Xylem Sap Flow As a Major Pathway for Oxygen Supply to the Sapwood Of

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Xylem Sap Flow As a Major Pathway for Oxygen Supply to the Sapwood Of Blackwell Science, LtdOxford, UKPCEPlant, Cell and Environment0016-8025Blackwell Science Ltd 2003? 2003 261118031814 Original Article Oxygen transport in the sapwood D. Gansert Plant, Cell and Environment (2003) 26, 1803–1814 Xylem sap flow as a major pathway for oxygen supply to the sapwood of birch (Betula pubescens Ehr.) D. GANSERT Institut für Ökologische Pflanzenphysiologie und Geobotanik, Universität Düsseldorf, Universitätsstraße 1, D-40225 Düsseldorf, Germany ABSTRACT Graham’s law of diffusion (Armstrong 1979; Grosse, Frye & Lattermann 1992; Grosse 1997). However, long-distance The role of xylem sap flow as an aqueous pathway for gaseous oxygen transport primarily takes places in the oxygen supply to the wood parenchyma of Betula pubes- intercellular gas-space continuum of the outer cortex sur- cens saplings was investigated. Using micro-optode sensors rounded by the phellogen (Hook et al. 1972), which has the oxygen status of the sapwood was quantified in relation been identified as a thermo-osmotically active partition in to mass flow of xylem sap. Sap flow was gradually reduced several tree species (Eschrich 1995; Grosse 1997). by an increasing oxygen depletion in the root space. The Radial gaseous diffusion of atmospheric oxygen across effect of sap flow on radial O transport between stem and 2 the cambial sheath towards the wood parenchyma can only atmosphere was assessed by a stoichiometrical approach be effective if continuity through cambium pores is main- between respiratory CO production and O consumption. 2 2 tained. In trees of Betula pendula Roth radial influx of Restriction of sap flow set in 36.5 h after the onset of O 2 oxygen into the sapwood has been suggested as a gaseous depletion, and was complete after 71 h. Interruption of sap pathway mainly effective at night, by which xylem sap will flow drastically increased the O deficit in the sapwood to 2 be enriched with dissolved oxygen (Gansert, Burgdorf & 70%. Sap flow contributed about 60% to the total oxygen Lösch 2001). With respect to species-specific wood anat- supply to the sapwood. Diurnal O flow rates varied 2 omy, oxygen supply to the various types of wood paren- between 3 and 6.3 nmol O m-2 leaf area (LA) s-1 during 2 chyma (Braun 1970; Grosser 1977; Schweingruber 1978; night- and daytime, respectively. Maximum O flow rates of 2 Eschrich 1995) principally depends on both the abundance 20 nmol O m-2 LA s-1 were reached at highest sap flow 2 of intercellular spaces and their effectiveness for gaseous rates of 5.7 mmol H O m-2 LA s-1. Sap flow not only 2 diffusion (i.e. the gaseous path), and xylem sap flow – the affected the oxygen status of the sapwood but also had an aqueous path – that primarily supports those parenchyma effect on radial O transport between stem and atmosphere. 2 strands that shield water transport from embolism and reg- ulate secretion of osmotica and hormones into the xylem Key-words: aquaporins; hypoxia; respiration; roots; sap sap. Oxygen concentrations measured in sapwood of differ- flow; stem heat balance. ent anatomical structure and metabolic activity vary over a broad range from pronounced hypoxia to near saturation INTRODUCTION (Eklund 1990, 1993, 2000; Gansert et al. 2001; Del Hierro et al. 2002; Mancuso & Marras 2003). It has long been recognized that the transpiration stream New types of miniaturized, high-sensitive oxygen sensors plays a vital role in aeration of living tissues surrounded by allow improved quantitative analyses of the oxygen status the cambium of woody plants (Bailey 1913; Haberlandt and oxygen flow rates in different compartments of the 1914). The importance of xylem sap flow for oxygen supply woody cormus on a high-resolution time scale. Previous to and removal of carbon dioxide from parenchymatous efforts on the measurement of oxygen concentrations in tissues of the sapwood was clearly recognized by Bailey the sapwood by use of these sensors focused on the preclu- (1913) when he stated that the xylem of arborescent plants sion from interference with atmospheric oxygen, and main- has an important function for transport of gases dissolved tenance of xylem sap flow by avoidance of embolism. Thus, in water from the roots to the cambium and leaves. Axial underwater access to the sapwood was used as a methodi- oxygen transport in flood-tolerant plant species from aerial cal approach for in situ measurements of diurnal and sea- parts to the roots has been a subject of broad interest sonal variations of endogenous oxygen concentrations in (Hook, Brown & Wetmore 1972) with special reference to woody plants (Gansert et al. 2001). This approach may con- physical processes involved in gaseous diffusion of oxygen tribute to identifying circumstances and metabolic depen- through intercellullar gas-spaces such as thermo-osmosis or dencies that are responsible for the different oxygen status of plant shoots under varying ontogenetic, environmental, Correspondence: D. Gansert. Fax: +49 211 81 13335; e-mail, and seasonal conditions. Using the new type of micro- [email protected] optode oxygen sensors, the purpose of this study was: (1) © 2003 Blackwell Publishing Ltd 1803 1804 D. Gansert to investigate the role of xylem sap flow as an aqueous interference in CO2 and O2 gas exchange due to bark pho- pathway for oxygen supply to the sapwood parenchyma tosynthesis, all internodes and the cuvettes were shielded of young mountain birch (Betula pubescens Ehr.); (2) to from light by strips of black silk cloth wrapped around the quantify its effect on the oxygen status of the sapwood; and woody plant parts. The data of all microclimatic variables (3) to evaluate the potential effect of xylem sap flow on were synchronously recorded at 10 s intervals and averaged oxygen transport between stem and atmosphere during over 5 min intervals by data loggers (Squirrel 1250 series; stem respiration. Grant Instruments Ltd, Barrington Cambridge, UK). MATERIALS AND METHODS Cuvettes for measuring stem gas exchange The experimental set-up Cuvettes for the measurement of O2 and CO2 gas exchange between ambient air and the stem were made out of In early June 2002, two potted plants of 5-year-old field- Plexiglass as shown schematically (Fig. 2). Each cuvette grown B. pubescens saplings about 1.7 m tall were brought consisted of two semi-cylinders (wall thickness =5 mm, into a climate chamber and preconditioned to the experi- thickness of top and bottom =6 mm) which enclosed a stem mental light and temperature regime for 10 d. The soil sub- internode of up to 8 mm in diameter and 20 mm in length. strate was natural loess (volume = 8.3 ¥ 10-3 m3) in which A rubber seal fixed in a groove (2 mm wide, 1.5 mm deep) the roots grew undisturbed for 1 year. In order to sim- along the plane side of one semi-cylinder ensured a leak- ulate a near-daylight spectrum, HRI-T 400 W/D lamps proof seal when both semi-cylinders were pressed onto (Radium; Osram, München, Germany) were used as the each other by two steel strings. Silicon rubber (Loctite no. light source during a 13 h day period (0700 to 2000 h). 5910; Loctite GmbH, München, Germany) was used to Prevention of upper crown parts from excessive warming seal the remaining gap between the stem and the cuvette. was achieved by insertion of a glass pane (4 mm thick) 8 cm Each cuvette was equipped with four Plexiglass tubes beneath the light unit. Horizontal air ventilation between (dout = 10 mm, l = 62 mm) with different inner diameters to the lamps and the glass pane efficiently reduced the effect be connected to different gas analysing instruments. The of excessive heat production on leaf gas exchange. Thus, air cuvette being used for O2 measurements was sealed from temperature measured at 27 cm beneath the lamps fluctu- ambient air by insertion of a silicon septum (3 mm thick) ated between 21 and 23 ∞C during night-time and between into each Plexiglass tube. The one being used for CO2 mea- 23 and 27 ∞C during daytime. Because air ventilation surements was run in a permanent open airflow modus (see started about 30 min prior to the onset of light a drop in air below). temperature of 2–3 ∞C always marked the end of the night. Each pot was packed in a polyethylene bag leaving the top open, and immersed in the water bath of a cryostat O2 cuvette (Type MC5S0; Colora Messtechnik GmbH, Lorch, Ger- The concentrations of molecular oxygen were simulta- many). In each pot three copper–constantan thermocouples neously measured both, in the cuvette atmosphere 3 were inserted at different soil depths (7, 13 and 17 cm from (Vair = 5.28 cm ), and in the aqueous phase of the sapwood the surface) 8 cm radially off the stem base. A mean soil at a depth of 2.9 mm from the stem surface. Measurements temperature of 17 ± 0.3 ∞C at a depth of 13 cm was main- of molecular oxygen were performed by fibre-optical tained by permanent temperature control of the water baths. micro-optode sensors (see below). Two opposite tubes were Figure 1 presents the experimental set-up for both trees used as mechanical guides for the plastic syringes and the schematically. Air temperature and relative humidity were attached cannulae that penetrated through the silicon simultaneously measured at 27 and 95 cm beneath the lamps septa. The third tube was filled with soda lime as the CO2 by use of two Vaisala sensors (HMP 35 A; Vaisala, Helsinki, absorbent (Fig. 2). Thereby, during the experiments total Finland). Photosynthetic photon flux density (PPFD) was pressure in the O2 cuvette remained near constant at atmo- measured at half crown length, 55 cm beneath the lamps by spheric pressure because an increase of CO2 partial pres- use of three sensors (SKP 215; Skye Instruments Ltd, Llan- sure due to continuous CO2 efflux from the stem, was drindod Wells, Powys, UK) which were evenly positioned compensated by an equivalent chemical binding of CO2.
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