AOBPreview originally published online on October 8, 2003
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Annals of Botany 92: 757-765, 2003
© 2003 Annals of Botany Company
Photosynthetic Responses of the Tropical Spiny Shrub Lycium nodosum (Solanaceae) to Drought, Soil Salinity and Saline Spray
1 Centro de Botánica Tropical, Instituto de Biología Experimental, Universidad Central de Venezuela, Apartado 47577, Caracas 1041-A, Venezuela and 2 Centro de Ecología, Instituto Venezolano de Investigaciones Científicas, Apartado 21827, Caracas 1020-A, Venezuela
* For correspondence. E-mail wtezara{at}strix.ciens.ucv.ve
Received: 26 June 2003; Returned for revision: 28 July 2003; Accepted: 20 August 2003 Published electronically: 8 October 2003
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Water relations and photosynthetic characteristics of plants of Lycium nodosum grown under increasing water deficit (WD), saline spray (SS) or saline irrigation (SI) were studied. Plants of this perennial, deciduous shrub growing in the coastal thorn scrubs of Venezuela show succulent leaves which persist for approx. 1 month after the beginning of the dry season; leaf succulence is higher in populations closer to the sea. These observations suggested that L. nodosum is tolerant both to WD and salinity. In the glasshouse, WD caused a marked decrease in the xylem water potential (
), leaf osmotic potential (s) and relative water content (RWC) after 21 d; additionally, photosynthetic rate (A), carboxylation efficiency (CE) and stomatal conductance (gs) decreased by more than 90 %. In contrast, in plants treated for 21 d with a foliar spray with 35 
NaCl or irrigation with a 10 % NaCl solution, and RWC remained nearly constant, while s decreased by 30 %, and A, CE and gs decreased by more than 80 %. An osmotic adjustment of 0·60 (SS) and 0·94 MPa (SI) was measured. Relative stomatal and mesophyll limitations to A increased with both WD and SS, but were not determined for SI-treated plants. No evidence of chronic photoinhibition due to any treatment was observed, since maximum quantum yield of PSII, Fv/Fm, did not change with either drought in the field or water or salinity stress in the glasshouse. Nevertheless, WD and SI treatments caused a decrease in the photochemical (qP) and an increase in the non-photochemical (qN) quenching coefficients relative to controls; qN was unaffected by the SS treatment. The occurrence of co-limitation of A by stomatal and non-stomatal factors in plants of L. nodosum may be associated with the extended leaf duration under water or saline stress. Additionally, osmotic adjustment may partly explain the relative maintenance of A and gs in the SS and SI treatments and the tolerance to salinity of plants of this species in coastal habitats.
Key words: Drought, Lycium nodosum, fluorescence, mesophyll limitation, saline stress, stomatal limitation, water deficit.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plant species growing in the semi-arid regions of the world need to be adapted to an environment in which drought strongly affects plant growth. Water availability is the main environmental factor limiting photosynthesis and growth even in plants well adapted to arid conditions. Another source of stress is soil salinity in non-tolerant species (Greenway and Munns, 1980).
Water deficit affects stomatal conductance, gs, thus diminishing photosynthetic rate, A; stomatal closure is assumed to be the main cause of decreased A, because it decreases CO2 availability in the mesophyll (Cornic, 2000). However, there is strong evidence that drought also affects mesophyll metabolism, reducing photosynthetic capacity (Tezara et al., 1999; Lawlor, 2002). Stomatal closure was not the main factor for the reduction in A under drought in plants of Amaranthus palmeri (Ehleringer, 1983), Encelia farinosa (Ehleringer and Cook, 1984) or Helianthus annuus (Tezara et al., 1999). An increase in the relative stomatal limitation (Ls) calculated from the response curve of A to the intercellular CO2 concentration (Ci) allows it to be ascertained as to whether A is reduced solely because of decreased gs, and not because of an increase in mesophyll limitation (Farquhar and Sharkey, 1982). Jacob and Lawlor (1991) defined the mesophyll limitation, Lm, as the proportional reduction in Ci-saturated A (Asat) of plants subjected to stress. Processes in photosynthetic metabolism which may be impaired by water stress include Rubisco enzyme activity, RuBP regeneration, ATP supply, electron transport rate (J) and efficiency of light capture in the photosystems (Lawlor, 2002; Lawlor and Cornic, 2002). Therefore, changes in Lm may reflect changes in parameters such as chlorophyll a fluorescence and carboxylation efficiency (CE), among others.
During water stress, restricted CO2 availability due to stomatal closure may lead to increased susceptibility to photodamage (Powles, 1984). However, such damage was not found to occur during the dry season in Quercus petraea (Epron et al., 1992), suggesting that the mechanisms of protection against an excess of absorbed excitation energy are efficient. The major process involved in protection against photo-damage is probably the increase in non-photochemical quenching energy dissipation, which reduces the relative quantum yield of PSII (
PSII) in order to maintain an adequate balance between photosynthetic electron transport and carbon metabolism (Weis and Berry, 1987; Krause and Weis, 1991).
In a similar manner to water deficit, salinity stress may alter photosynthesis mainly through a reduction of gs and/or of the mesophyll capacity to fix CO2 (Seemann and Critchley, 1985; Bethke and Drew, 1992; Delfine et al., 1998). A 50 % reduction in A of plants of Olea europaea occurred when they were irrigated with 200 mM NaCl, due to a reduction in gs and CE (Tattini et al., 1997). Salinity caused an 18 % reduction in Rubisco activity of leaves of Cicer arietinum (Soussi et al., 1998). In contrast, maize plants grown with low concentrations of NaCl (20–50 mM) showed slight increases in A and qN, but a decrease in qP (Shabala et al., 1998).
Changes in leaf anatomy, including an increase in thickness and succulence, are commonly observed in plants subjected to increased soil salinity, as in the case of many mangroves such as Laguncularia racemosa (Biebl and Kinzel, 1965) and Avicennia germinans (Suárez and Sobrado, 2000). Since salt-stressed leaves are generally thicker than in control plants and leaf thickening is likely to increase resistance to CO2 diffusion in the mesophyll (Delfine et al., 1998), these changes may have an influence on gas exchange (Bongi and Loreto, 1989).
Lycium nodosum Miers. (Solanaceae) is a perennial, deciduous shrub growing in coastal scrubs of Venezuela. Plants occupy exposed as well as shaded sites, but tend to grow more vigorously under the partial shade of evergreen trees, such as Prosopis juliflora. Foliage persists for approx. 1 month into the dry season. Leaf succulence, as well as the occurrence of appreciable photosynthetic rates at the beginning and middle of the dry season in the field, suggested the occurrence of particular strategies of drought resistance in L. nodosum. Since adult (approx. 2 m tall) individuals have a main root not longer than 1 m and soil water content in the field at that depth is less than 4 % dry mass (DM) (Herrera et al., 1994), it seems unlikely that plants tap any significant soil water during the dry season.
Gas exchange, water relations and parameters of chlorophyll a fluorescence of plants growing in the glasshouse, under frequent irrigation and water deficit (WD) and under two salinity treatments [foliar spray with 35 NaCl (SS) and irrigation with 10 NaCl (SI)] were measured to investigate the possible mechanisms of tolerance of L. nodosum plants to drought and salinity. To find out whether the reduction in A due to drought or salinity was attributable solely to stomatal closure or not was of particular interest. Plants were also measured in the field during the dry and the rainy season at locations either subject to or not subject to soil salinity and marine spray.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Field sites and plant material
Measurements in the field were carried out in Venezuela in a thorn scrub near the city of Coro (11°25'N, 69°36'W) at approx. 20 m above sea level (a.s.l.) during the rainy season (February 2000), by the seashore in Adícora (11°57'N, 69°48'W) during the rainy season (February 2000) and Chichiriviche de la Costa (10°33'N, 67°12'W) during the dry season (August 1999). At Coro, plants of L. nodosum were growing under the canopy of the evergreen tree Prosopis juliflora, whereas in both Adícora and Chichiriviche de la Costa they were unshaded and exposed to full sunlight. Lycium nodosum is a spiny shrub with profuse decumbent branches less than 2 m long and small (approx. 1 cm2) partly fleshy, sessile leaves. Leaves appear fully expanded a few centimetres from the branch tip, with lamina area and thickness showing a slight increase towards the main stem. For all measurements described below, only the youngest fully expanded leaves were sampled.
Glasshouse experiments
Whole plants collected in Chichiriviche de la Costa were grown in 15-L pots filled with commercial fertile garden soil in the glasshouse in Caracas (approx. 1000 m a.s.l.). Daily watering for 1 month ensured the production of abundant foliage; plants were fertilized weekly with a commercial fertilizer (N : P : K, 15 : 15 : 15). Three separate experiments were conducted: (1) WD, by suspension of watering; (2) SS, by spraying the leaves with a 35 NaCl solution three times a day for 21 d; and (3) SI, by irrigation every other day with 500 cm3 of a 10 % NaCl solution, and with tap water on alternate days to avoid water deficit. Ten plants were used per treatment. Measurements of the variables indicated below were taken on leaves or leaf-bearing branches from three to ten different individuals.
Microclimatic parameters
Photosynthetic photon flux density (PPFD) was measured with a quantum sensor model 190-S connected to a meter model LI-185 (LI-COR Inc., Lincoln, NB, USA). Air temperature was measured with YSI 400 thermistors connected to a telethermometer (Yellow Springs Instru ments, OH, USA), and relative humidity with a hair strand hygrometer (Abbeon model AB167B; Abbeon Cal., Santa Barbara, CA, USA). Soil salinity was measured with a refractometer model S/Mill-E (Atago Co., Ltd, Tokyo, Japan). Soil electrical conductivity was measured with an electrical conductivity meter, model 19101–00 (Cole-Parmer Instrument Co., Vernon Hills, IL, USA).
Water relations
Xylem water potential () was measured at 0600 h (n = 6) with a pressure bomb (PMS, Corvallis, OR, USA). Leaf osmotic potential (s) was measured in the sap expressed from frozen and defrosted leaves previously used for the determination of , using a Wescor 5000 osmometer (Wescor, Inc., Logan, UT, USA). In order to eliminate the salt deposited on them, leaves sprayed with NaCl were rinsed with distilled water and blotted dry prior to freezing. Leaf water content was determined in leaves (n = 10) taken at 0800–0900 h as LWC = (FM – DM)/DM). Relative water content (RWC) was determined in leaves (n = 10) collected at 0700 h and floated on distilled water in the dark at 4 °C for 1 h. Osmotic potential at full turgor (s100) was measured in the sap expressed from frozen and defrosted leaves (n = 6) of branches re-saturated in the dark for 1 h. Osmotic adjustment was calculated as the difference between s100 of control plants and that of plants after 21 d of treatment.
Leaf gas exchange
Gas exchange in attached leaves was measured with a portable IRGA model CIRAS 1 used in conjunction with a PLC(B) assimilation chamber (PP Systems plc, Hitchin, Herts., UK). Measurements were made at an ambient CO2 concentration (Ca) of 350 µmol mol–1, unless otherwise stated. Instantaneous A was measured at 1000 h with a PPFD of 800 µmol m–2 s–1 and leaf temperature of 28 °C ± 0·5, the time at which daily maximum A was determined to occur in control plants prior to treatments. A/Ci curves (n = 3) were determined in WD and SS plants by decreasing Ci [calculated by the program in the IRGA (infra-red gas analyser), after Farquhar et al., 1980] from approx. 220 µmol mol–1 (when A at Ca = 350 µmol mol–1 was initially measured) to zero, and then progressively increasing Ci to 1400 µmol mol–1. CO2 was provided by a cylinder filled with pure gas connected to the IRGA. A/Ci curves were fitted to the empirical equation A = b + dekCi, where b = CO2-saturated photosynthetic capacity (Asat) and (b + d) = y – intercept (Tezara et al., 1998). CE was calculated from the initial slope of the curve. The relative stomatal limitation of the photosynthetic rate was calculated as Ls = 100 x (Ao – A)/Ao, where Ao is the photosynthetic rate at Ci = Ca (Farquhar and Sharkey, 1982). The relative mesophyll limitation was calculated as Lm = 100 x (AC – AS)/AC, where AC is A of control leaves at Ci = 800 µmol mol–1 and AS the rate of stressed leaves at the same Ci (Jacob and Lawlor, 1991). Thus, Lm is a measure of the capacity of the mesophyll to fix CO2 at saturating Ci and its value in control plants is zero. Conditions during measurements were: leaf temperature 28 ± 0·5 °C, and PPFD 700 ± 20 µmol m–2 s–1. Previous determinations showed that increasing PPFD to 1200 µmol m–2 s–1 did not increase Ci-saturated A, but leaf temperature increased up to 34 °C. Response curves of A vs. PPFD (n = 3) were carried out by varying incident PPFD with neutral filters (Balzers, Handelsbank, Zürich); the light source was either the sun or a 50 W dichroic lamp (Phillips, Caracas, Venezuela).
Chlorophyll a fluorescence of PSII
Chlorophyll fluorescence was measured on attached dark-adapted leaves (n = 6) with a Mini PAM fluorometer (Walz, Effeltrich, Germany) using the protocol described by Genty et al. (1989). The maximum quantum yield of PSII (Fv/Fm) was measured in attached dark-adapted leaves. The relative quantum yield of PSII at steady-state photosynthesis was calculated as PSII = (F'm – Fs)/F'm, where Fs and F'm are fluorescence at steady-state photosynthesis and maximum fluorescence in the light, respectively. The coefficients qP and qN were calculated from measurements of fluorescence. Electron-transport rate of PSII was estimated by the method of Krall and Edwards (1992) as J = PSII x PPFD x a x 0·5, where a is the fraction of incident PPFD absorbed by the leaf, assumed to be 0·85 (leaves of L. nodosum are glabrous). Leaf chlorophyll content was determined after Bruinsma (1963) in acetone extracts of leaves (n = 4).
Statistical analysis
Results are presented as means ± s.e. Significance at P < 0·05 was assessed by ANOVA using the statistical packages Statistica, Excel and Sigmaplot.
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RESULTS |
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Field measurements
Values of variables in plants from the three field sites are presented in Table 1. Soil was more saline at Chichiriviche de la Costa and Adícora than at Coro. Plants had lower values of
in the dry season (Chichiriviche de la Costa) than in the rainy season (Coro and Adícora). Values of LWC were lower in Coro than at the other two, more saline, sites. Values of A and gs were lower during the dry season, whereas the average Fv/Fm did not change with either site or season.
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Glasshouse experiments
Leaf water status.
Microclimatic conditions in the glasshouse resembled values measured in Coro and Chichiriviche de la Costa (Fig. 1). Treatment effects in the parameters of water relations are shown in Fig. 2. After 21 d under the WD treatment, a decrease in
to –4·1 MPa was observed with a 10 % reduction in RWC. Treatments SS and SI had no effect on , whereas RWC was significantly reduced by 21 d of treatment SI. An average 30 % reduction in s was observed after 21 d for all treatments. Leaf water content was significantly reduced by WD (13 %) and SI (4 %), but not by SS. Control values were similar to those measured in Chichiriviche de la Costa and Adícora, whereas values measured in Coro resembled those obtained in the glasshouse after 14 d of WD.
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The apparent occurrence of negative turgor pressures due to higher values of
s than expected may have been the consequence of dilution of cell sap by apoplastic water; nevertheless, an osmotic adjustment of 0·60 ± 0·13 (SS) and 0·94 ± 0·10 MPa (SI) was measured after 14 and 21 d of treatment, respectively. The s100 was not affected by treatment WD, averaging –1·44 MPa.
Leaf gas exchange.
Control values of A and gs were approx. five and two times higher, respectively, than in plants growing in the field during the rainy season, showing the effect of frequent watering on glasshouse-grown plants. After 21 d of treatment, A and gs decreased by 92 and 94 % (WD), 75 and 82 % (SS) and 51 and 70 % (SI), respectively (Fig. 3). The relationship between A and gs was a straight line of zero intercept, which explained 87 % of the variation in A (Fig. 4).
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Both Asat and CE declined with WD and SS treatments (Figs 5 and 6A and B). The CO2 compensation point was 38 and 42 µmol mol–1 in control plants of the WD and SS treatments, respectively, and increased to 100 and 62 µmol mol–1 with length of time under treatment, remaining nearly constant in SS from day 4 to day 21. The Ls increased by 10 % a few days after the onset of the WD or SS treatments and remained constant thereafter, whereas Lm increased by 80 and 40 % with WD or SS, respectively (Fig. 6C and D).
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Response of A to PPFD.
In control plants, A was light-saturated at a PPFD of 800 µmol m–2 s–1. As water deficit developed, saturating PPFD, saturated A and apparent quantum yield of CO2 fixation progressively decreased (Fig. 7A). The same trend was observed under the SS treatment, although saturated A was approx. twice as large after 14 and 21 d as in WD plants (Fig. 7B).
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Chlorophyll a fluorescence.
No significant changes in chlorophyll content per unit area occurred under any treatment (Fig. 8A). The average Fv/Fm was 0·83 ± 0·01 and this was not affected by any treatment (Fig. 8B). However, a decrease in
PSII at PPFD = 1300 µmol m–2 s–1 was observed in all three treatments (Fig. 8C); consequently, J was reduced by 70, 52 and 45 % after 21 d of WD, SS and SI treatments, respectively (Fig. 8D). The qP followed the same trend as PSII, decreasing with time under each treatment (Fig. 8E), while qN increased in WD and remained constant in SS and SI (Fig. 8F).
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DISCUSSION |
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Limiting supplies of water lead to dehydration of plants, shown by decreased RWC and
and loss of turgor of leaves, which can result in stomatal closure, increased concentration of solutes and decreased s (Lawlor, 1995). In the present study water deficit resulted in a reduction in RWC and , while saline irrigation (but not spray) caused a reduction in s, RWC and LWC. Leaves of L. nodosum showed variable succulence; in populations near the sea leaves were more succulent than in the inland, less saline, population, indicating that these plants possess mechanisms of salt tolerance. Similarly, plants subjected to SS or SI showed maintenance of, or even an increase in, succulence. Plant exposure to high salinity at the root caused increases in leaf succulence in seedlings of the mangroves Aegiceras corniculatum (Ball and Farquhar, 1984) and Avicennia germinans (Suárez and Sobrado, 2000). In contrast, no changes or even decreases in LWC were found in the halophyte Halosarcia pergranulata (Short and Colmer, 1999) and the mangrove Avicennia marina (Ball and Farquhar, 1984), and a decrease in mesophyll and total leaf thickness was found in spinach (Delfine et al., 1998), suggesting that increased succulence is not a universal response to salinity.
Considerable osmotic adjustment occurred in leaves of L. nodosum subjected to saline spray or irrigated with saline solution. Osmotic adjustment, the lowering of s by active accumulation of osmotically active solutes, is generally thought to be the main mechanism for turgor maintenance under stress, enabling plants to maintain metabolic activity during drought (Turner and Jones, 1980), and is a mechanism reported to operate in plants in response to salt (Morgan, 1984). The s of H. pergranulata decreased 2·5 times with an increase in NaCl concentration in the soil from 10 to 800 mM (Short and Colmer, 1999). Leaf osmotic adjustment in salt-stressed plants of L. nodosum may result in the maintenance of a favourable water status, contributing substantially to the salt tolerance of this species.
Both water and salinity stress markedly inhibited A, CE and gs, although the effect of salinity on these variables was milder than water deficit. Similar results with water stress have been reported in Ipomoea carnea and Jatropha gossypifolia, species sympatric to L. nodosum (Herrera et al., 1994; Tezara et al., 1998). In flag leaves of barley (Belkhodja et al., 1999) and in salt-sensitive rice cultivars, salinity caused a substantial reduction in A and gs (Dionisio-Sese and Tobita, 2000), whereas leaf gas exchange was unaffected by high salinity (100–400 mM NaCl) in the halophyte, Suaeda salsa (Lu et al., 2003).
The decrease in both A and Ci with declining and the consequent decrease in gs may indicate that stomata were imposing a larger limitation on A under water and saline stress conditions. Many studies have reported that both stomatal and non-stomatal components are responsible for a decrease in A (Tezara et al., 1999; Lawlor, 2002). In the present study, in treatments WD and SI, Ls remained nearly constant after an initial increase a few days from the onset of treatments, whereas Lm increased to 80 % (WD) and 40 % (SS), suggesting that, as stress increased, metabolic regulation of photosynthesis became more important than stomatal closure.
The decreased CE and Asat suggest loss of Rubisco activity with decreasing RWC and . The amount and specific activity of Rubisco and the availability of RuBP affect CE and thus A. Conclusions relating to stomatal and non-stomatal limitations of A based on A/Ci curves may, in some cases, be misleading due to the erroneous calculation of Ci because of stomatal patchiness (Downton et al., 1988; Terashima et al., 1988) or to an increase in cuticular conductance to water vapour but not to CO2 (Boyer et al., 1997). Lawlor and Cornic (2002) attribute less importance to stomatal patchiness and more to the decrease in metabolism caused by a lowering of RWC. Little or no effect of patchy stomatal conductance on A measured at a given Ci has been reported (Cheeseman, 1991), and patchy stomatal distributions did not produce large differences in A compared with conditions of homogenous gs (Buckley et al., 1997). Patchiness has been shown to occur in heterobaric leaves, i.e. leaves in which the mesophyll continuity is interrupted by vascular bundles spanning the entire cross-section, but not in homobaric leaves (Terashima et al., 1988), the latter being the case in L. nodosum.
As for the influence of cuticular transpiration on Ci, in the present study it may be negligible since gs was lower than 30 mmol m–2 s–1 only in severely water-stressed leaves; this value is the lower limit, shown by Flexas et al. (2002) in water-stressed grapevine, of equality between Ci normally calculated (Farquhar et al., 1980) and that corrected for cuticular transpiration (Boyer et al., 1997). Also, Buckley et al. (1997) found that values of Ci became less reliable only when gs was lower than 30 mmol m–2 s–1.
Salinity reduced A of spinach leaves through a combined reduction in stomatal and mesophyll conductance. The reduction in the latter was attributed to a decrease in mesophyll intercellular spaces in thinner leaves, highlighting that a decrease in mesophyll conductance may be physical, rather than biochemical (Delfine et al., 1998). However, it has recently been demonstrated in salt-stressed olive that changes observed in the parameters of A/Ci curves between control and stressed plants were due to a decrease in mesophyll conductance to CO2 (Centritto et al., 2003).
The relationship between A and gs for all treatments was a straight line of zero intercept, and the Ci under any stress treatment was nearly constant with an average Ci/Ca = 0·73, which indicates that photosynthetic rate was co-limited by stomatal and non-stomatal factors (Schulze and Hall, 1982; Lawlor, 2002) under drought or salinity.
In L. nodosum, both apparent quantum yield and light-saturated A decreased with increasing water stress, similar to observations in the desert shrub Encelia farinosa (Ehleringer and Cook, 1984), and also with salinity. This suggests that either light harvesting or electron transport were affected by these stresses, or that enzymatic processes were responsible for decreasing CO2 fixation, or all of these factors together. Fv/Fm was not affected by water deficit, in agreement with other studies (Tezara et al., 1999; Lawlor and Cornic, 2002), or by salt stress, as previously reported by Dionisio-Sese and Tobita (2000) and Lu et al. (2003), suggesting that PSII activity is very resistant to these stresses. Also, qP at steady-state photosynthesis was hardly affected by water deficit in sunflower (Scheuermann et al., 1991) and was insensitive to water deficit in wheat (Biehler and Fock, 1993, 1996). However, the lower PSII of stressed plants was associated with lower qP, i.e. a higher reduction state of primary acceptors (the QA pool), than in control plants. In barley, salinity induced only small decreases in PSII at midday steady-state photosynthesis, indicating that the photosynthetic electron transport was little affected by salinity (Belkhodja et al., 1999). In S. salsa, Fv/Fm as well as PSII were insensitive to salinity (Lu et al., 2003). The higher light-saturated values of A in SS and SI plants than in WD plants after 21 d of treatment may have been the product of a slower reduction in J of saline-stressed plants. In contrast, J was reduced by approx. 40 % in maize leaves subjected to water deficit (Scheuermann et al., 1991).
The reduction in PSII and J due to water deficit, as well as salt stress, was lower than the decrease in A, possibly due to higher photorespiration at low , as suggested by Lawlor and Cornic (2002). This is supported by the observation that the CO2 compensation point in WD and SS plants was twice and half as high, respectively, than in their controls.
Water and saline stress increased qN in plants of L. nodosum, indicating that a greater proportion of the energy was thermally dissipated, thus accounting for the apparent down-regulation of PSII and supporting the protective role of the non-photochemical quenching against photoinhibition. In contrast, qN was unaffected by water deficit in wheat (Biehler and Fock, 1993), and salinity in salt-tolerant rice cultivars (Dionisio-Sese and Tobita, 2000) and in S. salsa (Lu et al., 2003), but increased with salinity in salt-sensitive rice cultivars.
The observed reductions in PSII, J, qP and CE may partly explain the increase in Lm and the occurrence of co-limitation of photosynthesis in plants of L. nodosum under drought or salinity. The decrease in J of L. nodosum may have contributed to the increase in Lm through a diminution in ATP and/or RuBP contents (Tezara et al., 1999; Lawlor and Cornic, 2002) since in A/Ci curves, Asat equates to the maximum rate of RuBP regeneration and maximum J (Farquhar et al., 1980). Increased Lm under stress may also be caused by decreased activity of some Calvin cycle enzymes (e.g. reduction in Rubisco activity and/or amount, which would be seen as a decrease in CE) and/or decreased mesophyll conductance to CO2 (Flexas et al., 2002; Centritto et al., 2003).
It is concluded that, in plants of L. nodosum subjected to water and saline stress, photosynthesis is co-limited by stomatal and non-stomatal factors and that these stresses do not cause chronic photoinhibition. Co-limitation would operate as a mechanism that optimizes water use and resource allocation when carbon acquisition through almost closed stomata is impaired. Plants of L. nodosum are capable of osmotic adjustment when subjected to salinity, and this apparently bears a relationship to the observed lower reduction of A in the SI treatment. In coastal habitats characterized by large temporal and spatial variations in rain, salinity and salt spray, osmotic adjustment, co-limitation of photosynthesis by stomatal and mesophyll factors and tolerance to high irradiance allow the plants to maintain a positive carbon balance and growth in a stressful environment.
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ACKNOWLEDGEMENTS |
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We thank Dr R. Urich for critically reading the manuscript and Martha Francisco for measurements of the soil electrical conductivity. We also thank T. D. Colmer and J. Flexas for reviewing the manuscript and making very useful comments and suggestions. This work was supported by CONICIT grants S1-99000054 and S1-96001345 and CDCH grants 03-33·4342·2000 (Venezuela).
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LITERATURE CITED |
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