Key message
Resilience to xylem embolism and the accumulation of cyclitols are promising criteria for the selection of drought-resilient Eucalyptus species.
Abstract
Due to the aridity of the climate in the southern Mediterranean region, the choice of suitable species for afforestation projects is crucial. The present study aims to compare resilience mechanisms against drought in two frequently used Eucalyptus species (E. camaldulensis and E. torquata). Two-year-old self-rooted cuttings of the two species were grown in sand-filled pots and subjected to a dehydration period followed by rehydration. At regular intervals, water relations, gas exchange, chlorophyll fluorescence and xylem embolism were measured on these plants. In addition, carbohydrates and cyclitols were quantified in their leaves. The results revealed that E. camaldulensis was more resilient to drought than E. torquata. During the dehydration phase, plant water status, cell turgor, net photosynthetic rate (Pn) and photosynthetic machinery integrity were less affected in E. camaldulensis than E. torquata. After rehydration, these variables were at levels similar to those of control plants in the case of E. camaldulensis, but not in the case of E. torquata. The restoration rate was 96% and 88% for predawn leaf water potential (Ψpd), and it was 98% and 77% for Pn in E. camaldulensis and E. torquata, respectively. The resilience of E. camaldulensis against drought may be due to the efficiency of two determinant survival mechanisms: osmotic adjustment and resistance to xylem embolism. Indeed, E. camaldulensis was less vulnerable to drought-induced xylem embolism and more able to repair embolized xylem vessels than E. torquata. Xylem refilling reduced embolism rate (percent loss of conductivity) to 15% in E. camaldulensis, compared to 22% in E. torquata. Furthermore, E. camaldulensis was found capable of efficient osmotic adjustment than E. torquata by accumulating soluble carbohydrates, especially cyclitols. Indeed, under severe drought (Ψpd of − 7 MPa), E. camaldulensis accumulated 9.27 mg g− 1 DW of quercitol and 3.81 mg g− 1 DW of pinitol; it also had three times more myo-inositol in its leaves than E. torquata. We suggest the use of resilience to xylem embolism and the accumulation of cyclitols to screen Eucalyptus germplasm for drought resistance.
Similar content being viewed by others
References
Albouchi A, Sebei H, Mezni M, El Aouni M (2000) Influence de la durée d’une alimentation hydrique déficiente sur la production de biomasse, la surface transpirante et la densité stomatique d’Acacia cyanophylla Lindl. Annales de l’INGRE 4:139–161
Allen CD, Macalady AK, Chenchouni H, Bachelet D, McDowell N, Vennetier M, Kitzberger T, Rigling A, Breshears DD, Hogg ET (2010) A global overview of drought and heat-induced tree mortality reveals emerging climate change risks for forests. For Ecol Manag 259:660–684
Al-Suod H, Ligor M, RatSiu IA, Rafinsk K, Góreckid R, Buszewski B (2017) A window on cyclitols: characterization and analytics of inositols. Phytochem Lett 20:507–519
Ameglio T, Decourteix M, Alves G, Valentin V, Sakr S, Julien JL, Petel G, Guilliot A, Lacointe A (2004) Temperature effects on xylem sap osmolarity in walnut trees: evidence for a vitalistic model of winter embolism repair. Tree Physiol 24:785–793
Anjum SA, Xie X-Y, Wang L-C, Saleem MF, Man C, Lei W (2011) Morphological, physiological and biochemical responses of plants to drought stress. Afr J Agric Res 6:2026–2032
Aranda I, Castro L, Pardos M, Gil L, Pardos J (2005) Effects of the interaction between drought and shade on water relations, gas exchange and morphological traits in cork oak (Quercus suber L) seedlings. Forest Ecol Manag 210:117–129
Arndt A, Westblad P, Winson I, Hashimoto T, Lundberg A (2004) Ankle and subtalar kinematics measured with intracortical pins during the stance phase of walking. Foot Ankle Int 25:357–364
Arnould P, Hotyat M (2003) Eau et environnement: Tunisie et milieux méditerranéens. ENS éditions
Bachelard E (1985) Effects of soil moisture stress on the growth of seedlings of three eucalypt species 1 seed germination. Aust For Res 15:103 14
Ben Haj Jilani I, Schweitzer P, Khouja ML, Zouaghi M, Gharbi Z (2008) Physicochemical properties and pollen spectra of honeys produced in Tunisia (southwest of Kef). Apiacta 43:38–48
Blum A (2017) Osmotic adjustment is a prime drought stress adaptive engine in support of plant production. Plant Cell Environ 40:4–10
Bohnert HJ, Nelson DE, Jensena RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099–1111
Bousnina R, Mannai SBM, Hamdi AM (2008) Etude d’un projet de reboisement dans la première série forestière de Tabarka. Mémoire de fin d’études. Forêt, Institut Sylvo-Pastoral de Tabarka, Tunisie, p 45
Bréda N, Huc R, Granier A, Dreyer E (2006) Temperate forest trees and stands under severe drought: a review of ecophysiological responses, adaptation processes and long-term consequences. Ann For Sci 63:625–644
Brodersen CR, McElrone AJ (2013) Maintenance of xylem network transport capacity: a review of embolism repair in vascular plants. Front Plant Sci 4:108
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
Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDSL (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna tree species: factors and mechanisms contributing to the refilling of embolized vessels. Plant Cell Environ 26:1633–1645
Cha-um S, Kirdmanee C (2010) Effects of water stress induced by sodium chloride and mannitol on proline accumulation, photosynthetic abilities and growth characters of eucalyptus (Eucalyptus camaldulensis Dehnh). New For 40:349–360
Chaves M (1991) Effects of water deficits on carbon assimilation. J Exp Bot 42:1–16
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought—from genes to the whole plant. Funct plant biol 30:239–264
Chen W, Feng C, Guo W, Shi D, Yang C (2011) Comparative effects of osmotic-, salt-and alkali stress on growth, photosynthesis, and osmotic adjustment of cotton plants. Photosynthetica 49:417
Chourabi S (2014) Elaboration d’un projet de reboisement: un million d’arbres en collaboration avec la société civile ‘Almadanya’. Institut national agronomique de Tunisie, Tunis, p 98
Cochard H, Granier A (1999) Fonctionnement hydraulique des arbres forestiers. Revue Forestière Française 50:121–134
Cochard H, Bodet C, Ameglio 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
Correia B, Pintó-Marijuan M, Neves L, Brossa R, Dias MC, Costa A, Castro BB, Araújo C, Santos C, Chaves MM (2014) Water stress and recovery in the performance of two Eucalyptus globulus clones: physiological and biochemical profiles. Physiol Plant 150:580–592
Demirevska K, Zasheva D, Dimitrov R, Simova-Stoilova L, Stamenova M, Feller U (2009) Drought stress effects on Rubisco in wheat: changes in the Rubisco large subunit. Acta Physiol Plant 31:1129
DGF (2007) Guide technique du reboisement en Tunisie. Ministère de l’Agriculture et des Ressources Hydriques, Tunis, p 286
DGF (2010) Guide pratique de production en hors sol de plants forestiers, pastoraux et ornementaux en Tunisie, Tunis
Dia A, Duponnois R (2010) Le projet majeur africain de la Grande Muraille Verte Concepts et mise en œuvre Marseille, Institut de Recherche pour le Développement, Tunis, p 439
Edenhofer O, Pichs-Madruga R, Sokona Y, Farahani E, Kadner S, Seyboth K, Adler A, Baum I, Brunner S, Eickemeier P (2014) Summary for policymakers. In: Climate change, mitigation of climate change. Contribution of working group III to the fifth assessment report of the Intergovernmental Panel on Climate Change
Eksteen AB, Grzeskowiak V, Jones NB, Pammenter NW (2013) Stomatal characteristics of Eucalyptus grandis clonal hybrids in response to water stress Southern Forests. J For Sci 75:105–111
El Atta HA, Aref IM, Ahmed AI, Khan PR (2012) Morphological and anatomical response of Acacia ehrenbergiana Hayne and Acacia tortilis (Forssk) Haynes subspp raddiana seedlings to induced water stress. Afr J Biotechnol 11:10188–10199
El-Euch F (2011) Atelier régional forets, parcours et changement climatique dans la région du moyen orient Rapport national
Ennajeh M, Vadel AM, Khemira H, Ben Mimoun M, Hellali R (2006) Defense mechanisms against water deficit in two olive (Olea europaea L.) cultivars ‘Meski’ and ‘Chemlali’. J Hortic Sci Biotechnol 81:99–104
Ennajeh M, Tounekti T, Vadel AM, Khemira H, Cochard H (2008) Water relations and drought-induced embolism in olive (Olea europaea) varieties ‘Meski’ and ‘Chemlali’ during severe drought. Tree physiol 28:971–976
Ennajeh M, Vadel AM, Khemira H (2009) Osmoregulation and osmoprotection in the leaf cells of two olive cultivars subjected to severe water deficit. Acta Physiol Plant 31:711–721
Ewers FW, Ameglio T, Cochard H, Beaujard FO, Martignac M, Vandame M et al (2001) Seasonal variation in xylem pressure of walnut trees: root and stem pressures. Tree Physiol 21:1123–1132
Gallé A, Haldimann P, Feller U (2007) Photosynthetic performance and water relations in young pubescent oak (Quercus pubescens) trees during drought stress and recovery. New Phytol 174:799–810
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim et Biophys Acta Gen Subj 990:87–92
Guarnaschelli AB, Lemcoff JH, Prystupa P, Basci SO (2003) Responses to drought preconditioning in Eucalyptus globulus Labill provenances. Trees 17:501–509
Hacke UG, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant Cell Environ 26:303–311
Hochberg U, Windt CW, Ponomarenko A, Zhang Y, Rockwell FE, Holbrook NM (2017) Stomatal closure, basal leaf embolism and shedding protect the hydraulic integrity of grape stems. Plant Physiol 174:764–775
Hoerling M, Eischeid J, Perlwitz J, Quan X, Zhang T, Pegion P (2012) On the increased frequency of Mediterranean drought. J Clim 25:2146–2161
Hu H, Chen H, Hu T, Zhang J (2012) Adaptability comparison between the seedlings of Eucalyptus grandis and Alnus cremastogyne under the condition of continuous drought stress. J Agric Sci 4:75–86
SAS Institute (1999) SAS/STAT User’s Guide. SAS Institute, Cary
Jacobsen AL, Valdovinos-Ayala J, Pratt RB (2018) Functional lifespans of xylem vessels: development, hydraulic function, and post-function of vessels in several species of woody plants. Am J Bot 105:142–150
Khouja ML (1999) Amélioration génétique: inventaire et bilan des recherché enterprises en Tunisie Communication présenté au séminaire organize par l’INGREF et la DGF sur la recherché pour le développement forestier tenu à Hammamet-Tunisie du 24 au 25 novembre 1999, 35p
Khouja ML, Khaldi A, Rejeb MN (2001) Resultants of the Eucalyptus introduction trialis in Tunisia Procedings of international conference on Eucalyptus in the Mediterranean Basin: Prospective and new utilization Ed, Centro Propozione Pubblicita, Taormina, Italy, pp163-168
Lamhamedi MS, Ammari Y, Fecteau B, Fortin JA, Margolis H (2000) Problématique des pépinières forestières en Afrique du Nord et stratégies de développement. Cahiers Agric 9:369–380
Lawlor DW, Cornic G (2002) Photosynthetic carbon assimilation and associated metabolism in relation to water deficits in higher plants. Plant Cell Environ 25:275–294
Lemcoff JH, Guarnaschelli AB, Garau AM, Prystupa P (2002) Elastic and osmotic adjustments in rooted cuttings of several clones of Eucalyptus camaldulensis Dehnh from southeastern Australia after a drought. Flora 197:134–142
Lima WDP, Jarvis P, Rhizopoulou S (2003) Stomatal responses of Eucalyptus species to elevated CO2 concentration and drought stress. Sci Agric 60:231–238
Li X, Blackman CJ, Rymer PD, Quintans D, Duursma RA, Choat B, Tissue DT (2018) Xylem embolism measured retrospectively is linked to canopy dieback in natural populations of Eucalyptus piperita following drought. Tree Physiol 38:1193–1199
Martin-StPaul N, Delzon S, Cochard H (2017) Plant resistance to drought depends on timely stomatal closure. Ecol Lett 20:1437–1447
Martorell S, Diaz-Espejo A, Medrano H, Ball MC, Chaot B (2013) Rapid hydraulic recovery in Eucalyptus pauciflora after drought: linkages between stem hydraulics and leaf gas exchange. Plant Cell Environ 37:617–626
Maxwell K, Johnson GN (2000) Chlorophyll fluorescence—a practical guide. J Exp Bot 51:659–668
Merchant A, Tausz M, Arndt SK, Adams MA (2006) Cyclitols and carbohydrates in leaves and roots of 13 Eucalyptus species suggest contrasting physiological responses to water deficit. Plant Cell Environ 29:2017–2029
Merchant A, Callister A, Arndt S, Tausz M, Adams M (2007) Contrasting physiological responses of six Eucalyptus species to water deficit. Ann Bot 100:1507–1515
Merchant A, Arndt S, Rowell D, Posch S, Callister A, Tausz M, Adams M (2010) Seasonal changes in carbohydrates, cyclitols, and water relations of 3 field grown Eucalyptus species from contrasting taxonomy on a common site. Ann For Sci 67:104
Moing A, Carbonne F, Rashad MH, Gaudillere JP (1992) Carbon fluxes in mature peach leaves. Plant Physiol 100:1878–1884
Mokotedi ME (2010) Physiological responses of Eucalyptus nitens × nitens under experimentally imposed water stress. South For 72:63–68
Morales C, Pino M, Del Pozo A (2013) Phenological and physiological responses to drought stress and subsequent rehydration cycles in two raspberry cultivars. Sci Hortic 162:234–241
Morgan JM (1984) Osmoregulation and water stress in higher plants. Annu Rev Plant Physiol 35:299–319
Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Sci 180:604–611
Navarrete-Campos D, Bravo LA, Rubilar RA, Emhart V, Sanhueza R (2013) Drought effects on water use efficiency, freezing tolerance and survival of Eucalyptus globulus and Eucalyptus globulus × nitens cuttings. New For 44:119–134
Ngugi MR, Doley D, Hunt MA, Ryan P, Dart P (2004) Physiological responses to water stress in Eucalyptus cloeziana and E argophloia seedlings. Trees 18:381–389
Nobel P (1991) Physicochemical and environmental plant physiology. Academic Press, San Diego
Nolf M, Lopez R, Peters JMR, Flavel RJ, Koloadin LS, Young IM, Choat B (2017) Visualization of xylem embolism by X-ray microtomography: a direct test against hydraulic measurements. New Phtytol 214:890–898
Orthen B, Popp M (2000) Cyclitols as cryoprotectants for spinach and chickpea thylakoids. Environ Exp Bot 44:125–132
Peltzer D, Dreyer E, Polle A (2002) Differential temperature dependencies of antioxidative enzymes in two contrasting species: Fagus sylvatica and Coleus blumei. Plant Physiol Biochem 40:141–150
Percival GC, Sheriffs CN (2002) Identification of drought-tolerance woody perennials using chlorophyll fluorescence. Arboric J 28:215–223
Perrone I, Pagliarani C, Lovisolo C, Chitarra W, Roman F, Schubert A (2012) Recovery from water stress affects grape leaf petiole transcriptome. Planta 235:1383–1396
Pinheiro C, Chaves M (2010) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882
Pita P, Pardos JA (2001) Growth, leaf morphology, water use and tissue water relations of Eucalyptus globulus clones in response to water deficit. Tree Physiol 21:599–607
Popp M, Lied W, Bierbaum U, Gross M, Grosse-Schulte T, Hams S, Oldenettel J, Schuler S, Wiese J (1997) Cyclitols—stable osmotica in trees. In: Rennenberg H, Eschrich W, Ziegler H (eds) Trees—contributions to modern tree physiology. Backhuys Publishers, Leiden, pp 257–270
Poupon H (1968) Premieres études des caracteristiques hydriques des feuilles d’Eucalyptus camaldulensis en Tunisie. Annales de l'Institut National de Recherches Forestières de Tunisie 1(03):1–22
Robyt J, White B (1987) Biochemical techniques—theory and practice. Cole Publishing Company, Monterey, pp 267–275
Salleo S, Lo Gullo MA, Trifilo 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
Samarah N, Alqudah A, Amayreh J, McAndrews G (2009) The effect of late-terminal drought stress on yield components of four barley cultivars. J Agron Crop Sci 195:427–441
Sánchez-Rodriguez J, Martinez-Carrasco R, Pérez P (1997) Photosynthetic electron transport and carbon-reduction-cycle enzyme activities under long-term drought stress in Casuarina equisetifolia. Forst Forst Photosynth Res 52:255–262
Sapeta H, Costa JM, Lourenco T, Maroco J, Van der Linde P, Oliveira MM (2013) Drought stress response in Jatropha curcas: growth and physiology. Environ Exp Bot 85:76–84
Schobert B (1977) Is there an osmotic regulatory mechanism in algae and higher plants? J Theor Biol 68:17–26
Scholander PF, Bradstreet ED, Hemmingsen E, Hammel H (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148:339–346
Sevanto S (2018) Drought impacts on phloem transport. Curr Opin Plant Biol 43:76–81
Shvaleva AL, Silva FCE, Breia E, Jouve J, Hausman JF, Almeida MH, Maroco J, Rodrigues M, Pereira JS, Chaves MM (2006) Metabolic responses to water deficit in two Eucalyptus globulus clones with contrasting drought sensitivity. Tree Physiol 26:239–248
Smirnoff N (1993) The role of active oxygen in the response of plants to water deficit and desiccation. New Phytol 125:27–58
Sperry J, Donnelly J, Tyree M (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant Cell Environ 11:35–40
Stape JL, Binkley D, Ryan MG (2004) Eucalyptus production and the supply, use and efficiency of use of water, light and nitrogen across a geographic gradient in Brazil. For Ecol Manag 193:17–31
Tognetti R, Longobucco A, Miglietta F, Raschi A (1999) Water relations, stomatal response and transpiration of Quercus pubescens trees during summer in a Mediterranean carbon dioxide spring. Tree Physiol 19:261–270
Toscano S, Ferrante A, Romano D (2019) Response of Mediterranean ornamental plants to drought stress. Horticulturae 5:6
Tyree MT, Zimmermann MH (2002) Xylem structure and the ascent of sap. Springer, New York
Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R (1999) Refilling of embolized vessels in young stems of laurel: do we need a new paradigm? Plant Physiol 120:11–21
Vendruscolo ECG, Schuster I, Pileggi M, Scapim CA, Molinari HBC, Marur CJ, Vieira LGE (2007) Stress-induced synthesis of proline confers tolerance to water deficit in transgenic wheat. J Plant Physiol 164:1367–1376
Villar E, Klopp C, Noirot C, Novaes E, Kirst M, Plomion C, Gion JM (2011) RNA-Seq reveals genotype-specific molecular responses to water deficit in Eucalyptus. BMC Genom 12:538
Warren CR, Aranda I, Cano FJ (2011) Responses to water stress of gas exchange and metabolites in Eucalyptus and Acacia spp. Plant Cell Environ 34:1609–1629
Warren CR, Aranda I, Cano FJ (2012) Metabolomics demonstrates divergent responses of two Eucalyptus species to water stress. Metabolomics 8:186–200
White DA, Turner NC, Galbraith JH (2000) Leaf water relations and stomatal behavior of four allopatric Eucalyptus species planted in Mediterranean southwestern Australia. Tree Physiol 20:1157–1165
Zaafouri MS (1993) Contraintes du milieu et réponses de quelques espèces arbustives exotiques introduites en Tunisie présaharienne Science et changements planétaires. Sécheresse 4:201–201
Zhu JK (2001) Plant salt tolerance. Trends Plant Sci 6:66–71
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Souden, S., Ennajeh, M., Ouledali, S. et al. 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 34, 1439–1452 (2020). https://doi.org/10.1007/s00468-020-02016-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00468-020-02016-4