheeler et al., 2013). Such results provide the motivation for this Update. We recognize that there is currently no consensus on the extent to which any particular experimental approach is subject to a problem; in addition, we note that the implications of such potential artifacts for the estimation of leaf xylem vulnerability involves further methodological considerations beyond our current scope. Our intention with this Update is to clarify the physical basis for a number of potential experimental artifacts relating to angiosperm stem xylem, in the hope that this will be useful for designing experiments that can resolve these issues.In this spirit, we begin with a discussion of how cavitation occurs, sketch an alternative model to meniscal failure for how air seeding across homogenous pit membranes could occur in the absence of discrete pores, and discuss the implications of these two models for the relative importance of probabilistic versus deterministic constraints on air-seeding resistance. We then turn to recent evidence that xylem vulnerability to cavitation in some species may have been overestimated and consider possible physical effects that could lead to biases sensitive to conduit size in the three principal methods of vulnerability estimation (dehydration, air injection, and centrifugation); to the extent that such biases are quantitatively important, these methods cannot be considered independent for long-vesseled species. Experimental approaches that may prove helpful in reconciling some of the divergent results between methods or protocols are proposed. The potential for measureme...

Xylem embolism refilling and resilience against drought‐induced mortality in woody plants: processes and trade‐offs

“…Validation and results from some of these newer techniques remain under debate (Rockwell et al 2014). High resolution imaging of xylem embolism has been enabled by cryogenic scanning electron microscopy for over a decade (cryo-SEM; Utsumi et al 1998), but this procedure laborious and not free of artefacts (Cochard et al 2000).…”

“…Destructive measurements of xylem hydraulics can potentially introduce a change to the native status of conduits, thus altering the object of study (Rockwell et al 2014). However, higher replication possibilities and lower equipment costs make these methods among the most accessible and used in different laboratories.…”

“…Trees can also repair the total conducting area following seasonal replacement through regrowth of new xylem (Brodersen and McElrone 2013;Nardini et al 2014). However, debate remains over how and when woody plants can refill embolized xylem conduits under residual negative water potential, so called ''novel refilling'' (Hacke and Sperry 2003;Brodersen and McElrone 2013) and which methods are appropriate for studying embolism formation and its reversal in plants (Rockwell et al 2014). The 'novel refilling' phenomenon is very controversial, and some researchers have argued that embolism refilling under any residual negative pressure in still functional xylem is unlikely or impossible due to thermodynamic constraints (Zwieniecki and Holbrook 2000;Rockwell et al 2014; but see also Gouin 2015).…”

“…However, debate remains over how and when woody plants can refill embolized xylem conduits under residual negative water potential, so called ''novel refilling'' (Hacke and Sperry 2003;Brodersen and McElrone 2013) and which methods are appropriate for studying embolism formation and its reversal in plants (Rockwell et al 2014). The 'novel refilling' phenomenon is very controversial, and some researchers have argued that embolism refilling under any residual negative pressure in still functional xylem is unlikely or impossible due to thermodynamic constraints (Zwieniecki and Holbrook 2000;Rockwell et al 2014; but see also Gouin 2015). Some researchers have also suggested that methodological uncertainties call for a thorough re-evaluation of current evidence for embolism reversal (Cochard and Delzon 2013;TorresRuiz et al 2015;Charrier et al 2016).…”

Acoustic Emissions to Measure Drought-Induced Cavitation in Plants

“…The phenomenon is called cavitation, which is the mechanical breakage of the continuous xylem water column and occurs when the tensile strength of the column is exceeded [25]. According to the current knowledge, the main cause of cavitation is the failure of a pit in the conduit wall to prevent gas from entering the conduit at strong tension [26], known as the air-seeding hypothesis [27]. Recently, Schenk et al [28] postulated that nanobubbles are snapped off during air-seeding.…”