Chemical fertilizers × plant growth-promoting rhizobacteria
Plant growth-promoting rhizobacteria (PGPR) is a well-known group of microorganisms
able to promote plant growth through enhanced biological nitrogen fixation (BNF),
synthesis of plant hormones, soil nutrient solubilization (as phosphorus [P] and potassium
[K]; Gupta et al., 2015), besides preventing deleterious effects of soil-borne phytopathogens
(Compant et al., 2005). Due to the high importance of nitrogen (N) for plant development
and the low persistence time that synthetic N fertilizer presents in the soil (Galloway
et al., 2003), most of the studies are focused on microorganisms able to biologically
fix atmospheric N. BNF is performed by symbiotic PGPR, which are restricted to association
of leguminous plants and rhizobial isolates (e.g., Rhizobium spp., Bradyrhizobium
spp., Mesorhizobium spp., and Allorhizobium spp.), or by free-living bacterial isolates
(e.g., Azospirillum spp., Pseudomonas spp., Burkholderia spp., Gluconacetobacter spp.,
and Herbaspirillum spp.; Remigi et al., 2016). However, the research focused only
in BNF neglects the high biotechnological potential of PGPR to agriculture.
Overuse of synthetic fertilizers and agrochemical pesticides has sustained the high
crop yield and, consequently, the population growth in the last century (Stewart et
al., 2005). However, environment does not sustain these practices any more. The consequences
are already observed as high eutrophication of rivers, groundwater contamination,
atmospheric pollution, and losses of soil quality (Stewart et al., 2005; Mondal et
al., 2017). These scenarios have stimulated several agricultural researches. Replacement
of synthetic N inputs by PGPR inoculation has been possible only due to the deep knowledge
about BNF. It is interesting to farmers, since it reduces production costs besides
being an environmental-friendly technique. However, PGPR inoculation can go further,
since it presents a potential to reduce the amount of the most important synthetic
inputs applied on crops, which is of paramount importance regarding fertilizers obtained
from finite sources.
Soil phosphorus (P) and P-fertilization
Phosphorus (P) is a good example of an essential nutrient for plant development derived
from finite resources. P fertilizer is extracted from P-rich rock in the form of phosphate.
Morocco, China, South Africa and the U.S. account for approximately 83% of the world's
reserves of exploitable phosphate rock (Vaccari, 2009). Therefore, P deficiency is
one of the major limitations to crop production and it is estimated that 5.7 billion
hectares of land worldwide are deficient in P (Mouazen and Kuang, 2016). These numbers
highlight the high importance of P fertilizers for achieving optimal crop production.
Bouwman et al. (2013) estimated that annual P consumption in agriculture will increase
around 2.5% per year. Considering the finite sources of P, this data and other studies
indicated that a global P crisis is near (Abelson, 1999; Vaccari, 2009; Jones et al.,
2015). However, none of these studies have considered the residual P in the soil (Sattari
et al., 2012).
Some tropical agricultural soils are P-fixing, and the vast majority of P fertilizer
added to them are adsorbed onto soil minerals [metal oxides (mainly iron and aluminum)
and clay minerals], precipitated as P minerals (predominantly apatite-like minerals),
and immobilized as organic P compounds (soil organic matter and phytate), making its
residual P less available to crops (Martinez-Viveros et al., 2010; Hinsinger et al.,
2011). Due to such P immobilization and environmental losses, producers need to apply
twice or more P fertilizers than are actually needed for optimal yield production
(Roy et al., 2016). It is estimated that 2–8 million tons of P fertilizer are applied
to the soils every year, and ~1–4 million tons remain in the soil as a residual part.
In a future scenario (2050), 4–14 million tons will be applied, and 2–7 million tons
will remain in the soils (Roy et al., 2016). Considering that P fertilizer costs approximately
US$ 400 per ton, around US$ 400 million to US$ 1.6 billion are lost with P fertilizers
in crops around the world every year. It certainly means a substantial increase on
the food prices for consumers.
Is phosphorus solubilization the forgotten child of PGPR?
Recently, Roy et al. (2016) made a tricky question: is it possible that the increasing
amount of immobilized P in the tropical agricultural soils eventually become available
to plants and support crop productivity? In the case we keep using the same fertilization
strategies used for many years, the answer is certainly no. However, we do believe
that using adequate biotechnological approaches, the immobilized P could return to
the plants in a soluble and available form. Screening of new PGP isolates for inoculant
production aiming to optimize plant growth and BNF comprise an essential stage of
in vitro phosphate solubilization analysis (Collavino et al., 2010; Souza et al.,
2013, 2015; Walitang et al., 2017; Marag et al., 2018). These studies identified several
bacterial isolates able to promote plant growth, improve rhizosphere area and solubilize
different sources of immobilized P. Given the low mobility of P in soils, the enlargement
of volume and geometry of the rhizosphere provided by PGPR inoculation determines
the amount of P available to plants (Richardson et al., 2009). Therefore, inoculation
of PGPR seems to be a reasonable tool to maximize such approach. Microorganisms increase
the availability of inorganic P through the production of protons, organic acids,
and ligands, which are ubiquitous among rhizosphere P-solubilizing microorganisms
(Hinsinger et al., 2011), and also mobilize phytate (organic P) probably by phytase
production (Jorquera et al., 2008). However, in greenhouse and/or field conditions,
most of the studies do not evaluate different P-fertilization levels, phosphate solubilization
in the soil and P uptake by the plants. The majority of the studies considers only
plant agronomic parameters and plant N content in conditions with or without N fertilization.
Reduction of P-fertilization through PGPR inoculation
Increasing P efficiency in crops without increasing or even decreasing P inputs requires
a more efficient exploitation of soil microbial resources in agroecosystems. Some
studies clearly report that plant inoculation with new PGPR can improve P uptake.
Rudresh et al. (2005) showed that chickpea plants inoculated with Rhizobium sp. and
Bacillus sp. present higher yield (two-fold) and higher P content (four-fold) in the
grain. Vyas and Gulati (2009) and Granada et al. (2013) demonstrated that inoculation
of maize (Zea mays) with Pseudomonas spp., and Lupinus albescens plants with free-living
Sphingomonas sp. results in almost three-fold increases in their shoot P contents,
respectively. Studying wheat (Triticum aestivum L.) plants, Kumar et al. (2014) showed
that inoculation of Bacillus megaterium, Arthrobacter chlorophenolicus, and Enterobacter
improves grain yield and the amount of P in the straw and grain up to two-fold in
greenhouse and field experiments. Thus, it is already known that inoculation of efficient
P-solubilizer bacteria significantly improve P absorption by plants, even though most
of the experiments use the recommended P fertilizer dose, and reduction of the P-fertilization
has not been evaluated.
Khalafallah et al. (1982) developed an important work inoculating Vicia faba plants
with P-solubilizing bacteria. This work showed the possibility of reducing the P-fertilization
up to 50%, once plants that received half of the recommended P-fertilizer dose presented
similar plant dry weight and P-uptake when compared to plants that received usual
P-fertilizer dose. More recently, Lavakush et al. (2014) observed the same potential
in rice plants inoculated with the P-solubilizing bacteria Azotobacter chroococcum,
Azospirillum brasilense, and combined Pseudomonas spp. culture. Inoculated rice plants
presented similar performance in plant height, panicle length, grain number per panicle
and grain yield when fertilized with 30 and 60 kg P ha−1 in a greenhouse experiment.
Dutta and Bandyopadhyay (2009) showed that reduction of up to one-third in P-fertilization
of chickpea plants (inoculated with P-solubilizing Pseudomonas sp.) did not cause
any decrease in plant development parameters.
Therefore, PGPR inoculation can probably be used to reduce P-fertilization, being
an excellent biotechnological tool. However, this research area is neglected by researches
and certainly needs more investigation. All plant species are able to establish a
relationship with some PGPR, and the selection of new bacterial isolates, able to
solubilize different forms of P in vitro, is an important and necessary first step.
We hope the results obtained in greenhouse and field inoculation experiments with
selected P-solubilizing bacterial isolates and plant species subjected to reduced
amounts of P-fertilizer could serve as an alert to producers about the high costs
of normally used fertilization strategies, the concerns about finite P sources, and
the environmentally friend biotechnological option of using PGPR. Based on previous
works which addressed P-solubilization potential by PGPR inoculation in plants (mainly
Khalafallah et al., 1982; Dutta and Bandyopadhyay, 2009; Kumar et al., 2014; Lavakush
et al., 2014; Anzuay et al., 2015; Kaur and Reddy, 2015), we consider that an average
reduction of 33% in P-fertilization could be achieved with the use of high efficient
P-solubilizing bacterial isolates as crop inoculants, as indicated on the proposed
biotechnological approach in Figure 1. Therefore, future experiments need to be specifically
designed for such purposes. Considering the complexity of these mechanisms, an interdisciplinary
approach taking into account molecular, biochemical, physiological, and agronomic
parameters has a good probability to generate positive results. We have a long way
to cross until reaching similar knowledge and applicability achieved by bacterial
inoculants regarding the reduction of N-fertilizers. However, reasonable use of environmental
resources should be the basis for modern and sustainable agriculture development.
Figure 1
Schematic model of current/traditional approach (A) and proposed/biotechnological
approach (B). *On the current agricultural approach, world demand of P fertilizer
is approximately 4.5 million tons, according to FAO (http://www.fao.org/3/a-i6895e.pdf).
From these, 2.2 million tons are unavailable to crops (soil immobilization or surface
runoff), and 2.3 million tons are harvested with the crops. On the proposed biotechnological
approach, we suggest the reduction of up to 33% on the P fertilizer dose applied on
the soil, along with PGPR inoculation. Such reduction on P fertilizer together with
PGPR inoculation would result in less P unavailable to the crops. Nearly half of such
unavailable P can be further solubilized by PGPR and uptaked by the crops, resulting
in the same 2.3 million tons of harvested P (adapted from Roy et al., 2016).
Author contributions
All authors listed have made a substantial, direct and intellectual contribution to
the work, and approved it for publication.
Conflict of interest statement
The authors declare that the research was conducted in the absence of any commercial
or financial relationships that could be construed as a potential conflict of interest.