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
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.
Table 1 Effect of different biofertilizer treatments and drought levels on biomass and morphological traits of salt tree
Biofertilizer treatment
Drought level
Photosynthetic trait
NPK
KSB
PSB
NFB
Control
58.1±3.1a
26.3±3.2bc
27.5±3.1bc
27.9±3.6bc
18.3±1.5cd
LD
Photosynthetic rate (μmol/(m2•s))
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 (mmol/(m2•s))
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 (mmol/(m2•s))
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 (m/s)
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. 1Effects 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. 2Effect 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
NPK
KSB
PSB
NFB
Control
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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