Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology

Starch-to-sugar conversion in wood parenchyma of field-growing Laurus nobilis plants: a component of the signal pathway for embolism repair?

Sebastiano Salleo A , Patrizia Trifilò B , Sara Esposito B , Andrea Nardini A and Maria A. Lo Gullo B C

A Dipartimento di Scienze della Vita, Università di Trieste, Via L. Giorgieri 10, 34127 Trieste, Italia.

B Dipartimento di Scienze della Vita, ‘M. Malpighi’ sezione Botanica, Università di Messina, Salita Sperone 31, 98166 Messina, S. Agata, Italia.

C Corresponding author. Email:

Functional Plant Biology 36(9) 815-825
Submitted: 7 May 2009  Accepted: 19 July 2009   Published: 3 September 2009


The ability of stems of Laurus nobilis (L.) to refill embolised xylem conduits was studied in plants both at optimal water supply (W) and under conditions of soil drought inducing xylem pressures (Px) of –1.54 (S1) and –2.35 MPa (S2). Starch depolymerisation in wood parenchyma was measured as percentage of cells ‘with high starch content’ (HSC-cells) counted under a microscope. HSC-cells decreased during embolism and increased again in refilled stems. A direct relationship was found between percentage of HSC-cells and Px, with HSC-cells between 65 and 75% of the total at Px ≥ –0.6 MPa, at which recovery from PLC was recorded. At low transpiration, starch re-appeared in wood parenchyma cells but only in plants that showed diurnal stomatal opening (W- and S1-plants). In S2-plants showing diurnal stomatal closure and nocturnal opening with Px between –1.2 to –2.4 MPa, HSC-cells were only 25% and plants did not recover from PLC. This finding suggests that (i) the Px threshold for embolism repair was ≥ –0.6 MPa, and (ii) impeded phloem loading limits starch content in wood parenchyma and embolism repair. We conclude that starch depolymerisation acts as a signal to phloem unloading sugars to embolised conduits thus generating the necessary osmotic gradients driving refilling.

Additional keywords: embolism repair, Laurus nobilis, starch-to-sugar conversion, transpiration, xylem pressures.


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 doi:10.1078/0176-1617-00503

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

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

Ameglio T 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

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

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 17555 17558

Braun HJ (1970) Funktionelle Histologie der sekundären Sprossachse. In ‘Encyclopedia of plant anatomy’, 2nd edn. (Eds W Zimmermann, P Ozenda, HD Wulff) pp. 1–190. (Gebrüder Borntraeger: Berlin, Germany)

Braun HJ 1984 The significance of the accessory tissues of the hydrosystem for osmotic water shifting as the second principle of water ascent, with some thoughts concerning the evolution of trees. The IAWA Bulletin 5 275 294

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

Canny MJ 1995 A new theory for the ascent of sap. Cohesion supported by tissue pressure. Annals of Botany 75 343 357 doi:10.1006/anbo.1995.1032

Canny MJ 1997 Vessels contents during transpiration-embolisms and refilling. American Journal of Botany 84 1223 1230 doi:10.2307/2446046

Canny MJ 1998 a Applications of the compensating pressure theory of water transport. American Journal of Botany 85 897 909 doi:10.2307/2446355

Canny MJ 1998 b Transporting water in plants. American Scientist 86 152 159

Canny MJ 2001 Embolism and refilling in the maize leaf lamina, and the role of the protoxylem lacuna. American Journal of Botany 88 47 51

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 doi:10.1071/FP06210

Cochard H Tyree MT 1990 Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiology 6 393 407

Cochard H Ewers FW Tyree MT 1994 Water relations of a tropical vine-like bamboo (Rhipidocladum racemiflorum): root pressures, vulnerability to cavitation and seasonal changes in embolism. Journal of Experimental Botany 45 1085 1089

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 doi:10.1104/pp.124.3.1191

Comstock JP 1999 Why Canny’s theory doesn’t hold water. American Journal of Botany 86 1077 1081 doi:10.2307/2656968

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 doi:10.1046/j.1365-3040.2003.00930.x

Decourteix M Alves G Brunel N Ameglio T Guillot A Lemoine R Pe’tel 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 doi:10.1111/j.1365-3040.2005.01398.x

Ewers FW Cochard H Tyree MT 1997 A survey of root pressures in vines of a tropical lowland forest. Oecologia 110 191 196 doi:10.1007/s004420050149

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

Facette MR McCully ME Shane MW Canny MJ 2001 Measurements of the time to refill embolized vessels. Plant Physiology and Biochemistry 39 59 66

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 doi:10.1086/297412

Fromm J Lautner S 2007 Electrical signals and their physiological significance in plants. Plant, Cell & Environment 30 249 257 doi:10.1111/j.1365-3040.2006.01614.x

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 doi:10.1111/j.1365-3040.2006.01570.x

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 doi:10.1111/j.1399-3054.2006.00848.x

Grace J (1993) Refilling of embolized xylem. In ‘Water transport in plants under climatic stress’. (Eds M Borghetti, J Grace, A Raschi) pp. 51–62. (Cambridge University Press: Cambridge, UK)

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 doi:10.1007/BF00330005

Hacke UG Sperry JS 2000 Drought experience and cavitation resistance in six desert shrubs of the Great Basin, Utah. Basic and Applied Ecology 1 31 41 doi:10.1078/1439-1791-00006

Hacke UG Sperry JS 2003 Limits to xylem refilling under negative pressure in Laurus nobilis and Acer negundo. Plant, Cell and Environment 26 303 311 doi:10.1046/j.1365-3040.2003.00962.x

Hacke UG , Sperry JS (2005) Water transport in plants. In ‘Molecular plant physiology’. (Ed. R Sharma) (Haworth Press: New York)

Holbrook NM Zwieniecki MA 1999 Embolism repair and xylem tension: do we need a miracle? Plant Physiology 120 7 10 doi:10.1104/pp.120.1.7

Holbrook NM Ahrens ET Burns MJ Zwieniecki MA 2001 In vivo observation of cavitation and embolism repair using magnetic resonance imaging. Plant Physiology 126 27 31 doi:10.1104/pp.126.1.27

Jaquish LL Ewers FW 2001 Seasonal conductivity and embolism in the roots and stems of two clonal ring-porous trees, Sassafras albidum (Laureaceae) and Rhus typhina (Anacardiaceae). American Journal of Botany 88 206 212 doi:10.2307/2657011

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 doi:10.1046/j.1365-3040.1997.d01-34.x

Läuchli A 1972 Translocation of inorganic solutes. Annual Review of Plant Physiology 23 197 218 doi:10.1146/annurev.pp.23.060172.001213

Lee SJ Kim Y 2008 In vivo visualization of the water-refilling process in xylem vessels using X-ray micro-imaging. Annals of Botany 101 595 602 doi:10.1103/PhysRevLett.98.186805

Lo Gullo MA Salleo S 1988 Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. The New Phytologist 108 267 276 doi:10.1111/j.1469-8137.1988.tb04162.x

Mayr S Wolfschwenger M Bauer H 2002 Winter-induced embolism in Norway spruce (Picea abies) at the Alpine timberline. Physiologia Plantarum 115 74 80 doi:10.1034/j.1399-3054.2002.1150108.x

McCully ME Canny MJ Huang CX 2009 Cryo-scanning electron microscopy (CSEM) in the advancement of functional plant biology. Morphology and anatomical applications. Functional Plant Biology 36 97 124 doi:10.1071/FP08304

Melcher PJ Goldstein G Meinzer FC Yount DE Jones TJ Holbrook NM Huang CX 2001 Water relations of coastal and estuarine Rhizophora mangle: xylem pressure potential and dynamics of embolism formation and repair. Oecologia 126 182 192 doi:10.1007/s004420000519

Milburn JA 1973 Cavitation in Ricinus by acoustic detection: induction in excised leaves by various factors. Planta 110 253 265 doi:10.1007/BF00387637

Milburn JA 1996 Sap ascent in vascular plants: challengers to the cohesion theory ignore the significance of immature xylem and the recycling of Munch water. Annals of Botany 78 399 407 doi:10.1006/anbo.1996.0135

Nardini A Salleo S 2000 Limitation of stomatal conductance by hydraulic traits: sensing or preventing water cavitation? Trees – Structure and Function 15 14 24

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

Passioura J 2006 Increasing crop productivity when water is scarce-from breeding to field management. Agricultural Water Management 80 176 196 doi:10.1016/j.agwat.2005.07.012

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

Salleo S , Lo Gullo MA (1993) Drought resistance strategies and vulnerability to cavitation of some Mediterranean sclerophyllous trees. In ‘Water transport in plants under climatic stress’. (Eds M Borghetti, J Grace, A Raschi) pp. 99–113. (Cambridge University Press: Cambridge)

Salleo S Hinckley TM Kikuta SB Lo Gullo MA Weilgony P Myung Yoon T Richter H 1992 A method for inducine xylem emboli in situ: experiments with a field grown tree. Plant, Cell & Environment 15 491 497

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. The New Phytologist 132 47 56 doi:10.1111/j.1469-8137.1996.tb04507.x

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 1076 doi:10.1111/j.1365-3040.2004.01211.x

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 doi:10.1071/FP06149

Salleo S Trifilo P Lo Gullo MA 2008 Vessel wall vibrations: trigger for embolism repair? Functional Plant Biology 35 289 297 doi:10.1071/FP07239

Sauter JJ 1966 Investigations on the physiology of the woody rays of poplar. I. The seasonal changes in starch content in the ray parenchyma. Zeitschrift für Pflanzenphysiologie 55 246 258

Sauter JJ 1980 Seasonal variation of sucrose content in the xylem sap of Salix. Zeitschrift für Pflanzenphysiologie 98 377 391

Sauter JJ Iten W Zimmermann MH 1973 Studies on the release of sugar into the vessels of sugar maple (Acer saccharum). Canadian Journal of Botany 51 1 8

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

Sperry JS (1993) Winter embolism and spring recovery in Betula cordifolia, Fagus grandifolia, Abies balsamifera, and Picea rubens. In ‘Water transport in plants under climatic stress’. pp. 86–98. (Cambridge University Press: Cambridge, UK)

Sperry JS 2000 Hydraulic constraints on plant gas exchange. Agricultural and Forest Meteorology 104 13 23

Sperry JS Holbrook NM Zimmermann MH Tyree MT 1987 Spring filling of xylem vessels in wild grapevine. Plant Physiology 83 414 417 doi:10.1104/pp.83.2.414

Sperry JS Hacke UG Wheeler JW 2005 Comparative analysis of end wall resistance in xylem conduits. Plant, Cell & Environment 28 456 465 doi:10.1111/j.1365-3040.2005.01287.x

Stiller V Sperry JS 1999 Canny’s compensating pressure theory fails a test. American Journal of Botany 86 1082 1086 doi:10.2307/2656969

Stiller V Lafitte HR Sperry JS 2003 Hydraulic properties of rice and the response of gas exchange to water stress. Plant Physiology 132 1698 1706 doi:10.1104/pp.102.019851

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 doi:10.3732/ajb.92.12.1970

Taneda H Sperry JS 2008 A case study of water transport in co-occurring ring- vs. diffuse-porous trees: contrasts in water status, conducting capacity, cavitation, and vessel refilling. Tree Physiology 28 1641 1651

Thompson MV 2006 Phloem: the long and the short of it. Trends in Plant Science 11 26 32

Thompson MV Holbrook NM 2003 Scaling phloem transport: water potential equilibrium and osmoregolatory flow. Plant, Cell & Environment 26 1561 1577 doi:10.1046/j.1365-3040.2003.01080.x

Trifilò P Gascó A Raimondo F Nardini A Salleo S 2003 Kinetics of recovery of leaf hydraulic conductance and vein functionality from cavitation-induced embolism in sunflower. Journal of Experimental Botany 54 2323 2330 doi:10.1093/jxb/erg259

Tyree MT Cochard H 1996 Summer and winter embolism in oak: impact on water relations. Annales des Sciences Forestieres 53 173 180 doi:10.1051/forest:19960201

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 doi:10.1104/pp.88.3.574

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 doi:10.1146/annurev.pp.40.060189.000315

Tyree MT Yang S 1992 Hydraulic conductivity recovery versus water pressure in xylem of Acer saccharum. Plant Physiology 100 669 676 doi:10.1104/pp.100.2.669

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

Tyree MT Alexander J Machado JL 1992 Loss of hydraulic conductivity due to water stress in intact juveniles of Quercus rubra and Populus deltoides. Tree Physiology 10 411 415

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 22

Van Bel AJE 1990 Xylem-phloem exchange via the rays: the undervalued route of transport. Journal of Experimental Botany 41 631 644 doi:10.1093/jxb/41.6.631

Van Bel AJE 2003 The phloem, a miracle of ingenuity. Plant, Cell & Environment 26 125 149 doi:10.1046/j.1365-3040.2003.00963.x

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 doi:10.1093/jexbot/51.345.769

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. The Plant Journal 45 523 539 doi:10.1111/j.1365-313X.2005.02593.x

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 doi:10.1093/aob/mcg022

Wheeler JW Sperry JS Hacke UG Hoang N 2005 Inter-vessel pitting and cavitation in woody Rosaceae and other vesseled plants: a basis for a safety vs. efficiency trade-off in xylem transport. Plant, Cell & Environment 28 800 812 doi:10.1111/j.1365-3040.2005.01330.x

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 doi:10.1046/j.1365-3040.1998.00342.x

Zwieniecki MA Holbrook NM 2000 Bordered pit structure and vessel wall surface properties. Implications for embolism repair. Plant Physiology 123 1015 1020 doi:10.1104/pp.123.3.1015

Zwieniecki MA Hutyra L Thompson MV Holbrook NM 2000 Dynamic changes in petiole specific conductivity in red maple (Acer rubrum L.), tulip tree (Liriodendron tulipifera L.) and northern fox grape (Vitis labrusca L.). Plant, Cell & Environment 23 407 414 doi:10.1046/j.1365-3040.2000.00554.x

Zwieniecki MA Melcher PJ Holbrook NM 2001 Hydrogel control of xylem hydraulic resistance in plants. Science 291 1059 1062 doi:10.1126/science.1057175

Zwieniecki MA Thompson MV Holbrook NM 2003 Understanding the hydraulics of porous pipes: tradeoffs between water uptake and root length utilization. Journal of Plant Growth Regulation 21 315 323 doi:10.1007/s00344-003-0008-9

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 girdling on xylem hydraulic conductance. Tree Physiology 24 911 917

Export Citation Cited By (62)