Abstract
Key message
A high-risk hydraulic strategy might be linked to embolism recovery in Eucalyptus hybrids, allowing plants to have high hydraulic conductivity regardless of safety.
Abstract
Plants use a variety of strategies to mitigate or reduce drought-induced hydraulic failure. Recovery of hydraulic conductivity after drought stress can be an important mechanism used to avoid drought-induced mortality; however, the underlying mechanism of hydraulic recovery is still poorly understood. We examined the hydraulic recovery response between E. grandis × camaldulensis (GC) and E. urophylla × grandis (GU) after drought. We aimed to determine if there is a trade-off between xylem safety and hydraulic recovery and what the underlying mechanism might be. Destructive measurements together with X-ray microtomography measurements were used to determine the extent of hydraulic recovery at various time intervals. We found two distinct hydraulic strategies used by plants. GC was more resistant to embolism formation as compared to UG; however, GC showed lower levels of hydraulic recovery after rewatering. Larger vessel sizes were related to increases in drought vulnerability. Hydraulic recovery was also related to functional traits of cells surrounding vessels, highlighting the possible role that these cells play to increase hydraulic conductance in the xylem and increasing connectivity between vessels. Our study suggest that hydraulic recovery can be an important hydraulic strategy used by Eucalyptus hybrids in response to drought. A high-risk hydraulic strategy might be linked to embolism recovery, allowing plants to have high hydraulic resistance regardless of safety.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Allen CD, Breshears DD, McDowell NG (2015) On underestimation of global vulnerability to tree mortality and forest die-off from hotter drought in the Anthropocene. Ecosphere 6:art129. https://doi.org/10.1890/ES15-00203.1
Anderegg WRL, Plavcová L, Anderegg LDL et al (2013) Drought’s legacy: Multiyear hydraulic deterioration underlies widespread aspen forest die-off and portends increased future risk. Glob Chang Biol 19:1188–1196. https://doi.org/10.1111/gcb.12100
Anderegg WRL, Hicke JA, Fisher RA et al (2015) Tree mortality from drought, insects, and their interactions in a changing climate. New Phytol 208:674–683. https://doi.org/10.1111/nph.13477
Barotto AJ, Fernandez ME, Gyenge J et al (2016) First insights into the functional role of vasicentric tracheids and parenchyma in eucalyptus species with solitary vessels: do they contribute to xylem efficiency or safety? Tree Physiol 36:1485–1497. https://doi.org/10.1093/treephys/tpw072
Barotto AJ, Monteoliva S, Gyenge J et al (2018) Functional relationships between wood structure and vulnerability to xylem cavitation in races of Eucalyptus globulus differing in wood density. Tree Physiol 38:243–251. https://doi.org/10.1093/treephys/tpx138
Becker P, Gribben RJ, Lim C (2000) Tapered conduits can buffer hydraulic conductance from path-lenght effects. Tree Physiol 20:965–967. https://doi.org/10.1093/treephys/20.14.965
Bonan GB (2008) Forests and climate change: forcings, feedbacks, and the climate benefits of forests. Science (80-) 320:1444–1449. https://doi.org/10.1126/science.1155121
Bourne AE, Creek D, Peters JMR et al (2017) Species climate range influences hydraulic and stomatal traits in Eucalyptus species. Ann Bot 120:123–133. https://doi.org/10.1093/aob/mcx020
Brodersen CR, McElrone AJ (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00108
Brodersen CR, McElrone AJ, Choat B et al (2010) The dynamics of embolism repair in xylem: In vivo visualizations using high-resolution computed tomography. Plant Physiol 154:1088–1095. https://doi.org/10.1104/pp.110.162396
Brodersen CR, Knipfer T, McElrone AJ (2018) In vivo visualization of the final stages of xylem vessel refilling in grapevine (Vitis vinifera) stems. New Phytol 217:117–126. https://doi.org/10.1111/nph.14811
Charrier G, Torres-Ruiz JM, Badel E et al (2016) Evidence for hydraulic vulnerability segmentation and lack of xylem refilling under tension. Plant Physiol 172:1657–1668. https://doi.org/10.1104/pp.16.01079
Choat B, Brodersen CR, Mcelrone AJ (2015) Synchrotron X-ray microtomography of xylem embolism in Sequoia sempervirens saplings during cycles of drought and recovery. New Phytol 205:1095–1105. https://doi.org/10.1111/nph.13110
Choat B, Badel E, Burlett R et al (2016) Noninvasive measurement of vulnerability to drought-induced embolism by X-Ray microtomography. Plant Physiol 170:273–282. https://doi.org/10.1104/pp.15.00732
Choat B, Nolf M, Lopez R et al (2018) Non-invasive imaging shows no evidence of embolism repair after drought in tree species of two genera. Tree Physiol 39:113–121. https://doi.org/10.1093/treephys/tpy093
Cochard H, Bodet C, Améglio T, Cruiziat P (2000) Cryo-scanning electron microscopy observations of vessel content during transpiration in walnut petioles. Facts or artifacts. Plant Physiol 124:1191–1202. https://doi.org/10.1104/pp.124.3.1191
Cochard H, Lemoine D, Ameglio T, Granier A (2001) Mechanisms of xylem recovery from winter embolism in Fagus sylvatica. Tree Physiol 21:27–33. https://doi.org/10.1093/treephys/21.1.27
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. https://doi.org/10.1111/pce.12391
Drew DM, Downes GM, Grzeskowiak V, Naidoo T (2009) Differences in daily stem size variation and growth in two hybrid eucalypt clones. Trees Struct Funct 23:585–595. https://doi.org/10.1007/s00468-008-0303-y
du Plessis A, le Roux SG, Guelpa A (2016) The CT scanner facility at stellenbosch university: an open access X-ray computed tomography laboratory. Nucl Instruments Methods Phys Res 384:42–49. https://doi.org/10.1016/j.nimb.2016.08.005
Duursma RA, Blackman CJ, Lopéz R et al (2019) On the minimum leaf conductance: its role in models of plant water use, and ecological and environmental controls. New Phytol 221:693–705. https://doi.org/10.1111/nph.15395
Fatichi S, Pappas C, Zscheischler J, Leuzinger S (2019) Modelling carbon sources and sinks in terrestrial vegetation. New Phytol 221:652–668. https://doi.org/10.1111/nph.15451
Fernández ME, Barotto AJ, Martínez Meier A et al (2019) New insights into wood anatomy and function relationships: how Eucalyptus challenges what we already know. For Ecol Manage. https://doi.org/10.1016/j.foreco.2019.117638
Gleason SM, Westoby M, Jansen S et al (2016) Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world’s woody plant species. New Phytol 209:123–136. https://doi.org/10.1111/nph.13646
Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311. https://doi.org/10.1046/j.1365-3040.2003.00962.x
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701. https://doi.org/10.1093/treephys/26.6.689
Hammond WM, Yu K, Wilson LA et al (2019) Dead or dying? Quantifying the point of no return from hydraulic failure in drought-induced tree mortality. New Phytol 223:1834–1843. https://doi.org/10.1111/nph.15922
Kim HK, Lee SJ (2010) Synchrotron X-ray imaging for nondestructive monitoring of sap flow dynamics through xylem vessel elements in rice leaves. New Phytol 188:1085–1098. https://doi.org/10.1111/j.1469-8137.2010.03424.x
Klein T, Cohen S, Yakir D (2011) Hydraulic adjustments underlying drought resistance of Pinus halepensis. Tree Physiol 31:637–648. https://doi.org/10.1093/treephys/tpr047
Klein T, Zeppel MJB, Anderegg WRL et al (2018) Xylem embolism refilling and resilience against drought-induced mortality in woody plants: processes and trade-offs. Ecol Res 33:839–855. https://doi.org/10.1007/s11284-018-1588-y
Knipfer T, Cuneo IF, Brodersen CR, McElrone AJ (2016) In situ visualization of the dynamics in xylem embolism formation and removal in the absence of root pressure: a study on excised grapevine stems. Plant Physiol 171:1024–1036. https://doi.org/10.1104/pp.16.00136
Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press Limited, San Diego
Lamarque LJ, Corso D, Torres-Ruiz JM et al (2018) An inconvenient truth about xylem resistance to embolism in the model species for refilling Laurus nobilis L. Ann for Sci. https://doi.org/10.1007/s13595-018-0768-9
Lens F, Sperry JS, Christman MA et al (2011) Testing hypotheses that link wood anatomy to cavitation resistance and hydraulic conductivity in the genus Acer. New Phytol 190:709–723. https://doi.org/10.1111/j.1469-8137.2010.03518.x
Liu J, Gu L, Yu Y et al (2019) Corticular photosynthesis drives bark water uptake to refill embolized vessels in dehydrated branches of Salix matsudana. Plant Cell Environ 42:2584–2596. https://doi.org/10.1111/pce.13578
Lobo A, Torres-Ruiz JM, Burlett R et al (2018) Assessing inter- and intraspecific variability of xylem vulnerability to embolism in oaks. For Ecol Manage 424:53–61. https://doi.org/10.1016/j.foreco.2018.04.031
Loepfe L, Martinez-Vilalta J, Piñol J, Mencuccini M (2007) The relevance of xylem network structure for plant hydraulic efficiency and safety. J Theor Biol 247:788–803. https://doi.org/10.1016/j.jtbi.2007.03.036
López R, Nolf M, Duursma RA et al (2018) Mitigating the open vessel artefact in centrifuge-based measurement of embolism resistance. Tree Physiol 39:143–155. https://doi.org/10.1093/treephys/tpy083
Martin-StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecol Lett 20:1437–1447. https://doi.org/10.1111/ele.12851
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. https://doi.org/10.1111/j.1469-8137.2008.02436.x
McDowell N, Allen CD, Anderson-Teixeira K et al (2018) Drivers and mechanisms of tree mortality in moist tropical forests. New Phytol 219:851–869. https://doi.org/10.1111/nph.15027
Myburg AA, Grattapaglia D, Tuskan GA et al (2014) The genome of Eucalyptus grandis. Nature 510:356–362. https://doi.org/10.1038/nature13308
Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: Is it a matter of phloem unloading? Plant Sci 180:604–611. https://doi.org/10.1016/j.plantsci.2010.12.011
Nardini A, Lo Gullo MA, Trifilò P, Salleo S (2014) The challenge of the Mediterranean climate to plant hydraulics: responses and adaptations. Environ Exp Bot 103:68–79. https://doi.org/10.1016/j.envexpbot.2013.09.018
Nardini A, Savi T, Losso A et al (2017) X-ray microtomography observations of xylem embolism in stems of Laurus nobilis are consistent with hydraulic measurements of percentage loss of conductance. New Phytol 213:1068–1075. https://doi.org/10.1111/nph.14245
Niu CY, Meinzer FC, Hao GY (2017) Divergence in strategies for coping with winter embolism among co-occurring temperate tree species: the role of positive xylem pressure, wood type and tree stature. Funct Ecol 31:1550–1560. https://doi.org/10.1111/1365-2435.12868
Nolf M, Lopez R, Peters JMR et al (2017) Visualization of xylem embolism by X-ray microtomography: a direct test against hydraulic measurements. New Phytol 214:890–898. https://doi.org/10.1111/nph.14462
Ogasa M, Miki NH, Murakami Y, Yoshikawa K (2013) Recovery performance in xylem hydraulic conductivity is correlated with cavitation resistance for temperate deciduous tree species. Tree Physiol 33:335–344. https://doi.org/10.1093/treephys/tpt010
Ogasa MY, Utsumi Y, Miki NH et al (2016) Cutting stems before relaxing xylem tension induces artefacts in Vitis coignetiae, as evidenced by magnetic resonance imaging. Plant Cell Environ 39:329–337. https://doi.org/10.1111/pce.12617
Petruzzellis F, Pagliarani C, Savi T et al (2018) The pitfalls of in vivo imaging techniques: evidence for cellular damage caused by synchrotron X-ray computed micro-tomography. New Phytol 220:104–110. https://doi.org/10.1111/nph.15368
Pittermann J, Sperry JS, Hacke UG et al (2006) Inter-tracheid pitting and the hydraulic efficiency of conifer wood: The role of tracheid allometry and cavitation protection. Am J Bot 93:1265–1273. https://doi.org/10.3732/ajb.93.9.1265
Rockwell FE, Wheeler JK, Holbrook NM (2014) Cavitation and its discontents: opportunities for resolving current controversies. Plant Physiol 164:1649–1660. https://doi.org/10.1104/pp.113.233817
Saadaoui E, Ben Yahia K, Dhahri S et al (2017) An overview of adaptative responses to drought stress in Eucalyptus spp. For Stud 67:86–96. https://doi.org/10.1515/fsmu-2017-0014
Salleo S, Lo Gullo MA, Trifilò P, Nardini & A, (2004) New evidence for a role of vessel-associated cells and phloem in the rapid xylem refilling of cavitated stems of Laurus nobilis L. Plant, Cell Environ 27:1065–1076. https://doi.org/10.1111/j.1365-3040.2004.01211.x
Sano Y, Morris H, Shimada H et al (2011) Anatomical features associated with water transport in imperforate tracheary elements of vessel-bearing angiosperms. Ann Bot 107:953–964. https://doi.org/10.1093/aob/mcr042
Savi T, Casolo V, Luglio J et al (2016) Species-specific reversal of stem xylem embolism after a prolonged drought correlates to endpoint concentration of soluble sugars. Plant Physiol Biochem 106:198–207. https://doi.org/10.1016/j.plaphy.2016.04.051
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of Image Analysis HHS Public Access
Secchi F, Zwieniecki MA (2010) Patterns of PIP gene expression in Populus trichocarpa during recovery from xylem embolism suggest a major role for the PIP1 aquaporin subfamily as moderators of refilling process. Plant Cell Environ 33:1285–1297. https://doi.org/10.1111/j.1365-3040.2010.02147.x
Secchi F, Pagliarani C, Cavalletto S et al (2021) Chemical inhibition of xylem cellular activity impedes the removal of drought-induced embolisms in poplar stems—new insights from micro-CT analysis. New Phytol 229:820–830. https://doi.org/10.1111/nph.16912
Souden S, Ennajeh M, Ouledali S et al (2020) Water relations, photosynthesis, xylem embolism and accumulation of carbohydrates and cyclitols in two Eucalyptus species (E. camaldulensis and E. torquata) subjected to dehydration–rehydration cycle. Trees Struct Funct 34:1439–1452. https://doi.org/10.1007/s00468-020-02016-4
Sperry JS (2003) Evolution of water transport and xylem structure. Int J Plant Sci 164:115–127. https://doi.org/10.1086/368398
Sperry JS, Love DM (2015) What plant hydraulics can tell us about responses to climate-change droughts. New Phytol 207:14–27. https://doi.org/10.1111/nph.13354
Sperry JS, Venturas MD, Anderegg WRL et al (2017) Predicting stomatal responses to the environment from the optimization of photosynthetic gain and hydraulic cost. Plant Cell Environ 40:816–830. https://doi.org/10.1111/pce.12852
Tomasella M, Casolo V, Aichner N et al (2019a) Non-structural carbohydrate and hydraulic dynamics during drought and recovery in Fraxinus ornus and Ostrya carpinifolia saplings. Plant Physiol Biochem 145:1–9. https://doi.org/10.1016/j.plaphy.2019.10.024
Tomasella M, Petrussa E, Petruzzellis F et al (2019b) The possible role of non-structural carbohydrates in the regulation of tree hydraulics. Int J Mol Sci 21:144. https://doi.org/10.3390/ijms21010144
Tombesi S, Johnson RS, Day KR, Dejong TM (2010) Relationships between xylem vessel characteristics, calculated axial hydraulic conductance and size-controlling capacity of peach rootstocks. Ann Bot 105:327–331. https://doi.org/10.1093/aob/mcp281
Torres-Ruiz JM, Sperry JS, Fernández JE (2012) Improving xylem hydraulic conductivity measurements by correcting the error caused by passive water uptake. Physiol Plant 146:129–135. https://doi.org/10.1111/j.1399-3054.2012.01619.x
Torres-Ruiz JM, Jansen S, Choat B et al (2015) Direct X-ray microtomography observation confirms the induction of embolism upon xylem cutting under tension. Plant Physiol 167:40–43. https://doi.org/10.1104/pp.114.249706
Trifilò P, Raimondo F, Lo Gullo MA et al (2014) Relax and refill: xylem rehydration prior to hydraulic measurements favours embolism repair in stems and generates artificially low PLC values. Plant Cell Environ 37:2491–2499. https://doi.org/10.1111/pce.12313
Trifilò P, Nardini A, Gullo MAL et al (2015) Diurnal changes in embolism rate in nine dry forest trees: Relationships with species-specific xylem vulnerability, hydraulic strategy and wood traits. Tree Physiol 35:694–705. https://doi.org/10.1093/treephys/tpv049
Trugman AT, Detto M, Bartlett MK et al (2018) Tree carbon allocation explains forest drought-kill and recovery patterns. Ecol Lett 21:1552–1560. https://doi.org/10.1111/ele.13136
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody plants. New Phytol 119:345–360. https://doi.org/10.1111/j.1469-8137.1991.tb00035.x
Tyree MT, Sperry JS (1988) Do woody plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Plant Physiol 88:574–0580. https://doi.org/10.1104/pp.88.3.574
Tyree MT, Salleo S, Nardini A et al (1999) Refilling of embolized vessels in young stems of laurel. Do We need a new paradigm? Plant Physiol 120:11–21. https://doi.org/10.1104/pp.120.1.11
Van der Willigen C, Pammenter NW (1998) Relationship between growth and xylem hydraulic characteristics of clones of Eucalyptus spp. at contrasting sites. Tree Physiol 18:595–600. https://doi.org/10.1093/treephys/18.8-9.595
Vazquez-Cooz I, Meyer RW (2002) A differential staining method to identify lignified and unlignified tissues. Biotechinic Histochem 77:277–282
Venturas MD, Sperry JS, Hacke UG (2017) Plant xylem hydraulics: what we understand, current research, and future challenges. J Integr Plant Biol 59:356–389. https://doi.org/10.1111/jipb.12534
Vesala T, Hölttä T, Perämäki M, Nikinmaa E (2003) Refilling of a hydraulically isolated embolized xylem vessel: model calculations. Ann Bot 91:419–428. https://doi.org/10.1093/aob/mcg022
Wheeler JK, Huggett BA, Tofte AN 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. https://doi.org/10.1111/pce.12139
Xiong D, Nadal M (2020) Linking water relations and hydraulics with photosynthesis. Plant J 101:800–815. https://doi.org/10.1111/tpj.14595
Zeppel MJB, Anderegg WRL, Adams HD et al (2019) Embolism recovery strategies and nocturnal water loss across species influenced by biogeographic origin. Ecol Evol 9:5348–5361. https://doi.org/10.1002/ece3.5126
Zwieniecki MA, Holbrook NM (2009) Confronting Maxwell’s demon: biophysics of xylem embolism repair. Trends Plant Sci 14:530–534. https://doi.org/10.1016/j.tplants.2009.07.002
Zwieniecki MA, Melcher PJ, Ahrens ET (2013) Analysis of spatial and temporal dynamics of xylem refilling in Acer rubrum L using magnetic resonance imaging. Front Plant Sci. https://doi.org/10.3389/fpls.2013.00265
Acknowledgements
We gratefully acknowledge the support of the following people: Sonia Di Buisson (Hans Merensky Holdings) for the provision of the hybrid Eucalyptus material used for this study. Dr Leandra Moller for her technical support. Dr Kim Martin for comments and discussions. Dr Anton Du Plessis and Muofhe Tshibalanganda for their assistance in running the CT scans. We would like to thank the anonymous reviewers for all their insightful comments and suggestions.
Funding
This work was fully funded by the Hans Merensky Foundation within the Hans Merensky Chair of Advanced Modelling of eucalypt wood formation.
Author information
Authors and Affiliations
Additional information
Communicated by Andrea Nardini.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Saunders, A., Drew, D.M. Measurements done on excised stems indicate that hydraulic recovery can be an important strategy used by Eucalyptus hybrids in response to drought. Trees 36, 139–151 (2022). https://doi.org/10.1007/s00468-021-02188-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-021-02188-7