Physiological response of field-grown cabbage to salinity and drought stress

Europ. J. Agronomy 23 (2005) 57–67

Physiological response of field-grown cabbage tosalinity and drought stress

A. Maggio, S. De Pascale∗, C. Ruggiero, G. Barbieri

Department of Agricultural Engineering and Agronomy, University of Naples Federico II, Via Universit`a 100, Portici (NA) 80055, Italy

Received 21 April 2004; received in revised form 13 September 2004; accepted 22 September 2004

Abstract

Soil salinization of arid and semiarid regions of the world is a major problem of irrigated agriculture. On a long-term salinizedsoil, we assessed growth response and water relations of cabbage plants irrigated with saline water. In addition, we comparedplant performances under salt and drought stresses. Two NaCl concentrations of the irrigation water were considered, 0.25%(SW1) and 0.50% (SW2), corresponding to electrical conductivity (ECw) of 4.4 and 8.5 dS m−1 and osmotic potentials (OP)of −0.22 and−0.35 MPa, respectively. Furthermore, a non-salinized control (NSC, ECw = 0.5 dS m−1; OP =−0.02 MPa) and anon-irrigated control (NIC) were included. In salinized plants, midday leaf total and osmotic water potentials decreased duringthe growth season. NIC plants had the lowest leaf water potential (−1.5 MPa at harvest). The shoot/root ratio of NIC plantswas 40% smaller than NSC plants. We did not find significant differences among the shoot/root ratios of plants under differentsalinity treatments. A 39% yield reduction was found upon salinization. Drought stress decreased the total head yield from50.5 t ha−1 (NSC) to 17.5 t ha−1 (NIC). A modified Maas–Hoffman relationship of the relative growth, expressed as leaf area or

sed plantsrrelation

o salinitydaptationse resultsy (0.25%

reas

aboveground dry mass per plant versus leaf total or osmotic water potentials of the combined drought and salt stresrevealed similar slope and threshold values for the two growth parameters. However, we did not find a significant cobetween leaf osmotic potential and leaf area per plant. Although it is known that plants share similar responses tand drought stresses, our results indicate that morphological (shoot/root ratio) and metabolic (osmotic adjustment) amechanisms may significantly diverge in salt versus drought stressed plants. While the agronomic implications of thesuggest that the cultivation of cabbage in some Mediterranean environments is still feasible at moderate/low salinitNaCl) they also highlight physiological responses, which certainly require further investigation.© 2004 Elsevier B.V. All rights reserved.

Keywords: Brassica oleraceaL. CapitataGroup; Root and leaf water potentials; Root density; Plant growth; Salt tolerance

∗ Corresponding author. Tel.: +39 0812539127;fax: +39 0817755129.

1. Introduction

Yield and quality traits of vegetable crops aadversely affected by environmental factors suchdrought and/or high salinity of the root zone (Goyal

E-mail address:[email protected] (S. De Pascale).

1161-0301/$ – see front matter © 2004 Elsevier B.V. All rights reserved.doi:10.1016/j.eja.2004.09.004

58 A. Maggio et al. / Europ. J. Agronomy 23 (2005) 57–67

et al., 2003). It is recognized that water and ion home-ostasis are the main physiological processes that plantsneed to optimize to resume growth in saline environ-ments (Lauchli and Luttge, 2002). Nevertheless, in thefield, salt stress induced detrimental effects on growthand yield depend on several factors such as the level ofstress experienced, the time of exposure to the stress,the rainfall pattern during the growth season and thesoil physical–chemical properties (Maas and Grattan,1999). All these factors may interact in a dynamicfashion throughout the growth season (Maggio et al.,2002a). The complexity of such response may lead tosubstantial variations of the salt tolerance threshold(Maas and Hoffman, 1977), the physiological basisof which has been critically discussed (Dalton etal., 1997; De Pascale et al., 2003a). As a consequence,alternative indexes to assess plant salt tolerance suchas the Salinity Stress Index (SSI) (Dalton et al., 2001)and the Water Stress Day Index (Katerji et al., 2003),have been described. One source of variability is theplant species (Ayers and Westcot, 1989). Even withinthe same species, different cultivars or ecotypes maydiverge significantly in terms of salt (and/or drought)stress tolerance. Such variability has been reportedwithin Brassica oleraceaL. CapitataGroup, a poly-morphic species, which has probably evolved fromthe wild sea cabbage (Csizinszky, 1996; Maas andGrattan, 1999). There has been a renewed interest incultivating Brassicaspecies as a consequence of thehigh concentration of isothiocyanates and similar com-p er,w oper-t ich,2o stalae ep forei ichm hiss -a alin-ie alinei ieldo jec-t aterr line

water in a long-term salinized soil, (2) to define itsphysiological response and (3) to specifically compareplant performances under salt and drought stresses.

2. Materials and methods

2.1. Study site and experimental treatments

The experiment was carried out in 1996 at the ex-perimental farm of the University of Naples (40◦31′N,14◦58′E) on a field that had been irrigated with salinewater for the past 8 years (De Pascale and Barbieri,2000). The experimental field was a clay loam soil with42% sand, 27% loam, 31% clay and trace amounts oflime. Water contents at field capacity (in situ) and at−1.5 MPa are reported inTable 1. The experimentaltreatments consisted of two NaCl concentrations of theirrigation water, 0.25% (SW1) and 0.50% (SW2), cor-responding to electrical conductivity (ECw) of 4.4 and8.5 dS m−1 and osmotic potentials (OP) of−0.22 and−0.35 MPa, respectively. Furthermore, a non-salinizedcontrol (NSC, ECw = 0.5 dS m−1; OP =−0.02 MPa)and a non-irrigated control (NIC) were included.Saline water was obtained by adding commercialsea salt (Na+, 12.3 mol kg−1; K+, 3.8 mol kg−1;Ca2+, 0.02 mol kg−1; Mg2+, 0.04 mol kg−1; Cl−,14.4 mol kg−1; SO4

2−, 0.03 mol kg−1) to the irriga-tion water (Na+, 0.53 mol m−3; K+, 0.05 mol m−3;Ca2+, 1.55 mol m−3; Mg2+, 0.84 mol m−3; Cl−,04i emw ieda tionb lass“ ed

TW (FC)a late(

S

0 6.60 6.6

N 1 =4

ounds found in cabbage, broccoli and cauliflowhich have been proved to possess anticancer pr

ies (Chung et al., 1996; Hecht et al., 1996; Wargov000). In Mediterranean environments,Brassicaandther vegetable crops are often cultivated in coareas, in which soil salinization often occurs (Beltraot al., 2000; Vallejo et al., 2003). Understanding thhysiological basis for salt stress tolerance is there

mportant to identify proper cultural practices, whay be functional to extend the cultivation of t

pecies in sub-optimal areas. Cabbage (Brassica olercea) has been ranked as moderately sensitive to s

ty (Bernstein and Ayers, 1949; Osawa, 1961). How-ver, data on the field response of this species to s

rrigation are rather scarce, either in terms of plant yr physiology of adaptation. In this respect, the ob

ives of this study were (1) to evaluate growth and welations of field-grown cabbage irrigated with sa

.38 mol m−3; SO42−, 0.15 mol m−3; HCO3

−,.73 mol m−3). Each experimental plot of 100 m2 was

rrigated every 7 days using a drip irrigation systith 2 l h−1 emitters. The amount of water applt each irrigation was equal to the net evaporaetween two irrigations as determined using a c

A” pan evaporimeter. A pan coefficient of 1 was us

able 1ater content (% volume) at field capacity determined in situ

nd water content at−1.5 MPa determined using a pressure pWP) in the 0–0.3 and 0.3–0.6 m soil layers

oil layer (m) NIC–NSC SW1 SW2

FC WP FC WP FC WP

–0.3 35.5 17.5 34.7 16.8 33.9 1.3–0.6 35.9 17.5 35.3 17.6 34.8 1

SC, non-salinized control; NIC, non-irrigated control; SW.4 dS m−1 and SW2 = 8.5 dS m−1.

A. Maggio et al. / Europ. J. Agronomy 23 (2005) 57–67 59

for the entire growing season to include a leachingfraction in the total volume of water applied at eachirrigation event. The estimated water consumption wasbased on a non-stressed crop so all treatments (withthe exception of NIC) received the same amount ofwater. However, since crop growth was reduced understress, the transpiration was reduced too. Therefore,salt-treated plants actually received higher leachingfractions compared to non-stressed plants.

2.2. Growth conditions

On June 10, cabbage seedlings (Brassica oler-acea CapitataGroup cv Peto PSX 286) were placed0.45 m apart within rows and rows were planted 0.70 mapart. Before transplanting, 80 kg N ha−1 (ammoniumsulphate), 100 kg P2O5 ha−1 (superphosphate) and150 kg K2O ha−1 (potassium sulphate) were applied tothe soil. After transplanting, plants were side-dressedwith additional nitrogen fertilizer (40 kg N ha−1 asurea). Two irrigations (30 mm) with non-saline wa-ter were used to ensure establishment of the plantlets.Saline treatments were initiated 17 days after trans-plant (June 27). The total amount of water applied fromthe beginning of the salt treatments until harvest was385 mm (distributed in eight irrigations). Harvest wasbegun 70 days after transplanting (August 19).

2.3. Water potential measurements

roxi-m cle( ntial( . ont ands ) ofs reat-m yer.M singa -m eds st icp

ingsΨ icp ed

plants (NSC) andΨ�RWC is the product of osmotic po-tential× relative water content of leaves from salinizedor non-irrigated plants. For each measurement, the rela-tive water content was calculated as: RWC = leaf freshweight− leaf dry weight/leaf saturated weight− leafdry weight (Morgan, 1984).

2.4. Soil

Soil samples from each experimental plot weretaken the day before and 2 days after each irrigation,at two soil layers (0–0.3 m and 0.3–0.6 m depth) formeasurements of electrical conductivity on saturatedsoil extracts (ECe) and soil water content (after dryingthe soil samples at 105◦C until steady weight). The soilmatric potential was estimated in the 0–0.6 m soil layerfrom the soil moisture characteristic curves [h (θ)]. Theosmotic potential of the soil water in the 0–0.6 m soillayer was derived by ECe measurements (Rhoades etal., 1992). Total soil water potentials were calculatedby adding to the matric water potential values the cor-responding osmotic potential values normalized for theactual soil water contents measured before each irriga-tion event.

2.5. Plant growth

After the first irrigation with saline water, nine plantsper treatment were collected, at 10-day intervals untilharvest, for growth analysis. Leaf area was measuredu ln,N d at7 asc leafa e ra-t ils m in-t areu a-r ith a1 ex-a ErbaO ass-i den-s Ther ther eachs bove

Plant water potentials were measured at appately 10-day intervals throughout the growth cy

total of seven measurements). Total water poteΨ t) was measured between 12:00 and 1:00 p.missue discs punched from fully expanded, healthyun-exposed leaf and on excised segments (8 cmecondary roots taken from nine plants per each tent (three per each block) in the 0–0.3 m soil laeasurements were performed before irrigation, uthermocouple psychrometer type B at 29◦C. The osotic potential (Ψ�) was measured on frozen/thaw

amples and pressure potential (Ψp) was estimated ahe difference betweenΨ t andΨ�, assuming a matrotential equal to zero (De Pascale et al., 2003b).

Leaf osmotic adjustment (OA) during the groweason was determined as the differenceΨ�oRWCo −�RWC, whereΨ�oRWCo is the product of osmototential× relative water content (RWC) of unstress

sing a Li-Cor 3000 leaf area meter (Li-Cor, LincoE, USA). Shoots (leaves and petioles) were drie0◦C and weighed. Specific leaf weight (SLW) walculated as the ratio between leaf dry weight andrea. Leaf succulence (LS) was calculated as th

io (leaf fresh weight− leaf dry weight)/leaf area. Soamples for root measurements were taken at 0.3-ervals in the 0–0.6 m soil layer, where most rootssually found (Katerji et al., 1994). Roots were sepated from soil particles by treating each sample w0% (w/v) Calgon wetting solution (85% sodium hmetaphosphate, 15% sodium carbonate: CarloTC-Pharmacia, Milan, Italy) and subsequently p

ng roots through a 0.2-mm metal screen. The rootity was estimated by Newman’s method (1966).oot dry mass per plant was estimated by weighingoot dry mass in 50 g soil sub-samples (three peroil depth). Roots were separated as described a


and dried in oven at 70◦C. The root dry mass per unitmass of soil (g g−1) was then referred to the entire rootsoil volume (0.05 m3).

At harvest, plants were cut at the soil surface,trimmed by removing the oldest external leaves,counted and weighed.

Growth responses to salt and drought stress weredescribed by using a modified version of the threshold-slope model proposed byMaas and Hoffman (1977):Yr = 100− S(T− Ψ ), whereYr is the relative growth,i.e. the plant growth (in terms of leaf area or above-ground dry mass per plant) expressed as percentageof the growth obtained under non-stress conditions,Tis the plant or soil water potential threshold expressedin MPa,S is the growth reduction percentage per unitwater potential below the thresholdT, andΨ is the time-weighted average water potential. Expressing the rela-tive growth (Yr) as a function of plant or soil water po-tential allowed us to combine the effects of both waterand salt stress on plant yield and growth performances.

Sodium and chloride concentrations were measuredin dried and ground tissue sub-samples from youngfully expanded not-senesced external leaves of nineplants per each treatment (three plants per block) byatomic absorption spectrophotometry and by coulo-metric titration, respectively (Walinga et al., 1995).

2.6. Experimental design

The experimental field used in this experiment hasb thatt ong-t al–c irri-g andn izedb acht imen-t db n’sM

3

3

m( 2nd

Fig. 1. Air temperature (Y1 (open square, 1996; closed square, 40-year averages)), rainfall (Y2 (open circle, 1996; closed circle 40-yearaverages)) and class A pan evaporation (Y2 (white histogram, 1996;grey histogram, 20-year averages)). On theX-axis, each month issubdivided in 10-day periods, as indicated by roman numerals.

decade of July), slightly lower than the 40-years meanvalue (58 mm). Mean temperature ranged between 22.2and 25.3◦C and was also a little lower compared tothe 40-year average temperature especially during Juneand July. Class “A” pan evaporation during the irriga-tion season was 494 mm, consistent with the 20-yearaverage (471 mm) (Fig. 1).

3.2. Soil water potential

Matric water potential in the NIC plots during thegrowth season decreased from−0.17 to −1.0 MPawith a sharpΨ decline at 51 days after transplant-ing (Fig. 2A). For all the other treatments, irrigationwas effective in maintaining the matric water poten-tial above−0.08 MPa. At transplanting (June 10) themean electrical conductivity of the saturated soil ex-tracts (ECe) in the 0–0.6 soil layer were 2.06, 2.44,2.65 and 1.47 dS m−1 for NSC, SW1, SW2 and NIC,respectively. At harvest the ECe reached 2.43, 4.94,7.92 and 1.67 dS m−1 for the same treatments. Conse-quently, the total water potential decreased at increas-ing salinity reaching−0.7 MPa for the most salinizedplants (SW2) (Fig. 2B).

3.3. Plant water potential

Fig. 3displays soil, leaf and root water potentials forNSC plants. Midday leaf and root total water potentials( ea-s he

een irrigated with saline water since 1988. Atime, we began a project aimed at evaluating the lerm effects of soil salinization on both soil physichemical properties and plant response to salineation. The salinity treatments plus non-salinizedon-irrigated controls were arranged in a randomlock design with three replications. Since 1988 e

reatment has been reassigned to the same experal plot (De Pascale et al., 2003b). Data were analyzey ANOVA and means were compared by Duncaultiple Range Test.

. Results

.1. Climatic conditions

Rainfall throughout the growing period was 49 m19 mm at the end of June and 21 mm during the

Ψ t) were relatively stable throughout the growth son with a slight drop during the first 10 DAT in t


Fig. 2. Soil matric (A) and total (B) water potentials in the0–0.6 m soil layer during the growth season. Samples were takenthe day before and 2 days after each irrigation. NSC, non-salinized control; NIC, non-irrigated control; SW1 = 4.4 dS m−1 andSW2 = 8.5 dS m−1. Mean± S.E. (n= 3).

roots and a moderate increase, at beginning of headenlargement (50 DAT), in the shoot. In contrast, weobserved a moderate yet constant decrease in both leafand root osmotic potentials. The increased leaf waterpotential during head enlargement was associated to a

Fig. 3. Soil, leaf and root water potentials vs. time (days after trans-planting) for non-salinized control plants (NSC). Mean± S.E. (n= 3for soil andn= 9 for leaf and roots).

moderate increase of leaf turgor as shown by the in-creased differences between total and osmotic leaf wa-ter potentials. InFig. 4, leaf and root water potentials forSW1, SW2 and NIC are compared to the non-stressedcontrol (NSC). NIC plants had the lowest leaf water po-tential, which decreased throughout the growth season(−1.5 MPa at harvest) at decreasing soil water poten-tial. Salinity decreased the leaf water potential also,although differences between the two salt treatmentswere not significant. The total root water potential ofSW1 plants was quite similar to NSC plants, whereas,with the exception of the first 30 DAT, there were nodifferences between NIC and SW2 treatments. Leafand root osmotic potentials decreased with salinity anddrought stress and they resembled the leaf and rootwater potential patterns. For all treatments it was ob-served a moderate increase of leaf turgor at the end ofthe growth cycle (data not shown).

3.4. Root growth

Root development was affected by salinity(Fig. 5A). The maximum root length was reached 63days after transplanting. Root length was greater in NICcompared to salinized plants. NSC plants had the mostexpanded root system while SW2 plants had the least.Root dry mass proportionally decreased at increasingsalinity of the irrigation water. However, drought stressdid not affect root dry mass accumulation (Fig. 5B).

3

antr c-c no aftert ntsr ftert ntilh r in-cs er ofl ents(

entf ym ntlyh of ir-

.5. Plant growth and yield

Irrigation with saline water resulted in a significeduction of leaf area and aboveground dry matter aumulation (Fig. 6). The negative effect of salinization leaf area development was evident one month

ransplanting. Leaf area of salinized and NIC plaeached its maximum during the first 45 days aransplanting and it did not significantly change uarvest. In contrast, leaf area of NSC plants furthereased during the same time period (Fig. 6A). Droughttress affected mostly the leaf size since the numbeaves per plant was similar among stress treatmTable 2).

Dry matter accumulation and leaf area developmollowed similar patterns (Fig. 6B). However, the dratter accumulation of SW1 plants was significaigher compared to the SW2 plants. The absence


Fig. 4. Leaf and root total and osmotic potentials vs. time (days after transplanting). NSC, non-salinized control; NIC, non-irrigated control;SW1 = 4.4 dS m−1 and SW2 = 8.5 dS m−1. Mean± S.E. (n= 9).

rigation caused a significant reduction in plant growth.By the end of the season, leaf area and aboveground dryweight were 32 and 22% smaller in salt stressed plants(average of the two treatments), respectively, comparedto NSC plants, whereas in NIC plants both parameterswere 46% smaller than NSC plants. Plant dry matter ac-cumulation increased in irrigated plants until harvest. Incontrast, dry matter accumulation in NIC plants endedapproximately 60 days after transplanting.

For all treatments, the shoot/root ratio increased un-til 45 DAT during which time the shoot growth wasfaster than root (Fig. 7). From this stage until 65 DAT,

shoot and root growth rates were similar. Consequently,the shoot/root ratios remained relatively stable withthe exception of a slight drop in absence of irriga-tion. At 65 DAT there was a sharp increase in theshoot/root ratio, most likely associated with both thereduced root growth (Fig. 5) and the end of head en-largement occurred during the last part of the growthcycle. Drought-induced shoot growth inhibition wasgreater compared to root growth inhibition. As a con-sequence the shoot/root ratio of NIC plants was 40%smaller than NSC plants (Table 2). We did not findsignificant differences among the shoot/root ratios of

Table 2Growth parameters at harvest in non-salinized and salinized cabbage plantsa

Plants (n, m−2) Head FW (kg) Leaves (n, plant−1) Leaf area (dm2 plant−1) Shoot/root Mean leaf area (cm2)

NSC 2.9 1.15 a 16.3 a 104.9 a 1.35 a 643 abSW1 2.8 0.76 b 10.3 b 68.2 b 1.24 a 662 aSW2 2.9 0.68 b 10.0 b 59.6 bc 1.22 a 596 bNIC 2.8 0.34 c 11.3 b 54.5 c 0.63 b 482 c

Head FW, trimmed head mean fresh weight; NSC, non-salinized control; NIC, non-irrigated control; SW1 = 4.4 dS m−1 and SW2 = 8.5 dS m−1.a Mean separation within columns by MRT atP≤ 0.05.


Fig. 5. Root length (A) and root dry matter accumulation (B) duringthe growth season. NSC, non-salinized control; NIC, non-irrigatedcontrol; SW1 = 4.4 dS m−1 and SW2 = 8.5 dS m−1. Mean± S.E.(n= 9).

plants under different irrigated treatments (Table 2andFig. 7).

The head fresh weight was affected by salinity(39% reduction) with no difference between SW1 andSW2 plants (Table 2). Drought stress decreased the to-tal head yield from 50.5 t ha−1 (NSC) to 17.5 t ha−1

(NIC). The reduced yield was mainly caused by a re-duction in head size rather than head number, sinceplants survival at harvest remained unaffected by noirrigation or salinity (Table 2). Increasing salinity ofthe irrigation water proportionally reduced the headfresh weight, yet it increased the dry matter per-centage both in leaves and heads. The dry matterpercentage in leaves and heads of the NIC plantswere significantly higher than those of salinized plants(Table 3).

Both salt and drought stress affected the specificleaf weight, which was significantly higher in NIC andSW2 plants, relative to NSC plants. Leaf succulencewas similar in non-salinized and non-irrigated control

Fig. 6. Leaf area development (A) and dry matter accumulation(B) during the growth season. NSC, non-salinized control; NIC,non-irrigated control; SW1 = 4.4 dS m−1 and SW2 = 8.5 dS m−1.Mean± S.E. (n= 9).

plants, whereas it increased at increasing salinity(Table 3).

When the relative growth, expressed either as leafarea or as aboveground dry mass per plant, was plot-ted versus leaf total or osmotic water potentials of the

Fig. 7. Shoot/root ratio vs. time (days after transplanting). NSC, non-salinized control; NIC, non-irrigated control; SW1 = 4.4 dS m−1 andSW2 = 8.5 dS m−1. Mean± S.E. (n= 9).


Table 3Leaf and head dry matter (DM) percentage, osmotic adjustment (OA), specific leaf weight (SLW), leaf succulence (LS) and leaf Na and Clcontent of cabbage plantsa

Leaf DM(%)

Head DM(%)

Leaf OA(MPa)

SLW(g DM dm−2)

LS(g H2O dm−2)

Leaf Na(moles kg DM−1)

Leaf Cl(moles kg DM−1)

NSC 13.46 a 5.31 a – 1.17 a 7.48 a 0.042 a 0.048 aSW1 13.80 a 7.34 b 0.41 b 1.23 b 7.88 b 0.312 b 0.304 bSW2 15.94 b 7.99 b 0.48 a 1.44 c 7.94 b 0.537 c 0.554 cNIC 16.84 b 10.68 c 0.34 c 1.47 c 7.54 a 0.048 a 0.042 a

NSC, non-salinized control; NIC, non-irrigated control; SW1 = 4.4 dS m−1 and SW2 = 8.5 dS m−1.a Mean separation within columns by MRT atP≤ 0.05.

combined drought and salt stressed plants, slope andthreshold values were very similar for the two growthparameters. Interestingly, we did not find a significantcorrelation between leaf osmotic potential and leaf areaper plant, suggesting that accumulation of inorganicand/or organic osmolytes may affect differently plantgrowth and adaptation in saline or drought environment(Fig. 8).

Fd aterp

3.6. Osmotic adjustment and leaf Na+ and Cl−contents

The leaf osmotic adjustment was higher in salinizedcompared to drought stressed plants and it was propor-tional to the salt concentration of the irrigation water(Table 3). A significant increase in leaf concentrationof Na+ and Cl− was observed in salt stressed plants(Table 3). Using the Van’t Hoff equation (Nobel, 1991)to calculate the osmotic pressure for the cell sap of theleaves (at 20◦C), we found that the contribution of Na+

and Cl− ions to the overall leaf osmotic potential was1.4% for NSC and NIC plants, whereas it increasedfrom 9 to 18% in SW1 and SW2 plants, respectively.The accumulation of Na+ and Cl− ions may have par-tially accounted for the observed differences in osmoticadjustment between salinized and non-irrigated plants(Table 3).

4. Discussion

Salinity and drought caused a significant reduc-tion of the photosynthesizing leaf area and a re-markable decrease of plant dry matter accumulation.However, salt stressed plants were much more sen-sitive in terms of leaf area development comparedto aboveground dry matter accumulation. At the endof the growth season, a 50% leaf area reductiono ina antsa to a2 u-m useda ro-m ther

ig. 8. Relative growth (expressed as leaf area and as abovegroundry mass per plant) vs. leaf total (A) and leaf osmotic (B) wotentials. Each point is the mean of nine samples.

f NIC plants, coincided with a 50% reductionboveground dry mass. In contrast, in salinized pl50% leaf area reduction corresponded only

5% reduction of the aboveground dry matter acculation. These results suggest that salinity can increase in leaf thickness or, alternatively, poted reallocation of photosynthates in stems or o


green organs, which did not occur in drought stressedplants.

Drought stress inhibited shoot more than rootgrowth and it caused a remarkable decrease of theshoot/root ratio. Although drought and salinity stressmay promote similar morphological responses, thiswas not the case of the shoot/root ratio. While itis well established that a decreased shoot/root ratiois a morphological adaptation to drought (Cuarteroand Fernandez-Munoz, 1999), its functional role un-der salinity is to date a controversial issue (Maggio etal., 2001). Indeed low shoot/root ratios may be detri-mental under salt stress since they may enhance theaccumulation of toxic ions into the shoot and, conse-quently, may anticipate the oncoming of the salt tol-erance threshold (Dalton et al., 1997; Munns, 2002).Consistent with this view, salinized cabbage plants didnot significantly decrease their shoot/root ratios, as oc-curred for drought stressed plants. Although this find-ing may be interpreted as a functional adaptation to thestress, we cannot assess at the moment a cause–effectrelationship for this response.

Head growth inhibition was associated with smallerleaf size since the leaf number was affected similarlyby salinity or drought. This was probably caused by areduced leaf expansion during the head growth. Leafturgor potential, calculated as the difference betweenleaf total and osmotic water potentials, significantly in-creased during the growth season in NSC plants (0.28and 0.57 MPa at 25 and 58 DAT, respectively) (Fig. 3).A ants( ly).C able( t theg ofh eadg soci-a ty tooB eo tainh if-i u-m tes( is-t cu-l edl r to

an increased number of spongy cell layers (Longstrethand Nobel, 1979; Shannon, 1997).

To simultaneously compare plant response to bothsalt and drought stress, we used a modified versionof the threshold-slope model based on the soil wa-ter potential (Ψs) as independent variable. The relativeyield (Yr) was correlated to the soil water potential forthe salinity plus NSC treatments (r = 0.987* ) (data notshown). In contrast, drought stressed plants appearedto be much more sensitive than salt stressed plants atsimilarΨs, indicating that a decrease inΨs due to a de-crease in soil matric potential (Ψm) may be more harm-ful for plant growth than a similar decrease in osmoticpotential (Ψ�). Alternatively, it is possible that the re-sponses of salt and drought stressed plants to variationsin soil water potentials cannot be directly compared.Similar results were previously reported for celery (DePascale et al., 2003b). Interestingly, when the relativegrowth was plotted versus leaf water potentials of thecombined drought and salt stressed plants (Fig. 8), weidentified a linear relationship between growth and leafwater potential components. The significant correla-tion between relative growth and leaf water potentialssuggests that yield may better respond to the internal(plant water potential) than to the external plant en-vironment (root zone soil water potential). In this re-spect,Dalton et al. (1997, 2000), have recently dis-cussed this issue and have proposed a dynamic Salin-ity Stress Index to evaluate plant salt tolerance, whichintegrates the roots biophysical properties that controli blest ug-g atesm evelt ootr ,2 lantm nsi al-l linee eenr re-v cpd tot leafo enta s via

n opposite response was observed for NIC pl0.20 and 0.10 MPa at 25 and 58 DAT, respectiveonversely, the turgor pressure was relatively st

SW1) or moderately increased (SW2) throughourowth season (Fig. 4). Possibly, the maintenanceigh leaf turgor was functional to support the hrowth upon salinization. Several authors have asted tissue turgor maintenance to the plant’s abilismotically adjust in saline environments (Meyer andoyer, 1981; Munns and Termaat, 1986). In the absencf irrigation, cabbage plants were unable to mainigh leaf cellular turgor and their growth was sign

cantly impaired relatively to salinized plants. Acculation of inorganic and, possibly, organic osmoly

Maggio et al., 2002b) in salinized plants was consent with higher osmotic adjustment and leaf sucence (Table 3), which may also reflect an increaseaf thickness due either to longer palisade cells o

on loading to the shoot under environmental variahat affect both transpiration and growth. The SSI sests that adaptation to saline environments implicetabolic adjustments at cellular and whole plant l

hat ultimately lead to regulate the ion flux to the shelative to the plant growth rate (Maggio et al., 2001002a). The proposed model also implicates that paymorphologicallyadjust to cope with excess io

n the nutrient solution. In line with a functional reocation of photosyntates to control growth in sanvironment, there was a strong relationship betwelative growth versus leaf osmotic potential thatealed interesting insights (Fig. 8B). The leaf osmotiotential was strongly correlated to the abovegroundry mass (r = 0.99** ), whereas it was not correlated

he leaf area per plant, indicating that a decreasedsmotic potential may contribute to osmotic adjustmnd may enhance growth under salt/drought stres


turgor maintenance (Morgan, 1984; Hare et al., 1998)until a certainstress threshold.Once such thresholdhas been reached, ion toxicity may cause reallocationof photosynthates among plant organs to functionallyadjust leaf versus root development to control transpi-ration and, ultimately, the ion flux to the shoot. Similarresults have recently been reported byKaterji et al.(2003), who also found that the salinity effect on leafarea does not seem to be correlated with the plant’s ap-titude for osmotic adjustment. The resource allocationefficiency within the plant may be therefore an impor-tant aspect of drought or salt tolerance (Hare et al.,1998). Although upon salinization Na+ and Cl− ionsare readily available and plants use these to maintainturgor, after a certain concentration they may act asa signal to control the shoot/root ratio for optimizinggrowth in a specific environment. Thissignal is notpresent in drought stress plants, which at similar leafosmotic potential had a larger leaf area compared towhat we would have expected by the leaf area versusosmotic potential relationship (Fig. 8B) and, moreover,had a larger root system. Certainly, drought stressedplants have a limited access to Na+ and Cl− ions andthey may divert sugars and other metabolic compoundsfor osmotic adjustment at the expense of growth. Thismay provide an explanation for higher yield of salin-ized versus drought stressed plants at similar levels ofsoil Ψs.

Overall our results indicate that morphological(shoot/root ratio) and metabolic (osmotic adjustment)a e ins nismsc vels ss.

at inM linity( houte s ath iont d bes

R

A re., pp.

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Cuartero, J., Fernandez-Munoz, R., 1999. Tomato and salinity. Sci-entia Hort. 78, 83–125.

Dalton, F.N., Maggio, A., Piccinni, G., 1997. Effect of root tem-perature on plant response functions for tomato: comparison ofstatic and dynamic salinity stress indices. Plant Soil 192, 307–319.

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Dalton, F.N., Maggio, A., Piccinni, G., 2001. Assessing the affect ofsolar radiation on plant salt tolerance using static and dynamicsalinity stress indices. Plant Soil 229, 189–195.

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De Pascale, S., Maggio, A., Ruggiero, C., Barbieri, G., 2003a. Phys-iological responses of pepper to salinity and drought. J. Am. Soc.Hort. Sci. 128 (1), 48–54.

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G on in. Ha-

H roles. 21,

H ova,96.4-

cti-17,

K ctyieldr Re-Bari),

K lin-ler-ater

daptation mechanisms may significantly divergalt versus drought stressed plants. Such mechaertainly require further investigation to identify notrategies for improving plant productivity under stre

From an agronomic perspective we may say thediterranean environments at moderate water sa

0.25%), cabbage plants are able to acclimate witxcessively impairing the marketable yield, whereaigher salinity (0.5%) or in the absence of irrigat

he economic benefits of cultivating cabbage wouleriously jeopardized.

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Physiological response of field-grown cabbage to salinity and drought stress