Response of Sweet Potato to Application of Pgpr and N Fertilizer
Farzana Yasmin1,Radziah Othman2, Hemapriyaa Vijayan1and Nazmul MHM3*
1Faculty of Science, Lincoln University, 12-18, Jalan SS6/12 off JalanPerbandaran, 47301 Petaling Jaya, Selangor, Malaysia.
2Faculty of Agriculture, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia.
3Graduate School of Medicine, Perdana University, 9.2, Wisma Chase Perdana, Damansara Heights, 50490 Kuala Lumpur, Malaysia.
*Corresponding author : [email protected] ABSTRACT
This study was conducted to evaluate the response of sweet potatogrowth and yield to theapplication of PGPR and Nitrogen fertilizer.The field experiment was established under a design of Randomized Complete Block Designwith 3 replications.The inoculation for this study was comprised of 4 treatmentsand a control (Klebsiella sp.
UPMSP9, Erwinia sp. UPMSP10,Azospirillumbrasilense SP7, Bacillus sphaericus UPMB10 and Uninoculated control) combinations with 3 levels of N fertilizer (0, 33, and 100 kg N ha-1).The results indicated that the inoculation of the Klebsiella and supplied with 33kg Nha-1increased sweet potato yield significantly compared to control. Similarly, the application of the bacterium Klebsiella and supplied with 33kg Nha-1 recorded higher uptake of N, P and K compared to control. Soil P, K, Ca and Mg Concentrations were higher with PGPR and N application of 33kg N ha- 1 compared with the 100kg N ha-1. The concentrations of IAA in soils inoculated with rhizobacterial isolates were significantly higher than uninoculated control. Highest IAA was observed with Klebsiella inoculation at33kg Nha-1 fertilization rate. These findings showed that PGPR could be a potential inoculant at a reduced rate of N fertilizer for sweet potato production.
Keywords: Sweet potato, Indole-acetic acid, Klebsiella sp., Erwinia sp., Azospirillumbrasilense, Bacillus sphaericus,Nitrogen fertilizer,
INTRODUCTION
Sweet potato (Ipomoea batatas L.) is an important root crop worldwide and is considered as a main source of food. It is the most promising food commodity around the world as it is ranked as the seventh most important food crop after rice and maize(FAO, 2009).
Sweet potato is also considered to have a very high amount of carbohydrate which serves as a great source of energy. Besides being a wide range of food source, many developed countries have utilized sweet potato as raw material for various industries including fermentation, textiles and cosmetics (Vosawai et al., 2015).In Malaysia, many areas in the states of Terengganu, Perak and Kelantan are involved in sweet potato production and it is known as the second highest tuber crop producer after cassava (Hanimet al., 2014).
Generally, sweet potatorequires high amount of fertilizer for commercial cultivation which can lead to increased production cost and environmental pollution due to the over usage of chemical fertilizers. This indirectly contributes to the negative impact on the sustainability of the ecosystem. Biofertilizer is globally popular as an alternative source
of chemical fertilizer which improves plant growth through increased uptake of water and mineral nutrients(Saravanakumaret al., 2007, Umairet al., 2018). In the environment, plants and bacteria has a natural relationship existence that plays a vital role in the growth and the health of plants (Abdisaet al., 2012).
Plant growth promotingRhizobacteria (PGPR) is used as biofertilizer and bioenhancer for different crops as an alternative source of chemical fertilizer.PGPRencompasses all microorganism that inhabit and colonize plant roots and exert positive effects on plant improvement by various mechanisms, ranging from direct growth promotion, such as increased solubilization and uptake of nutrients or production of plant growth regulators, to indirect growth promotion, such as pathogen suppression in biological control and production of phytohormones(Deyet al., 2004, Naseriet al., 2013).Azospirillum and other groups of PGPR bacteria have been found to produce and release a broad spectrum of plant growth regulators, such as auxin, gibberellin and cytokinin. Among these indole-3- acetic acid (IAA) is considered as the most physiologically active auxin in plants and involved on diverse plant growth and IAA is well known to stimulate both rapid responses (e.g. increases in cell elongation) and long term (e.g. cell-division and differentiation) in plants (Kumar et al., 2002, Glick, 2012). Eighty percent of microorganisms isolated from the rhizosphere of various crops have the ability to produce auxins as secondary metabolites which help in stimulating plant growth (Adesemoyeet al., 2008).Nutrients are required for plant growth similarly sweetpotato requires high amounts of nutrients especially nitrogen. Nitrogen is one of the most abundant elements in plants andanimals, as it is a major component of proteins. it is also a highly demanding key element for sweetpotato and other root crop yield (Canbolatet al., 2006, Adeyeyeet al., 2016).
Thereare environmental factors under field conditions that can affect the activities of PGPR. Theconcentration of IAA in soildepends on bacterial population.The variations in bacterial population due to rapid wetting and drying of soil, rainfall distribution, temperature variations, pest and disease could affect the performance of PGPR (Beneduziet al., 2012).However, the survival and performance of these bacteria in the presence of added fertilizers under normal agronomic cultural condition need to be evaluated.Therefore, thefield studieswereconducted to evaluateperformance of the PGPR with different levels of nitrogen fertilizer on growth and yield of sweet potato.
MATERIALS AND METHODS
The field experiment was conducted at UPM experimental plot. The experiment was comprised of 5treatments(Klebsiella sp. UPMSP9, Erwinia sp.
UPMSP10,Azospirillumbrasilense SP7, Bacillus sphaericus UPMB10 and Uninoculated control) combinations with three levels of N fertilizer (0, 33, and 100 kg N ha-1). The experiment was laid out in a Randomized Complete Block Design (RCBD) with three replications. The cuttings of sweetpotatoshoot were inoculated with four rhizobacterial isolatesas per treatment. The cuttings without inoculation were used as control.The cuttings were planted slanting with 1/3 buried in the soil. The soil was covered with plastic mulch to control weeds, combat insects, prevent soil loss during heavy rains and maintain soil moisture. The interspaces between planting rows were weeded manually
when necessary. The crop was irrigated regularly. Each plant was inoculated with the respective inoculum at planting and one month after planting with 20 mL inoculum per plant (approximately 109 CFU mL-1).The plants were harvested after4 months of planting. Driedshoot samples were digested with concentrated sulphuric acid (H2SO4) and hydrogen peroxide (H2O2) according to micro-kjeldahl method (Thomas et al., 1967).N, P, K concentrations were determined using autoanalyzer (Technicon II, Technicon Ltd.) and Ca, Mg by using Atomic Absorption Spectrophotometer(Perkin- Elmer, 5100 PC, Perkin Elmer).
Leaf chlorophyll content was measured based on SPAD value of youngest fully expanded leaf using a chlorophyll meter The chlorophyll content was determined using the acetone extraction method as described by Coombs et al., (1985).Fresh soil samples were collectedfor soil pH and nutrient analysis (N, P, K, Ca, Mg, IAA). Soil pH was measured with a glass electrode pH meter (PHM 210, Metrolab) in a 1:2.5 soil-water suspension.
The total nitrogen was determined following the micro-Kjeldahl method (Thomas et al., 1967). The available phosphorus was measured by Bray-2 method (Bray and Kurtz, 1945).Total N and the available P were analyzed by autoanalyzer. Concentrations of exchangeable K, Ca and Mg were determined using the shaking method (Schollenberger and Simon, 1945) and their concentrations were measured using Atomic Absorption Spectrophotometer. A modified method of Sarwaret al., (1992) wasused to determine the concentrations of IAA in soil.
Data wereanalyzedbyStatistical Analysis System (SAS,1989).Differences among treatment means were determinedusing Tukey,sStudentized Rangetest (HSD) comparison method at p=0.05.
RESULTS AND DISCUSSION Sweet potato growth parameters
There was a significant response of PGPR inoculation, N fertilizationand interaction of both factors on sweetpotatoyield and shoot-storage root ratio (Table 1).Preciselysweetpotatoyield and shoot-storage root ratio increased with increasing N rates andinoculated plants showed higher sweetpotatoyield and shoot -storage root ratio compared to the uninoculated control. The action of PGPR has improved the plant growth and yield by altering the root architecture and converting nutrients from unavailable to available form through various biological processes(Radziah and Zulkifli, 2003).Nitrogen is known to be the most essential components for plant growth. Nitrogen is present in a high amount in the atmosphere, approximately 78% but it remains unavailable to plants as there is no plants which are available to convert atmospheric dinitrogen into ammonia and to be used directly for plant growth and development. Nitrogen starvation in plant resulted in loss of vegetative vigor and depletion of growth hormone. Growth hormone concentration varies with nitrogen supply and growth vigor(Koodi et al., 2017). In general, low concentration of hormone is required for plant growth. Studies have found that application of higher N usually showed reduction in growth and yields of sweetpotato. Thus, reduction of N by 1/3 normal N rate to inoculated plant gave
comparable yields with the full fertilizer application consequently presenting a 67%
saving in N fertilizer (Vosawai et al., 2015).
Only nitrogen fertilization rates significantly (P<0.05) influenced the leaf chlorophyll content. The highest chlorophyll content was observed at plants applied with 33kg Nha-1 (Table 1).Thus, application of N increased the available N for increased chlorophyll content of leaves which is important in photosynthesis.Kalamet al.,2017, had suggested inoculation of wheat plants with biofertilizers, Bacillus polymyxa or Azospirillumbrasilinseas that produced auxin significantly increased the chlorophyllas compared with uninoculatedtreatment. The rhizobacterial inoculation has been proven to directly and indirectly stimulate the plant growth. The indirect ways include triggering the systemic resistance in plants to combat broad spectrum plant pathogen(Khalid et al., 2004,Vurukondaet al., 2016).
Table 1:Rhizobacterial inoculation and N fertilization effects onchlorophyll contentof shoot, sweet potato yield and shoot to storage rootratio
Treatments mg Clp/mg
LFW
Sweet potato yield
(t ha-1)
Shoot/storage rootratio
(S/R) Bacterial
Isolates
N Fertilizer (N ha-1)
Control 0 kg 0.009d 4.41g 2.86c
33kg 0.014ab 12.70b 3.10bc
100kg 0.012bcd 8.32cde 3.90a
Klebsiellasp 0 kg 0.010cd 8.97cd 3.70ab
33kg 0.015a 17.69a 3.88a
100kg 0.013ab 16.27a 3.79a
Erwinia sp. 0 kg 0.009d 7.97def 3.70ab
33kg 0.014ab 14.13b 3.94a
100kg 0.014ab 13.55b 3.43abc
Azospirillumsp. 0 kg 0.010cd 6.31f 3.38abc
33kg 0.015a 13.68b 3.72 ab
100kg 0.013ab 9.76c 3.86 a
Bacillussp 0 kg 0.010cd 7.09ef 3.60 ab
33kg 0.015ab 13.34b 3.66 ab
100kg 0.013ab 9.26cd 3.79 a
Significance due to PGPR. NS * *
N Fert * * *
PGPR * N Fert NS * *
Note: *Significant (P<0.05), Means in column followed with same letter (s) are not significantly different (P>0.05). mg Clp/ mg LFW: mg chlorophyll / mg leaf fresh weight
Nutrient uptake in shoots
PGPR inoculation and N fertilization rate significantly (P<0.05) influenced the shoot nutrient uptake (Table 2). Plants inoculated withKlebsiella and supplied with33kg Nha-1 recorded higher uptakeof N, P and K compared to control. There were also significant interaction effects of PGPR inoculation and N fertilizer onN, P, K, Ca and Mg uptake.
The increased plant growth could have increased the uptake of minerals and increased the content of nutrients in plant.
Researchers have found that the inoculation with PGPR can increase the yield and N,P and K uptake in non-leguminous crops (Basetet al.,2010, Souza et al.,2015).Combined inoculation of Azospirillumbrasilense and thephosphate–solubilizing bacteria Pseudomonas strica or Bacillus polymyxa on field grown sorghum significantly increased grain and dry matter yields and N and P uptake as compared with single inoculation of individual organisms.Beneficial effects of PGPR can affect the mineral nutrition of plants by changing root uptake characteristics of different crop plants (Okon and Itzigsohn, 1995, Farzanaet al., 2020). Inoculation of PGPR may improve sweetpotato plant growth through production of growth promoting substances and enhanced mineral uptake by the roots (Umesh.,2014).
One of the important phytohormones synthesized by PGPR is indole acetic acid (IAA) which is considered to be the most physiologically active auxin in plants. IAA induce plant growth by stimulating cell division and differentiation and increases root hair for higher nutrient uptake (Richardson et al., 2009 and Farzanaet al., 2017). The inoculation with PGPR can increase the yield and N, P, K content in plants by changing root uptake characteristics of different crop plants (Dinesh et al.,2015).
Vegetable crops like tomato, cucumber and pepperinoculated with various strains of PGPR having IAA producing ability showed significantly increased in growth parameter(Kidogluet al., 2007). In case of rice crop IAA producing PGPR confirmed promising effects on plant growth and N,P, K uptake in plants (Ahemad and Kibret., 2014).
Table 2:The effect of Rhizobacterial inoculation and N fertilization on sweet potato shoot nutrient uptake
Treatments Nutrient Uptake (g plant-1) Bacterial
Isolates
N Fertilizer
(N ha-1) N P K Ca Mg Control 0 kg 1.83h 0.57f 3.88h 0.65h 0.30h
33 kg 6.49c 1.38c 10.54e f
1.76d 0.88e 100 kg 5.03def 1.10de 8.81ef
g
1.40 def
0.51gh Klebsiellasp. 0 kg 5.34de 1.08de 9.12ef 1.38ef 0.61efg 33 kg 9.86a 2.63a 19.29a 2.63ab 1.99a 100 kg 8.65b 2.19b 16.19b
c
2.55abc 1.49bc Erwinia sp. 0 kg 4.44ef 1.10de 8.64fg 0.95gh 0.59fgh
33 kg 8.43b 2.18b 16.88b 2.80a 1.73ab 100 kg 6.43c 1.47c 12.59d 2.25c 1.30cd Azospirillum
sp.
0 kg 3.40g 0.91e 6.87g 1.12fg 0.46gh 33 kg 8.39b 2.11b 16.73b
c
2.54abc 1.49bc 100 kg 5.66cd 1.23cd 10.69d
e
1.51de 0.81ef Bacillus sp. 0 kg 4.19fg 0.91e 6.80g 1.09fg 0.58fgh
33 kg 8.41b 2.00b 14.71c 2.35bc 1.28cd 100 kg 5.58cd 1.39c 10.14e
f
1.58de 1.18d Significance due to PGPR
N Fert
*
*
*
*
*
*
*
*
*
*
PGPR * NFert * * * * *
Note: NS: non significance, and *: significant difference at (P<0.05).Means in column followed with same letter (s) are not significantly different(P>0.05).
Soil pH and nutrient concentration
There was a significant effect of PGPR and nitrogen fertilizer onsoil P, Ca and Mg, but not the soil pH,and N and K concentrations.The results showed that soil pH was almost neutral in all treatments. The interaction effect of PGPR and nitrogen fertilization significantly influenced the soil P, Ca and Mg.Plants inoculated with PGPR and 33kg N ha-1showed higher Nconcentration compared to the control plants without N fertilizer (Table 3).Concentrations of P, K, Ca and Mg were higher with PGPR and N application of 33kg N ha- 1 compared to the 100kg N ha-1(Table 4).
The effects of PGPR applied alone on in combination with fertilizers on sensitive biochemical indices reflecting soil quality (Gravelet al.,2007 and Kavinoet al.,2010). The present study focuses chemical parameters that reflect the fertilizers and activity of Rhizobacterial processes. Chemical properties are more sensitive to environmental stress, degradation and provide soil quality. Soil nitrogen varied with the rate of N applied. The N in soil at harvest was low due to uptake by plants and some probably lost through leaching.
The biochemical parameters are different because it is related to microbial activity. The activities of enzymes are involved in the N and P cycles in soil. (Dinesh et al., 2013).
Similarly, the soil enzymes were activated to varying degrees by PGPR and NPK applied alone or in combination.The stronger effects of PGPR + NPK fertilization positively influenced soil enzymes might be due to the greater metabolism by soil microorganisms.
Most of the biofertilizers belongs to several groups such as nitrogen fixation, phosphate solubilization and cellulolyzation. The phosphate solubilizing bacteria secrete various organic acids which enhances the phosphorus absorption by dissolving the rock phosphate anduptakingtricalcium phosphates in soil (Datoniyaet al., 2016).In Malaysia, biofertilizers are being utilized in a very large scale predominantly for the plant nutrient supply, reducing the toxic effect of the soil contaminants and thus improving soil fertility and moisture.
Table 3:Effect of Rhizobacterial inoculation and N fertilization on soil pH and nitrogen concentration
Treatments Soil
pH
N (%)
Bacterial N
Fertilizer
Isolates (N ha-1)
Control 0 kg 6.72 0.07
33 kg 6.53 0.09 100 kg 6.66 0.08 Klebsiella sp. 0 kg 6.76 0.08 33 kg 6.62 0.12 100 kg 6.72 0.10 Erwiniasp. 0 kg 6.71 0.09 33 kg 6.62 0.11 100 kg 6.83 0.10 Azospirillum
sp.
0 kg 6.54 0.09 33 kg 6.46 0.12 100 kg 6.56 0.10 Bacillus sp. 0 kg 6.64 0.07 33 kg 6.40 0.11 100 kg 6.66 0.08 Significance due to PGPR
N Fert.
PGPR * N Fert.
NS NS NS
NS * NS
Note: NS: non significance, and *: significant difference at (P<0.05). Means in column followed with same letter (s) are not significantly different (P>0.05).
Table 4:Effect of Rhizobacterial inoculation and N fertilization on soil nutrient concentration
Treatments Nutrient concentration
Bacterial Isolates
N P (mg
K cmol
(+)
Ca cmol(+)
Mg cmol(+)
Fertilizer (N ha-1)
kg-1) kg-1 kg-1 kg-1
Control 0 kg
19.27e
0.25 9.71fg 0.47b 33 kg 38.62b
c
0.29 11.13def 0.59b 100 kg 30.48c
d
0.27 12.00bcd e
0.57b Klebsiella sp. 0 kg 29.40d 0.26 10.65def
g
0.52b 33 kg 48.31a 0.30 16.18a 0.73b 100 kg 46.06a 0.29 15.65a 0.60b Erwiniasp. 0 kg 33.15c
d
0.27 9.23g 0.60b 33 kg 44.33a
b
0.28 15.49a 1.18a 100 kg 41.61a
b
0.30 13.11bc 0.68b Azospirillum
sp.
0 kg 28.31d 0.27 10.40efg 0.56b 33 kg 42.86a
b
0.28 12.05bcd 0.69b 100 kg 32.59c
d
0.30 11.50cde 0.64b Bacillus sp. 0 kg
27.11de
0.25 10.71def g
0.57b 33 kg 42.36a
b
0.29 13.36b 0.67b 100 kg 30.96c
d
0.30 12.23bcd 0.64b Significance due to PGPR
N Fert.
PGPR * N Fert.
*
*
*
NS
* NS
*
*
*
*
*
*
Note: NS: non significance, and *: significant difference at (P<0.05). Means in column followed with same letter (s) are not significantly different (P>0.05).
Concentrations of IAA in soil
PGPR inoculation and N fertilization influenced the concentration of IAA in soil (Fig.1a, b, c). There was significant (P≤0.05) interaction between PGPR and N fertilization on IAA concentration. In general, the concentration of IAA in soil decreased with increased in growth period. Theconcentrations of IAA in soils inoculated with rhizobacterial isolates were significantly higher than uninoculatedcontrol. Highest IAA was observed with Klebsiella inoculation at33kg Nha-1 fertilization rate.
PGPR inoculation and nitrogen fertilization significantly increased the IAA like compounds in soil. The increased IAA like compounds in soilcould be due to IAA synthesized by the bacterial inoculant. The bacteria probably synthesized IAA throughTRP pathways by utilizing L-TRP excreted from the root. It has been reported that up to 85% of Rhizobacteriaare able to synthesize indole acetic acid (IAA) which colonize seed or root is able to induce the cell proliferation and enhancement of IAA in soil (Bashan et al.,2014).
Different soils have been reported to vary in their native auxin content depending on the microbial population and other environmental factors such as substrate concentration, carbon source, temperature, aeration, pH (Khalid et al., 2004,Gupta et al., 2015).
BesidesIAA, PGPR is known to produce plant-growth substances such as ethylene and cytokinins which are also important in improving plant growth and causing some physiological events. The increase instoragerootyield in this study could probably due to the production of IAA by the introduced isolates.
-0,1 0 0,1 0,2 0,3 0,4 0,5 0,6
30 60 90
Time (Days)
Concentration of IAA (mg kg-1) Control
Kleb siella Erwinia Azosp Bacillus
a
Figure 1: Effect of Rhizobacterial inoculation and nitrogen on concentration of IAA in soil at different sweet potato growth stages;(a)0 kg Nitrogen,(b) 33kg Nitrogenand (c)100 kg Nitrogen.
CONCLUSION
We can conclude that a considerable amount of nitrogen fertilizer could be saved by substituting it with Klebsiellainoculum, which may be equally effective as one-third of the recommended nitrogen fertilizer used.Application of 33 kg Nha-1 generally increased yield but at higher application of 100kg Nha-1yield was reduced. Field inoculation of Klebsiella with 33kg N ha-1 enhancedthe nutrient uptake and produces IAA, thus, stimulate growth of sweetpotato and improve soil chemical properties. There is a potential in developing bacterial inoculant for use in commercial sweetpotato production.
This can be incorporated into the agricultural sector for the promising growth and yield of sweet potato.
0 0,5 1 1,5
30 60 90
Time (Days)
Concentration of IAA (mg kg-1) Control
Kleb siella Erwinia Azosp Bacillus
-0,5 0 0,5 1 1,5
30 60 90
Time (Days)
Concentration of IAA (mg kg-1) Control
Kleb siella Erwinia Azosp Bacillus
b
c
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