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

Phloem as a possible major determinant of rapid cavitation reversal in stems of Laurus nobilis (laurel)

Sebastiano Salleo A , Patrizia Trifilò B and Maria A. 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 Botaniche, Università di Messina, Salita Sperone 31, 98166 Messina S. Agata, Italy.

C Corresponding author. Email: mlogullo@unime.it

Functional Plant Biology 33(11) 1063-1074 https://doi.org/10.1071/FP06149
Submitted: 14 June 2006  Accepted: 18 September 2006   Published: 1 November 2006

Abstract

Xylem recovery from embolism was studied in stems of Laurus nobilis L. that were induced to cavitate by combining negative xylem pressures with positive air pressures applied with a pressure collar. Xylem refilling was measured 2 and 20 min and 15 h after air pressure release in January, March and June when increasing percentages of wood parenchyma cells with high starch content (HSC-VAC) were counted (from 0% in January to 87.3% in June). In January, no xylem repair was measured. In June, stems refilled by 75% of previous conductivity loss with a parallel decrease of HSC-VAC. Xylem refilling was tested for stems with phloem either intact or excised by 20 and 50% and with phloem inactivated by girdling stems at both sides of the embolised segment. Stems with 50% of the cortex removed showed some recovery 15 h after embolism. Girdled stems did not recover from embolism and no starch depolymerisation was measured. Girdled stems where a radial mechanical pressure was applied for 20 min after embolism refilled in the same way as stems with intact phloem. Our conclusion is that phloem may export some signal for starch depolymerisation and this, in turn, would drive sugar efflux into embolised conduits with consequent osmotic water flows and refilling.

Keywords: cavitation, laurel, phloem, starch depolymerisation, xylem refilling.


Acknowledgments

This study was funded by the University of Messina (individual research funds 2004).


References


Alexandersson E, Scalbach G, Larsson C, Kjellbom P (2004) Arabidopsis plasma membrane proteomics identifies components of transport, signal transduction and membrane trafficking. Plant & Cell Physiology 45, 1543–1556.
CrossRef | PubMed |

Alves G, Sauter JJ, Julien JL, Fleurat-Lessard P, Améglio T, Guillot A, Pétel 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 |

Alves G, Améglio 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.
PubMed |


Ameglio T, Cruiziat P (1992) Tension / pressure alternation in walnut xylem sap during winter: the role of winter temperature. Comptes Rendus de l’Académie des Sciences III Sciences de la vie 315, 429–435.

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, 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 |


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 |


Antognoni F, Fornalè 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 |

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 |

Boyer JS, Silk WK (2004) Hydraulics of plant growth. Functional Plant Biology 31, 761–773.
CrossRef |

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 |

Canny MJ (1995) A new theory for he ascent of sap. Cohesion supported by tissue pressure. Annals of Botany 75, 343–357.
CrossRef |

Canny MJ (1997) Vessels contents during transpiration-embolisms and refilling. American Journal of Botany 84, 1223–1230.
CrossRef |

Canny MJ (1998a) Applications of the compensating pressure theory of water transport. American Journal of Botany 85, 897–909.
CrossRef |

Canny MJ (1998b) Transporting water in plants. American Scientist 86, 152–159.
CrossRef |

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.
PubMed |


Comstock JP (1999) Why Canny’s theory doesn’t hold water. American Journal of Botany 86, 1077–1081.
CrossRef | PubMed |

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 |

Esau K (1977) ‘Plant anatomy.’ (J Wiley and Sons: New York)

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

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 |


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 |

Gould N, Minchin PEH, Thorpe MR (2004) Direct measurements of sieve element hydrostatic pressure reveal strong regulation after pathway blockage. Functional Plant Biology 31, 987–993.
CrossRef |

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 |

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 |

Haddad Y, Clair-Maczulajtys D, Bory D (1995) Effects of curtain-like pruning on distribution and seasonal patterns of carbohydrate reserves in plane (Platanus acerifolia Wild) trees. Tree Physiology 15, 135–140.
PubMed |


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

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.
CrossRef | PubMed |

Just J, Sauter JJ (1991) Changes in hydraulic conductivity upon freezing of the xylem of Populus × canadensis Moench ‘robusta’. Trees 5, 117–121.
CrossRef |

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 49, 120–130.
CrossRef |

Lalonde S, Tegeder M, Throne-Holst M, Frommer WB, Patrick JW (2003) Phloem loading and unloading of sugars and amino acids. Plant, Cell & Environment 26, 37–56.
CrossRef |

Lo Gullo MA, Salleo S (1988) Different strategies of drought resistance in three Mediterranean sclerophyllous trees growing in the same environmental conditions. New Phytologist 108, 267–276.
CrossRef |

Lo Gullo MA, Salleo S (1991) Three different methods for measuring xylem cavitation and embolism: a comparison. Annals of Botany 67, 417–424.

Mayr S, Wolfschwenger M, Bauer H (2002) Winter-induced embolism in Norway spruce (Picea abies) at the Alpine timberline. Physiologia Plantarum 115, 74–80.
CrossRef | PubMed |

Milburn JA (1996) Sap ascent in vascular plants: challengers to the cohesion theory ignore the significance of immature xylem and the recycling of Münch water. Annals of Botany 78, 399–407.
CrossRef |

Milburn JA (1973) Cavitation studies on whole Ricinus plants by acoustic detection. Planta 112, 333–342.
CrossRef |

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 |

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

Pate JS , Jeschke WD (1995) The role of stems in transport, storage and circulation of ions and metabolites by the whole plant. In ‘Plant stems. Physiology and functional morphology’. (Ed. BL Gardner) pp. 177–204. (San Diego: Academic Press)

Peuke AD, Windt C, van As H (2006) Effect of cold-girdling on flows in the transport phloem in Ricinus communis: is mass flow inhibited? Plant, Cell & Environment 29, 15–25.
CrossRef |

Pignatti S (1982) ‘Flora d’Italia 2.’ (Edagricole: Bologna)

Pockman WT, Sperry JS (1997) Freezing-induced xylem cavitation and the northern limit of Larrea tridentate. Oecologia 109, 19–27.
CrossRef |

Pockman WT, Sperry JS (2000) Vulnerability to cavitation and the distribution of Sonoran desert vegetation. American Journal of Botany 87, 1287–1299.
CrossRef | PubMed |

Rolland F, Moore B, Sheen J (2002) Sugar sensing and signalling in plants. The Plant Cell 14, 185–205.

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 | PubMed |

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

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 |

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.
CrossRef |

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 stems. Plant, Cell & Environment 27, 1065–1066.
CrossRef |

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

Sauter JJ, Van Cleve B (1994) Storage, mobilization and interrelations of starch, sugars, protein and fat in the ray storage tissue of poplar trees. Trees 8, 297–304.
CrossRef |

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.

Sheikholeslam SN, Curier HB (1977) Phloem pressure differences and 14C assimilate translocation in Ecballium elaterium. Plant Physiology 59, 376–380.
PubMed |


Sovonic-Dunford S, Lee DR, Zimmerman M (1981) Direct and indirect measurements of phloem turgor pressure in white ash. Plant Physiology 68, 121–126.
PubMed |


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, UK)

Sperry JS (1995) Limitations on stem water transport and their consequences. In ‘Plant stems. Physiology and functional morphology’. (Ed. BL Gartner) pp. 105–121. (Academic Press: San Diego)

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

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


Sperry JS, Donnelly JR, Tyree MT (1988) A method for measuring hydraulic conductivity and embolism in xylem. Plant, Cell & Environment 11, 35–40.
CrossRef |

Stiller V, Sperry JS (1999) Canny’s compensating pressure theory fails a test. American Journal of Botany 86, 1082–1086.
CrossRef | PubMed |

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.

Thompson MV (2006) Phloem: the long and the short of it. Trends in Plant Science 11, 26–32.
CrossRef | PubMed |

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

Thompson MV, Holbrook NM (2004) Scaling phloem transport: information transmission. Plant, Cell & Environment 27, 509–519.
CrossRef |

Tretiach M (1993) Photosynthesis and transpiration of evergreen Mediterranean and deciduous trees in an ecotone during a growing season. Acta Oecologica 14, 341–360.

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 |


Tyree MT, Sperry JS (1989) The vulnerability of xylem to cavitation and embolism. Annual Review of Plant Physiology and Molecular Biology 40, 19–38.
CrossRef |

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

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.
CrossRef | PubMed |

Van Bel AJE (1990) Xylem-phloem exchange via the rays: the undervalued route of transport. Journal of Experimental Botany 41, 631–644.

Van Bel AJE (2003) The phloem, a miracle of ingenuity. Plant, Cell & Environment 26, 125–150.
CrossRef |

Vesala T, Hölttä T, Perämäki M, Nikinmaa E (2003) Refilling of a hydraulically isolated embolized xylem vessel: model calculations. Annals of Botany 91, 419–428.
CrossRef | PubMed |

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 | PubMed |

Wright JP, Fisher DB (1980) Direct measurement of sieve tube pressure using severed aphid stylets. Plant Physiology 65, 1133–1135.
PubMed |


Wu J, Lin L (2002) Elicitor-like effects of low-energy ultrasound on plant (Panax ginseng) cells: induction of plant defence responses and secondary metabolite production. Applied Microbiology and Biotechnology 59, 51–57.
CrossRef | PubMed |

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 |

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

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.
CrossRef |

Zwieniecki MA, Melcher PJ, Feild 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.
PubMed |








Rent Article (via Deepdyve) Export Citation Cited By (46)