TY - JOUR
AU - Cavender-Bares,, Jeannine
AB - Increased frequency in plant mortality associated with climate change-induced drought has been reported across the globe (Allen et al. 2010), and several studies have attempted to understand the precise mechanisms underlying drought vulnerability (e.g., Brodribb and Cochard 2009, McDowell 2011, Anderegg et al. 2012, Sevanto et al. 2014). One of the main physiological mechanisms by which drought causes tree mortality is hydraulic failure. Hydraulic failure occurs when water loss from transpiration exceeds water uptake by roots causing highly negative water potential in the xylem. Low water potentials can cause embolism through air-seeding that obstructs water transport in the xylem and can lead to plant death (McDowell et al. 2008). Hydraulic failure is most typically assessed via a percent loss of xylem conductivity (PLC)—or vulnerability—curve, showing the variation in the percentage of embolism as a function of xylem pressure potential. Despite the relative simplicity of the approach, there is still no consensus on the best method for measuring stem PLC in plants. In this issue of Tree Physiology, Pratt et al. (2020) present measurements of xylem vulnerability to cavitation of a native California oak species (Quercus douglasii) using three different methods. In doing so, they rigorously test for hypothesized artifacts and analyze discrepancies in the results of each approach. Their measurements span 1-, 2- and 3-year-old stems to capture ontogenetic changes in the structure and function of the xylem. Their work highlights a suite of anatomical attributes of oak xylem whose function remains poorly understood. Quercus douglasii is reported to be one of the most embolism-resistant species among the California oaks (Skelton et al. 2018, 2019), making it an important study system in which to address these questions. Many techniques for inducing cavitation (air injection, centrifugation, bench-dehydration) and measuring PLC (e.g., loss of hydraulic conductivity and counts of air-filled vessels) have been proposed over the years. Yet, the most widely used is the benchtop hydraulic method as proposed by Sperry et al. (1988). As pointed out by Pratt et al. (2020), this method has the advantage of directly measuring xylem hydraulic conductivity and accounts for the resistances of pit membranes and perforation plates. Yet, this method can be prone to artifacts that may arise during the induction of cavitation or measurement of PLC. These include air entry during branch cutting (e.g, Wheeler et al. 2013), the potential for flushing water through non-functional or open conduits—avoided by presenting raw hydraulic conductivity values—and possible difficulties in accurately quantifying maximum hydraulic conductivity following flushing (e.g., Choat et al. 2010, Cochard et al. 2013). A substantial advance in the last decade has been the use of imaging technology to visualize vessel contents. Two methods to measure PLC that have emerged in recent years are X-ray microtomography (micro-CT) (Fromm et al. 2001, Cochard et al. 2015) and optical techniques for tissue scanning (Brodribb et al. 2016, 2017). Using these methods, fully intact plants grown in containers can be examined, avoiding cutting and flushing artifacts. However, hydraulic conductivity and thus PLC, are not directly measured but instead calculated based on the vessel dimensions and/or the number of embolized vessels (Cochard et al. 2015, Brodribb et al. 2017). Percent loss of xylem conductivity measurements can be very informative in assessing plant vulnerability and response to drought, especially when linked with minimum xylem water potential measurements under field conditions (Choat et al. 2012). Previous studies have shown that xylem water potentials measured in the field may be more negative than minimum values from vulnerability curves using centrifugation, indicating that oak trees maintain transpiration under lower xylem water potential than indicated by the curves at total loss of conductivity (e.g., Cavender-Bares and Holbrook 2001). Reconciling P50 (50% loss of hydraulic conductivity) values generated by different methods with field observation is thus an important step to understand whether plants are operating close to water potentials that cause complete loss of hydraulic capacity (Bucci et al. 2016). Many oak species are known for having relatively long xylem vessels and ring-porous wood (e.g., Cochard and Tyree 1990, Jacobsen et al. 2007, Robert et al. 2017), and a substantial debate surrounds the capacity of these species to resist embolism. The long vessels make assessing vulnerability difficult, given that terminal vessel elements that likely play a central role in embolism resistance may be largely missing in cut stems (Jacobsen et al. 2007, 2014, Sperry et al. 2012, Martin-StPaul et al. 2014, Skelton et al. 2018). The mechanisms that maintain drought resistance of wood in oaks and contribute to variation in their drought tolerance have thus been tricky to study and to firmly establish. Furthermore, the discrepancy between the results has been argued to be a consequence of the specific method used (Sperry et al. 2012, Cochard et al. 2013), but the debate is far from closed. Pratt et al. (2020) report discrepancies in estimates of stem PLC of up to 3.22 MPa in P50 for the same species using micro-CT, optical and hydraulic methods. The study does not use the centrifugation method, presumably due to uncertainties about its use on short stems to estimate xylem vulnerability of long-vesseled species (Cavender-Bares and Holbrook 2001). Pratt et al. (2020) found the largest difference in P50 between the hydraulic and micro-CT method. The P50 value generated by the optical technique was not significantly different from the value produced using micro-CT. It is worth noting that Pratt et al. (2020) used a variation of the original optical method proposed by Brodribb et al. (2017). They quantified PLC as the number of embolized vessels in a given image out of the total number of embolized vessels by the end of the drydown period, rather than as the number of embolized pixels per image out of the total number of embolized pixels. The impact of this variation in protocol is unknown, yet their P50 for 1-year-old stems was not significantly different from what was reported for the same species in other studies (Skelton et al. 2018, 2019). Furthermore, Pratt et al. (2020) found that 1-year-old branches were generally more embolism resistant than older stems. Even though other studies have reported distal tissues to be more vulnerable to xylem embolism than basal organs (e.g., in Acer saccharum, Choat et al. 2005), their finding is consistent with the hypothesis that in Q. douglasii distal stems, which experience more negative water potentials, are more resistant to cavitation (e.g., Melcher et al. 2003, Johnson et al. 2016). Optical methods as applied to stems by Skelton et al. (2018, 2019) capture the most recent growth but do not detect processes in wood at different ontogenetic stages, across which vessel structure can shift markedly (Figure 1). Different methods of xylem analysis may, in effect, lead to studying different parts of the ‘elephant’. The analogy refers to the parable of The Blind Men and the Elephant in which the protagonists examine different parts of an elephant, each conceptualizing it based on the incomplete information before them. Limits of detection are such that the whole elephant can only be deciphered from integration of different viewpoints—and filling in the gaps with new information. An integrated understanding of how oaks respond to drought likely involves continued careful use of multiple approaches and advancing technology. Figure 1. Open in new tabDownload slide (A) Stylized diagram of a branch showing segments of different ontogenetic stages. Numbers and lines represent, respectively, cambial age and annual growth rings produced in successive conical layers. (B) A cross-section of a 1-year-old stem showing the pith surrounded by diffuse-porous rings and (C) a 3-year-old stem showing the transition between diffuse to ring-porous wood often seen with progression of ontogenetic stages in oak species. Only vessels are shown. The numbers indicate the year of cambial growth from the earliest age (1) to the most recent growth year (3). For simplicity, only part of the stem section is detailed in (C). (D) Tangential diagram showing vessel elements, perforation plates, pits that connect neighboring conduits, vasicentric tracheids (dark gray; pits are only shown on some for simplicity), fibers, axial parenchyma and uniseriate ray parenchyma. The flow of water through connecting vessels and vessel elements is shown with blue solid arrows; and the hypothesized flow of water between vessels and vasicentric tracheids is shown with red dashed arrows. Multi-seriate rays are not shown. Figure 1. Open in new tabDownload slide (A) Stylized diagram of a branch showing segments of different ontogenetic stages. Numbers and lines represent, respectively, cambial age and annual growth rings produced in successive conical layers. (B) A cross-section of a 1-year-old stem showing the pith surrounded by diffuse-porous rings and (C) a 3-year-old stem showing the transition between diffuse to ring-porous wood often seen with progression of ontogenetic stages in oak species. Only vessels are shown. The numbers indicate the year of cambial growth from the earliest age (1) to the most recent growth year (3). For simplicity, only part of the stem section is detailed in (C). (D) Tangential diagram showing vessel elements, perforation plates, pits that connect neighboring conduits, vasicentric tracheids (dark gray; pits are only shown on some for simplicity), fibers, axial parenchyma and uniseriate ray parenchyma. The flow of water through connecting vessels and vessel elements is shown with blue solid arrows; and the hypothesized flow of water between vessels and vasicentric tracheids is shown with red dashed arrows. Multi-seriate rays are not shown. A critical point raised by Pratt et al. (2020) and also documented in other studies (e.g., Rodriguez-Zaccaro et al. 2019) is the delayed onset of ring-porosity in oaks. By analyzing stems of different ages, they show that 1-year-old branches are mainly diffuse-porous, and that ring-porosity only develops in later years (illustrated in Figure 1). Given that ring-porous wood in oaks tends to have higher hydraulic conductivity and to be more vulnerable to cavitation than diffuse-porous wood (Robert et al. 2017, Rodriguez-Zaccaro et al. 2019), different ontogenetic stages of wood are likely to differ in their vulnerability to drought. The ontogenetic stage at which ring-porosity develops may actually be an important characteristic of oak species that influences their water regulation. Another interesting and yet poorly explored anatomical characteristic of oaks is the presence of vasicentric tracheids (Carlquist 1985). Tracheids in oaks are tiny and inefficient for water transport relative to vessels. However, vasicentric tracheids are hypothesized to connect vessels laterally and potentially to allow sapflow between conduits from different growth rings, maintaining a minimal conductive stream when vessels are embolized (Figure 1D; Ewers et al. 2015, Pan and Tyree 2019). As Pratt et al. (2015, 2020) have previously documented, these tracheids may provide sufficient water to support transpiration during dry periods, playing a key role in the drought tolerance of oaks. This anatomical characteristic is not unique to oaks and has been reported for other dry-habitat species (Carlquist 1985, Ewers et al. 2015, Pratt et al. 2015), as well as species that have vulnerable hydraulic systems like lianas (Ewers et al. 2015), suggesting that vasicentric tracheids can be an important trait that allows plants to survive during drought conditions. These poorly explored anatomic characteristics of oaks highlight the importance of using ecohydrological approaches to understand oak species distributions and predict their response to changes in climate. Careful examination of ‘the elephant’ from many dimensions integrating approaches that capture wood development over time and at different ontogenetic stages will be critical to reconciling contrasting views of the aspects of wood that are most critical to the variation in drought tolerance in oaks. The oaks, which are highly diverse and dominate North American forests occupying a wide range of ecological habitats (Cavender-Bares 2019), are subject to climate change. The fate of northern temperate forests will be heavily influenced by how oaks respond to changing precipitation and thermal regimes. Understanding the various mechanisms by which oaks are able to maintain function during drought is critical to understanding and managing forests on our warming planet. Acknowledgments We thank Anna Jacobsen, Brandon Pratt, Robert Skelton, David Ackerly, Rachel Spicer and Maurizio Mencuccini for generously sharing their knowledge and showing us details of the methods they used and/or for comments on the manuscript and/or figure. References Allen CD , Macalady AK , Chenchouni H et al. ( 2010 ) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests . For Ecol Manage 259 : 660 – 684 . Google Scholar Crossref Search ADS WorldCat Anderegg WRL , Berry JA , Smith DD , Sperry JS , Anderegg LDL , Field CB ( 2012 ) The roles of hydraulic and carbon stress in a widespread climate-induced forest die-off . Proc Natl Acad Sci USA 109 : 233 – 237 . Google Scholar Crossref Search ADS PubMed WorldCat Brodribb TJ , Cochard H ( 2009 ) Hydraulic failure defines the recovery and point of death in water-stressed conifers . Plant Physiol 149 : 575 – 584 . Google Scholar Crossref Search ADS PubMed WorldCat Brodribb TJ , Skelton RP , McAdam SAM , Bienaimé D , Lucani CJ , Marmottant P ( 2016 ) Visual quantification of embolism reveals leaf vulnerability to hydraulic failure . New Phytol 209 : 1403 – 1409 . Google Scholar Crossref Search ADS PubMed WorldCat Brodribb TJ , Carriqui M , Delzon S , Lucani C ( 2017 ) Optical measurement of stem xylem vulnerability . Plant Physiol 174 : 2054 – 2061 . Google Scholar Crossref Search ADS PubMed WorldCat Bucci SJ , Goldstein G , Scholz FG , Meinzer FC ( 2016 ) Physiological significance of hydraulic segmentation, nocturnal transpiration and capacitance in tropical trees: Paradigms revisited. In: Goldstein G., Santiago L. (eds) Tropical tree physiology, vol. 6 . Springer , Cham , pp 205 – 225 . Google Scholar Crossref Search ADS Google Scholar Google Preview WorldCat COPAC Carlquist S ( 1985 ) Vasicentric tracheids as a drought survival mechanism in the woody flora of southern California and similar regions; review of vasicentric tracheids . Aliso 11 : 37 – 68 . OpenURL Placeholder Text WorldCat Cavender-Bares J ( 2019 ) Diversification, adaptation, and community assembly of the American oaks (Quercus), a model clade for integrating ecology and evolution . New Phytol 221 : 669 – 692 . Google Scholar Crossref Search ADS PubMed WorldCat Cavender-Bares J , Holbrook NM ( 2001 ) Hydraulic properties and freezing-induced cavitation in sympatric evergreen and deciduous oaks with contrasting habitats . Plant Cell Environ 24 : 1243 – 1256 . Google Scholar Crossref Search ADS WorldCat Choat B , Drayton WM , Brodersen C , Matthews MA , Shackel KA , Wada H , McElrone AJ ( 2010 ) Measurement of vulnerability to water stress-induced cavitation in grapevine: a comparison of four techniques applied to a long-vesseled species . Plant Cell Environ 33 : 1502 – 1512 . Google Scholar PubMed OpenURL Placeholder Text WorldCat Choat B , Jansen S , Brodribb TJ et al. ( 2012 ) Global convergence in the vulnerability of forests to drought . Nature 491 : 752 – 755 . Google Scholar Crossref Search ADS PubMed WorldCat Choat B , Lahr EC , Melcher PJ , Zwieniecki MA , Holbrook NM ( 2005 ) The spatial pattern of air seeding thresholds in mature sugar maple trees . Plant Cell Environ 28 : 1082 – 1089 . Google Scholar Crossref Search ADS WorldCat Cochard H , Badel E , Herbette S , Delzon S , Choat B , Jansen S ( 2013 ) Methods for measuring plant vulnerability to cavitation: a critical review . J Exp Bot 64 : 4779 – 4791 . Google Scholar Crossref Search ADS PubMed WorldCat Cochard H , Tyree MT ( 1990 ) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism . Tree Physiol 6 : 393 – 407 . Google Scholar Crossref Search ADS PubMed WorldCat Cochard H , Delzon S , Badel E ( 2015 ) X-ray microtomography (micro-CT): a reference technology for high-resolution quantification of xylem embolism in trees . Plant Cell Environ 38 : 201 – 206 . Google Scholar Crossref Search ADS PubMed WorldCat Ewers FW , Rosell JA , Olson ME ( 2015 ) Lianas as structural parasites. In: Hacke U. (eds) Functional and ecological xylem anatomy . Springer , Cham , pp 163 – 188 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Fromm JH , Sautter I , Matthies D , Kremer J , Schumacher P , Ganter C ( 2001 ) Xylem water content and wood density in spruce and oak trees detected by high-resolution computed tomography . Plant Physiol 127 : 416 – 425 . Google Scholar Crossref Search ADS PubMed WorldCat Jacobsen AL , Pratt RB , Ewers FW , Davis SD ( 2007 ) Cavitation resistance among 26 chaparral species of Southern California . Ecol Monogr 77 : 99 – 115 . Google Scholar Crossref Search ADS WorldCat Jacobsen AL , Pratt RB , Davis SD , Tobin MF ( 2014 ) Geographic and seasonal variation in chaparral vulnerability to cavitation . Madroño 61 : 317 – 328 . Google Scholar Crossref Search ADS WorldCat Johnson DM , Wortemann R , McCulloh KA , Jordan-Meille L , Ward E , Warren JM , Palmroth S , Domec J-C ( 2016 ) A test of the hydraulic vulnerability segmentation hypothesis in angiosperm and conifer tree species . Tree Physiol 36 : 983 – 993 . Google Scholar Crossref Search ADS PubMed WorldCat Martin-StPaul NK , Longepierre D , Huc R , Delzon S , Burlett R , Joffre R , Rambal S , Cochard H ( 2014 ) How reliable are methods to assess xylem vulnerability to cavitation? The issue of ‘open vessel’artifact in oaks . Tree Physiol 34 : 894 – 905 . Google Scholar Crossref Search ADS PubMed WorldCat McDowell N , Pockman WT , Allen CD et al. ( 2008 ) Mechanisms of plant survival and mortality during drought: why do some plants survive while others succumb to drought? New Phytol 178 : 719 – 739 . Google Scholar Crossref Search ADS PubMed WorldCat McDowell NG ( 2011 ) Mechanisms linking drought, hydraulics, carbon metabolism, and vegetation mortality . Plant Physiol 155 : 1051 – 1059 . Google Scholar Crossref Search ADS PubMed WorldCat Melcher PJ , Zwieniecki MA , Holbrook NM ( 2003 ) Vulnerability of xylem vessels to cavitation in sugar maple. Scaling from individual vessels to whole branches . Plant Physiol 131 : 1775 – 1780 . Google Scholar Crossref Search ADS PubMed WorldCat Pan R , Tyree MT ( 2019 ) How does water flow from vessel to vessel? Further investigation of the tracheid bridge concept . Tree Physiol . OpenURL Placeholder Text WorldCat Pratt RB , Percolla MI , Jacobsen AL ( 2015 ) Integrative xylem analysis of chaparral shrubs. In: Hacke U. (eds) Functional and ecological xylem anatomy . Springer , Cham , pp 189 – 207 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Pratt RB , Castro V , Fickle J , Jacobsen A ( 2020 ) Embolism resistance of different aged stems of a California oak species (Quercus douglasii): optical and microCT methods differ from the benchtop-dehydration standard . Tree Physiol , 40 : 5 – 18 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Robert EMR , Mencuccini M , Martínez-Vilalta J ( 2017 ) The anatomy and functioning of the xylem in oaks. In: Gil-Pelegrín E, Peguero-Pina J, Sancho-Knapik D. (eds) Oaks physiological ecology. exploring the functional diversity of genus Quercus L. Tree Physiology, vol 7 . Springer , Cham , pp 261 – 302 . Google Scholar Google Preview OpenURL Placeholder Text WorldCat COPAC Rodriguez-Zaccaro FD , Valdovinos-Ayala J , Percolla MI , Venturas MD , Pratt RB , Jacobsen AL ( 2019 ) Wood structure and function change with maturity: age of the vascular cambium is associated with xylem changes in current-year growth . Plant Cell Environ 42 : 1816 – 1831 . Google Scholar Crossref Search ADS PubMed WorldCat Sevanto S , McDowell NG , Dickman LT , Pangle R , Pockman WT ( 2014 ) How do trees die? A test of the hydraulic failure and carbon starvation hypotheses . Plant Cell Environ 37 : 153 – 161 . Google Scholar Crossref Search ADS PubMed WorldCat Skelton RP , Dawson TE , Thompson SE , Shen Y , Weitz AP , Ackerly D ( 2018 ) Low vulnerability to xylem embolism in leaves and stems of north American oaks . Plant Physiol 177 : 1066 – 1077 . Google Scholar Crossref Search ADS PubMed WorldCat Skelton RP , Anderegg LDL , Papper P , Reich E , Dawson TE , Kling M , Thompson SE , Diaz J , Ackerly DD ( 2019 ) No local adaptation in leaf or stem xylem vulnerability to embolism, but consistent vulnerability segmentation in a north American oak . New Phytol 223 : 1296 – 1306 . Google Scholar Crossref Search ADS PubMed WorldCat Sperry J , Donnelly J , Tyree M ( 1988 ) A method for measuring hydraulic conductivity and embolism in xylem . Plant Cell Environ 11 : 35 – 40 . Google Scholar Crossref Search ADS WorldCat Sperry JS , Christman MA , Torres-Ruiz JM , Taneda H , Smith DD ( 2012 ) Vulnerability curves by centrifugation: is there an open vessel artefact, and are ‘r’ shaped curves necessarily invalid? Plant Cell Environ 35 : 601 – 610 . Google Scholar Crossref Search ADS PubMed WorldCat Wheeler JK , Huggett BA , Tofte AN , Rockwell FE , Holbrook NM ( 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 . Google Scholar PubMed OpenURL Placeholder Text WorldCat © The Author(s) 2020. Published by Oxford University Press. All rights reserved. For permissions, please e-mail: journals.permission@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Toward an integrated view of the ‘elephant’: unlocking the mysteries of water transport and xylem vulnerability in oaks
JF - Tree Physiology
DO - 10.1093/treephys/tpz116
DA - 2020-01-01
UR - https://www.deepdyve.com/lp/oxford-university-press/toward-an-integrated-view-of-the-elephant-unlocking-the-mysteries-of-S5cX1oKzRC
SP - 1
VL - 40
IS - 1
DP - DeepDyve
ER -