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. 2005 Jan 11;95(4):641–648. doi: 10.1093/aob/mci059

Extension Growth of Impatiens glandulifera at Low Irradiance: Importance of Nitrate and Potassium Accumulation

M ANDREWS 1,*, H G MAULE 1, J A RAVEN 2, A MISTRY 1
PMCID: PMC4246850  PMID: 15644384

Abstract

• Background and Aims The summer annual Impatiens glandulifera can reach 3 m in height within deciduous woodland. The primary objective was to determine if Inline graphic accumulation, and hence its osmotic effect, is an important physiological mechanism allowing Impatiens to achieve substantial height under low irradiance.

• Methods Stem extension, concentrations of K+ and Inline graphic in leaves and concentrations of K+, Inline graphic and other inorganic anions, malate, sugars, total N and total osmoticum in stem were measured in I. glandulifera sampled at different irradiance levels in deciduous woodland and in a glasshouse. Also, the energetic costs, as absorbed photons, of generating osmolarity in stem cell vacuoles with KNO3, K2malate or hexose sugar were determined.

• Key Results Results were similar in the woodland and glasshouse. At 50–100 % relative irradiance (Ir; open ground PAR = 100 % Ir) and 2–10 % Ir, plant height increased from 7–14 cm to 130–154 cm in 64–67 d. Leaf and stem Inline graphic concentrations were negligible at 50–100 % Ir while K+, malate2− and sugars, respectively, accounted for 33·2–50·1 %, 19·3–20·8 % and 2·0–2·6 % of total osmoticum in stems. At 2–10 % Ir, Inline graphic concentrations were four to eight times greater in stems than leaves. Here, Inline graphic constituted 26·7–34·3 % of the total osmotic concentration in the stem and Inline graphic constituted 69–81 % of total N in stem tissue. Also at 2–10 % Ir, K+ comprised 44·9–45·9 % and malate plus sugars 2·2–3·1 % of total osmotic concentration. The energy cost of osmoticum as KNO3 was calculated as less than half that of malate and less than one-seventh that for hexose. Further calculations suggest that use of KNO3, K2malate or glucose as osmoticum at low irradiance would, respectively, cost approx. 7 %, 16 % and 50 % of the total construction cost of the stem.

• Conclusions It is concluded that accumulation of Inline graphic in place of organic molecules in stems is an important mechanism allowing I. glandulifera to achieve substantial height at low irradiance.

Keywords: Impatiens glandulifera, extension growth, nitrate, potassium, malate, glucose, osmoticum, shade acclimation, photon costs

INTRODUCTION

Nitrate (Inline graphic) is an important form of nitrogen (N) taken up and assimilated by many higher plant species in a wide range of habitats (Raven et al., 1992). Depending on plant genotype and environmental conditions, Inline graphic taken up from the soil can be assimilated or accumulated/stored in the root or transported to the shoot where it is assimilated or accumulated/stored; evidence indicates that there is little transport of Inline graphic from shoot to root (Andrews et al., 2004). Generally, N is the major soil nutrient factor limiting plant growth and the major proportion of Inline graphic taken up by plants is rapidly assimilated to amino acids. However, for some species, under conditions in which photosynthesis is reduced, such as low irradiance, Inline graphic can be an important osmoticum in leaves, taking the place of organic molecules, in particular, organic acids (mainly malate) and sugars (mainly glucose) (Raven et al., 1980; Blom-Zandstra and Lampe, 1985; Steingröver, 1986; Lieffering et al., 1996; McIntyre, 1997).

Impatiens glandulifera Royle (hereafter referred to as Impatiens) is a herbaceous summer-annual species native to the Himalayas which was introduced into several European countries in the 19th century and which is now widespread throughout north-western Europe (Beerling, 1993; Beerling and Perrins, 1993; Pysek and Prach, 1995). Impatiens occurs primarily in riparian habitats, fens, mesotrophic grassland and deciduous woodland and is more common in nutrient/nitrogen-rich soils, although it does occur in nutrient/nitrogen-poor soils (Ellenberg, 1992; Beerling and Perrins, 1993; Pysek and Prach, 1995; Maule et al., 2000). Once established, it tends to produce dense stands after the ‘synchronous’ germination of a large seed bank in spring. Impatiens is the tallest annual in Europe and often reaches 2 m in height (Perrins et al., 1990; Stace, 1991; Pysek and Prach, 1995). It shows fast extension growth. For example, it can reach approx. 1·3 m in height in 72 d from an air-dry seed weight of 2–35 mg (Perrins et al., 1990; Beerling and Perrins, 1993).

Maule et al. (2000) determined the major environmental correlates of the distribution and biomass of Impatiens in a deciduous woodland and the effect of Impatiens on native species within the woodland. Quadrats within the woodland were sampled for soil water, organic matter, pH and plant available N, phosphorus and potassium (K) concentration, irradiance, total plant biomass and biomass of Impatiens. There was a strong positive correlation between total plant biomass and irradiance, and it was argued that irradiance is likely to be the primary factor limiting total plant biomass in the woodland. Impatiens was the dominant plant species in the woodland interior often attaining a height of approx. 3 m at maturity, which is greater than that usually quoted as the maximum for this species (Perrins et al., 1990; Stace, 1991; Pysek and Prach, 1995). Tree species were not found in dense stands of Impatiens. Clearing of dense stands of Impatiens in the wood interior resulted in an increase in native herbaceous, shrub and tree species, indicating that under some conditions, Impatiens can suppress woodland regeneration. The ability of Impatiens to achieve substantial growth at low irradiance levels is likely to be a key factor in its success as a weed in deciduous woodland.

The present study on Impatiens focuses on individual plants. Stem extension, dry matter partitioning between leaf and stem, concentrations of K+ and Inline graphic in leaves and concentration of K+, Inline graphic and other inorganic anions, malate2−, sugars, total N and total osmoticum in the stem were measured in Impatiens sampled at different irradiance levels in deciduous woodland or grown under different irradiance under glasshouse conditions. Also, the energetic costs, as absorbed photons, of generating osmolarity in stem cell vacuoles with KNO3, K2malate or hexose sugar were determined. The primary objective of the study was to determine if Inline graphic accumulation, and hence its osmotic effect, is an important physiological mechanism allowing Impatiens to achieve substantial height under low irradiance conditions.

MATERIALS AND METHODS

Field studies

Field studies 1 and 2 were carried out at Thornley Wood Nature Reserve, Gateshead, Tyne and Wear, England (field site 1; national grid ref. NZ 178601). Impatiens has been present in the reserve for at least 25 years. The initial field study was carried out from 30 June to 2 July 1996 on a site with a canopy of primarily Alnus glutinosa (L.) Gaertner and a sparse shrub layer. Three 20-m transects were set up at 10-m intervals running from a pasture edge into the woodland. Thirty 0·25-m2 quadrats were laid at 2-m intervals along the transects and Impatiens plants counted. Shoots of three plants were sampled from each quadrat for individual plant measurements. The remaining Impatiens shoots in the quadrat were removed for biomass determination. All plants were kept in polythene bags on ice until processed in the laboratory that day.

Irradiance at each quadrat was determined using two Delta-T MV2 microvolt integrators (Delta-T Devices Ltd, Cambridge, UK) fitted with Skye SKP 211 M quantum sensors (Skye Instruments Ltd, Powys, UK). Readings were taken simultaneously in the open and at each quadrat from 1200 to 1500 h on fine days within 7 d of sampling. Open ground PAR was defined as 100 % relative irradiance (Ir).

Bulk shoots sampled for biomass determination were dried at 70 °C then weighed. With respect to the individual shoots sampled, height of the main stem was determined. These shoots were then separated into leaf and stem tissue, weighed, dried at 70°C for 96 h and reweighed. The dried material was ground prior to determination of its Inline graphic and K+ concentration. For six plants sampled at 85–100 % Ir and six at 2–3 % Ir, total N concentration in stem tissue was determined.

Field study 2 was initiated in late April 1998, shortly after the Impatiens emergence flush. Three 4-m2 quadrats were established at high irradiance (>80 % Ir) sites and three at low irradiance sites (5–10 % Ir) in areas of the woodland with dense cover of Impatiens. Whole shoots of three plants from each quadrat were sampled on 7 May and 13 July 1998 and their height and dry weight (d. wt) determined. For plants sampled on 13 July, fresh stem was analysed for total solute concentration. The remaining plant material was used for determination of the dry weight of leaf and stem and the concentrations of K+, Inline graphic, chloride (Cl−), sulphate (Inline graphic), phosphate (Inline graphic), malate, sugars (glucose, fructose and sucrose), total N and total osmoticum in stem.

Field study 3 was carried out on 26 July 2001 in woodland at the Durham College of Agriculture and Horticulture, Durham, England (field site 2, national grid ref. NZ 284412). Six pairs of plants were sampled at low irradiance sites (2–10 % Ir). Shoot height was determined, then fresh stem was analysed for total solute, and all ions and sugars measured in field study 2. The remaining plant material was used for determination of leaf and stem dry weight. Stem material was then ground and its total N concentration determined.

Glasshouse experiment

Seeds were collected in late summer 2001 from plants at field site 2. These seeds were air dried at room temperature for 24 h then stored in airtight jars at 4 °C until used in the experiment in 2002. The experiment was carried out in a glasshouse from 26 May to 29 July. The temperature in the glasshouse was maintained above 15 °C. Prior to the experiment, seeds were wet chilled at 4 °C for 10 weeks then transferred to seed trays containing moist perlite in the glasshouse. Once the seedlings had reached a late cotyledon/early first true leaves stage (approx. 2 weeks) similar sized seedlings were transferred to 5-dm3 pots (one per pot) containing a vermiculite/perlite (1 : 1) mixture soaked with basal nutrient solution (Andrews et al., 1989) containing 1 mol m−3 Inline graphic as KNO3. The rooting medium was flushed with the nutrient solution every 2 d for 1 week at which point the first true leaves were approximately half fully expanded. Six plants were harvested and their dry weight and height determined. The remaining plants were then exposed to 55 % Ir (high irradiance) or 6 % Ir (low irradiance) and supplied 5·0 mol m−3 Inline graphic throughout the experiment. The irradiance level in the glasshouse was approx. 55 % that in the open and was the high irradiance treatment. The 6 % Ir treatment was obtained by using layers of shade cloth covering 2-m-high wooden frames. There were five replicates of each irradiance treatment with three plants per replicate treatment. All pots were flushed with nutrient solution every 2 d. At harvest, measurements were carried out as in field study 3.

Plant tissue analysis

In field studies 1 and 2, leaf and stem Inline graphic concentration was determined in aqueous extracts of 0·01–0·025 g of dried ground material as described in Mackereth et al. (1978). Potassium concentration in leaf and stem was determined from the same extracts using a Jenway PFP7 flame photometer (Jenway, Essex, UK). In field study 2, Cl−, Inline graphic, Inline graphic, malate, glucose, fructose and sucrose were measured in aqueous extracts of 0·1–0·15 g of dried ground material with a DX500 ion chromatograph system (Dionex, Sunnyvale, CA, USA) using the manufacturer's standard methods. These ions and sugars were determined along with Inline graphic and K+ in the aqueous extracts of 0·5–1·0 g fresh material used in determining total solute concentration in field study 3 and the glasshouse experiment. In all cases, total solute concentrations in stems were determined on aqueous extracts of 0·5–1·0 g fresh material with a CAMLAB (Cambridge, UK) MOD 200 micro-osmometer. In the initial and final field studies and glasshouse experiment, total N concentration of stem was determined in 0·5–1·0 mg samples of dried ground material using a Carlo-Erba 1106 CHN Elemental Analyser (Strumentazione, Milan, Italy).

Energy costs of different osmotica

The energy costs of the transport of inorganic osmotica, and of the synthesis and transport of organic osmotica, were computed from the stoichiometries of the photon costs of photosynthesis, and of the energetics of respiration, membrane transport and intermediary metabolism. The general approach was that used by Raven (1985), but with more recent parameterizations from the references cited in Tables 2–4.

Table 2.

Energetics of use of KNO3 (or KCl) as an osmoticum in plant stem cell vacuoles

Energy-requiring process
 Mechanism
 Energy cost
 Reference
Uptake of 1 mole KNO3 into root cell symplast Uptake of K+ by 1 K+/H+ symport, Inline graphic by 2H+ : 1 Inline graphic symport. H+ gradient generated by P ATPase, 1 H+ per ATP 3 ATP to pump 3H+ out of cells, re-enter with 1 KNO3 Bloom et al. (1992); Buchanan et al. (2000); Williams and Miller (2001)
Transfer of 1 mole KNO3 from root symplast to xylem conduit Flux of K+ and Inline graphic from root symplast to xylem via ion channels None Bloom et al. (1992); Buchanan et al. (2000); de Boer and Volkov (2003)
Uptake of 1 mole KNO3 from xylem to stem cell symplast As for uptake into root cell symplast 3 ATP Bloom et al. (1992); Buchanan et al. (2000); Williams and Miller (2001)
Transfer of 1 mole KNO3 from stem cellsymplast to vacuole 1 H+ : 1 K+ antiport, 1 H+ : 1 Inline graphic antiport; H+ gradient generated by V ATPase; 2 H+ per ATP 1 ATP Buchanan et al. (2000); Maeshima (2001)
Production of 7 ATP (rows 1–4) by oxidativephosphorylation Glycolysis; oxidative phosphorylation with 2·33 ADP phosphorylated per NADH oxidized by 1/2 O2 (10 H+ pumped per NADH oxidized); 4·33 H+ used to phosphorylate 1 ADP in the matrix, and move the ATP to the cytosol Respiration of 1·5 (CH2O) Buchanan et al. (2000); Nicholls and Ferguson (2002)
Movement of 1·5 (CH2O) (row 5) as sucrose from leaf cytosol to cytosol of root or stem Sucrose loading into phloem using 1 H+ (≡1 ATP) per sucrose. Symplasmic unloading into root and stem symplast (no ATP). 1/12 ATP per (CH2O) 0·026 (CH2O) Van Bel (1992); Patrick (1997); Buchanan et al. (2000); Nicholls and Ferguson (2002)
Total (CH2O) cost (sum of rows 5 and 6) Sum of respiration of (CH2O) in cytosol of root and stem, (CH2O) used in moving this (CH2O) from leaf cytosol to stem and root cytosol 1·526 (CH2O)
Absorbed photon cost to produce 1·526 (CH2O) (from row 7) as sucrose in leaf cytosol 13 mole photons per mole CO2 converted to (CH2O), assuming 4·67 ATP, 3·0 NADPH per CO2 fixed into (CH2O) in C3 plants, and 3H+ per electron transferred in non-cyclic electron transport, 4 H+ per electron transferred in cyclic electron transport; 4·67 H+ per ADP phosphorylated, 2 photons per electron in non-cyclic, electron transport, 1 photon per electron in cyclic electron transport 19·84 mole photons per 1·526 mole (CH2O), equals 1 mole KNO3 moved from root medium to stem cell vacuoles Edwards and Walker (1983); Buchanan et al. (2000); Nicholls and Fergusson (2002); Allen (2003)
Transfer of 1 osmole of KNO3 from root medium to stem cell vacuoles (from row 8) 1 mole of KNO3 = 1·8 osmole, assuming an osmotic coefficient of 0·9 11·0 absorbed mole photons Robinson and Stokes (1965); Milburn (1979)
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Table 3.

Energetics of use of 2 K+ malate2− as an osmoticum in plant stem cell vacuoles

Energy-requiring process
 Mechanism
 Energy cost
 Reference
Synthesis of 1 mole malic acid in cytosol of root cells Carboxylation of phosphoenolpyruvate derived from sucrose (supplied by symplastic unloading of phloem) using sucrose phosphate synthase 3 (CH2O), i.e. 0·25 sucrose; generates 0·25 ATP in root cytosol Buchanan et al. (2000)
Efflux of 2 H+ generated in malic acid synthesis, influx of 2 K+ K+ influx by 1 H+ : 1 K+ symport; efflux of 2 H+ per K+ using P ATPase (1 H+ : 1ATP) 4 ATP Buchanan et al. (2000)
Transfer of 2 K+ and 1 malate2− from root symplast to xylem conduit Flux of K+ and malate2− from root symplast to xylem via ion channels None Buchanan et al. (2000); de Boer and Volkov (2003)
Transfer of 2 K+ and 1 malate2− from xylem conduit to stem cell symplast K+ influx by 1 H+ : 1 K+ symport; malate2− influx by 3 H+ : 1 malate2− symport; efflux of 4 H+ per 2 K+ malate2− using P ATPase (1 H+ : 1 ATP) 4 ATP Buchanan et al. (2000)
Transfer of 2 K+ and 1 malate2− from stem cell symplast to vacuole 1 H+ : 1 K+ antiport, electrically driven malate2− influx; H+ influx into vacuole driven by 2 H+ : 1ATP V ATPase 1 ATP Buchanan et al. (2000); Maeshima (2001)
Production of 8·75 ATP (from rows 1–5) by oxidative phosphorylation As for Table 2, row 5 Respiration of 1·88 (CH2O) Buchanan et al. (2000); Nicholls and Ferguson (2002)
Sum of (CH2O) moved from leaf cytosol to stem or root cytosol as sucrose (from rows 1 and 6) 1·88 + 3·0 (CH2O) 4·88 (CH2O)
Movement of 4·88 (CH2O) (from row 7) as sucrose from leaf cytosol to root or stem cytosol As for Table 2 Respiration of 0·085 (CH2O) Van Bel (1992);Patrick (1997);Buchanan et al. (2000); Nicholls and Ferguson (2002)
Total (CH2O) cost (from rows 7 and 8) 4·88 + 0·085 (CH2O) 4·965 (CH2O)
Absorbed photon cost to produce 4·965 (CH2O) (from row 9) as sucrose in leaf cytosol, equivalent to 2 K+ and malate2− in stem cell vacuoles As for Table 2, row 8 64·55 mole photons per 4·965 mole (CH2O) equals 2 K+ and 1 malate2− in stem cell vacuoles Edwards and Walker (1983); Buchanan et al. (2000); Nicholls and Ferguson (2002); Allen (2003)
Generation of 1 osmole of 2 K+ malate2− in stem cell vacuoles (from row 10) 2 mole K+ and 1 mole malate2− = 2·7 osmole, assuming an osmotic coefficient of 0·9, as for KHmalonate and KHsuccinate 24 absorbed mole photons Robinson and Stokes (1965)
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Table 4.

Energetics of hexose as an osmoticum in stem cell vacuoles

Energy-requiring process
 Mechanism
 Energy cost
 Reference
Transfer of 1 hexose (as sucrose) from leaf cytosol to leaf sieve tubes, then symplastic unloading into stem cell cytosol As for Table 2, row 6 and Table 3, row 8 Respiration of 0·108 (CH2O) Van Bel (1992); Patrick (1997);Buchanan et al. (2000); Nicholls and Ferguson (2002)
Transfer of 1 hexose from stem cell cytosol to vacuole 1 H+ : 1 glucose antiport; 2 H+ per ATP consumed by V ATPase, i.e. 0·5 ATP Respiration of 0·108 (CH2O) Buchanan et al. (2000); Maeshima (2001)
Total cost of (CH2O) to synthesize 1 hexose in leaf cytosol and transfer to stem cell vacuoles (from rows 1 and 2) Sum of 1 hexose and 0·216 (CH2O) 6·216 (CH2O)
Absorbed photon cost to produce 6·216 (CH2O) as sucrose in leaf cytosol (from row 3) As for Table 2, row 8 80·81 absorbed mole photons
Generation of 1 osmole of hexose in stem cell vacuoles (from row 4) 1 mole hexose = 1·01 osmole, assuming an osmotic coefficient of 1·01, i.e. that the coefficient for hexose is the same as for sucrose 80 absorbed mole photons Robinson and Stokes (1965); Milburn (1979)
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Statistical analysis

In field study 1, correlation analysis was carried out on all variates versus irradiance. In cases where a significant (P < 0·05) correlation was found, regression analysis was then carried out: straight line, quadratic and quadratic in √N models were tested. Model choice was based on the value of R2. In field study 2 and the glasshouse experiment, an analysis of variance was carried out on all data with irradiance as the factor. All effects discussed have a probability P < 0·05. Variability quoted in the text is the standard error. All data were analysed using the Minitab Version 13 (Minitab Inc., Pennsylvania, USA) package.

RESULTS

Field studies

In field study 1, Impatiens was sampled at 100 % Ir to 2 % Ir. Population biomass increased with decreasing irradiance from 100 % Ir to approx. 30 % Ir then decreased with decreasing irradiance thereafter with values ranging from 0 to 559 g d. wt m−2 (Fig. 1A). There was a significant positive correlation (r = 0·86) between population biomass and plant population which ranged from 0 to 1232 plants m−2 (data not shown). There was also a strong positive relationship (r = 0·79) between population biomass and irradiance below 30 % Ir.

Fig. 1.

Fig. 1.

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Population biomass (A) and individual shoot dry weight (B) and shoot height (C) of Impatiens sampled at different irradiance levels in a deciduous woodland (field study 1).

In general, individual shoot dry weight increased with decreasing irradiance throughout from approx. 0·8 g at 100 % Ir to approx. 2·1 g at 2 % Ir but there was quite a spread in values for similar irradiance levels (Fig. 1B). The partitioning of dry matter between leaves and stem did not change significantly with irradiance; 65·2 ± 0·97 % of shoot dry weight was in the stem. Plant height increased fairly steadily with decreased irradiance throughout from approx. 60 cm at 100 % Ir to approx. 100 cm at 2 % Ir (Fig. 1C). Water comprised 95·0 ± 0·17 % and 97·3 ± 0·15 % of stem fresh weight at 85–100 % Ir and 2–3 % Ir, respectively.

Leaf Inline graphic concentration was negligible at irradiance levels of 100–10 % Ir but increased with decreasing irradiance there after to a maximum of approx. 0·3 mmol g−1 d. wt (Fig. 2A). Stem Inline graphic concentration was <0·05 mmol g−1 d. wt at 100–50 % Ir but generally increased with decreasing irradiance thereafter. The magnitude of this increase was substantially greater than for leaves and at 2–10 % Ir, Inline graphic concentrations were four to eight times greater in stem than leaves. At 85–100 % Ir, total N concentration in stems was 0·37 ± 0·01 mmol g−1 d. wt: the corresponding Inline graphic concentration was <0·02 mmol g−1 d. wt. At 2–3 % Ir, total N concentration in stems was 2·45 ± 0·06 mmol g−1 d. wt while Inline graphic concentration was 1·68 ± 0·08 mmol g−1 d. wt. Thus, Inline graphic constituted approx. 70 % of total N in stems at low irradiance. Leaf K+ concentration increased steadily from approx. 0·6 mmol g−1 d. wt at 100 % Ir to 1·2 mmol g−1 d. wt at 2 % Ir (Fig. 2B). Stem K+ concentration showed no obvious relationship with irradiance and fluctuated around 3 mmol g−1 d. wt.

Fig. 2.

Fig. 2.

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Concentrations of nitrate and potassium in leaves (filled squares) and stem (filled circles) of Impatiens sampled at different irradiance levels in a deciduous woodland (field study 1).

Table 1 presents shoot dry weight and height, and concentrations of total osmoticum, K+, Inline graphic, other inorganic ions, malate and sugars in stems of Impatiens sampled at harvest 2 in field study 2 and the single harvests in field study 3 and the glasshouse experiment. The contributions of the different osmotica to total osmoticum now described are based on these values. At both sampling times in field study 2, values for shoot dry weight and height were similar at low and high irradiance sites. At the initial harvest, mean dry weight and height across low and high irradiance treatments were 0·26 ± 0·04 g and 14·2 ± 1·0 cm, respectively; comparable values at the second harvest (67 d later) were 4·00 ± 0·80 g and 131 ± 12·3 cm, respectively (Table 1). Considering the second harvest, the concentration of total osmoticum was 15 % greater at high irradiance (230 osmol m−3) than at low irradiance (200 osmol m−3), while water comprised 93·9 ± 0·4 % and 95·8 ± 0·4 % of stem fresh weight at high and low irradiance, respectively. At high irradiance, K+ constituted 50·1 % of total osmoticum in cells assuming an osmotic coefficient of 0·9 for ions (Robinson and Stokes, 1965) while Inline graphic, other inorganic anions (Cl−, Inline graphic and Inline graphic), malate and sugars, respectively, comprised <0·5 %, 10·6 %, 20·8 % and 1·99 % of total stem osmoticum (Table 1). At low irradiance, K+ constituted 44·9 % of total osmoticum in stems, while Inline graphic, other inorganic anions and malate, respectively, comprised 26·7 %, 7·7 % and 3·1 % of total stem osmoticum. Sugar concentration was negligible at low irradiance. Values obtained at low irradiance in field study 3 (NB different site) were similar to those at low irradiance in field study 2. Here, K+, Inline graphic, other inorganic anions, malate2− and sugars, respectively constituted 44·9 %, 34·3 %, 10·3 %, 2·2 % and <0·1 % of total osmoticum in stems (Table 1): Inline graphic constituted 75 ± 2·2 % of total N in stems (data not shown).

Table 1.

Shoot dry weight and height and concentrations of total osmoticum, K,Inline graphic, other inorganic anionsInline graphic, malate and sugars in stems of Impatiens sampled at high and low irradiance in field study 2, low irradiance in field study 3 and high and low irradiance in the glasshouse experiment

Irradiance
 Dry weight (g)
 Height (cm)
 Osmoticum (osmol m−3)
 K+ (mol m−3)
 Inline graphic (mol m−3)
 Inline graphic (mol m−3)
 Malate (mol m−3)
 Sugars (mol m−3)
Field study 2
    High 4·91 143 230 128 1·20 27·1 53·2 4·54
    Low 3·11 118 200 99·7 59·4 17·0 6·95 <0·1
    s.e. (n = 3) 1·11 17·2 5·36 14·2 1·53 2·84 5·18 1·26*
Field study 3
    Low 5·89 164 168 83·8 64·0 19·2 4·05 <0·1
    s.e. (n = 6) 0·42 7·71 13·3 6·56 2·86 1·86 0·55 –
Glasshouse experiment
    High 14·2 132 561 207 1·12 62·9 120 14·2
    Low 5·1 154 210 107 71·3 27·4 6·88 <0·1
    s.e. (n = 5) 0·41 5·26 9·52 7·18 1·00 3·65 3·49 1·06*
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*

Standard error (s.e.) relates to high irradiance value only.

Glasshouse experiment

At planting in the glasshouse, total plant dry weight was 0·39 ± 0·021 g and shoot height was 7·2 ± 0·3 cm. At harvest 64 d later, shoot dry weight was almost three times greater at high than low irradiance but shoot height was greater at low irradiance reaching 154 cm over the course of the experiment (Table 1). Water constituted 93·0 ± 0·13 % and 96·4 ± 0·10 % of stem fresh weight at high and low irradiance, respectively. The concentration of total osmoticum in stems at high irradiance (561 osmol m−3) in the glasshouse was two to three times greater than that at high or low irradiance in the field, but in the glasshouse as in the field, Inline graphic concentration was negligible in relation to total osmoticum (Table 1) and Inline graphic constituted only 3·6 % of total tissue N (data not shown), while K and malate were substantial, respectively, constituting 33·2 % and 19·3 % of total osmoticum. Sugar concentrations in stems at high irradiance were greater in the glasshouse than in the field but still only accounted for 2·6 % of total osmoticum. Values for total and specific osmoticum concentrations in stems at low irradiance were similar in the glasshouse and in field studies 2 and 3 (Table 1). In the glasshouse, K+, Inline graphic and other inorganic anions, respectively, accounted for 45·9 %, 30·6 % and 11·7 % of total osmoticum in stems with malate2− and sugars accounting for only 2·9 % and <0·1 % of total stem osmoticum, respectively (Table 1); Inline graphic constituted 81 % of stem N at low irradiance (data not shown).

Photon costs of different osmotica

Tables 2–4 show the energy cost, as absorbed photons, of generating osmolarity in stem cell vacuoles with KNO3, K2-malate and hexose (details of the mechanisms involved are given in the tables). The calculations show that the energy cost of KNO3 (11 absorbed mole photons per osmole) is less than half that of K2-malate (24 mole photons absorbed per osmole), and less than one-seventh that for hexose (80 absorbed mole photons per osmole).

DISCUSSION

Impatiens is the tallest annual in the European flora: it commonly achieves a height of 2 m (Beerling and Perrins, 1993; Pysek and Prach, 1995). Also, it shows fast extension growth and has been reported to reach a height of 1·3 m in 72 d when growing in open ground (Perrins et al., 1990). Here it is shown that a similar extension rate can occur at <10 % Ir. This ability to achieve substantial height quickly at low irradiance is likely to be an important factor enabling Impatiens to outcompete other species in the woodland interior (Grime, 1987; Maule et al., 2000).

In field study 1, population biomass of Impatiens increased with decreased irradiance from 100 % Ir to approx. 30 % Ir then decreased with decreasing irradiance thereafter (Fig. 1). Similar results were obtained in other years (Maule, 2000). The most likely explanation for low population biomass of Impatiens at the wood edge is competition from established plants (Maule et al., 2000). There was a strong positive relationship between Impatiens population biomass and irradiance (r = 0·79) from 2 to 30 % Ir in the woodland and it is likely that irradiance is the primary factor limiting biomass of Impatiens in the woodland interior. This conclusion gains further weight from the finding that changes in stem N and Inline graphic concentration associated with decreased irradiance in the woodland were similar to those associated with decreased irradiance in the glasshouse (Fig. 2 and Table 1). Also, changes in specific leaf area and leaf photosynthetic pigment and soluble protein concentrations associated with decreased irradiance in the woodland and glasshouse were similar and were as expected for plants acclimating to shade conditions (Maule, 2000). These findings indicate that any light quality effects caused by differences between shade in the woodland and under the shade cloth were negligible relative to the light intensity effects on the measurements taken.

In the woodland, changes in population biomass were closely correlated with plant density and not individual plant dry weight which was as great or greater at 2–10 % Ir as at 50–100 % Ir (Fig. 1). This contrasts with the substantial decrease in individual plant dry weight with decreased irradiance in the glasshouse (Table 1). Similar or greater dry weight of individual plants with decreased irradiance in the field is likely to be due to decreased intraspecific competition with decreased population. Possible reasons for reduced population at low irradiance are lower seed levels in the soil or self-thinning.

The concentration of total osmoticum in shoot tissue of higher plants is dependent on genotype, stage of development and environmental conditions (Wyn-Jones and Gorham, 1982; Lieffering et al., 1996). Generally, values quoted for leaves of plants grown under non-stressed conditions range from 300 to 500 osmol m−3 (Wyn-Jones and Gorham, 1982; Nobel, 1991). For stem tissue of Impatiens, the concentration of total osmoticum was 561 osmol m−3 under high irradiance in the glasshouse but ranged from 168 to 230 osmol m−3 at low and high irradiance in the field and low irradiance in the glasshouse (Table 1). Values in this range have been reported previously for plant tissues with a high water content such as Kalanchoë daigremontiana mesophyll cells undergoing CAM (Wyn-Jones and Gorham, 1982) and lettuce (Lactuca sativa L.) leaves under good growing conditions (Seginer, 2003). The water content of Impatiens stems at low irradiance was consistently high (95·8–97·3 %).

Under conditions in which photosynthesis is reduced, such as low irradiance, Inline graphic can accumulate in leaves to levels which are important osmotically (Blom-Zandstra and Lampe, 1985; Steingröver, 1986; Lieffering et al., 1996). For Impatiens in the field, Inline graphic concentration in leaves was greater at low than high irradiance but reached a maximum of approx. 0·3 mmol g−1 d. wt only (Fig. 2A). In stems, Inline graphic concentration was negligible at 50–100 % Ir but increased 100–1000-fold with decreased irradiance and at 2–10 % Ir in two separate woodlands and in the glasshouse, Inline graphic constituted 27–34 % of total osmoticum in stems (assuming an osmotic coefficient of 0·9; Robinson and Stokes, 1965) and Inline graphic constituted 69–81 % of total N in stem tissue (Table 1). Also, at low irradiance levels, K+ consistently accounted for approx. 45 % of total osmoticum in stem. Therefore, at low irradiance, 70–80 % of osmoticum in Impatiens stem was composed of the inorganic ions Inline graphic and K+. Indeed at low irradiance, Inline graphic and K+ together constituted approx. 20 % of stem dry weight.

K2malate and hexose sugars, in particular glucose, are common vacuolar osmotica in land plants (Raven et al., 1980) and their concentrations were determined in stems of Impatiens. In the field and glasshouse, sugar concentrations were one to two orders of magnitude greater at high than low irradiance but at most constituted 2·6 % of stem osmoticum (Table 1). In contrast, K and malate, respectively, constituted 33·2–50·1 % and 19·3–20·8 % of total osmoticum in the stem at high irradiance in the field and glasshouse and, while K was important osmotically at high and low irradiance, malate decreased to approx. 3 % of total osmoticum at low irradiance. Thus, the increase in Inline graphic concentration with decreased irradiance was ‘matched’ by a decrease of similar magnitude in malate concentration.

The energy costs, as absorbed photons, of generating osmolarity in stem cell vacuoles with KNO3, K2-malate and hexose were calculated (Tables 2–4). The energy cost of KNO3 (11 absorbed mole photons per osmole) is less than half that of K2-malate (24 mole photons absorbed per osmole), and less than one-seventh that for hexose (80 absorbed mole photons per osmole). Accordingly, the use of KNO3 as osmoticum can yield a significant energetic advantage. This can be expressed in terms of the fraction of the total energy involved in the production of stem material that is used in generating osmolarity. At low irradiance in the glasshouse experiment, stems had a water content of 27 g per g dry matter (96·4 % water) and an osmolarity of 210 osmol m−3 (Table 1). If it is assumed that organic carbon is 40 % of the dry matter in these stems and that the assimilation of one mole of carbon from atmospheric CO2 into stem organic C involves the absorption of 26 mole photon (i.e. half of the photosynthate is lost in respiration in growth on Inline graphic as N source) (Raven, 1976; Table 2, entry 8), then this yields a total photon cost of 0·867 mole photon per gram stem dry matter produced, with the photon costs of osmolarity generation (Tables 2–4) at 0·0624 mole photon for KNO3, 0·136 mole photon for K2-malate and 0·454 mole photon for hexose. These calculations suggest that the use of KNO3 as osmoticum costs only 7 % of the total construction cost of the stem, while K2-malate costs 16 % and glucose would cost 52 %. It is concluded that accumulation of Inline graphic in place of organic molecules in stems is an important mechanism allowing Impatiens to achieve substantial height at low irradiance.

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