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. 2018 Aug 16;8(9):377. doi: 10.1007/s13205-018-1400-2

Differential modulation of phytoelemental composition by selected Pseudomonas spp.

Aswathy Jayakumar 1, Athira Perinchery 1, Farha M Jaffer 1, E K Radhakrishnan 1,✉
PMCID: PMC6095743  PMID: 30148027

Abstract

Plant growth promoting rhizobacteria (PGPR) are bioresources with potential application in ecofriendly agricultural practices. The beneficial effects of PGPR have been attributed to their ability to produce phytohormone, organic acid, siderophore, and also due to nitrogen fixation among others. In the present study, previously isolated plant growth promoting rhizospheric Pseudomonas spp.  were evaluated for growth enhancement effect in Vigna unguiculata seedlings. Elemental profiling of treated plant was further carried out by inductively coupled plasma-mass spectroscopy. Results of the study showed significant increase in growth parameters such as shoot length, root length and root numbers for treated plants when compared to control. Most of the macro and micro elements were also found to get modulated by interaction with applied Pseudomonas spp. However, a differential modulation was observed for plants when treated with each of the Pseudomonas spp., which could be due to their variable interaction with the selected plant. The results of the study indicate the role of each of the associated microbial partner to specifically influence the plant nutrient mobilization along the soil plant axis. The cumulative effect of the plant microbiome hence may decide the global nutritional status of plants as per the available environmental conditions.

Keywords: Rhizobacteria, ICP-MS, V. unguiculata, Plant growth promotion

Introduction

Plant–rhizobacterial interactions have been studied extensively for various agrological as well as environmental aspects (Chandra and Kumari 2017). Plant growth promoting rhizobacteria (PGPR) can be extracellular (Agrobacterium, Arthrobacter, Azotobacter, Azospirillum, Bacillus, Burkholderia, Caulobacter, Chromobacterium, Erwinia, Flavobacterium, Micrococcus, Pseudomonas and Serratia) or intracellular (Allorhizobium, Bradyrhizobium, Mesorhizobium and Rhizobium, endophytes and Frankia) (Gupta et al. 2015). The diverse mechanisms employed by these organisms include the production of phytohormones, ACC deaminase, siderophore, nitrogen fixation, enhanced mineral uptake and biocontrol against numerous phytopathogens (Vacheron et al. 2013). By IAA production, they have been demonstrated to modulate the cell elongation, division and differentiation in plants. Microbial population also secrete organic acids which convert the insoluble phosphates into soluble monobasic and dibasic ions and thereby making it available to plants. Siderophore producing bacteria restrict the growth of plant pathogens due to their strong affinity towards Fe(III). The enzyme 1-aminocyclopropane-1-carboxylate (ACC) deaminase of microbial origin facilitates plant growth and development by decreasing the ethylene level, inducing salt tolerance and reducing drought stress in plants (Zahir et al. 2008). These beneficial features of rhizobacteria have significant impact on growth and yield of plants. Among the various rhizobacteria, Pseudomonas spp. have ubiquitous distribution and have diverse plant growth promoting as well as biocontrol mechanisms. However, the global changes introduced in plants due to rhizobacterial interaction are not fully known. The wide range of antifungal compounds produced by plant growth promoting rhizobacteria includes amphisin, 2,4-diacetylphloroglucinol (DAPG), oomycin A, phenazine, pyoluteorin, pyrrolnitrin, tensin, tropolone, and cyclic lipopeptides (Loper et al. 2007). Among these, phenazine derivatives are one of the important antifungal products of Pseudomonas spp.

Due to the easiness with culture handling and large-scale production, many Pseudomonas spp. based formulations have already been introduced. Hence the Genus Pseudomonas forms an important candidate to study the global impact of plant beneficial mechanisms of rhizobacteria on plant system. Such studies are very important to explore the opportunities to design tailor made rhizobacterial formulations to specifically modulate the nutritional composition of plants. As they have been isolated from rhizosphere of numerous plants like cotton, rice, banana, rape, sugar cane, wheat and barley, they have immense promises to explore (Loaces et al. 2010; Ravindra Naik et al. 2008; Patten and Glick 2002; Rameshkumar 2012; Mavrodi et al. 2001; Parejko et al. 2012). So, in this study selected Pseudomonas spp. have been investigated in detail to identify their impact on elemental composition of the model plant Vigna unguiculata.

Materials and methods

For the study, previously isolated Pseudomonas spp. from Western Ghat rhizosphere were  selected. These include P. putida (KY823010), P. monteilii (KY823008), P. rhodesiae (KY823009), P. fluorescens (KY823007) and P. taiwanensis (KY823006). For the plant growth promotion studies, seeds of V. unguiculata were collected and surface sterilized using sodium hypochlorite for 10 min (Jasim et al. 2013). The seeds were further washed several times with sterile distilled water and were allowed to germinate. The germinated seedlings were then treated with overnight grown cultures (107 CFU/mL) of P. putida, P. monteilii, P. rhodesiae, P. fluorescens and P. taiwanensis for 30 min. Treated seedlings along with control (distilled water and nutrient broth) were then observed for enhanced plant growth by planting it in double-sterilized soil. In each set of growth promotion  study, ten seedlings were used per set in triplicate. Both control and treated seedlings were watered daily and observed periodically. The plants were harvested after 1 week and growth parameters such as root length, shoot length and root numbers were analysed (Jimtha John et al. 2017).

Pseudomonas spp. with enhanced plant growth enhancement effects were selected further to identify its potential to modulate the elemental composition of V. unguiculata. So, the plant samples treated with P.monteilii, P. rhodesiae and P.fluorescens were selected for ICP-MS analysis. These were oven dried for half an hour at 50 °C and powdered using mortar and pestle. From this, aliquotes of 0.1 g were digested at 85 °C with 8 mL HNO3 (Supra pure) in a microwave digestion system. The digested samples were further made up to 25 mL with ultrapure water and then stored in sterile vials. The samples for ICP-MS (THERMO FISCHER iCAP, Q) analysis were diluted with 10% acid and from that 1 mL was again diluted to 25 mL. After ICP-MS analysis, the elemental concentration in ppb was converted to µg/mg using the formula (ICP-MS result × 25 × 0.025) ÷ 0.1. Triplicates were maintained for each plant samples. The results were analysed using statistical programme Origin Pro 7. One-way analysis of variance was used for comparison among the groups. Post hoc multiple comparison tests were used to determine the significant difference among groups, P < 0.05 was considered as significant.

Results and discussion

Among the selected Pseudomonas spp., three of them enhanced the growth of V. unguiculata when compared to control. P. monteilii treatment showed the highest enhancement of mean shoot length, root length and root numbers when compared to control. The shoot length of P. monteilii-treated seedlings was 20.73 ± 0.69 cm and was high when compared to that of the distilled water and nutrient broth control (DW-14.48 ± 0.79 cm, NB-13.11 ± 0.27 cm). The root length of the same (5.49 ± 0.27 cm) was also found to get enhanced when compared to the control. The root numbers were more in the case of P. fluorescens (9.85 ± 0.99) treatment and the same for control were 6.38 ± 0.55 and 6.38 ± 0.75 for DW and NB, respectively. The shoot length (18.73 ± 0.28 cm), root length (3.92 ± 0.22 cm) and root numbers (9 ± 0.50) were also higher in P. rhodesiae-treated seedlings than that of DW and NB control. P. putida treatment showed a shoot length of 16.25 ± 0.42 cm, root length of 3.74 ± 0.06 cm and root numbers of 9.33 ± 0.60; whereas P. taiwanensis mediated shoot length to 16.14 ± 0.23 cm, root length to 2.9 ± 0.12 cm and root numbers to 9.19 ± 0.37 (Fig. 1). The bacterial isolates used in the study have been demonstrated to have efficient growth enhancement effect in various plant  systems (Jimtha John et al. 2017). Hence, the result can be due to the colonization of selected bacteria on V. unguiculata. Seed bacterization with Pseudomonas spp. has previously been described to result in increased growth parameters such as root length, shoot length and dry mass of sorghum seedlings (Praveen Kumar 2012). The inoculation of Pseudomonas sp. on peanut and maize has also reported to result in increased seed germination, growth and phosphorous content (Anzuay et al. 2017).

Fig. 1.

Fig. 1

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Growth promotion analysis of Pseudomonas spp. on Vigna unguiculata seedlings by pot experiment along with untreated control. a Shoot length and root length. b Root number. DW distilled water and NB nutrient broth

By ICP-MS analysis, P. fluorescens treated plants were found to have enhancement of phosphorous and magnesium while there was decrease of potassium and calcium contents when compared to control. Micronutrients like aluminium, iron, zinc and sodium of same plants were lower than control. However, nickel, manganese, caesium, strontium, cerium, neodymium, ytterbium, europium, bismuth, beryllium and lanthanum concentrations in P. fluorescens treated plants were observed to be higher than in controls. Chromium, cobalt, praseodymium, scandium, lutetium, rhenium, thallium, indium, rubidium, arsenic, holmium, erbium, thulium, thorium, gadolinium, dysprosium, lithium, barium, lead, boron, vanadium, gallium, selenium and cadmium  concentrations were lower in P. fluorescens treated plants than in control (Fig. 2).

Fig. 2.

Fig. 2

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Elemental composition variation (macronutrients) in Pseudomonas spp. (P. monteilii, P. fluorescens and P. rhodesiae treated seedlings of Vigna unguiculata when compared to control obtained from ICP-MS data. DW distilled water, NB nutrient broth control

In P. rhodesiae treated plants macro elements like phosphorous and magnesium were high, but potassium and calcium contents were lower. Aluminium, manganese, iron, chromium, gallium, vanadium, neodymium, rubidium, strontium, barium, lanthanum, cerium, lead, lithium, boron, arsenic, cadmium, praseodymium, gadolinium, samarium, beryllium, indium, caesium, europium, scandium, terbium, bismuth, thorium, uranium, holmium, erbium, thulium, ytterbium, lutetium, thallium and dysprosium concentrations in plants treated with P. rhodesiae were higher than control. However, zinc, sodium, cobalt, copper, nickel, yttrium, selenium and rhenium of P. rhodesiae treated plants showed decreased concentration than control (Fig. 2).

The macro elements like phosphorous, potassium, calcium and magnesium contents in P. monteilii treated plants were lower than controls. Manganese, sodium, nickel, copper neodymium, lanthanum, barium and thorium of treated plants were higher than control. Aluminium, iron, chromium, gallium, vanadium, neodymium, rubidium, strontium, barium, cerium, lead, lithium, arsenic, cadmium, zinc, praseodymium, gadolinium, samarium, beryllium, indium, caesium, europium, scandium, terbium, bismuth, uranium, holmium, erbium, thulium, ytterbium, lutetium, thallium and dysprosium  concentrations in P. monteilii treated plants were lower than control (Fig. 2) (Table 1).

Table 1.

Elemental composition variation in Pseudomonas spp. (P. monteilii, P. fluorescens, P. rhodesiae) treated seedlings of V. unguiculata when compared to control (DW distilled water, NB nutrient broth) obtained from ICP-MS data

Concentration of elements in µg/mg (DW) Concentration of elements in µg/mg (NB) Concentration of elements in µg/mg (P. fluorescens) Concentration of elements in µg/mg (P. monteilii) Concentration of elements in µg/mg (P. rhodesiae)
Al 2773.419 ± 0.579785 2362.462 ± 0.300888 2644.735 ± 0.519615 2279.399 ± 0.057735 4322.849 ± 0.57735
Fe 1548.341 ± 0.57735 1529.137 ± 0.015275 1437.867 ± 0.608276 1141.111 ± 0.057735 2362.847 ± 0.57735
Zn 1018.497 ± 0.574485 1093.336 ± 0.060828 692.4619 ± 0.635085 395.8311 ± 0.057735 556.2129 ± 0.057735
Na 798.2303 ± 0.635085 731.2288 ± 0.028868 648.3131 ± 0.057735 607.5434 ± 0.057735 539.4947 ± 0.11547
Mn 315.6843 ± 0.611991 569.3644 ± 0.011547 658.2657 ± 0.608276 604.6754 ± 0.057735 618.3861 ± 0.23094
Cu 287.652 ± 0.57735 371.3465 ± 0.110151 137.1203 ± 0.550757 70.57084 ± 0.288675 398.2044 ± 0.635085
Ni 95.74449 ± 0.57735 231.4784 ± 0.110151 274.1513 ± 0.608276 126.2504 ± 0.11547 51.16571 ± 0.608276
Rb 73.07984 ± 0.57735 65.63367 ± 0.060828 64.49175 ± 0.057735 65.13879 ± 0.057735 76.60876 ± 0.173205
Ba 48.95014 ± 0.57735 50.54808 ± 0.090185 40.48197 ± 0.57735 38.16625 ± 0.057735 55.73448 ± 0.057735
Pb 39.20162 ± 0.264575 40.24077 ± 0.058026 28.5152 ± 0.11547 11.7652 ± 0.11547 41.74654 ± 0.057735
Ce 17.31047 ± 0.763763 46.77984 ± 0.191594 47.63744 ± 0.11547 24.23715 ± 0.057735 72.37724 ± 0.057735
Sr 34.12062 ± 0.8544 34.06756 ± 0.066583 36.20203 ± 0.11547 25.50155 ± 0.11547 38.36365 ± 0.057735
La 9.635971 ± 0.52915 22.24709 ± 0.063509 25.37034 ± 0.23094 33.07198 ± 0.011547 36.2054 ± 0.057735
Nd 7.148222 ± 0.519615 20.55475 ± 0.005774 25.33701 ± 0.173205 21.82394 ± 0.57735 31.43724 ± 0.173205
Cr 12.1051 ± 0.46188 16.44843 ± 0.055076 11.19034 ± 0.173205 10.33974 ± 0.057735 23.71692 ± 0.057735
B 9.644166 ± 0.80829 8.268384 ± 0.057166 6.790562 ± 0.057735 12.50646 ± 0.57735 10.5506 ± 0.057735
Co 12.6119 ± 0.51316 13.24436 ± 0.057449 11.22673 ± 0.057735 11.04435 ± 0.005774 12.04435 ± 0.005774
V 7.825573 ± 0.503322 7.136994 ± 0.057166 5.167253 ± 0.57735 6.115242 ± 0.57735 15.33155 ± 0.057735
Y 14.56597 ± 0.503322 11.21149 ± 0.060828 10.89192 ± 0.057735 6.321809 ± 0.57735 16.93436 ± 0.011547
Ga 4.764481 ± 0.623538 9.072364 ± 0.011547 3.195728 ± 0.680686 5.055294 ± 1.154701 14.80622 ± 0.005774
Pr 6.855615 ± 0.011547 5.335955 ± 0.05 5.051339 ± 0.028868 3.046101 ± 0.034641 8.327819 ± 0.057735
Se 4.424484 ± 0.057735 4.375814 ± 0.05837 3.63396 ± 0.34641 2.525315 ± 0.017321 3.321944 ± 0.057735
Gd 5.304772 ± 0.190539 4.122109 ± 0.057735 3.855442 ± 0.57735 2.249681 ± 0.005774 6.251332 ± 0.057735
Sm 4.240168 ± 0.042564 3.91512 ± 0.057822 3.410008 ± 0.173205 2.031552 ± 0.005774 5.6794 ± 0.173205
Li 2.208819 ± 0.000902 2.493184 ± 0.046159 2.011212 ± 0.014565 1.668211 ± 0.57735 3.313335 ± 0.057735
As 4.642374 ± 0.041886 3.339049 ± 0.046194 2.744356 ± 0.34641 1.673618 ± 0.57735 4.752068 ± 0.057735
Dy 1.679462 ± 0.005774 1.92816 ± 0.054271 1.01443 ± 0.005774 1.032609 ± 0.017321 2.933963 ± 0.057735
Sc 0.847444 ± 0.005774 0.809872 ± 0.058014 0.473593 ± 0.1 0.656396 ± 0.057735 1.230956 ± 0.023094
Cd 1.58425 ± 0.112694 0.924124 ± 0.11576 0.405736 ± 0.208167 0.37792 ± 0.23094 1.663265 ± 0.04772
Th 0.432498 ± 0.017559 0.865954 ± 0.003464 0.181 ± 0.057735 0.933131 ± 0.011547 1.452252 ± 0.011547
Er 0.978176 ± 0.026458 0.81665 ± 0.005508 0.633949 ± 0.11547 0.424043 ± 0.011547 1.26346 ± 0.011547
Cs 0.455627 ± 0.028918 0.438053 ± 0.01 0.310439 ± 0.057735 0.408961 ± 0.005774 0.654966 ± 0.005774
Yb 0.171043 ± 0.017321 0.452301 ± 0.034641 0.607498 ± 0.057735 0.120148 ± 0.005774 0.767828 ± 0.005774
Eu 0.174358 ± 0.025981 0.455287 ± 0.021362 0.497044 ± 0.057735 0.023871 ± 0.005774 0.752082 ± 0.028868
Tb 0.436285 ± 0.002887 0.459525 ± 0.058924 0.328601 ± 0.057735 0.235315 ± 0.005774 0.643939 ± 0.002887
Ho 0.426438 ± 0.017321 0.367546 ± 0.058832 0.256826 ± 0.057735 0.235315 ± 0.028868 0.511165 ± 0.009033
U 0.089015 ± 0.01 0.288567 ± 0.055664 0.02649 ± 0.005774 0.035929 ± 0.005774 0.73126 ± 0.005774
Tl 0.096498 ± 0.001 0.119401 ± 0.027555 0.014297 ± 0.005774 0.076135 ± 0.028868 0.120861 ± 0.005774
Tm 0.0399 ± 0.010536 0.096134 ± 0.002517 0.035139 ± 0.005774 0.027294 ± 0.017321 0.157744 ± 0.023094
Be 0.050758 ± 0.002887 0.049947 ± 0.004071 0.051831 ± 0.000577 0.027745 ± 0.005774 0.087557 ± 0.001732
In 0.05772 ± 0.006429 0.076439 ± 0.005292 0.040781 ± 0.005774 0.040492 ± 0.005774 0.116225 ± 0.005774
Lu 0.090961 ± 0.006083 0.080174 ± 0.015319 0.062445 ± 0.005774 0.029883 ± 0.011547 0.111271 ± 0.005774
Re 0.0043 ± 0.005196 0.00513 ± 0.005947 0.002436 ± 0.00052 0.001627 ± 0.000173 0.000466 ± 0.000561
Bi 0.052993 ± 0.000643 0.057524 ± 0.001 0.074106 ± 0.005774 0.045035 ± 0.003464 0.078048 ± 0.001155
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Data represented as mean ± standard deviation

While comparing the macronutrient enhancement by Pseudomonas spp., both P. fluorescens and P. rhodesiae treated plants showed an elevated level of phosphorous and magnesium with a decrease in potassium and calcium concentrations than P. monteilii treated plants. In the case of micronutrients, most of the elements (aluminium, manganese, iron, vanadium, boron) in P. rhodesiae treated plants were elevated than in P. fluorescens and P. monteilii treated plants. Other elements like neodymium, rubidium, strontium, barium, lanthanum, cerium, lead, lithium, arsenic, cadmium, praseodymium, gadolinium, samarium, beryllium, indium, caesium, europium, scandium, terbium, bismuth, chromium, gallium, thorium, uranium, holmium, erbium, thulium, ytterbium, lutetium, thallium and dysprosium were lower in P. monteilii treated plants than that of P. fluorescens treated plants except nickel, caesium, strontium, cerium, neodymium, ytterbium, europium, bismuth, beryllium and lanthanum. In case of P. rhodesiae treated plants, other elements except zinc, sodium, cobalt, copper, nickel, yttrium, selenium and rhenium were elevated than in P. fluorescens and P. monteilii. Even though similar studies have not been conducted previously in detail, current results confirm the role of rhizobacterial interaction in determining the elemental composition of plants. In a previous study, Pseudomonas sp. A3R3 have been reported to be effective in promoting the phytoremediation potential of both host (Alyssum serpyllifolium) and nonhost (Brassica juncea) plants by improving either the Ni accumulation or biomass production (Ma et al. 2011). At the same time, inoculation of plants with phosphate solubilizing organism has also reported to result in increased P contents and associated 10–15% increase in crop yields (Gyaneshwar et al. 2002). Another study has also suggested bacterial role in protecting plants from the inhibitory effects of nickel, lead, and zinc by providing the plants with sufficient iron (Burd et al. 2000). Inoculation of P. fluorescens at a concentration of 109 cfu/mL was also observed to cause significant increase in availability of Fe by 34.75% in plants (Pratiwi et al. 2016). Macro and micronutrient modulation and associated increase of growth have also been reported in Sorghum due to seed bacterization with Pseudomonas spp. (Kumar et al. 2012). In another study, nutrient content (P, Fe, Zn, K and Mg) and plant growth of strawberry have been suggested to be modulated by Bacillus and Pseudomonas sp. (Esitken et al. 2010). These indicate the remarkable modulatory effect of plant elemental composition by associated microorganisms.

Plant growth promoting rhizobacteria are potential tools for the sustainable agricultural trend for the future. In the study, previously isolated Pseudomonas species were found to enhance the growth of V. unguiculata seedlings when compared to that of control. From the ICP-MS analysis result, differential modulatory effect of Pseudomonas species on the elemental composition of plants could be confirmed. Hence, a detailed insight into the plant growth promoting and element modulatory functions Pseudomonas can pave the way to make use of rhizobacteria to engineer plants with desired nutritional composition.

Acknowledgements

The authors gratefully acknowledge Dr. Mahesh Mohan, School of Environmental Sciences, Mahatma Gandhi University, Kottayam for the help and support provided for ICP-MS analysis and also KSCSTE-SRS for the  funded project.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

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