Enhancing
Phosphorus Bioavailability in Maize through Phosphorus Solubilizing Fungi
Madeeha Khan1, Abdul Latif1*,
Muhammad Arsalan1, Marjan Aziz1, Rehmat Ullah2,
Muhammad Bilal2, Waleed Asghar3*, Rizwan Latif4,
Muhammad Ehsan4 and Muhammad Tariq Mehmood5
1Barani
Agricultural Research Institute, Chakwal, Pakistan
2Department
of Agriculture, Soil and Water Testing Laboratory for research Dera Ghazi Khan,
Punjab, Pakistan
3Department
of Environmental Sciences, Faculty of Life and Environmental Sciences,
University of Yamanashi, Kofu, Japan
4Department
of Agriculture, Soil and Water Testing Laboratory Chakwal, Punjab, Pakistan
5Gram Breeding
Research Station, Kallurkot, Bhakkar, Pakistan
For correspondence: farhanqais@yahoo.com;
waleedasghar978@gmail.com
Received 11 February 2022; Accepted 09 April 2022;
Published 30 April 2022
Abstract
This study was to explore the beneficial
interactive effects of fungal inoculum alone or in conjunction with phosphatic
fertilizer on maize (Zea mays L.). We conducted a greenhouse pot
experiment in soil which included four treatments such as control, Penecillium
oxalicum, Aspergiilus niger, P. oxalicum + A. niger at
three different levels of phosphatic fertilizers (0, 100, and 200 mg kg-1).
The plant height, fresh weight of root/shoot biomass and dry weight of
root/shoot biomass and soil chemical properties were recorded. We evaluated the
growth parameters of maize and phosphorus (P) uptake in maize were highest in
treatment I3 ื F2 (Penecillium+Aspergillus +
200 mg P kg-1) followed by I2 ื F2 (Aspergillus
+ 200 mg P kg-1) over rest of the treatments. The beneficial
effect was decreased where alone fertilizer dose was added as compared to those
where it was added with the co-inoculation of phosphorus solubilizing fungi
(PSF). It was observed that soil pH, total organic carbon and available P
significantly changed because of various treatments. Based on these evidences,
it could be inferred that increasing the maize growth by fungal culture
improves soil P fertility, which is favorable to succeeding crops. Further
research is needed to understand the chemistry of co-inoculation of fungal
inoculum with phosphatic fertilizer. ฉ 2022 Friends Science Publishers
Keywords: Phosphorus; Bioavailability; Fungi; Phosphatic
fertilizers; Maize
Introduction
Phosphorus
(P) is the second most crucial macronutrient after nitrogen, and due to its low
bio availability in soil, limits plant growth and development (Anand et al.
2016). Many physiological processes, such as photosynthesis,
respiration, and cell division, depend on plants via P availability. It also aids in the formation of a more
profound and more abundant root system (Farooq et al. 2009). Phosphate anions,
such as primary orthophosphate (H2PO4-) or secondary
orthophosphate (HPO42-), are used by plants to obtain
phosphate anions, on the other hand, they are highly reactive and could be
immobilized through precipitation with cations such as Ca2+, Mg2+,
Fe3+, and Al3+, depending on the specific properties of
the soil. Phosphate is exceedingly insoluble and inaccessible to plants in
these forms, which consequences a minimal amount of P available to plants (Sharma et al.
2011).
Despite the widespread deficiency of soil P (Pradhan and Sukla 2006; Richardson and Simpson 2011),
plants are usually unable to obtain it in adequate
quantities, even in fertile soils (Talboys et al. 2016). Athar (2005) and Fatima et al.
(2006) reported
that 90% of the soils have P deficient in Pakistan. However, there is a need to
overcome this problem for getting high yield in crop production. Chemical P
fertilizers are often used to minimize the P shortage issues and increase plant
yield; however, phosphatic fertilizers are costly. The bulk of P applied in
phosphatic fertilizer is transformed to insoluble forms (Chen et al. 2006). As a
result, only a small portion of the fertilizer supply reaches the plant roots.
Excessive use of phosphatic fertilizers has resulted in a significant buildup
of P in most agricultural soils. Phosphorus recovery from phosphatic
fertilizer, on the other hand, is often just 10 to 30% (Schr๖der et al. 2011).
To achieve sustainable agriculture, it is vital to limit the use of chemical
fertilizers while providing the necessary P by other methods. In this
context, studies on the efficacy of biological fertilizers containing the
needed quantity of P for diverse crops are particularly important.
Despite the widespread deficiency of soil P (Pradhan and Sukla 2006; Richardson and Simpson 2011),
plants are usually unable to obtain it in adequate
quantities even in fertile soils (Talboys et al. 2016). In Pakistani soils, almost 90%
of the soils are P deficient (Athar 2005; Fatima
et al. 2006). Chemical P fertilizers are often used to address P
shortage issues and increase plant yield, however phosphatic fertilizers are
costly. The bulk of P applied in the form of phosphatic fertilizer is
transformed to insoluble forms (Chen et al.
2006). On the other hand, biological fertilizers containing the needed
quantity of P for diverse crops seems to be a cheap and environmental friendly
option.
Phosphorus is
essential to growth, and microorganisms are fierce competitors for the
nutrient. In addition to compensating for the higher cost of fertilizer
production, they also activate the fertilizer applied to the soil (Pradhan and Sukla 2006). Phosphorous
solubilizing micro-organisms (PSMs) include a variety of fungi, bacteria, actinomycetes, and yeast due to their
capacity to solubilize sparingly soluble P (Wani
et al. 2007). PSMs are
involved in numerous mechanisms for phosphate solubilization in the growth
environment, including acid generation that lowers pH, exchange reactions, and
ion chelation (Khan et al. 2009).
Fungi are a major component in the solubilization
of insoluble P by generating by releasing organic acids such as lactic, citric,
2-ketogluconic, glycolic malic, malonic, oxalic, succinic and tartaric acids,
all of which have chelating properties (Krishnaraj
et al. 2014), and also by decreasing pH (Seshadri et al. 2004). According to Pradhan and Sukla (2006), Aspergillus and Penecillium
strains exhibit varying amounts of phosphate solubilization activity
in liquid broth culture in the presence of different carbon and nitrogen
sources. Dual inoculation of these
strains also has a significant effect on increasing yield of soybeans plant (Soe et al. 2012). However, there is not
much literature available on the inoculation of phosphorus solubilizing fungi
(PSF) and phosphatic fertilizer on maize crop. This study was conducted with
the objective to compare P absorption by maize and to evaluate the impact of
PSF on soil and plant growth parameters.
Materials
and Methods
Soil collection and preparation
Soil was taken from the field
surface (015 cm) at experimental area of
PMAS-Arid Agriculture University Rawalpindi. A composite soil sample was drawn
from the whole soil lot and analyzed for soil texture, soil moisture content,
pH, ECe, bulk density, calcium carbonate, total organic carbon (TOC),
exchangeable K and available phosphorous.
Fungal strains selection, preparation and application of PSF inoculants
Two
strains of fungi (Aspergillus and Penicillium) were selected based on of
their high P solubilizing efficiency and obtained from the Department of Soil
Science, PMAS-Arid Agriculture University, Rawalpindi. These strains were
cultured in 250 mL broth by using reciprocal shaker at 200 rpm for 45 days. Before seed sowing, ten milliliters of each fungal strain (3.93 ื
105 CFU/mL) was inoculated
with irrigation water (500 mL) to each pot (6 kg) of respective treatment kept
under greenhouse. Maize variety NARC-2704 was used in this pot experiment.
Seven seeds of maize were sown at 2 cm depth of earthen pots. The distance
between two plants was maintained by thinning and keeping five seedlings per
pot after ten days of sowing.
Experimental layout and treatments
It was
a two factors factorial experiment arranged in the completely randomized design
(CRD) with three replications. Treatments were inoculum strains such as I0 =
Control, I1 = P. oxalicum, I2
= A. niger and I3 = P. oxalicum + A. niger, and phosphorus fertilizer levels such as F0=
Control, F1 = Fertilizer @ 100 mg P kg-1 soil and F2
= Fertilizer @ 200 mg P kg-1 soil.
Basic dose of N and K fertilizers were applied at 120 and 50 mg kg-1,
respectively. The sources for N, P, and K were used as urea, single super
phosphate, and murate of potash, respectively. To control insects and pests of
maize carbofuran 7G was applied at 5 g/pot. Pots were irrigated with tap water
according to the need of crop. At flowering stage, the data were recorded on
crop growth parameters. The plant samples were collected and analyzed for total
phosphorus.
Data recording
Data
on plant growth parameters such as plant height, dry weight of shoot/root, and
dried weight of shoot/root and root length were collected.
From each pot plant height was measured
in centimeters with the help of meter rod and then averaged. From each pot fresh weight of shoot and root
was determined in grams with the help of weighing balance. Shoot and root sample were placed in oven at
65ฐC for 48 h and dry matter yield was recorded.
Plant analysis for phosphorus
Total phosphorus was determined
from plant samples through dry ashing. For this, plant sample were washed, air dried and dried in oven for 24 h at 60ฐC.
Samples were ground and then again
dried at 60ฐC to obtain constant
weight prior to sample preparation. The concentration of phosphorus was
determined using this curve through spectrophotometer reading at 440 nm
(Chapman and Pratt 1961).
Where,
R = Ratio between total volume of the aliquot and the aliquot volume, Wt
= Weight of dry plant sample (g).
Soil characterization
Soil was analyzed for the
following characteristics: Soil moisture content, particle size distribution,
soil pH, electrical conductivity, available phosphorus, TOC, calcium carbonate
(Table 1).
Statistical analysis
This experiment was conducted
using a completely randomized design (CRD). The acquired data was statistically
analyzed using the analysis of variance (ANOVA) technique and the mean value
was compared using the least significant difference (LSD) test at a probability
level of 5%.
Results
Plant height
The results of interactive
effect of inoculation and phosphorus fertilizer showed that I3 ื F2
(Penecillium+Aspergillus + 200 mg P kg-1) recorded the
highest plant height (137.67 cm) followed by I2 ื F2, and
I1 ื F2. The I0 ื F0 recorded the
minimum value of plant height (106.67 cm) (Table 2).
Dry weight of shoot and root
The
results of interactive effect of inoculation and phosphorus fertilizer showed that
I3 ื F2 (Penecillium + Aspergillus + 200 mg
P kg-1) recorded the highest dry weight of shoot and root (7.67 g
and 0.56 g, respectively), followed by I2 ื F2, and I1
ื F2. The I0 ื F0 recorded the minimum
value of dry weight of shoot and root (3.03 g and 0.13 g, respectively) (Table 2).
Root length
The results of interactive
effect of inoculation and phosphorus fertilizer showed that I3 ื F2
(Penecillium + Aspergillus + 200 mg P kg-1)
recorded the highest root length (30.67 cm), followed by I2 ื F2,
and I1 ื F2. The I0 ื F0 recorded
the minimum value of root length (7.67 cm) (Table 3).
Total phosphorus of plant
The results of interactive
effect of inoculation and phosphorus fertilizer showed that I3 ื F2
(Penecillium + Aspergillus + 200 mg P kg-1) with
a value of 0.28% proved best in P uptake followed by I2 ื F2,
and I1 ื F2. The minimum value of P uptake (0.2%) was
observed where I0 ื F0 recorded were treated. The results
of individual effect of inoculation showed that I3 recorded the
highest P uptake (0.25%), followed by I2 and I1. The
minimum P uptake was observed in I0 (0.21%) (Table 3).
Table 1: Physico-chemical properties of soil before the start
of experiment
Characteristics |
Values |
Clay |
15% |
Sand |
71% |
Silt |
14% |
Texture |
Sandy
loam |
ECe |
0.314
dS m-1 |
Soil pH |
7.61 |
Soil Moisture |
14.6% |
Bulk Density |
1.40
Mg m-3 |
Available P |
7.63
ตg g-1 |
Exchangeable K |
129
ตg g-1 |
Calcium carbonate |
0.139
g kg-1 |
Total Organic Carbon |
0.50% |
ECe=
Electrical conductivity extract, P = Phosphorous, K= Potassium
Table 2: Interactive effect of phosphatic fertilizer and P
solubilizing fungal inoculum on plant height (cm), shoot and root dry weight
(g) of maize
Parameter of maize plant |
Inoculum (I) |
Fertilizer levels |
|||
F0 |
F1 |
F2 |
|||
Plant height |
I0 |
106.67 f |
102.67 g |
132.00 b |
|
|
I1 |
94.67 h |
114.67 de |
133.00 b |
|
|
I2 |
112.33 e |
115.33 d |
133.33 b |
|
|
I3 |
116.33 cd |
118.67 c |
137.67 a |
|
Shoot dry weight |
|
|
|
|
|
|
I0 |
3.03 j |
3.67 i |
6.30 d |
|
|
I1 |
3.83 h |
4.83 g |
6.57 c |
|
|
I2 |
4.83 g |
5.53 f |
7.20 b |
|
|
I3 |
6.00 e |
6.23 d |
7.67 a |
|
Root dry weight |
|
|
|
|
|
|
I0 |
0.13 d |
0.20 cd |
0.43 ab |
|
|
I1 |
0.30 bc |
0.33 bc |
0.36 bc |
|
|
I2 |
0.30 bc |
0.36 bc |
0.46 ab |
|
|
I3 |
0.40 ab |
0.43 ab |
0.56 a |
|
Table 3: Interactive effect of phosphatic fertilizer and P
solubilizing fungal inoculum on root length (cm) Phosphorous contents (%) of
maize plants of maize
Parameter of maize plant |
Inoculum ( I ) |
Fertilizer levels |
||
|
|
F0 |
F1 |
F2 |
Root length |
I0 |
7.67 i |
11.67 h |
20.00 d |
|
I1 |
13.33 g |
15.00 f |
25.67 c |
|
I2 |
13.33 g |
16.67 e |
27.67 b |
|
I3 |
19.33 d |
19.00 d |
30.67 a |
|
|
|
|
|
Phosphorous contents (%) |
I0 |
0.2 d |
0.23 d |
0.23 d |
|
I1 |
0.21 f |
0.21 f |
0.25 c |
|
I2 |
0. 22 e |
0.22 e |
0.26 b |
|
I3 |
0.23 d |
0.24 cd |
0.28 a |
Change in soil pH,
TOC and available P after crop harvesting
The results of interactive effect of
inoculation and phosphorus fertilizer showed that I3 ื F2 recorded
the maximum change % in soil pH, TOC and available P (19.71, 30.0 and 38.40%),
followed by I2 ื F2, and I1 ื F2.
The I0 ื F0 recorded the minimum change % in pH, TOC and available P (1.5, 4.0
and 1.70%) Table 4.
Table 4: Effect of different fungal inoculum and phosphorous
rates on soil pH, TOC and available P
Treatments |
pH |
Change after harvest (%) |
TOC (%) |
Change after harvest (%) |
Available P |
Change after harvest (%) |
Io ื Fo
(Control) |
7.53 |
1.05 |
0.52 |
4 |
7.5 |
1.70 |
I1 ื Fo (Penecillium spp.) |
6.91 |
9.19 |
0.55 |
10 |
7.8 |
2.22 |
I2 ื Fo (Aspergillus spp.) |
6.82 |
10.38 |
0.55 |
10 |
7.9 |
3.53 |
I3 ื Fo (Penecillium + Aspergills) |
6.54 |
14.06 |
0.6 |
20 |
8.2 |
7.47 |
Io ื F1(100
mg P kg-1) |
7.21 |
5.25 |
0.54 |
8 |
8.0 |
4.84 |
I1 ื F1 (Penecillium + 100 mg P kg-1) |
6.72 |
11.69 |
0.55 |
10 |
8.4 |
10.09 |
I2 ื F1 (Aspergillus + 100 mg P kg-1) |
6.63 |
12.87 |
0.56 |
12 |
8.7 |
14.02 |
I3 ื F1 (Penecillium + Aspergillus + 100 mg P
kg-1) |
6.42 |
15.24 |
0.63 |
26 |
9.0 |
17.95 |
Io ื F2 (200
mg P kg-1) |
7.12 |
6,43 |
0.54 |
8 |
9.2 |
20.57 |
I1 ื F2 (Penecillium + 200 mg P kg-1) |
6.71 |
11.82 |
0.56 |
12 |
9.5 |
24.50 |
I2 ื F2 (Aspergillus + 200 mg P kg-1) |
6.51 |
14.45 |
0.57 |
14 |
10.23 |
34.07 |
I3 ื F2 (Penecillium + Aspergillus + 200 mg P
kg-1) |
6.11 |
19.71 |
0.65 |
30 |
10.56 |
38.40 |
Discussion
In
this study it was observed that the interaction PSF with P fertilizer (Penecillium +
Aspergillus + 200 mg P kg-1) had a profound effect on plant height, fresh weight of shoot/root,
and dried weight of shoot/root and root length as compared to control.
With the application of PSF, it can increase the soil P-available so that plant
growth increase, this is because the application of PSF can produce organic
acids that can chelate Al and Fe so that P is available for plants (Silitonga et al. 2019). The
PSF strain with inorganic phosphatic fertilizer greatly influenced the plant
height, which could be due to increased bioavailability of nutrients (K, N and
P). These findings are consistent with Wu et al. (2005), who reported
that combination inoculation of PSF and inorganic phosphatic fertilizer
resulted in a significant increase in plant height of maize.
Similarly, the
interactive effect of phosphatic fertilizer and PSF inoculum had significant
effect on shoot and root dry weight. This is because plants are able to absorb
P nutrients, with the increasing of P-available causing P content to also
increase
(Silitonga et al. 2019). These results were in agreement with the
finding of Wakelin et al. (2007), who tested the combination of PSF
inoculum (P. radicum and P. bilaiae) with phosphate fertilizer,
and found a 15% increase in shoot growth and shoot dry matter of lentil crop.
Similarly, Richa et al. (2007) found that when phosphatic fertilizer was
combined with PSF inoculum, root dry weight was considerably higher than when
fertilizer or fungus were applied alone.
The root length of maize crops at various
levels of phosphatic fertilizer with various fungal inoculum combinations
revealed the fact that interactive effect of both fertilizer and inoculum had
the highest root length. With the application of phosphate solubilizing fungi,
it can increase the soil P-available so that plant growth increase, this is
because the application of phosphate solubilizing fungi can produce organic
acids that can chelate Al and Fe so that P is available for plants (Silitonga et al. 2019). These results are in line with that of Wu et al.
(2005), who stated that growth of maize plant increased by combined inoculation
of PSF and chemical fertilizer include increase in plant height, plant weight
and root length. The results regarding effect of individual fungal strains,
rate of fertilizer application and combination of both factors on total P of
maize crop are consistent with those of Wahid and Mehana (2000), who concluded
that mixed inoculation of rock phosphate and super phosphate with PSF (Penecillium) increases the production of
Faba bean (Vicia faba L.)
and the P uptake. Wahid and Mehana were of the view that these strains
secrete organic acid in soil that increases the plant uptake of P from a water
soluble P.
The data after the
maize crop has been harvested revealed that the interaction PSF with P
fertilizer (Penecillium + Aspergillus + 200 mg P kg-1)
significantly altered the soil pH, TOC and available P as compared to control.
The decrease in soil pH could be due to release of organic acids by PSF (He et
al. 2002). These results are in accordance with the finding of Iman and
Azouni (2008), who suggested that co inoculation of PSF with phosphate
fertilizer cause decrease in pH as compared to single inoculation of these
strains and fertilizer. Similarly, Caravac et
al. (2004) found more available P, more water soluble carbon, and a lower
soil pH when compared to the control soil upon the addition of phosphatic
fertilizer and PSF.
Conclusion
The results of the study
revealed that growth parameters of maize and P uptake were improved where PSF (Aspergillus and Penecillium)
co-inoculated with phosphatic fertilizer at 200 mg kg-1. The
combined impacts of amendments were greater than the effects of individual
amendments and control. Solubilized P increased soil fertility and as a result
yield of maize was increased. Thus, it is concluded that the combined use of
PSF and phosphatic fertilizer may increase the P uptake and yield of crops.
Acknowledgements
Not applicable
to this article
Author Contributions
Madeeha Khan planned and
performed the experiments, Abdul
Latif assisted in research theme and writing, Muhammad Arsalan technical
guidance, Marjan Aziza data
analysis, Rehmat Ullah and Muhamad Bilal technical guidance, Waleed Asghar data analysis,
Rizwan Latif, Muhammad Ehsan and Muhammad
Tariq Mehmood data analysis.
Conflicts of
Interest
Authors declare
no conflicts of interests among institutions
Conflict of interest
The authors declare that they
have no competing interests.
Data
Availability
The datasets
generated during the study are all included in the manuscript
Ethics Approval
Not applicable
to this article
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