Ion-mediated compensation for drought-induced loss of xylem hydraulic conductivity in field-growing plants of Laurus nobilis
Patrizia Trifilò A , Andrea Nardini B C , Fabio Raimondo A , Maria A. Lo Gullo A and Sebastiano Salleo BA Dipartimento di Scienze della Vita, Università di Messina, Salita Sperone 31, 98166 Messina S Agata, Italy.
B Dipartimento di Scienze della Vita, Università di Trieste, Via L. Giorgieri 10, 34127 Trieste, Italy.
C Corresponding author. Email: nardini@units.it
Functional Plant Biology 38(7) 606-613 https://doi.org/10.1071/FP10233
Submitted: 30 November 2010 Accepted: 10 May 2011 Published: 12 July 2011
Abstract
Xylem cavitation is a common occurrence in drought-stressed plants. Cavitation-induced embolism reduces xylem hydraulic conductivity (kxylem) and may lead to stomatal closure and reduction of photosynthetic rates. Recent studies have suggested that plants may compensate for kxylem loss through ion-mediated enhancement of the residual water transport capacity of functioning conduits. To test this hypothesis, field-grown laurel (Laurus nobilis L.) plants were subjected to mild drought stress by suspending irrigation. Drought treatment induced a significant increase in xylem embolism compared with control (well watered) plants. Xylem sap potassium concentration ([K+]) increased during the day both in control and water stressed plants. Midday values of sap [K+] were significantly higher in water stressed plants. The recorded increase in sap potassium concentration induced significant enhancement of residual kxylem when solutions with different [K+] were perfused through excised stems sampled in the field and measured in the laboratory. In planta measurements of stem hydraulic conductance revealed no change between water stressed plants and controls. Our data suggest that ion-mediated enhancement of residual kxylem buffered the actual loss of hydraulic conductance suffered by plants during the warmest hours of the day as well as under mild drought stress conditions.
Additional keywords: cavitation, gas exchange, hydraulic conductivity, laurel, potassium, water stress, xylem.
References
Aasamaa K, Sober A (2010) Sensitivity of stem and petiole hydraulic conductance of deciduous trees to xylem sap ionic concentration. Biologia Plantarum 54, 299–307.| Sensitivity of stem and petiole hydraulic conductance of deciduous trees to xylem sap ionic concentration.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkslaku74%3D&md5=f14302f35797ba63637bf72cf48ac797CAS |
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 Physiology 24, 785–793.
Ansley RJ, Dugas WA, Heuer ML, Trevino BA (1994) Stem flow and porometer measurements of transpiration from honey mesquite (Prosopis glandulosa). Journal of Experimental Botany 45, 847–856.
| Stem flow and porometer measurements of transpiration from honey mesquite (Prosopis glandulosa).Crossref | GoogleScholarGoogle Scholar |
Boyce CK, Zwieniecki MA, Cody GD, Jacobsen C, Wirik S, Knoll AH, Holbrook NM (2004) Evolution of xylem lignification and hydrogel transport regulation. Proceedings of the National Academy of Sciences of the United States of America 101, 17 555–17 558.
| Evolution of xylem lignification and hydrogel transport regulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhslOhsA%3D%3D&md5=10b2bae17690dfdbeaa330af0379cd00CAS |
Brodribb TJ, Holbrook NM (2006) Declining hydraulic efficiency as transpiring leaves desiccate: two types of response. Plant, Cell & Environment 29, 2205–2215.
| Declining hydraulic efficiency as transpiring leaves desiccate: two types of response.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVaitA%3D%3D&md5=a8f2d6b8c0b1f5db966b02fa94e8c688CAS | 17081253PubMed |
Buckley TN (2005) The control of stomata by water balance. New Phytologist 168, 275–292.
| The control of stomata by water balance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1Smu7bI&md5=11e8fd58776c89c591c621922f074b5aCAS | 16219068PubMed |
Choat B, Cobb AR, Jansen S (2008) Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function. New Phytologist 177, 608–626.
| Structure and function of bordered pits: new discoveries and impacts on whole-plant hydraulic function.Crossref | GoogleScholarGoogle Scholar | 18086228PubMed |
Cochard H, Herbette S, Hernàndez E, Hölttä T, Mencuccini M (2010) The effects of sap ionic composition on xylem vulnerabilty to cavitation. Journal of Experimental Botany 61, 275–285.
| The effects of sap ionic composition on xylem vulnerabilty to cavitation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsFGgu7bO&md5=1b30828450ac5d8cbf7a83e03944342cCAS | 19841058PubMed |
Dye PJ, Christie SI, Olbrich BW, Ferreira E, Tallon N (1990) Determining transpiration from Pinus patula shoots – a comparative evaluation of the cut shoot method and two null-balance diffusion porometers. South African Forestry Journal 155, 10–15.
Gascò A, Nardini A, Gortan E, Salleo S (2006) Ion-mediated increase in the hydraulic conductivity of laurel stems: role of pits and consequences for the impact of cavitation on water transport. Plant, Cell & Environment 29, 1946–1955.
| Ion-mediated increase in the hydraulic conductivity of laurel stems: role of pits and consequences for the impact of cavitation on water transport.Crossref | GoogleScholarGoogle Scholar | 16930320PubMed |
Gascò A, Salleo S, Gortan E, Nardini A (2007) Seasonal changes in the ion-mediated increase of xylem hydraulic conductivity in stems of three evergreens: any functional role? Physiologia Plantarum 129, 597–606.
| Seasonal changes in the ion-mediated increase of xylem hydraulic conductivity in stems of three evergreens: any functional role?Crossref | GoogleScholarGoogle Scholar |
Goodger JQD, Sharp RE, Marsh EL, Schachtman DP (2005) Relationships between xylem sap constituents and leaf conductance of well-watered and water- stressed maize across three xylem sap sampling techniques. Journal of Experimental Botany 56, 2389–2400.
| Relationships between xylem sap constituents and leaf conductance of well-watered and water- stressed maize across three xylem sap sampling techniques.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVahtLvL&md5=74d4a892cfe547aa0cee5328312be4ddCAS | 16043455PubMed |
Jansen S, Gortan E, Lens F, Lo Gullo MA, Salleo S, Scholz A, Stein A, Trifilò P, Nardini A (2011) Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem? New Phytologist 189, 218–228.
| Do quantitative vessel and pit characters account for ion-mediated changes in the hydraulic conductance of angiosperm xylem?Crossref | GoogleScholarGoogle Scholar | 20840611PubMed |
López-Portillo J, Ewers F, Angeles G (2005) Sap salinity effects on xylem conductivity in two mangrove species. Plant, Cell & Environment 28, 1285–1292.
| Sap salinity effects on xylem conductivity in two mangrove species.Crossref | GoogleScholarGoogle Scholar |
Malone M, Herron M, Morales MA (2002) Continuous measurement of macronutrient ions in the transpiration stream of intact plants using the meadow spittlebug coupled with ion cromatography. Plant Physiology 130, 1436–1442.
| Continuous measurement of macronutrient ions in the transpiration stream of intact plants using the meadow spittlebug coupled with ion cromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovVOmsLg%3D&md5=24ef52422faf46f588098223f8ffde02CAS | 12428008PubMed |
Metzner R, Thorpe MR, Breuer U, Blümler P, Schurr U, Schneider HU, Schroedr WH (2010) Contrasting dynamics of water and mineral nutrients in stems shown by stable isotope tracers and cryo-SIMS. Plant, Cell & Environment 33, 1393–1407.
Nardini A, Gascò A, Trifilò P, Lo Gullo MA, Salleo S (2007) Ion-mediated enhancement of xylem hydraulic conductivity is not always suppressed by the presence of Ca2+ in the sap. Journal of Experimental Botany 58, 2609–2615.
| Ion-mediated enhancement of xylem hydraulic conductivity is not always suppressed by the presence of Ca2+ in the sap.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFWitLg%3D&md5=c019fb6d08abfce0903f37a58db37d89CAS | 17545227PubMed |
Nardini A, Grego F, Trifilò P, Salleo S (2010) Changes of xylem sap ionic content and stem hydraulics in response to irradiance in Laurus nobilis. Tree Physiology 30, 628–635.
| Changes of xylem sap ionic content and stem hydraulics in response to irradiance in Laurus nobilis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXntFCqtrk%3D&md5=f0ba8f148defbfefdd39a1c7ffe9e82eCAS | 20339142PubMed |
Nardini A, Lo Gullo MA, Salleo S (2011) Refilling embolized xylem conduits: is it a matter of phloem unloading? Plant Science 180, 604–611.
| Refilling embolized xylem conduits: is it a matter of phloem unloading?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXisFyhs7g%3D&md5=89c25418073ca9f933316499e896735fCAS | 21421408PubMed |
Ryden P, MacDougall AJ, Tibbits CW, Ring SG (2000) Hydration of pectic polysaccharides. Biopolymers 54, 398–405.
| Hydration of pectic polysaccharides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXnvVGnt7c%3D&md5=9d6a28b9e47c6e5ce668a61321e5878aCAS | 10951326PubMed |
Sack L, Melcher PJ, Zwieniecki MA, Holbrook NM (2002) The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53, 2177–2184.
| The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xpt1KgtLg%3D&md5=c62c0b2424f0d31430335ae2ee2b14d0CAS | 12379784PubMed |
Salleo S, Lo Gullo MA, De Paoli D, Zippo M (1996) Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism. New Phytologist 132, 47–56.
| Xylem recovery from cavitation-induced embolism in young plants of Laurus nobilis: a possible mechanism.Crossref | GoogleScholarGoogle Scholar |
Salleo S, Nardini A, Pitt F, Lo Gullo MA (2000) Xylem cavitation and hydraulic control of stomatal conductance in laurel (Laurus nobilis L.). Plant, Cell & Environment 23, 71–79.
| Xylem cavitation and hydraulic control of stomatal conductance in laurel (Laurus nobilis L.).Crossref | GoogleScholarGoogle Scholar |
Salleo S, Trifilò P, Esposito S, Nardini A, Lo Gullo MA (2009) Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair? Functional Plant Biology 36, 815–825.
| Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair?Crossref | GoogleScholarGoogle Scholar |
Sellin A, Õunapuu E, Karusion A (2010) Experimental evidence supporting the concept of light-mediated modulation of stem hydraulic conductance. Tree Physiology 30, 1528–1535.
| Experimental evidence supporting the concept of light-mediated modulation of stem hydraulic conductance.Crossref | GoogleScholarGoogle Scholar | 21071503PubMed |
Siebrecht S, Herdel K, Schurr U, Tischner R (2003) Nutrient translocation in the xylem of poplar – diurnal variations and spatial distribution along the shoot axis. Planta 217, 783–793.
| Nutrient translocation in the xylem of poplar – diurnal variations and spatial distribution along the shoot axis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmvFCju7c%3D&md5=aa74349c04bb743431ff04d136076427CAS | 12721678PubMed |
Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13–23.
| Hydraulic constraints on plant gas exchange.Crossref | GoogleScholarGoogle Scholar |
Sperry JS, Pockman WT (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant, Cell & Environment 16, 279–287.
| Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis.Crossref | GoogleScholarGoogle Scholar |
Trifilò P, Lo Gullo MA, Salleo S, Callea K, Nardini A (2008) Xylem embolism alleviated by ion-mediated increase in hydraulic conductivity of functional xylem: insights from field measurements. Tree Physiology 28, 1505–1512.
Tsuda M, Tyree MT (1997) Whole-plant hydraulic resistance and vulnerability segmentation in Acer saccharinum. Tree Physiology 17, 351–357.
Tsuda M, Tyree MT (2000) Plant hydraulic conductance measured by the high pressure flowmeter in crop plants. Journal of Experimental Botany 51, 823–828.
| Plant hydraulic conductance measured by the high pressure flowmeter in crop plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsLY%3D&md5=78820443094296d8a85c323d51d96ae9CAS | 10938875PubMed |
Tyree MT, Sperry JS (1989) The vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Plant Molecular Biology 40, 19–36.
| The vulnerability of xylem to cavitation and embolism.Crossref | GoogleScholarGoogle Scholar |
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 Physiology 120, 11–21.
| Refilling of embolized vessels in young stems of laurel. Do we need a new paradigm?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjt1Sru78%3D&md5=c206141c20a40a45439b6c746cca1bb5CAS | 10318679PubMed |
van Ieperen W, van Meeteren U, van Gelder H (2000) Fluid ionic composition influences hydraulic conductance of xylem conduits. Journal of Experimental Botany 51, 769–776.
| Fluid ionic composition influences hydraulic conductance of xylem conduits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjtF2jsLw%3D&md5=c1f50892db9c2fbaa6484b9f69898ebeCAS | 10938869PubMed |
Zimmermann MH (1978) Hydraulic architecture of some diffuse-porous trees. Canadian Journal of Botany 56, 2286–2295.
| Hydraulic architecture of some diffuse-porous trees.Crossref | GoogleScholarGoogle Scholar |
Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059–1062.
| Hydrogel control of xylem hydraulic resistance in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhtFGksLY%3D&md5=04c9d4c27b9f0184162e2d3b72adacf1CAS | 11161220PubMed |
Zwieniecki MA, Melcher PJ, Field TS, Holbrook NM (2004) A potential role for xylem-phloem interactions in the hydraulic architecture of trees: effects of phloem girdling on xylem hydraulic conductance. Tree Physiology 24, 911–917.