Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Vessel wall vibrations: trigger for embolism repair?

Sebastiano Salleo A , Patrizia Trifilò B and Maria Assunta Lo Gullo B C
+ Author Affiliations
- Author Affiliations

A Dipartimento di Biologia, Università di Trieste, Via L. Giorgieri 10, 34127 Trieste, Italy.

B Dipartimento di Scienze della Vita ‘M. Malpigli’, Università di Messina, Salita Sperone 31, 98166 Messina S. Agata, Italy.

C Corresponding author. Email: mlogullo@unime.it

Functional Plant Biology 35(4) 289-297 https://doi.org/10.1071/FP07239
Submitted: 11 October 2007  Accepted: 4 April 2008   Published: 3 June 2008

Abstract

Xylem embolism repair is preceded by starch depolymerisation in vessel-associated cells (VAC) of Laurus nobilis L. (laurel) twigs, but the primary signal triggering such a process is still unknown. We tested the hypothesis that conduit wall vibrations during cavitation may be sensed by VAC inducing starch-to-sugar conversion. Twigs of laurel from watered or stressed plants were exposed to ultrasound for 60 min to simulate acoustic waves emitted by cavitating conduits. Preliminary tests showed that ultrasound caused no damage to cell membrane integrity nor did they cause xylem embolism. The number of VAC with high starch content (HSC-cells) was estimated microscopically by counting the cells with more than 50% of their lumen filled with starch granules. Sonication had no effect on HSC-cells in twigs from watered plants while it induced a drop in the percentage HSC-cells from 80 to 40% in twigs from stressed plants, at the ultrasound source location. No effect was recorded in these twigs 20 mm from the ultrasound source. Sonication was a good simulator of cavitation in inducing starch depolymerisation which suggests a possible bio- physical nature for the signal initiating embolism repair.

Additional keywords: embolism repair, Laurus nobilis, starch depolymerisation, stem sonication, wood parenchyma cells, xylem cavitation.


Acknowledgements

All authors are very grateful to both anonymous referees and especially to referee #1 for thorough improvement of the text and fruitful suggestions.


References


Alves G, Sauter JJ, Julien JL, Fleurat-Lessard P, Ameglio T, Guillot A, Petel G, Lacointe A (2001) Plasma membrane H+-ATPase, succinate and isocitrate dehydrogenases activities of vessel-associated cells in walnut trees. Journal of Plant Physiology 158, 1263–1271.
Crossref | GoogleScholarGoogle Scholar | open url image1

Alves G, Ameglio T, Guilliot A, Fleurat-Lessard P, Lacointe A, Sakr S, Petel G, Julien JL (2004) Winter variation in xylem sap pH of walnut trees: involvement of plasma membrane H+-ATPase of vessel associated cells. Tree Physiology 24, 99–105.
Crossref | PubMed |
open url image1

Ameglio T, Ewers FW, Cochard H, Martignac M, Vandame M, Bodet C, Cruiziat P (2001) Winter stem pressures in walnut trees: effects of carbohydrates, cooling and freezing. Tree Physiology 21, 384–394. open url image1

Ameglio TC, Bodet A, Lacointe A, Cochard H (2002) Winter embolism, mechanisms of xylem hydraulic conductivity recovery and springtime growth patterns in walnut and peach trees. Tree Physiology 22, 1211–1230.
PubMed |
open url image1

Ameglio T, Decourteix M, Alves G, Valentin V, Sakr S, Julien J-L, 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.
PubMed |
open url image1

Antognoni F, Fornale S, Grimmer C, Komor E, Bagni N (1998) Long-distance translocation of polyamines in phloem and xylem of Ricinus communis L. plants. Planta 204, 520–527.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bais HP, Ravishankar GA (2002) Role of polyamines in the ontogeny of plants and their biotechnological applications. Plant Cell, Tissue and Organ Culture 69, 1–34.
Crossref | GoogleScholarGoogle Scholar | open url image1

Böhm H, Anthony P, Davey MR, Briarty LG, Power JB, Lowe KC, Benes E, Gröschl M (2000) Viability of plant cell suspensions exposed to homogeneous ultrasonic fields of different energy density and wave type. Ultrasonics 38, 629–632.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boyer JS, Silk WK (2004) Hydraulics of plant growth. Functional Plant Biology 31, 761–773.
Crossref | GoogleScholarGoogle Scholar | open url image1

Bucci SJ, Scholz FG, Goldstein G, Meinzer FC, Sternberg LDSL (2003) Dynamic changes in hydraulic conductivity in petioles of two savanna species: factors and mechanisms contributing to the refilling of embolized vessels. Plant, Cell & Environment 26, 1633–1645.
Crossref | GoogleScholarGoogle Scholar | open url image1

Canny MJ, Sparks JP, Huang CX, Roderick ML (2007) Hypothesis: air embolism exsolving in the transpiration water – the effect of constrictions in the xylem pipes. Functional Plant Biology 34, 95–111.
Crossref | GoogleScholarGoogle Scholar | open url image1

Cochard H, Bodet C, Ameglio T, Cruiziat P (2000) Cryo-scanning electron microscopy observations of vessels contents during transpiration in walnut petioles. Facts or artefacts? Plant Physiology 124, 1191–1202.
Crossref | GoogleScholarGoogle Scholar | open url image1

Crombie DS, Hipkins MF, Milburn JA (1985) Gas penetration of pit membranes in the xylem of Rhododendron as the cause of acoustically detectable sap cavitation. Australian Journal of Plant Physiology 12, 445–453. open url image1

Davies E , Stankovic B (2006) Electrical signals, the cytoskeleton, and gene expression: a hypothesis on the coherence of the cellular responses to environmental insult. In ‘Communication in plants – neuronal aspects of plant life’. (Eds F Baluska, S Mancuso, D Volkmann) pp. 309–320. (Springer-Verlag: Berlin)

De Boer AH, Volkov V (2003) Logistics of water and salt transport through the plant: structure and functioning of the xylem. Plant, Cell & Environment 26, 87–101.
Crossref | GoogleScholarGoogle Scholar | open url image1

Decourteix M, Alves G, Brunel N, Ameglio T, Guillot A, Lemoine R, Pétel G, Soulaiman S (2006) JrSUT1, a putative xylem sucrose transporter, could mediate sucrose influx into xylem parenchyma cells and be up-regulated by freeze-thaw cycles over the autumn-winter period in walnut tree (Juglans regia L.). Plant, Cell & Environment 29, 36–47.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ewers FW, Cochard H, Tyree MT (1997) A survey of root pressures in vines of a tropical lowland forest. Oecologia 110, 191–196.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ewers FW, Ameglio T, Cochard H, Beaujard F, Martignac M, Vandame M, Bodet C, Cruiziat P (2001) Seasonal variation in xylem pressure of walnut trees: root and stem pressures. Tree Physiology 21, 1123–1132.
PubMed |
open url image1

Facette MR, McCully ME, Shane MW, Canny MJ (2001) Measurements of the time to refill embolized vessels. Plant Physiology and Biochemistry 39, 59–66.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fisher JB, Angeles G, Ewers FW, Lopez Portillo J (1997) Survey of root pressures in tropical vines and woody species. International Journal of Plant Sciences 158, 44–50.
Crossref | GoogleScholarGoogle Scholar | open url image1

Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30, 249–257.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gascò A, Nardini A, Salleo S (2004) Resistance to water flow through leaves of Coffea arabica is dominated by extra-vascular tissues. Functional Plant Biology 31, 1161–1168.
Crossref | GoogleScholarGoogle Scholar | open url image1

Gascò A, Nardini A, Gortan E, Salleo S (2006) Ion-mediated increase in the hydraulic conductivity of laurel: role of pits and consequences for the impact of cavitation on water transport. Plant, Cell & Environment 29, 1946–1955.
Crossref | GoogleScholarGoogle Scholar | open url image1

Grossnickle SC (1992) Relationship between freezing tolerance and shoot water relations of western red cedar. Tree Physiology 11, 229–240.
PubMed |
open url image1

Hacke U, Sauter JJ (1996) Xylem dysfunction during winter and recovery of hydraulic conductivity in diffuse-porous and ring-porous trees. Oecologia 105, 435–439.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hacke U, Sperry JS (2003) Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant, Cell & Environment 26, 303–311.
Crossref | GoogleScholarGoogle Scholar | open url image1

Holbrook NM, Zwieniecki MA (1999) Embolism repair and xylem tension: do we need a miracle? Plant Physiology 120, 7–10.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Holtta T, Vesala T, Peramaki M, Nikinmaa E (2006) Refilling of embolized conduits as a consequence of ‘munch-water’ circulation. Functional Plant Biology 33, 949–959.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ikeda T, Ohtsu M (1992) Detection of xylem cavitation in field-grown pine trees using the acoustic emission technique. Ecological Research 7, 391–395.
Crossref | GoogleScholarGoogle Scholar | open url image1

Jackson GE, Irvine J, Grace J (1995) Xylem cavitation in two mature Scots pine forests growing in a wet and a dry area of Britain. Plant, Cell & Environment 18, 1411–1418.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kikuta S, Richter H (2003) Ultrasound acoustic emissions from freezing xylem. Plant, Cell & Environment 26, 383–388.
Crossref | GoogleScholarGoogle Scholar | open url image1

Kikuta SB, Lo Gullo MA, Nardini A, Richter H, Salleo S (1997) Ultrasound acoustic emission from dehydrating leaves of deciduous and evergreen trees. Plant, Cell & Environment 20, 1381–1390.
Crossref | GoogleScholarGoogle Scholar | open url image1

Konrad W, Roth-Nebelsick A (2003) The dynamics of gas bubbles in conduits of vascular plants and implications for embolism repair. Journal of Theoretical Biology 224, 43–61.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kuznetsov VV, Rakitin VY, Sadomov NG, Dam DV, Stetsenko LA, Shevyakova NI (2002) Do polyamines participate in the long distance translocation of stress signals in plants? Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 49, 120–130.
Crossref | GoogleScholarGoogle Scholar | open url image1

Lin L, Wu J, Ho K-P, Shuyan Q (2001) Ultrasound-induced physiological effects and secondary metabolite (Saponin) production in Panax ginseng cell cultures. Ultrasounds in Medicine and Biology 27, 1147–1152.
Crossref | GoogleScholarGoogle Scholar | open url image1

Milburn JA (1973) Cavitation studies on whole Ricinus plants by acoustic detection. Planta 112, 333–342.
Crossref | GoogleScholarGoogle Scholar | open url image1

Milburn JA, Johnson RPC (1966) The conduction of sap. II. Detection of vibrations produced by sap cavitation in Ricinus xylem. Planta 69, 43–52.
Crossref | GoogleScholarGoogle Scholar | open url image1

Nardini A, Salleo S (2000) Limitation of stomatal conductance by hydraulic traits: sensing or preventing water cavitation? Trees – Structure and Function 15, 14–24. open url image1

Nardini A, Lo Gullo MA, Tracanelli S (1996) Water relations of six sclerophylls growing near Trieste (Northeastern Italy): has sclerophylly a univocal functional significance? Giornale Botanico Italiano 130, 811–828. open url image1

Park SH, Bean SR, Wilson JD, Schober TJ (2006) Rapid isolation of sorghum and other cereal starches using sonication. Cereal Chemistry 83, 611–616.
Crossref | GoogleScholarGoogle Scholar | open url image1

Ritman KT, Milburn JA (1988) Acoustic emissions from plants: ultrasonic and audible compared. Journal of Experimental Botany 39, 1237–1248.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sakr S, Alves G, Morillon R, Maurel K, Decourteix A, Guilliot A, Fleurat-Lessard P, Julien JL, Chrispeels MJ (2003) Plasma membrane aquaporins are involved in winter embolism recovery in walnut tree. Plant Physiology 133, 630–641.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Salleo S, Lo Gullo MA (1989) Different aspects of cavitation resistance in Ceratonia siliqua, a drought avoiding Mediterranean tree. Annals of Botany 64, 325–336. open url image1

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.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salleo S, Lo Gullo MA, Raimondo F, Nardini A (2001) Vulnerability to cavitation of leaf minor veins: any impact on leaf gas exchange? Plant, Cell & Environment 24, 851–859.
Crossref | GoogleScholarGoogle Scholar | open url image1

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 Laurus nobilis L. cavitated. Plant, Cell & Environment 27, 1065–1066.
Crossref | GoogleScholarGoogle Scholar | open url image1

Salleo S, Trifilò P, Lo Gullo MA (2006) Phloem as a possible major determinant of rapid cavitation reversal in of Laurus nobilis (laurel). Functional Plant Biology 33, 1063–1074.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sandford AP, Grace J (1985) The measurement and interpretation of ultrasound from woody. Journal of Experimental Botany 36, 298–311.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sauter J, Wisniewski M, Witt W (1996) Interrelationships between ultrastructure, sugar levels, and frost hardiness of ray parenchyma cells during frost acclimation and deacclimation in poplar (Populus ×canadensis Moench ‘robusta’) wood. Journal of Plant Physiology 149, 451–461. open url image1

Sperry JS (1993) Winter xylem embolism and spring recovery in Betula cordifolia, Fagus grandifolia, Abies balsamea and Picea rubens. In ‘Water transport in plants under climatic stress’. (Eds M Borghetti, J Grace, A Raschi) pp. 86–98. (Cambridge University Press: Cambridge)

Sperry JS (2000) Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104, 13–23.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sperry JS, Pockman WT (1993) Limitation of transpiration by hydraulic conductance and xylem cavitation in Betula occidentalis. Plant, Cell & Environment 16, 279–287.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sperry JS, Tyree MT (1990) Water stress induced xylem embolism in three species of conifers. Plant, Cell & Environment 13, 427–436.
Crossref | GoogleScholarGoogle Scholar | open url image1

Sperry JS, Holbrook NM, Zimmermann MH, Tyree MT (1987) Spring refilling of xylem vessels in wild grapevine. Plant Physiology 83, 414–417.
PubMed |
open url image1

Sperry JS, Stiller V, Hacke UG (2003) Xylem hydraulics and the soil-plant-atmosphere continuum: opportunities and unresolved issues. Agronomy Journal 95, 1362–1370. open url image1

Stiller V, Sperry JS, Lafitte HR (2005) Embolized conduits of rice (Oryza sativa L., Poaceae) refill despite negative xylem pressure. American Journal of Botany 92, 1970–1974.
Crossref | GoogleScholarGoogle Scholar | open url image1

Thompson MV (2006) Phloem: the long and the short of it. Trends in Plant Science 11, 26–32.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Thompson MV, Holbrook NM (2003) Scaling phloem transport: water potential equilibrium and osmoregolatory flow. Plant, Cell & Environment 26, 1561–1577.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tyree MT, Hammel HT (1972) The measurement of the turgor pressure and water relations of plants by the pressure bomb technique. Journal of Experimental Botany 23, 267–282.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tyree MT, Sperry JS (1988) Do plants operate near the point of catastrophic xylem dysfunction caused by dynamic water stress? Plant Physiology 88, 574–580.
PubMed |
open url image1

Tyree MT, Sperry JS (1989a) Characterization and propagation of acoustic emissions signals in woody plants: towards an improved acoustic emission counter. Plant, Cell & Environment 12, 371–382.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tyree MT, Sperry JS (1989b) The vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Molecular Biology 40, 19–38.
Crossref | GoogleScholarGoogle Scholar | open url image1

Tyree MT, Yang S (1992) Hydraulic conductivity recovery versus water pressure in xylem of Acer saccharum. Plant Physiology 100, 669–676.
PubMed |
open url image1

Tyree MT , Zimmermann MH (2002) ‘Xylem structure and ascent of sap.’ (Springer-Verlag: Berlin)

Tyree MT, Salleo S, Nardini A, Lo Gullo MA, Mosca R (1999) Refilling of embolized vessels in young of laurel. Do we need a new paradigm? Plant Physiology 120, 11–21.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Verslues PE, Agarwal M, Katyar-Agarwal S, Zhu J, Zhu JK (2006) Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant Journal 45, 523–539.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Vesala T, Holtta T, Peramaki M, Nikinmaa E (2003) Refilling of a hydraulically isolated embolized xylem vessel: model calculations. Annals of Botany 91, 419–428.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wan X, Steudle E, Hartung W (2004) Gating of water channels (aquaporins) in cortical cells of young corn roots by mechanical stimuli (pressure pulses): effects of ABA and of HgCl2. Journal of Experimental Botany 55, 411–422.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wang L, Wang YJ (2004) Application of high-intensity ultrasound and surfactants in rice starch isolation. Cereal Chemistry 81, 140–144.
Crossref | GoogleScholarGoogle Scholar | open url image1

Yang S, Tyree MT (1992) A theoretical model of hydraulic conductivity recovery from embolism with comparison to experimental data on Acer saccharum. Plant, Cell & Environment 15, 633–643.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zwieniecki MA, Holbrook NM (1998) Diurnal variation in xylem hydraulic conductivity in white ash (Fraxinus americana L.), red maple (Acer rubrum L.) and red spruce (Picea rubens Sarg.). Plant, Cell & Environment 21, 1173–1180.
Crossref | GoogleScholarGoogle Scholar | open url image1

Zwieniecki MA, Holbrook NM (2000) Bordered pit structure and vessel wall surface properties. Implications for embolism repair. Plant Physiology 123, 1015–1020.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zwieniecki MA, Melcher PJ, Holbrook NM (2001) Hydrogel control of xylem hydraulic resistance in plants. Science 291, 1059–1062.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zwieniecki MA, Melcher PJ, Field TS, Holbrook NM (2004) A potential role for xylem-pholem interactions in the hydraulic architecture of trees: effects of phloem girdiling on xylem hydraulic conductance. Tree Physiology 24, 911–917.
PubMed |
open url image1