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Journal of Arid Land  2023, Vol. 15 Issue (2): 205-217    DOI: 10.1007/s40333-023-0092-6
Research article     
Rhizobacteria facilitate physiological and biochemical drought tolerance of Halimodendron halodendron (Pall.) Voss
Mohammad Hossein TAGHIZADEH1, Mohammad FARZAM1,*(), Jafar NABATI2
1Department of Range and Watershed Management, Ferdowsi University of Mashhad, Mashhad 9178169371, Iran
2Legume Department, Research Center for Plant Sciences, Ferdowsi University of Mashhad, Mashhad 9177948974, Iran
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Growth-promoting bacteria (GPB) have shown promising effects on serving plants against environmental constraints such as drought. Nevertheless, simultaneous effects of different GPB have less been considered for arid land plants and under field conditions. We investigated the effects of single and combined application of GPB, including free-living nitrogen-fixing bacteria (NFB), phosphate solubilizing bacteria (PSB), potassium solubilizing bacteria (KSB), a combination of NFB, PSB, and KSB (NPK), and control, at three drought stress treatments. In order to better understand the interactions between drought and GPB, we measured the morphological, biochemical, and physiological plant traits. The target plant was salt tree (Halimodendron Halodendron (Pall.) Voss), a legume shrub native to arid lands of Central and West Asia. All biofertilizer treatments enhanced the growth, physiology, and biochemistry of salt tree seedlings, and there were significant differences among the treatments. KSB and PSB treatments increased photosynthetic pigments, but KSB treatment was more efficient in transpiration rate and stomatal regulation and increased the soluble carbohydrates. PSB treatment had the highest effect on root traits, such as taproot length, root volume, cumulative root length, and the ratio of root to shoot. NFB treatment enhanced root diameter and induced biomass translocation between root systems. However, only the application of mixed biofertilizer (i.e., NPK treatment) was the most significant treatment to improve all plant morphological and physiological characteristics of salt tree under drought stress. Therefore, our results provided improvement of some specific plant traits simultaneous with application of three biofertilizers to increase growth and establishment of salt tree seedlings in the degraded arid lands.

Key wordsgrowth-promoting bacteria      physiological traits      drought stress      biofertilizer      root traits      Halimodendron Halodendron (Pall.) Voss     
Received: 13 June 2022      Published: 28 February 2023
Corresponding Authors: *Mohammad FARZAM (E-mail:
Cite this article:

Mohammad Hossein TAGHIZADEH, Mohammad FARZAM, Jafar NABATI. Rhizobacteria facilitate physiological and biochemical drought tolerance of Halimodendron halodendron (Pall.) Voss. Journal of Arid Land, 2023, 15(2): 205-217.

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Biofertilizer treatment Drought level Biomass and morphological trait
41.36±2.10a 22.44±1.79g 23.83±1.83f 31.56±1.33c 19.72±1.21h LD Total plant height (cm)
34.72±1.04b 17.12±0.86i 17.67±1.04i 26.83±0.63e 14.11±0.87j MD
29.61±0.87d 13.33±1.49j 11.61±1.35k 21.67±1.33g 7.61±1.38l HD
2.140±0.159a 1.250±0.111c 0.870±0.140de 0.924±0.175d 0.670±0.028defgh LD Stem dry weight (g/Plant)
1.560±0.152b 0.589±0.112efghi 0.644±0.026defgh 0.798±0.007defg 0.505±0.137ghi MD
0.825±0.088def 0.540±0.127fghi 0.416±0.061hi 0.582±0.045efghi 0.312±0.085i HD
2.180±0.212a 1.580±0.091b 1.450±0.110 b 0.995±0.101cd 0.837±0.117de LD Leaf dry weight (g/Plant)
1.190±0.112c 0.572±0.060fg 0.654±0.063ef 0.576±0.060fg 0.383±0.081g MD
0.630±0.046ef 0.474±0.110fg 0.458±0.098fg 0.460±0.084fg 0.364±0.020g HD
131.0±15.0a 119.7±23.0a 90.3±9.2b 74.8±5.6bc 57.1±14.4cd LD Leaf area
80.4±14.8bc 46.7±5.7de 56.4±8.4cd 46.2±7.5de 27.4±6.1e MD
35.4±5.4de 33.7±6.9de 33.5±6.5de 34.8±5.8de 24.6±1.4e HD
44.5±3.4ab 43.7±2.6ab 45.4±2.0a 33.0±0.7def 37.9±2.0cde LD Taproot length (cm)
45.6±3.4a 30.9±3.2f 32.5±0.3ef 37.5±4.2cde 30.2±0.6f MD
37.9±7.0cd 36.6±4.8cde 46.0±7.0a 39.6±5.2bc 37.0±4.7cde HD
2.180±0.225a 2.160±0.364a 1.210±0.101bc 0.749±0.130def 0.678±0.101ef LD Root dry weight (g/plant)
1.580±0.198b 0.730±0.021def 0.900±0.017cde 1.110±0.151cd 0.689±0.019ef MD
0.680±0.051ef 0.364±0.016f 0.907±0.142cde 0.912±0.253cde 0.964±0.055cde HD
6.33±0.67a 5.18±0.82ab 3.67±0.88cd 3.00±0.01def 2.00±0.01fgh LD Root volume (cm3/plant)
4.33±0.33bc 1.33±0.33gh 3.63±0.67cd 3.67±0.33cd 2.00±0.00fgh MD
2.33±0.33efg 1.00±0.01h 3.33±0.33cde 2.42±0.42efg 2.00±0.58fgh HD
95.3±10.7b 56.4±17.9c 142.0±12.8a 41.4±8.3cde 52.5±18.6cd LD Cumulative root length (m)
58.5±13.2c 95.0±14.2b 30.1±5.5cde 32.5±4.6cde 42.6±11.7cde MD
26.0±4.4cde 26.1±6.9cde 47.3±18.6cde 16.9±0.7e 21.2±4.7de HD
0.504±0.120cdef 0.956±0.081ab 0.402±0.149def 0.776±0.087bcd 0.797±0.086abc LD Mean root diameter (mm)
0.730±0.244bcde 0.376±0.102ef 0.856±0.216abc 0.783±0.133abcd 0.331±0.060f MD
0.696±0.083bcdef 0.700±0.157bcdef 0.669±0.085bcdef 1.170±0.112a 1.046±0.125ab HD
0.504±0.046def 0.781±0.163bcde 0.461±0.096ef 0.387±0.055f 0.527±0.066cdef LD Ratio of root to shoot
0.582±0.083cdef 0.658±0.105cdef 0.888±0.232bc 0.814±0.129bcde 0.700±0.055bcdef MD
0.469±0.017ef 0.362±0.030f 1.506±0.264a 0.849±0.146bcd 1.036±0.155b HD
Table 1 Effect of different biofertilizer treatments and drought levels on biomass and morphological traits of salt tree
Biofertilizer treatment Drought level Photosynthetic trait
58.1±3.1a 26.3±3.2bc 27.5±3.1bc 27.9±3.6bc 18.3±1.5cd LD Photosynthetic rate
35.5±5.1b 21.6±4.2cd 25.8±2.9bc 27.6±5.0bc 13.7±3.6d MD
27.1±4.0bc 20.8±4.6cd 21.3±3.7cd 19.7±6.1cd 10.7±2.3d HD
0.433±0.101g 0.590±0.208efg 0.397±0.154g 0.373±0.121g 0.197±0.012g LD Transpiration rate
1.180±0.285cd 1.050±0.102cdef 0.640±0.139defg 1.120±0.220cde 0.525±0.102fg MD
0.542±0.312fg 0.993±0.384cdef 1.900±0.617b 2.590±0.406a 1.310±0.772c HD
0.087±0.026cde 0.173±0.085cde 0.097±0.048cde 0.113±0.053cde 0.053±0.003e LD Stomatal conductance
0.228±0.053bc 0.299±0.040b 0.110±0.028cde 0.270±0.069b 0.110±0.055cde MD
0.063±0.049d 0.207±0.098bcd 0.283±0.141b 0.680±0.152a 0.212±0.167bcd HD
2919±416ef 2534±862f 3029±1055def 5382±909abc 3273±382def LD Stomatal resistance
6052±358ab 4682±241bcd 4337±696cde 3150±821def 3722±162cdef MD
6585±832a 3344±178def 3686±487def 4183±725cdef 2737±48ef HD
296±40b 355±16ab 322±4ab 303±19b 292±24bc LD Substomatal CO2 concentration (mg/m3)
356±17ab 353±21ab 395±34a 352±17ab 348±20ab MD
218±38c 306±23b 325±37ab 360±9ab 356±25ab HD
291±8cde 257±41e 413±7a 380±28ab 409±16a LD Adaxial stomatal density (number/cm2)
280±26de 329±27bcd 352±29abc 352±5abc 282±33de MD
297±4cde 275±25de 270±32de 356±10abc 352±26abc HD
253±29cdef 261±15cdef 288±19cde 290±0bcde 350±16b LD Abaxial stomatal density (number/cm2)
222±27f 252±26cdef 299±29bcd 236±19ef 432±19a MD
241±27def 248±28def 275±22cdef 292±10bcde 310±20bc HD
Table 2 Effect of different biofertilizer treatments and drought levels on photosynthetic traits of salt tree
Fig. 1 Effects of different drought levels and biofertilizer treatments on leaf chlorophyll fluorescence of salt tree. (a), minimum chlorophyll fluorescence; (b), maximum chlorophyll fluorescence; (c), quantum efficiency of photosystem II. Control, without the application of biofertilizer; NFB, free-living nitrogen-fixing bacteria; PSB, phosphate solubilizing bacteria; KSB, potassium solubilizing bacteria; NPK, the combination of NFB, PSB, and KSB; LD, low drought; MD, moderate drought; HD, high drought. Different lowercase letters indicate significantly difference among drought levels and biofertilizer treatments (P≤0.05). Bars are stand errors.
Fig. 2 Effect of different drought levels and biofertilizer treatments on the concentration of photosynthetic pigments of salt tree. (a), chlorophyll a; (b), chlorophyll b; (c), carotenoids; (d), total pigments. Different lowercase letters indicate significantly difference among drought levels and biofertilizer treatments (P≤0.05). Bars are stand errors.
Biofertilizer treatment Drought level Biochemical trait
1.08±0.03cd 1.85±0.09a 1.53±0.05b 1.13±0.08cd 1.48±0.06b LD Soluble carbohydrates (mg/g)
1.20±0.09cd 1.33±0.21bc 1.07±0.03cd 1.29±0.09bc 1.48±0.19b MD
0.95±0.04d 1.97±0.13a 1.09±0.09cd 1.17 ±0.13cd 1.02±0.03d HD
0.009±0.004d 0.201±0.187cd 0.347±0.158cd 0.419±0.129cd 0.010±0.004d LD Proline (mg/g)
0.656±0.009de 0.615±0.274c 1.710±0.384ab 1.280±0.251b 0.210±0.155cd MD
1.820±0.171a 0.096±0.055d 0.096±0.051d 0.217±0.162cd 0.483±0.092cd HD
4.72±0.22a 3.43±0.58bc 2.03±0.36e 2.42±0.23de 3.60±0.14bc LD Phenol (mg/g)
3.29±0.44bc 3.30±0.32bc 3.06±0.24cd 3.54±0.22bc 4.00±0.42ab MD
2.95±0.12cd 3.28±0.42bc 3.69±0.18bc 3.50±0.29bc 3.53±0.43bc HD
0.209±0.035bcde 0.181±0.027defg 0.140±0.014fg 0.155±0.006efg 0.162±0.030efg LD DPPH (mg/g)
0.183±0.043defg 0.268±0.052ab 0.168±0.035efg 0.259±0.052abc 0.215±0.066bcde MD
0.283±0.044a 0.201±0.020cdef 0.179±0.039defg 0.132±0.012g 0.237±0.048abcd HD
4.39±1.28cd 3.43±1.02d 4.64±0.75cd 5.92±0.20bc 3.18±0.19d LD Osmotic potential (MPa)
5.01±0.48bcd 3.64±0.30d 3.73±0.02d 4.68±0.50cd 4.75±0.46bcd MD
8.05±0.62a 5.78±0.46bc 6.56±0.94ab 4.91±0.39bcd 4.31±0.96cd HD
Table 3 Effect of different drought levels and biofertilizer treatments on biochemical traits of salt tree
Taproot length Root dry weight Root volume Cumulative root length Mean root diameter Ratio of root to shoot Soluble carbohy-drates Proline Phenol DPPH Osmotic potential
Taproot length 1.000
Root dry weight 0.546** 1.000
Root volume 0.476** 0.867** 1.000
Cumulative root length 0.306* 0.399** 0.341* 1.000
Mean root diameter 0.168 0.097 0.028 -0.612** 1.000
Ratio of root to shoot 0.131 0.088 0.146 -0.271 0.320* 1.000
Soluble carbohydrates 0.027 0.038 -0.124 0.187 -0.088 -0.214 1.000
Proline -0.173 -0.145 -0.062 -0.220 0.045 -0.052 -0.414** 1.000
Phenol 0.216 0.335* 0.288 -0.090 -0.021 0.199 -0.050 -0.183 1.000
DPPH 0.051 -0.101 -0.172 -0.130 -0.142 -0.074 -0.252 0.282 0.201 1.000
Osmotic potential 0.008 -0.339* -0.215 -0.324* 0.006 -0.001 -0.294* 0.208 -0.127 0.148 1.000
Table 4 Correlation coefficients between root traits and biochemical traits of salt tree
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