mycorrhizal influence on fruit yield and mineral content of tomato

JOURNAL OF PLANT NUTRITION, 24(8), 1311±1323 (2001)

MYCORRHIZAL INFLUENCE ON FRUIT YIELD AND MINERAL CONTENT OF TOMATO GROWN UNDER SALT STRESS Ghazi N. Al-Karaki* and R. Hammad Faculty of Agriculture, Jordan University of Science and Technology, P.O. Box 3030, Irbid, Jordan

ABSTRACT Tomato (Lycopersicon esculentum Mill.) yields are known to decrease for plants grown in saline soils. This study was conducted to determine the effects of arbuscular mycorrhizal fungi (AMF) inoculation on fruit yield and mineral content of salt-tolerant and salt-sensitive tomato cultivars grown with varied levels of salt. NaCl and CaCl2 were added to soil in the irrigation water in equal molar ratios to give ECe values of 1.4 (nonstressed) and 4.9 dS mÿ 1 (salt stressed). Plants were grown in a greenhouse using unsterilized, low phosphorus (P) (silty clay) soil-sand mix. Mycorrhizal root colonization occurred whether cultivars were salt stressed or nonstressed, but the extent of AMF root colonization was higher in AMF inoculated than uninoculated plants. The salt tolerant cultivar `Pello' generally had higher AMF root colonization than the salt sensitive cultivar `Marriha'. Shoot dry matter (DM) yield, fruit fresh yield, and AMF colonization were higher for plants grown under *Corresponding author. E-mail: [email protected] 1311 Copyright # 2001 by Marcel Dekker, Inc.

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AL-KARAKI AND HAMMAD

nonstressed than for plants grown under salt stressed conditions. Shoot DM and fruit fresh yields were higher in AMF inoculated than uninoculated plants grown with or without salt stress. Pello generally had higher fruit fresh yield per plant and fruit weight than Marriha, but these differences were only signi®cant for fruit weight in unioculated plants grown under salt stressed conditions. The enhancement in fruit fresh yield due to AMF inoculation was 26 and 23% under nonstressed and 28 and 46% under salt stressed treatments for Pello and Marriha, respectively. For both cultivars, fruit contents of P, potassium (K), zinc (Zn), copper (Cu), and iron (Fe) were higher in AMF inoculated compared with uninoculated plants grown under nonstressed and salt stressed conditions. Fruit Na concentrations were lower in AMF inoculated than uninoculated plants grown under salt stressed conditions. The enhancement in P, K, Zn, Cu, and Fe acquisition due to AMF inoculation was more pronounced in Marriha than in Pello cultivar under salt stressed conditions. The results of this study indicated that AMF inoculated plants had greater tolerance to salt stress than unioculated plants. INTRODUCTION Soil salinity is a major factor responsible for decreasing plant productivity on irrigated arid and semiarid land (1,2). These areas are characterized by limited rainfall and high evapotranspiration because of high temperatures. Irrigation water containing concentrated dissolved salts as water evaporates leads to a build up of salts in soil over time. If salts are not leached from soil, roots must grow with increasing amounts of detrimental salt levels. As a result of increased salinity, plant growth and yield potential are reduced (3,4). Increased salinity also reduces water availability and nutrient uptake by plants (5,6). Detrimental effects of salinity on plant growth result from direct effects of ion toxicity (5,7,8) or indirect effects of saline ions that cause soil/plant osmotic imbalances (9). Using conditions which enable plants to withstand salt stress would be helpful for improving crop production under saline conditions. The introduction of AMF to sites with saline soil may improve plant tolerance and growth (10,11,12). The improved productivity of AMF plants has been attributed especially to enhanced acquisition of low mobile nutrients such as P, Zn, and Cu (10,13,14,15,16), and to improved water relations (17,18,19). The ability of AMF inoculant to stimulate plant growth was found to vary in sterile soils and in natural soils in the presence of indigenous AMF (20). Information on AMF effects on fruit yield is limited, possibly because most experiments with AMF are

TOMATO GROWN UNDER SALT STRESS

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conducted in pot cultures, where plants are not usually grown to maturity and where root-volume constraints limit AMF effectiveness (21,22). Symbiotic interactions between AMF and host plants grown under salt stress conditions, especially relative to fruit yield and mineral contents, need to be studied to optimize the bene®cial effects of AMF. The objectives of this study were to determine effects of salt stress and AMF inoculation on fruit yield and mineral contents by tomato cultivars differing in salt tolerance. MATERIALS AND METHODS A greenhouse experiment was conducted at 25 5 C under natural illumination during March±June 1999, at Jordan University of Science and Technology campus. Tomato plants were grown in a nonsterilized silty clay soil (®ne, mixed, thermic, Typic Xerochrept) mixed with sand [soil:sand, 2:1 (v/v)]. Soil properties before mixture with sand were 7% sand, 45% silt, and 48% clay; 1.2% organic matter; pH 8.1 (soil:water, 1:1); electrical conductivity (ECe) 1.4 dS mÿ 1; 0.26 P (NaHCO3-extractable), 23.1 K, 6.2 Na, 0.2 Fe, 0.02 Zn, and 0.03 Cu (5 mM DTPA-extractable) in mmol kgÿ 1 soil. Soil contained indigenous AMF spores; 360 chlamydospores kgÿ 1 air-dried soil. The soil mix was dispensed into plastic pots (16 L) for plant growth. No P was added to the soil. Half of the pots received the AMF Glomus mosseae (Nicol. and Gerd.) Gerd. and Trappe by placing 50 g (moist weight) of inoculum in soil below tomato seedlings prior to planting. The AMF inoculum consisting of soil and root fragments and spores; 1350 chlamydospores kgÿ 1 air-dried soil was placed directly adjacent to seedling roots. Mycorrhizal inoculum (Glomus mosseae) was initially isolated from a wheat (Triticum durum Desf.) ®eld in northern Jordan (23) and multiplied in pot cultures using chickpea (Cicer aritinum L.) as a host (13). Control treatments received no AMF inoculum. Seeds of tomato cultivars [Pello (salt-tolerant) and Marriha (salt sensitive); Al-Karaki (24)] were germinated in moist mix of peat and sand in polystyrene trays. Two uniform sized 20-d-old seedlings, uniform in size were transplanted into each pot. Nitrogen was added at 30 mg N kgÿ 1 soil as NH4NO3 after 7 and 30 days of seedlings transplantation. Plants were established for three weeks before they were subjected to two salt levels by adding solutions of NaCl and CaCl2 in equal molar ratios (1 M NaCl:1 M CaCl2) to soil through irrigation water, which resulted in saturation extract (ECe) values of 1.4 (nonstressed) and 4.9 dS mÿ 1 (salt stressed). To avoid osmotic shock, the salt was added in equal increments twice a week until the desired level had been reached after 3 weeks. Thereafter, plants were watered with tap water (EC 0.4 dS mÿ 1) until harvested. When leaching occurred, the leachate was collected and added to soil to maintain salinity treatments near target levels.

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The plants were grown to fruit maturity. Red and ®rm fruits were collected after they were mature for determination of fruit yield, fruit number, individual fruit fresh weight, total soluble solids (TSS) and mineral content. After fruit harvest, shoots were severed, oven-dried at 70 C, and weighed. Fruit samples from each replicate were oven-dried, weighed and saved for mineral analysis. Roots were rinsed free from soil, cut into 1 cm fragments, mixed thoroughly, and representative fresh samples (1 g) were removed for determination of root AMF colonization. The remaining roots were dried and weighed. Root samples for determination of root colonization with AMF were cleared with 10% KOH and stained with 0.05% trypan blue in lactophenol as described by Phillips and Hayman (25), and microscopically examined for AMF colonization by determining percentage of root segments containing arbuscules vesicles using a gridline intercept method (26). Dried fruits were ground to pass a 0.5 mm sieve in a cyclone laboratory mill, and prepared for determination of mineral nutrients. Fruit P concentration was determined colorimetrically (27) and Zn, Fe and Cu concentrations were determined by atomic absorption spectroscopy. Potassium and Na concentrations in fruits were determined using ¯ame photometer. The experiment was randomized in complete blocks with two salt stress levels, two AMF inoculum treatments, and two tomato cultivars to give a 222 factorial with four replications. Data was statistically analyzed using analyses of variance in the MSTATC program (Michigan State University, East Lansing, MI). Probabilities of signi®cant among treatments and interactions and LSDs (P 0.05) were used to compare means within and among treatments. Mean percentages of AMF colonization were calculated from arcsine transformed data. RESULTS The analysis of variance showed that nearly all salinity and AMF treatment effects were signi®cant for the various measured traits (Table 1). Signi®cant differences were noted only for shoot and root DM yields, individual fruit weight, root AMF colonization, fruit Na, Cu and Fe concentrations and Cu and Fe contents of the cultivars (Table 1). The only signi®cant treatment interactions noted were SaltAMF for root AMF colonization, Na concentration and Cu and Zn contents; and SaltCultivar for Na concentration. The AMF root colonization was noted in roots of both AMF inoculated and uninoculated plants, and the AMF inoculated plants had higher root AMF colonization than uninoculated plants regardless of salinity level (Table 2). The AMF root colonization in both tomato cultivars was reduced by salinity stress regardless of AMF inoculation status. No cultivar differences were noted for root AMF colonization for plants grown under both nonstressed and salt stressed conditions (Table 2).


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Table 1. Probabilities of Signi®cance for Growth, Fruit Yield, Total Soluble Solids (TSS), Root Colonization with Arbuscular Mycorrhizal Fungi (AMF) and Fruit Mineral (P, Na, K, Fe, Cu, and Zn) Concentrations, and Contents in Tomato Cultivars Grown With or Without Salt Stress and Inoculated or Not with AMF Trait Shoot DM Root DM Fruit yield Fruit number Fruit weight Fruit TSS Root colonization P concentration P content K concentration K content Na concentration Na content Cu concentration Cu content Fe concentration Fe content Zn concentration Zn content

Salt Level

AMF Status

Cultivar (C)

** ** **

** ** **

** *

** ** ** ** ** ** * ** * ** ** ** ** ** **

** * ** * **

*

** ** ** ** ** ** **

SaltAMF

*

*

**

**

* * * **

SaltC

*

**

**

* P 0.05. ** P 0.01.

The AMF inoculated plants generally had higher shoot and root DM yields than uninoculated plants regardless of salinity level (Table 2). However, these differences were only signi®cant for the salt sensitive cultivar Marriha grown under salt stressed conditions. Shoot and root DM decreased in plants grown under salt stressed compared to nonstressed conditions. The salt tolerant cultivar Pello had higher shoot dry matter than the salt sensitive cultivar Marriha only for uninoculated plants grown under salt stressed conditions (Table 2). Fruit fresh yield per plant of AMF inoculated plants was higher than that of uninoculated plants for both cultivars regardless of salt stress level (Table 3). However, no signi®cant differences were recorded for Pello grown under salt stressed conditions. Fruit yield decreased in both AMF inoculated and uninoculated plants grown under salt stressed compared to nonstressed conditions. The cultivar Pello generally had higher fruit yield per plant than

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Table 2. Root AMF Coloniztion, Shoot and Root Dry Matter (DM) by AMF Inoculated and Uninoculated Tomato Cultivars Grown with and without Salt Stress Dry Matter Salt Level dS mÿ 1 1.4

AMF Status Uninoculated Inoculated

4.9

Uninoculated Inoculated

Cultivar

Root Colonization %

Shoot

Root

g Plantÿ 1

Pello Marriha Pello Marriha

31.0 28.2 53.6 48.7

b{ b a a

42.8 35.1 52.5 44.1

abc bcd a ab

5.46 4.19 7.09 5.97

abc bcd a ab

Pello Marriha Pello Marriha

15.0 10.0 27.8 23.6

c c b b

24.4 12.5 32.8 25.8

e f cde de

2.94 1.03 3.92 3.26

de e cd d

{

Values in each column followed by the same letter are not signi®cantly different (P 0.05) according to LSD.

Table 3. Fruit Fresh Yield, Fruit Number, Fruit Weight, and Total Soluble Solids (TSS) by AMF Inoculated and Uninoculated Tomato Cultivars Grown with and without Salt Stress Salt Level dS mÿ 1

AMF Status

Cultivar

Fruit Yield Fruit Number Fruit Weight g Plantÿ 1 Plantÿ 1 g

TSS %

1.4

Uninoculated Pello Marriha Inoculated Pello Marriha

532 b{ 521 b 673 a 641 a

20 21 24 25

a a a a

26 ab 25 ab 28 a 26 ab

4.8 4.6 6.1 6.1

b b ab ab

4.9


367 cd 307 d 470 bc 448 bc

19 21 20 20

a a a a

20 c 15 d 23 bc 23 bc

6.7 6.5 6.9 7.6

a a a a

{


Marriha, although these differences were not signi®cant regardless of salinity level or AMF inoculation status (Table 3). No cultivar differences were noted for fruits number per plant regardless of salinity level or AMF inoculation status in both cultivars (Table 3). Fruit weight of AMF inoculated plants was higher than


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uninoculated plants only for Marriha grown under salt stressed conditions (Table 3). Salinity resulted in a reduction in individual fruit weight except for AMF inoculated Marriha. The cultivar Pello had greater fruit weight than Marriha only in uninoculated plants grown under salt stressed conditions (Table 3). Total soluble solids (TSS) in fruits of both tomato cultivars were similar for AMF inoculated and uninoculated plants, regardless of salinity level (Table 3). Salt treatment resulted in higher fruit TSS in uninoculated but not in AMF inoculated plants. The TSS was fairly similar for the cultivars regardless of salinity level or AMF inoculation status (Table 3). The AMF inoculated plants had higher fruit P contents, but not concentrations, than fruits of uninoculated plants only under nonstressed conditions (Table 4). Fruit P contents were lower for AMF inoculated and uninoculated plants grown under salt stressed compared to nonstressed conditions, while fruit P concentrations were lower only in uninoculated Marriha when grown under salt stressed conditions. No cultivar differences were noted for fruit P contents, but cultivar differences for P concentrations were noted only in uninoculated plants grown under salt stressed conditions (Table 4). Fruit K concentration of AMF inoculated and uninoculated tomato plants were similar for plants grown under nonstressed and salt stressed conditions, while fruit K contents of AMF inoculated were higher than uninoculated plants only for Pello grown under nonstressed conditions (Table 4). Fruit K contents

Table 4. Fruit Concentrations and Contents of P, K, and Na by AMF Inoculated and Uninoculated Tomato Cultivars Grown with and without Salt Stress Concentration Salt Level dS mÿ 1

AMF Status

P

K

Content Na

mg gÿ 1 DM

Cultivar

K

Na

mg Plantÿ 1

1.4


3.11 3.08 3.60 3.52

a{ a a a

55 52 58 55

ab abc a ab

1.16 1.21 1.01 1.15

d d d d

4.9


2.89 1.88 3.07 2.72

a b a ab

43 39 46 45

bc c abc abc

3.28 4.48 2.34 2.86

b a c bc

{

P

83 bc 75 cd 121 a 108 ab

1473 1244 1940 1663

b bc a ab

31 ab 29 b 34 ab 35 ab

42 de 611 d 49 ab 22 e 454 d 51 a 54 cde 816 cd 42 ab 41 e 700 d 43 ab


1318


decreased for plants grown under salt stressed conditions compared to the plants grown under nonstressed conditions. No signi®cant differences between salt treatments for K concentrations or between cultivars for fruit K concentrations and contents were noted. Fruit Na concentrations, but not contents, were lower in AMF inoculated plants than uninoculated tomato plants only for plants grown under salt stressed conditions (Table 4). No signi®cant differences were noted for fruit Na contents regardless of salinity level or AMF inoculation status. Fruit Na concentrations were higher in both AMF inoculated and uninoculated plants grown under salt stressed compared to plants grown under nonstressed conditions (Table 4). Cultivar differences for fruit Na concentrations, but not contents, were noted only in uninoculated plants grown under salt stressed conditions (Table 4). Fruit concentrations of Cu and Zn were generally higher for AMF inoculated than uninoculated plants regardless of salinity level, although the differences for Zn was not signi®cant under salt stressed conditions (Table 5). The AMF inoculated plants had higher fruit Cu and Zn contents than uninoculated plants grown only under nonstressed conditions. Fruit Fe concentrations of AMF inoculated plants did not differ from uninoculated tomato plants regardless of salt levels (Table 5), while fruit Fe contents were higher for AMF inoculated plants than uninoculated plants only in Pello grown under nonstressed conditions

Table 5. Fruit Concentrations and Contents of Cu, Fe, and Zn AMF Inoculated and Uninoculated Tomato Cultivars Grown with and without Salt Stress Concentration Salt Level dS mÿ 1

AMF Status

Cu

Fe

Content Zn

Cu

Fe

mg gÿ 1 DM

Cultivar

Zn

mg Plantÿ 1

1.4

Uninoculated Pello 9.3 b{ Marriha 8.1 bc Inoculated Pello 13.4 a Marriha 11.7 a

170 150 173 159

a a a a

46 44 55 53

b b a a

249 196 451 354

c cd a b

4542 3620 5829 4739

b bc a ab

1229 1067 1843 1597

b b a a

4.9


142 112 148 144

ab b a ab

31 30 34 32

c c c c

86 58 136 113

e e de de

2061 1290 2536 2171

de e cd de

453 348 576 483

c c c c

{

5.9 5.1 8.1 7.3

de e bc cd



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Table 6. Percentage Change in Fruit Yield and Nutrient Contents of AMF Inoculated and Uninoculated Tomato Cultivars Grown with or without Salt Stress Nutrient Contentz Salt Level dS mÿ 1

P

K

Na

P

K

Na

Cultivar

Fruit Yield{

1.4

Pello Marriha

26 23

46 44

32 34

1 20

81 81

28 31

50 50

4.9

Pello Marriha

28 46

29 86

34 54

ÿ 14 ÿ 16

58 95

23 68

27 39

% Change

{ z

Fruit yield (FY) change = FYInoculated 7 FYUninoculated100 / FYUninoculated. Nutrient Content (NC) change = NCInoculated 7 NCUninoculated100 / NCUninoculated.

(Table 5). No cultivar differences were noted for fruit concentrations and contents of Cu, Fe, and Zn except for Cu contents of inoculated plants grown under nonstressed conditions. The fruit concentrations and contents of Cu, Fe, and Cu were lower for plants grown under salt stressed compared to nonstressed conditions (Table 5). The overall effects of AMF inoculation on the yield and mineral contents (percentage-wise) of plants grown under control and saline soil conditions are summarized in Table 6.

DISCUSSION Plants inoculated with AMF had higher fruit yield per plant when grown under both nonstressed and salt stressed conditions, but these effects were not signi®cant for Pello grown under salt stressed conditions. Shoot DM and fruit weight were higher in AMF inoculated than uninoculated plants only in Marriha under saline conditions. The enhancement in fruit yield per plant due to AMF inoculation might be attributed to enhanced photosynthesis associated with increased P uptake in plants (28), and hence high amounts of assimilates were likely produced to support both symbiosis and fruit development. In this study, AMF inoculated plants had higher fruit P contents than uninoculated plants, but the differences in P contents were only signi®cant for plants grown under nonstressed and no salt stressed conditions. Reduced acquisition of P by AMF inoculated plants grown under saline conditions has been reported by others (10,29,30,31).

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Marriha, but not Pello, plants inoculated with AMF produced larger (more weight) fruits than uninoculated plants grown under salt stressed conditions. Trimble and Knowles (32) reported that cucumber (Cucumis sativus L.) plants inoculated with AMF had slightly larger fruits than uninoculated plants. Many studies have indicated that AMF contributes to plant growth via enhancement of mineral nutrient uptake especially immobile soil nutrients (P, Cu, Zn) (13,14,16,18). In our study, the AMF inoculated tomato plants had higher fruit P contents than uninoculated plants. Higher fruit Cu, Fe and Zn contents in AMF inoculated compared to uninoculated plants were also noted for plants grown under nonstressed conditions. The higher mineral nutrient acquisition in AMF inoculated compared to uninoculated plants likely occurred because of increased availabilities or transport (absorption and/or translocation of minerals) by AMF hyphae. Enhanced acquisition of P, Cu, Fe, and Zn by AMF inoculated plants has been reported (13,14,16,32). However, AMF root colonization did not signi®cantly enhanced fruit K concentrations, while fruit K contents of AMF inoculated plants were higher than uninoculated plants of Pello grown under nonstressed conditions. Poss et al. (31) reported that K uptake was affected little by AMF root colonization in tomato grown under saline conditions. Fruit Na concentrations, but not contents, were lower in AMF inoculated than uninoculated plants grown under salt stressed conditions only. The lack of response of Na contents to AMF treatments might be explained by dilution effects due to fruit yield enhancement caused by AMF colonization. Similar results were reported by other researchers (33,34). Plant growth (shoot DM and fresh fruit yields) responses to AMF inoculation were higher in Marriha than in Pello when grown under salt stressed but not under nonstressed conditions, even though AMF colonization was higher in Pello than in Marriha. However, enhanced growth may be not related to degree of AMF root colonization in some plants (10,14). The host plant species, cultivar and growing conditions can in¯uence the effectiveness of AMF symbiosis in nutrient acquisition (10,13,14,35). From results of our study, it appears that AMF colonization was more effective in increasing P, Cu, Fe, and Zn acquisition in fruits of plants grown under salt stressed conditions for the salt-sensitive cultivar Marriha than for the salt-tolerant cultivar Pello. Greater nutrient acquisition in response to AMF colonization was suggested to be a plant strategy for salt stress tolerance (29,30,31). The improved shoot growth and fruit yield and nutrient acquisition in fruits of AMF inoculated tomato demonstrated the potential of AMF colonization for protection of plants from salt stress in arid and semiarid regions. However, several AMF isolates should be investigated to maximize effectiveness of AMF symbiosis under saline conditions.


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ACKNOWLEDGMENTS This work was supported by grant from the Deanship of Scienti®c Research, Jordan University of Science and Technology. Valuable suggestions by Professor Ralph B. Clark are greatly appreciated. REFERENCES 1. 2. 3. 4. 5. 6. 7. 8. 9.

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