fsufs-04-00106

REVIEW
published: 10 July 2020

doi: 10.3389/fsufs.2020.00106
The Roles of Plant Growth Promoting

Microbes in Enhancing Plant
Tolerance to Acidity and Alkalinity
Stresses
Levini A. Msimbira and Donald L. Smith*
Department of Plant Science, McGill University, Montreal, QC, Canada
Plant growth often occurs under a range of stressful conditions, including soil acidity
and alkalinity. Hydrogen ion concentration, which determines pH of the soil, regulates
the entire chemistry of plant nutrient colloidal solutions. Beyond certain levels of pH,
multiple stresses such as hydrogen ion toxicity, and nutrient imbalance, toxicities and
deficiencies are induced in plants. Breeding for stress coupled with suitable agronomic
practices has been a way to deal with this situation in agriculture. However, plant
growth promoting microbes (PGPM) have shown potential as sustainable plant growth
Edited by: enhancers and have potential to help with a range of stresses in their environment.
Everlon Cid Rigobelo, Considering the long-term evolutionary relationships between plants and microbes, it is
São Paulo State University, Brazil
probably that much remains unknown about potential benefits of microbes that could
Reviewed by:
Noemi Carla Baron Cozentino, be harnessed from PGPM. This article reviews the current understanding of acidity and
São Paulo State University, Brazil alkalinity stress effects on plants and various approaches have or could address these
Saddam Hussain,
University of Agriculture, Faisalabad,
stresses. This review provides a detailed account of the current understanding regarding
Pakistan the role of PGPM in acidity and alkalinity stress management, including when agronomic
*Correspondence: practices and plant breeding are combined. Approaches already evaluated have shown
Donald L. Smith limitations because acidity and alkalinity in soils are gradual and progressive conditions.
donald.smith@mcgill.ca
Greater exploitation of PGPM in this regard, would be interesting to explore as they have
Specialty section: the potential to address multiple stresses in a more sustainable fashion. Future crop
This article was submitted to
production will require further breeding for pH stress resistance, but also implementation
Crop Biology and Sustainability,
a section of the journal of microbial technologies that provide enhanced tolerance to pH stress.
Frontiers in Sustainable Food
Keywords: acidity, alkalinity, PGPM, soil pH, plant stress
Systems
Received: 20 May 2020
Accepted: 16 June 2020
Published: 10 July 2020
INTRODUCTION
Citation: Abundant microscopic life resides in the soil including bacteria, algae, protozoa and fungi (Glick,
Msimbira LA and Smith DL (2020) 1995; Müller et al., 2016), together with below-ground plant parts. The vigor of the microbes in the
The Roles of Plant Growth Promoting
soil depends on nutrient availability, temperature, water and pH, among others. Plants, partition
Microbes in Enhancing Plant
Tolerance to Acidity and Alkalinity
significant amounts of photosynthetically synthesized carbon to their root systems (Zhalnina et al.,
Stresses. 2018) for the important roles of root growth and maintenance. Additionally, this C partitioning,
Front. Sustain. Food Syst. 4:106. to a large extent, is released from the roots into the rhizosphere in the form of exudates and
doi: 10.3389/fsufs.2020.00106 sloughed off cells, together called rhizodeposition (Paterson et al., 1997; Badri and Vivanco, 2009).
Frontiers in Sustainable Food Systems | www.frontiersin.org 1 July 2020 | Volume 4 | Article 106
Msimbira and Smith PGPR for Plant pH Stress Tolerance
Rhizodeposition serves as the main reduced C source for the stress alleviation related to the evolutionary understanding
microscopic life inhabiting in the soil and sustains diverse groups that microbes have co-evolved with plants, each benefiting the
of microbes and microbial feeding life forms (Nguyen, 2009). other. Microbes, having a large surface area to volume, are very
The root exudates are organic compounds which include: organic exposed to environmental stressors, so that their mode(s) of
acids, sugars, fatty acids and amino acids (Huang et al., 2014); adaptation is of great importance for survival and, potentially
all these have nutritional, preferential microbe selection and of high impact, if these could be translated to multicellular
soil colloidal effects. Exudates therefore, control interactions organisms. While optimum pH is a crucial factor for survival in
between plants and microbes in part because they contain an evolutionary context, challenging conditions improve fitness
signal molecules that facilitate the interactions (Bulgarelli et al., over the course of evolution. Other factors of great importance
2013). Many studies have shown that plants expend this C to include temperature and nutrients, which will also be touched
attract beneficial microbes such as rhizobia, involved in biological upon as related to pH.
nitrogen fixation in legumes (Msimbira et al., 2016; Chagas
et al., 2018) and mycorrhizal associations (Van Der Heijden
et al., 2015). The legume-rhizobia symbiosis is a plant growth PLANT MICROBE INTERACTION
promoting mechanism acting through nitrogen fixation that is
well described as compared to other plant-microbe associations Plants do not exist alone; always have complex interactions with
(Oldroyd, 2013); it is reported to contribute to about 50% of microbes. Plants co-live with microorganisms (fungi, bacteria
the biologically fixed nitrogen on earth (Lindström et al., 2010). and archaea), allowing them to inhabit almost all of their tissues;
The second-most largely studied mechanism is that of a set of and the resulting assemblage of microbes is collectively known as
plant-fungal interactions, which involves about 90% of all plant the plant-microbiome or phytomicrobiome (Knack et al., 2015;
species on planet Earth, by way of mycorrhizal symbioses (Gough Smith et al., 2017). This perspective has helped, in recent years, to
and Cullimore, 2011; Zifcakova, 2020). Such interactions benefit start answering some common evolutionary questions regarding
plants by improving nutrient acquisition, water uptake and ability how microbes have evolved, together with their host organisms,
to survive various stresses. The usefulness of plant-microbe from their original ancestors. It is of critical importance to
interactions has been the focus of intensive research, focused on understand how plant adaptation has been influenced by their
unlocking key unanswered question, since their first description interactions with microbes, though much remains unknown.
(Kloepper et al., 1989). Since then, beneficial interactions and Plant-microbe interactions are a lifelong process for plants, as
better understanding of the mechanism(s) involved in microbial some microbes may be leaving the plant-associated community,
enhancement of plant growth have been demonstrated (Lira, while others will be entering the community (Baltrus, 2017).
2015; Smith et al., 2015). The ability of plants and microbes to communicate prior to
Beneficial symbiotic associations between early plants and physical contact being established is a very important (Chagas
mycorrhizal fungi are thought to have evolved to overcome et al., 2018) as it helps the partners maximize the chance
limitations of terrestrial ecosystems, such as restricted water of benefiting from one another, without harm. There are a
and nutrient availability (Kenrick and Crane, 1997; Kenrick and number of phytomicrobiome groupings, for instance depending
Strullu-Derrien, 2014). In soils, nutrient availability is related to on the plant part colonized by microbes: rhizomicrobiome –
hydrogen ion concentration (H+ ), which is the measure of soil roots, caulomicrobiome – stem, phyllomicrobiome – leaves,
pH. The pH variation in the environment has a direct impact anthromicrobiome – flowers, carpo microbiome – fruit, or degree
on the availability of nutrients and plant growth; the critical and of intimacy with the plant tissue which are termed as endophyte
important effects of these conditions on microbial communities (interaction inside plant parts), epiphyte (on the surface of
are not well understood. In soils, pH is an important driver plant structures such as shoots, stems, leaves, flowers and fruits)
for soil microbial community structures. Microbial survival and (Laksmanan et al., 2014; Chagas et al., 2018). The rhizosphere
colonization in such conditions requires the capacity to sense, phytomicrobiome richness, activities and diversity is far greater
and adapt to, environmental changes (Biswas et al., 2007). than the phyllosphere (Laksmanan et al., 2014). This is primarily
Recent years have witnessed considerable interest in because much of the root exudation and sloughed off cells contain
unraveling the role and potential of microbes in the success nutrient rich compounds for microbes associated with roots
of plants and animals. Of all, the human microbiome is the (Meharg and Killham, 1990; Beneduzi et al., 2012; Daguerre
most studied, as reviewed by Gilbert et al. (2018); more recently, et al., 2017). Even with many questions unanswered about
much attention has been focused on plants and their associated their full potential role in each of their tissues of colonization,
phytomicrobiome (Compant et al., 2019); terrestrial plants being plant-associated microbes provide promising insights around
the entry point of most energy into the terrestrial biosphere. some best ways to augment plant growth and productivity, and
Much has been done, mostly on symbiotic microbes and understanding continues to expand.
particularly under optimum conditions for plant growth. This For agriculture, microbes hold great promise in promoting
review investigates the current understanding of one of the productivity through synergistic interactions with host plants.
common, but complex and less explored abiotic factors, pH, All agricultural production taking place under field conditions
as a determinant factor of the distribution and survival of face a range of challenges. This means increasing production
microbes and plants. This review also wishes to understand with a constant, or even decreasing, land resource, and the
how much is known regarding aspects of acidity and alkalinity need for a breakthrough to find possible sustainable means
for food production under field conditions. Plant growth have direct impacts on plant growth and development. It is clear
promoting elements in the rhizomicrobiome provide promising soil and crop productivity are linked to pH. The United States
potential for sustainable crop production and there has been Department of Agricultural National Resources Conservation
increased interest in optimizing their use under a range of Service has categorized soil pH as follows: ultra-acidic (<3.5),
stresses, such as salinity and drought (Booth et al., 2002; extremely acidic (3.5–4.4), very strongly acid (4.5–5.0), strongly
Subramanian et al., 2016). As the world faces changing, and acidic (5.1–5.5), moderately acidic (5.6–6.0), slightly acidic (6.1–
generally harsher, crop-growth conditions related to ongoing 6.5), neutral (6.6–7.3), slightly alkaline (7.4–7.8), moderately
climate change, preparedness requires multiple options for alkaline (7.9–8.4), strongly alkaline (8.5–9.0) and very strongly
sustainability. Apart from drought and salinity two other key alkaline (>9.0) (Burt, 2014).
growth stressors of the phytomicrobiome are increasing acidity Agricultural crop production is generally conducted within
and alkalinity of the soils. the range of slightly acidic to slightly alkaline, a window that
Many recent studies have identified beneficial microbes that is associated with optimal availability of soil nutrients. In all
help plants, including crop plants, to survive the stresses they soils, solubility, mobility and bioavailability of trace elements
encounter, including nutrient imbalance (Mylona et al., 1995; is strongly affected by pH. However, soils which fall outside of
Yazdani et al., 2009), salinity (Subramanian et al., 2016), and the range of optimum nutrient availability are grouped as either
drought (Lim and Kim, 2013), with much less being reported acidic or alkaline and pose a range of challenges to plants. Though
regarding soil acidity and alkalinity. Thus, there is potential to plants differ in their tolerance to extreme pH, most agricultural
understand better and move forward with a more sustainable plants perform optimally at a pH near neutrality (Läuchli and
agriculture based on knowledge at hand on each physical stress, Grattan, 2012). In the context of crop production, pH variation
and the role microbes can play in agricultural management of is associated with all the ways the soil is managed before, during
these stresses. A key factor in microbial proliferation in the wild is and after crop production, which includes; soil tillage, planting
pH. The acidity and alkalinity of soils has been linked directly to of cover crops, fertilizer application and lime addition, as well as
soil and plant associated microbial population dynamics (Biswas precipitation and other climate variables.
et al., 2007; Zhalnina et al., 2015). Despite its obvious importance A full understanding of pH is necessary for optimizing
much seems unclear as to why microbes behave the way they do nutrient cycling, soil remediation and plant nutrition, as it
at varying pH levels. affects the entire interacting system. In order to establish ways
to deal with various aspects that are affected by soil pH, one
should initially understand what causes variation in the soil
SOIL: A CENTER FOR PLANT MICROBE pH. One of the major causes of pH variation is the inherent
INTERACTION mineral composition of the parent soil material. In this review,
acidification and alkalization of soil are discussed to enlighten
Soil is a reservoir of basic natural resources, such as nutrients, our understanding of causes of pH changes in the soil below and
for animals, plants and microbes. It is a life support system above neutrality.
that provides a wide range of necessary ecosystem goods and
services ranging from storage of carbon, to water purification, Soil Acidification
soil fertility and agricultural production (Rojas and Caon, 2016). Soil acidification is the result of various direct and indirect factors
Variation in soil characteristics throughout the world is affected interacting with the soil; these include nutrient cycling and
by weather/climate and how it is geopositioned on the globe. organic matter decomposition, high and acidic rainfall, fertilizer
Apart from nutrients, soil also contains plant-available water application, crop growth and weathering (Figure 1). Acidification
which plays a key role in creating an aqueous nutrient solution, is a gradual and progressive process which is influenced by
the form taken up by plants (Sassenrath et al., 2018). The fact agricultural practices and now by climate change (Bolan et al.,
that all living biological cells are water-based systems makes a 1991; Filipek, 1994; Hao et al., 2019). It is the result of increased
cell’s survival very dependent on aqueous equilibria. For any H+ concentration with the H+ released from Carbon (C),
aqueous solution reaction to occur, presence of anions and Nitrogen (N) and Sulfur (S) during transformation and cycling.
cations is needed. The necessity of appropriate pH in a biological For example S and N oxides released from burning of fossil
system is crucial as it helps maintaining biochemical equilibria, fuels react with rain water to form tetraoxosulfate (vi) acid and
correct levels of proton dissociable groups and maintain the trioxonitrate (v) acid (Oshunsanya, 2018). Mineralization and
cell pH at near neutral all the time. Like any other living oxidation of organic N and S release H+ , thus lowering the soil
cells, microbes need an appropriate pH balance to maintain pH. Organic matter decomposition causes release of CO2 into the
physiological functions. soil air which, when dissolved in soil water, forms H2 CO3 which
causes a decline in pH (Bolan et al., 1991).
Soil pH High rainfall is also a cause of soil acidification because
The measure of soil reaction (alkalinity or acidity) is expressed rainwater is slightly acidic (around pH 5.7), a result of reaction
as pH. It is mostly measured in water solutions and to lesser with atmospheric CO2 forming carbonic acid, hence reducing the
extent, for research purposes, 0.01 M calcium chloride is used pH of soil. In addition, water in the soil causes leaching of basic
(Blake et al., 1999). Soil pH is a key condition with substantial cations, such as bicarbonate, leaving more Al3+ and H+ relative
influence on soil biology, chemistry and physical processes which to other cations in the soil (Oshunsanya, 2018).
FIGURE 1 | An illustration of various soils with respect to pH, nutrient availability, deficiencies, and imbalances.
In agricultural soils a major contributor to acidity is the and carbonate containing compounds such as Na+ , Mg2+ ,
application of ammonium-based fertilizers, urea, sulfur and K+ , and Ca2+ is linked to silicates being hydrolyzed and
legume cultivation. The salts from applied fertilizers have strong subsequent OH− release, which increases soil pH. Irrigation is
effects on acidification of the soil through nitrification. This also associated with alkalinity of the soil, especially when the
happens only when NH4 + undergoes nitrification and/or NO3 − used water contain large quantities of bicarbonates (Oshunsanya,
is leached but not when the nitrate is taken up by plants 2018). Drought is another natural cause of soil alkalinity
(Marschner, 2011). The scope of the problem is becoming due to insufficient water to leach soluble salts, allowing their
worrisome as the occurrence of acid rain and continued intensive accumulation in the upper soil profile. Alkaline soils are
use of synthetic fertilizers. In addition, N2 fixation also has impact characterized by high concentrations of carbonates (CO3 2− )
on soil acidification. Comparatively, legumes are known to cause and bicarbonates (HCO3 − ) which have the ability to neutralize
more soil acidification than non-legumes, due to excessive uptake acids (Bailey, 1996). As a result, alkaline soils are associated
of cations relative to anions during N2 fixation, and also leaching with desertification in most parts of the world, and this is also
of nitrates eventually resulting from fixed N (Tang, 1998; Tang closely associated with soil salinity. Recently, the demand for
et al., 1999). However, variation in N2 fixation among legumes aluminum in the world has contributed to increased alkalinity
exists, which results in variation of the acid generated with a range in surrounding ecosystems because mining and disposing of
of 0.2 to 1 mol H+ for each mol of fixed N (Bolan et al., 1991). the alkaline bauxite residue (Kong et al., 2017). Lastly, over
Other factors which influence acidification by legumes are soil liming also leads to alkalization of soil. Therefore, liming
nutrients and nitrogen (Yan et al., 1996; Marschner, 2011). should carefully consider the knowledge of soil acidity so that
Crop growth is another factor which causes localized soil required liming material can be calculated before it can result in
acidification as a result of nutrient uptake. Plants take up soil alkalization.
nutrients from the soil solution in ionic form with a preference
for cations over anions, which leads to cation reduction in the
soil (Tang and Rengel, 2003). To counteract the effect of charge MICROBIAL COMMUNITIES IN
imbalance, plants release H+ from roots to the rhizosphere, hence RELATION TO SOIL Ph
lowering soil pH. In addition, roots naturally exude organic acids
which cause acidification of the soil. Environmental factors are the main drivers of the
phytomicrobiome composition (Chu et al., 2016; Baltrus,
Soil Alkalization 2017) with soil pH exerting a large effect in microbial community
Soil alkalinity can be a result of natural weathering processes or structure (Zhalnina et al., 2015). According to Graham et al.
man-made conditions. Weathering of silicates, aluminosilicates (1994), prokaryotic lifeforms are profoundly influenced by the
pH of their environment. For all living cells there are optimum (Watkin et al., 2003). However, the relationship between these
pH requirements for normal physiological functions. The pH microbial survival mechanisms and plant growth promotion is
range 5.5–6.5 is optimal for plant growth as the availability of not well understood.
nutrients is optimal. This is also so for most soil microbes, in Cells’ major functions, such as nutrient acquisition,
part because in this range plants grow well and produce more cytoplasmic pH homeostasis and protection of DNA and
root exudates as a carbon source available for survival and proteins are largely affected by low pH (Booth et al., 2002).
multiplication of microbes. Though, some microbes have the Mechanisms involved in the induction of protective systems pose
ability to alter soil pH by acidifying their surroundings, as a way a considerable challenge. The advent of proteomics (Blankenhorn
to outcompete other microbes, most bacteria do best around et al., 1999) has complemented the genome information in this
neutral pH. Fungal activities on the other hand are favored by at area, for example, Lactobacillus spp., like many microorganisms,
least somewhat acidic pH conditions, which explains why they produces a thin biofilm composed of polysaccharides and
are dominant in forest acidic soils compared to range land soils proteins, which protects the cell against changes in the pH of the
and sub-humid and arid prairies which are mildly acidic and are environment (Wang et al., 2018).
dominated by bacteria (Zifcakova, 2020).
Bacteria are among the single celled organisms most Alkalinity Tolerance in PGPM
able to adapt to and thrive under harsh environmental pH High pH disrupts the bonds holding together the DNA helix
conditions. Acidic soils are dominated by Acidobacteria and strands, and lipid hydrolysis occurs more readily as the
Alphaproteobacteria (Shen et al., 2019) while Actinobacteria environment becomes more basic (Rousk et al., 2010; Shen
abundance increases toward alkalinity (Jeanbille et al., 2016). et al., 2019). Most microbes adjust their surrounding medium
However, the most sensitive component of the cell to pH changes to near neutrality as a way to survive high pH. Sodium is
is its workhorse, the protein (Hyyryläinen et al., 2001). Slight very important in intracellular pH maintenance for microbes
changes in pH have been reported to interfere with amino acid because it allows exchange of H+ /Na+ antiporters into the
functional group ionization and impair hydrogen bonding, as a culture media (Satyanarayana et al., 2005). Furthermore, the
result protein folding is changed, leading to denaturation and H+ concentration gradients across the membranes plays an
cessation of enzymatic or other activities (Booth et al., 2002). important role in producing ATP during cellular respiration,
Variation of pH in the environment has a direct impact through proton motive force (Celiker and Gore, 2013). It is not
on the availability of Al, Fe, Mn, Cu, and plant growth; the very clear how PGPM are able to use sodium-dependent ATP
critical and important effects of these conditions on microbial synthases as an alkali tolerance mechanism.
communities are not well understood. Graham et al. (1994),
reported that there were two pH related mechanisms influencing
microbial communities, the direct and indirect, the latter being ACIDITY AND ALKALINITY STRESS IN
the spillover effects of pH. PLANTS
Acidity Tolerance in PGPM Acidity Stress
In general, organisms have developed mechanisms to survive Acidification of the soil is currently a major limit for sustainable
environmental variation. Among other abiotic factors, most agricultural production in the world. Acid soil covers about
organisms need to sense and adapt to hydrogen ion concentration 30–40% of the arable land worldwide, and about 70% of the
(pH) (Booth et al., 2002). In soils, pH is an important driver for world’s potential agricultural land (Von Uexküll and Mutert,
soil microbial community structures. Microbial survival under 1995; Kochian et al., 2004). In the soil plant roots are in constantly
such conditions requires the capacity to sense, and adapt to, adjusting to varying pH as a result of water status variability
environmental changes (Biswas et al., 2007). (Misra and Tyler, 1999). Soil pH has significant influence on
However, little is known about optimal pH ranges and plants because it affects almost every aspect of nutrient uptake by
nutrient availabilities for many species of microorganisms them. In acid soil plants face three major toxicities, Al3+ , Mn2+
(Ratzke and Gore, 2018). Plant–microbe interactions such as and H+ , which inhibit plant growth. In any acidic soil Al toxicity
that of legumes and rhizobia are affected by Ca, P, Fe, and is the major and often first limitation to plant growth. Effects of
Mo; they influence rhizobia and their optimal growth, which is Al toxicity include; inhibition of root growth, inhibition of root
near pH 6. Biochemical properties and activities of microbes are cell division, modification of the cytoskeleton and inhibition of
partly affected by pH, leading to diversity effects in microbial nutrient uptake (Bojórquez-Quintal et al., 2017; Kaur et al., 2019).
community structure (Roe et al., 1998). In many cases direct Al toxicity effects are not obvious, instead
Microbes have developed various means to tolerate extreme they are manifest as P deficiency symptoms with overall stunting,
pH changes. Production of extracellular polysaccharides by dark green leaves, late maturity and purpling of stems, leaves
rhizobia is one of the reported behaviors (Gopalakrishnan et al., and leaf veins. All these P deficiency symptoms occur because of
2015). Rhizobium tropici demonstrated an ability to tolerate delocalized P metabolism by Al. Also P ends up being fixed by
acidic pH by producing glutathione, a tripeptide (Muglia et al., Fe in most acidic soils, degrading conditions for crop production
2007; Wang et al., 2018). Some rhizobia are known for their (Kaur et al., 2019).
ability to accumulate high levels of potassium and phosphorus as The second prevalent toxic metal in acidic soil is Mn. In
a means to tolerate low pH, as compared to acid sensitive strains contrast with Al toxicity, Mn as an essential plant nutrient,
toxic when plants absorb it in excess. Mn toxicity is prevalent uptake of Na+ and Fe+ , respectively (Zhang et al., 2012; Singh
at pHs as high as 5.6; this makes it more important as a et al., 2018). High levels of Na+ interfere with stomatal closure,
constraint in crop production, in some acid mineral soils, than which worsens the problem of water loss for plants (Bernstein,
Al (Sumner et al., 1991). 1975), a common phenomenon under saline conditions, which
Low pH stress has been associated with inhibition of root can be similar under alkalinity conditions. Bicarbonates reduce
growth (Yang et al., 2005) by facilitating H+ influx into Fe absorption and sometimes increase internal precipitation of
roots, which causes poor plant growth. High H+ influx causes Fe (Norvell and Adams, 2006), all of which affects synthesis of
depolarization of the plasma membrane, impacting the acidity of chlorophyll, and hence leads to chlorosis. Chlorosis, which is
the cytoplasm (Babourina et al., 2001). Thus generally, low pH linked to diminished photosynthesis, has an ultimate impact on
stress caused by H+ adversely affects root tissues, which leads to plant growth. Similarly, in calcareous soils reports have shown Fe
reduced growth and development of crops. There is a meaningful and lime-induced chlorosis are dominant factors leading to iron
lack of knowledge regarding how various plants respond to low deficiency (Coulombe et al., 1984). Conversely, the concentration
pH conditions; low pH tolerance would be a good trait to select of bicarbonate ions in the soil is known to induce minor to
for in plant breeding programs. severe stunting in plants. For instance, cucumber plants were
reported to experience negative effects of HCO3 − on their growth
Alkalinity Stress (Rouphael et al., 2010).
Most land desertification in the world is linked with soil Alkalinity stress causes inhibition of root growth due to high
alkalization and lower water availability and retention ability, concentrations of HCO3 − in the soil solution, though this varies
soil erodibility and also reduced biodiversity. Alkaline soils are among crop species. The suppression of root growth by HCO3 − is
characterized by high concentrations of carbonates (CO3 2− ) associated with inhibition of respiration by the roots (Alhendawi
and bicarbonates (HCO3 − ) which have the ability to neutralize et al., 1997). The inhibition of root growth may also result from
acids (Bailey, 1996; Rashid et al., 2019), high pH and poor excessive accumulation of organic acids (OAs) in root cells. Of
amounts of organic carbon, leading ultimately to poor availability the OAs commonly reported to stop root elongation, malate is a
of nutrients. Other minor contributors to soil alkalinity are problem when concentrated in the elongation zone, as a result of
those which result from hydroxides (OH− ), borates, organic bicarbonate in calcifuge grass species (Lee and Woolhouse, 1969).
bases, silicates, phosphates and ammonia. The problem of Furthermore, plant hormones are known for variation in their
alkalinity in soils is prevalent, as a secondary effect of drought activity under a range of stresses, leading to alleviation of negative
in many places. Most arid and semi-arid regions of the globe impacts on plants, though their final mechanisms of action
experience soil alkalinity since concentrations of salts decrease are often unclear. Under alkaline stress abscisic acid (ABA) is
and levels of carbonates and bicarbonates increase, leading to secreted by roots into the rhizosphere, which negatively impacts
alkalinity of the soils. Alkalinity stress effects on crop plants root growth as water becomes limiting (Slovik et al., 1995).
are remarkably similar to those of salt stress (Xu et al., 2013),
though it has remained a less researched area. Most of the
studies to date have dwelt on the relationship between salinity
stress and alkalinity stress by showing a strong link between MANAGEMENT OF ACIDITY AND
them (Bui et al., 2014). The stress caused by carbonate salts is ALKALINITY STRESSES IN PLANTS
sometimes higher than that of salinization by NaCl and NaSO4
(Shi and Sheng, 2005). Acid soil management is the application of indirect and direct
The higher pH of sodic soils results in nutrient imbalance means to ensure that production potential of a particular soil is
stress in crop production by affecting bioavailability of regained or attained. Some of the direct acidic soil amendments
phosphorus, iron, copper, boron and zinc (Chen et al., 2011). include correction of acidity by liming and manipulation of
However, it is important to note that under high pH (more agricultural practices for optimum crop yield (Yirga et al., 2019).
OH− than H+ ) the activity of the OH− ions comes into play, Liming is one of the major known ways to manage acid soils.
increasing alkalinity at pHs greater than 11, whereas below pH However, breeding for acidity tolerance and use of PGPM are also
11 forms of carbonates are responsible for alkalinity (Whipker becoming established mechanisms to address soil acidity stress.
et al., 1996). In alkaline soils with pH < 11 there are major effects The combination of two or more of these methods could be more
of pH on plants that are largely due to carbonate ions, rather helpful than single method strategies. The problem is recurrent
than hydroxide ions. for soils that are prone to acidification.
Nutrient availability for plant uptake is related to soil To ensure optimum plant growth, soil pH should be
chemistry, which is predominantly influenced by pH. When monitored and the soil amended to optimal pH levels, near
addressing pH related stresses, many other associated neutrality. Generally, it has been established that soils with
stresses come into play; under alkalinity stress, apart from high organic matter, >5%, have pHs between 5.0 and 5.5. In
essential element stresses, there are also osmotic, ion-induced contrast with soil acidity, which can be tolerated by some crops,
injury or high pH effects that are automatically problematic very few crops survive in even moderately alkaline soils, due
(Lynch and Clair, 2004). to restricted nutrient mobility and availability. Alkaline soil
Most plants under alkalinity stress manifest stunted growth amendment for crop production involves the use of cultural
due to poor nutrient uptake and leaf chlorosis due to high and low practices (conservation tillage, crop covers and rotation, organic
matter amendments, avoiding bare fallow), use of PGPM and (AM), ericoid and orchidoid associations (Parniske, 2005). The
production of alkali stress tolerant crop varieties. promiscuity of AM make them associate with a wide range of
hosts and assist most plant species with a range of stresses, and
assist plants under nutrient imbalance situations, most notably P
PGPM Enhance Plant Resilience to deficiencies (Zhu et al., 2007). Plants depend on AM particularly
Acidity and Alkalinity Stresses for P uptake from the nutrient stressed soils and the fungi
Acidity involved depend on plants for their C requirements (Mishra
Sustainable agricultural innovations are not immune to the effects et al., 2017). Acidic soils are also associated with metal toxicities,
of acidic soils. Considerable effort has been made regarding the ultimately resulting in decreased root growth, which hinders
use of PGPM as a strategy for dealing with various environmental overall plant growth and development. The major constraint to
stresses of plants. Current understanding indicates that about plant growth in acidic soil is the toxic effects of Al, Mn, and
2–5% of culturable rhizobacteria are plant growth promotors, Fe, together with P deficiency. AM associations with plants is
either directly and or indirectly (Dutta and Bora, 2019); the one of the most important plant-microbe associations, due to its
need to exploit this resource in agriculture is increasing. Legume ability to help plants with multiple stresses, compared to other
symbioses with rhizobia, a well-studied beneficial plant microbe association which may address only one stress. Many reports have
interaction, are constrained with regard to nodule formation and shown that a wide variety of AM fungal species exist in acidic
poor and/or failed bacterial survival (Correa and Barneix, 1997) soils and help plants survive in such conditions; dealing with
by various stresses, including soil acidity. Many reports share a soil pH is always complex as it has numerous effects on both
similar perspective, indicating that selecting for acid-soil tolerant roots and mycorrhizal associations (Clark, 1997; Bloom et al.,
symbiotic partners can improve the survival and productivity of 2006). Even though more investigation is required to determine
crop plants (Zhang et al., 2020). With Sinorhizobium, for instance, the best ways to exploit the potential benefits of both partners,
the genetic control of acid tolerance is becoming increasingly some development has already been achieved. Studies of plants
understood (Draghi et al., 2016). In legume symbioses, as with associations with AM fungi as a strategy to thrive in acid soils
other interactions, there is a requirement for specific recognition has revealed that these fungi provided benefit to plant growth
of signal molecules produced by both bacterial and plant partners. through the ability to bind to toxic ions, secrete organic acids
One of the factors affecting the signal molecule exchange and and glomalin (Thangavelu et al., 2014; Figure 2). Like plants
recognition process is pH, with effects on both plant and bacterial AM fungal species also vary in their tolerance to acidic soils.
partners (Zhang et al., 2020). Though there have been few AM fungal colonization of plant roots in soils is decreased at
advances in understanding the direct effect of PGPM on acid pH < 4 (Higo et al., 2011), which can explain differences in the
stress, there is a substantial body of research literature indicating ability of various AM fungal species to enhance plant growth
the potential for using microbes to address secondary effects of under acidity stress and their variation in mechanisms to be
acidity in the soil, such as Al toxicity (Zerrouk et al., 2016) and P employed (Figure 2).
deficiency (de la Luz Mora et al., 2017; Delfim et al., 2018). Despite the advantages of AM to plants their beneficial impact
It has been established that, within the legume-rhizobia on plants in acidic soils is less well documented than in non-
nitrogen fixing symbiosis, rhizobia isolated from acidic soils acidic soils. The few studies that have examined the potential of
have more ability to colonize and improve plant growth under AM fungi to assist plants in dealing with acidity stress (Table 1)
acidic conditions. Several genes contributing to rhizobial survival have shown clearly that there are numerous benefits that can
under acidic conditions have been identified. Some of them be acquired by plants. Clark (2002), revealed that use of various
are those which code for stress tolerance proteins, including species of AM resulted in variable effects on switchgrass growth,
ActA (apolipoprotein N-acyl transferase) and ActR (response but that all AM fungi caused greater yields than the control.
regulator) (Tiwari et al., 1996a,b). Despite advances regarding
tolerance and ability of legumes to nodulate under low pH Alkalinity
conditions, much remains unknown regarding signal molecules Developing proper and economically beneficial techniques for
in this capacity. managing major challenges in crop plants, such as alkalinity
The other highly studied plant microbe interaction is stress, requires intensive research. PGPM with dual (salinity and
mycorrhiza associations, which are associated with about 90% alkalinity) stress tolerance, termed as haloalkaliphilic, have the
of all terrestrial plants. With this degree of interaction, it ability to alleviate both salinity and alkalinity stresses of plants
is clear that for a large proportion of acid dominated soils and improve growth (Siddikee et al., 2011; Table 2). Bacteria
where these plants occur there are mycorrhizal associations with the ability to maintain their intrinsic pH below 9 when
with the plants growing there. There are two main groups of external pH is 9–11 are called alkaliphilic. This tolerance to
these fungi: ectomycorrhiza and endomycorrhiza (Bonfante and alkalinity is achieved through a cytoplasmic membrane proton
Genre, 2010). Endomycorrhiza reside inside plant cells and form transfer system (Torbaghan et al., 2017). The Bacillaceae family
arbuscules within cortical root cells, which are directly involved of rhizobacteria is among the best described in this capacity,
in the symbiosis beneficial effects. This type of mycorrhizal and has a wide range of host plants; the group of PGPM
association is as old as the evidence of first terrestrial plants on consists of 15 genera which include Alkalibacillus, Bacillus
the earth (Chagas et al., 2018) and is the most widespread type. and Haloalkalibacillus, among others (Radhakrishnan et al.,
Endomycorrhiza are further divided into arbuscular mycorrhiza 2017; Torbaghan et al., 2017). The use of alkalinity tolerant
FIGURE 2 | Differences in mechanisms used by microbes (fungal versus bacterial) to alleviate different environmental stressors.
TABLE 1 | Effectiveness of PGPM on plant growth under acidity stress.
Plant species Microbe Stress type Response of plant to microbe References
Alfalfa Sinorhizobium meliloti Acidity Ability to nodulate under low pH and increase plant Segundo et al., 1999
LPU63 growth
Rice Burkholderia thailandensis, Acidity Promote plant growth by increasing root volume and Panhwar et al., 2014
Burkholderia seminalis seedling dry weight
Sphingomonas pituitosa
Mung bean AM Acidity Increase and decrease of plant dry weight dependent Lin et al., 2001
on the AM species
Cowpea AM Acidity Increase in biomass of plants with decreasing pH when Rohyadi, 2008
inoculated with AM
Chickpea AM (Rhizophagus clarus) Acidity Increased shoot dry matter Alloush et al., 2000
Wheat AM Acidity Significant increase in straw and grain yield Suri et al., 2011
Switchgrass AM Acidity Increased shoot dry weight Clark, 2002
Sweet potato AM Acidity Increased biomass of the plants Yano and Takaki, 2005
rhizobacteria, with ability to produce indole acetic acid (IAA) and The use of legumes is also regarded as a means of alkalinity
1-aminocyclopropane-1-carboxylate (ACC), has the advantage of management and has been applied in various parts of the
reducing ethylene production, and increasing K levels (Figure 2). world, as they have an inherent ability to acidify the soil.
This increases the relative humidity in plants and helps maintain The combination of legumes and their symbionts to alleviate
ion homeostasis (Soleimani et al., 2018) which increased wheat alkalinity problems is a sustainable way to redeem unproductive
growth. Several other mechanisms are also reported (Figure 2) soils for agricultural use again. The use of AM fungi and rhizobia
by which PGPM alleviate abiotic stress in plants, such as by are among the oldest and best documented plant symbioses,
modulating hormones, enzymes, photosynthesis, secretion of and our understanding of them has shed light on helping
organic acids and secondary metabolites (Bisht et al., 2019; Dixit plants withstand a range of stress conditions (Kumar et al.,
et al., 2020). Moreover, rhizobacteria are involved in cycling of 2009). Abd-Alla et al. (2014) demonstrated that rhizobia and
key nutrients such as N and C, which ensures long term reserves mycorrhizae can work together on faba bean to help the crop
of nutrients in the soil. grow well under alkaline stress conditions; they found clear and
TABLE 2 | Effectiveness of PGPM on plants growth under alkalinity stress.
Plant species Microbe Stress type Response of plant to microbe References
Wheat Bacillus clausii Alkalinity Increased root and shoot growth, increased grain yield Torbaghan et al., 2017
Virgibacillus marismortui Saline-alkaline Increased root and shoot growth, increased grain yield Torbaghan et al., 2017
Lysinibacillus sp. Alkalinity Improved seed germination and vegetative growth Damodaran et al., 2019
Enterobacter sp. alkalinity Increased photosynthetic rate
Corn Bacillus sp. NBRI YN4.4 Alkalinity Photosynthetic pigment and sugar content improvement Dixit et al., 2020
and decreased level of proline in corn
Soybeans Burkholderia spp. PER2F Alkalinity Increased plant growth and N/P ratio Fernández et al., 2007
Chrysanthemum Bacillus licheniformis Alkalinity Increased plant survival rate, photosynthesis and yield Zhou et al., 2017
Faba beans Bacillus subtilis Alkalinity Increased germination percentage, seedling growth and Yousef, 2018
yield due to increased production of IAA by microbe at high
pH
Tall fescue Klebsiella sp. D5A Saline-alkaline Increased plant growth through the activity of ACC Liu et al., 2016
Wheat Bacillus simplex Alkalinity Significant decrease in pH of the rhizosphere and increased Hansen et al., 2020
plant growth and root P concentration
Chickpea Mesorhizobium ciceri Alkalinity Efficient in nodulation under high pH and increase plant Müller et al., 2016
growth
synergistic contributions of inoculated symbionts to alkalinity Use of Acidifying Agents

stress resilience of faba bean, and that this resulted in increased Lowering soil pH to reduce alkalinity can be achieved by adding
nodulation, nitrogenase activity and yield. organic carbon to the soil; minimum tillage also helps to improve
water retention and soil structure improvement, as does the
Plant Breeding and PGPM to Improve use of cover crops and legumes, all of which acidify the soil.
Crop Yield Under Conditions of Acidity Furthermore, the use of elemental sulfur acidifies the soil by
and Alkalinity Stresses neutralizing alkalinity (Goulding, 2016).
Use of Alkalizing Agents in Acidic Soils The use of manure and compost is a common practice
for management alkaline soils, as it improves organic carbon
Acidic soil causes negative effects on plant growth and
pools and soil structure. Manure and compost decrease soil
development (Rengel, 2011) leading to poor or no crop yield.
pH greatly, as a result of releasing NH4 + , CO2 and organic
Liming is a practice that corrects soil pH, moving it toward
acids during microbial decomposition (Walker et al., 2003). All
neutrality by addition of alkalizing materials rich in Ca and
these sum up to improvement of soil structure, water holding
Mg. This material can be in solid (limestone, chalk) or liquid
capacity and nutrient availability and, hence, soil health and
(hydrated lime) forms. Liming is the most common amendment
productivity is regained.
technique and uses CaCO3 or MgCO3 as they have substantial
Planting of cover crops helps alkaline soils in many ways,
ability to neutralize acids, hence increasing soil pH. By increasing
including reduction of exposure of the soil to agents of
soil pH, Al toxicity, which inhibits root growth is alleviated;
erosion. The cover crops also help in dissolution of carbonates,
P, which is fixed by Fe, becomes available leading to improved
through root exudates, improvement of the soil structure
crop productivity and yield. This is the reason for the popularity
and addition of organic matter to soil. Best cover crops for
of liming (Fageria and Baligar, 2008) as an amendment for
alkaline soils are sorghum and legumes with high carbon
acidic soils. How much lime to be applied for soil acidity
sequestration by stabilizing soil organic matter and structure,
amendment depends mainly on the type of lime, fertility status,
hence carbon and nitrogen concentration in the soil is increased
crop grown, management practices and cost benefit analysis
(Williams et al., 2016).
(economic) considerations.
Ammonium sulfate and other sulfur containing fertilizers
Use of Acid-Tolerant Crop Varieties cause quick declines in soil pH, which makes them good fertilizer
In acidic soils some plants are more tolerant than others, with options for alkaline soils. When oxidized elemental S and SO2
variation even among genotypes of the same species; choosing from the atmosphere produce acids which decrease the pH
the right crops based on the pH status of the soil is important of alkaline soils. Similarly, nitrogen fixation by legumes forms
(Hede et al., 2001). Though the soil may continue acidifying if no NH4 + inside the nodule, and excessive uptake of K+ causes
liming is done, it is advisable to include management practices, charge imbalance, both of which leads to proton release by
such as reducing the use of nitrogen fertilizers to reduce nitrate the roots to balance the charge (Marschner, 2011), resulting in
leaching, which increases soil acidity. Plowing crops or pasture rhizosphere pH decline.
into the soil will help reduce acidification of soil. In addition,
rotation of legumes, which are rhizosphere acidifiers, with less Use of Alkalinity Tolerant Crop Varieties
acidifying crops would be of great importance in reducing soil Plants have developed various strategies in response to
acidity effects. environmental stimuli, such as activation of various metabolic
defense molecules. Among the metabolic molecules produced Currently we use synthetic fertilizers as part of our approach
by plants to enhance defense capacity are salicylic acid, to feeding the growing global population. The uptake efficiency
ethylene, calcium and jasmonic acid (Klessig and Malamy, 1994). of these fertilizers by plants is generally 30–50%, leading to
Of the mentioned defense molecules salicylic acid has been economic losses and large environmental impacts, due to large
confirmed to confer alkalinity tolerance to tomato plants, when quantities of the fertilizer being lost to water bodies and the
applied exogenously, by reducing reactive oxygen species (ROS) atmosphere (Adesemoye and Kloepper, 2009). PGPM have
generation and improving antioxidant defense against alkaline shown their ability to increase the efficiency of nutrient release
stress (Khan et al., 2019). Similarly, it was demonstrated that SA from fertilizer and subsequent uptake by plants. Bearing in mind
applied in combination with Si had positive effects on alkalinity that soil acidification and alkalization are both gradual and
tolerance in tomatoes (Khan et al., 2019). From such reports, it is progressive processes, preparing ahead of time is not optional.
clear that much is still to be understood regarding how different The future of crop production sustainability meaningfully
tolerance molecules and beneficial elements work together in depends on better understanding of PGPM in conferring stress
helping plants grow under such alkaline stress conditions. alleviation and ways to effectively introducing them under field
Plant breeding is one important approach to ensuring crop conditions, to provide the same results that are observed under
productivity in stress prone areas, including alkalinity of soil controlled environment conditions.
and water. A range of plants have shown various mechanisms
of tolerance to alkaline stress, most of them showing early
seed germination and seedling establishment. Cultivars of lentil CONCLUSION
tolerant to alkalinity stress are known to have shoots with a
thicker epidermis than sensitive cultivars (Singh et al., 2018). The importance of pH in agriculture is well understood,
Similarly, tolerant lentils (Singh et al., 2018), finger millet and similar to a patient’s temperature in humans. Most of
(Krishnamurthy et al., 2014) and Lotus tenuis (Paz et al., the literature has acknowledged pH is a “master” variable in
2012) minimize Na+ uptake by having intact pericycle and productivity of agricultural soils as it controls soil chemistry. This
stele regions. Despite the presence of tolerance mechanisms review started with an evolutionary perspective regarding plants
for alkalinity stress by plants much remains unknown in and microbes, an interaction that has always been present, to
relation to other related stresses, such as salinity and drought. the benefit of both members of the partnership. It is becoming
According to Bui et al. (2014), the success of breeding for salinity clearer that the interaction has always provided plants with
tolerance required that increased attention also be placed on a mechanism of survival even in harsh environmental stress
alkalinity tolerance. conditions. With the ongoing development of climate change
As previously indicated a major limiting nutrient under conditions and associated multiple stresses, potentially occurring
alkaline stress is Fe; plants have developed two strategies to simultaneously and impacting plant productivity. This is quite
deal with this problem. Firstly, most plants optimize Fe uptake similar to pH stress which is accompanied by other stresses
via transporter by first reducing Fe+++ to Fe ++ in the root in its effects. The reviewed literature has shown that most of
plasma membrane. Secondly, development of specific iron uptake the acid and alkaline soil remediation measures are focused on
by release of phytosiderophores for chelating iron (Curie et al., cultural practices and breeding for tolerance. Little has been
2001). The iron chelators have high affinity to Fe+++ when established regarding utility of PGPM as a mechanism of dealing
released into the rhizosphere; the chelated iron is then taken up with acidity and alkalinity stresses. Our future will require further
by the plant through yellow stripe-like (YSL) transporters a family breeding for pH stress and the help of microbes that provide
of protein used by maize (Yordem et al., 2011). enhanced tolerance to pH stress. With this consideration in mind
Plants have also been shown to have mechanisms for alkaline the potential for alleviation of extreme pH stress by PGPM has
stress management through acidification of the rhizosphere become clearer and there is a need to now focus more research
by H+ ATPase activity related to plasma membrane proton effort specifically on acid and alkaline stresses in this regard.
extrusion (Xu et al., 2013).
AUTHOR CONTRIBUTIONS
FUTURE PERSPECTIVES
LM structured and prepared manuscript initially. DS provided
From various studies of tolerance to extreme pH there is a the conceptual framework for the manuscript as well as feedback
wider range of adaptation of microbes than plants. Our limited and guidance during manuscript development. Both authors
knowledge on the full information available in the genome of contributed to the article and approved the submitted version.
microbes that help them in adapting to such extremes will pave
the way to understanding and broadening their application in
biotechnology and crop production. The constant need to explore FUNDING
the unknown potential of microbes in helping enhance plant
productivity under various unfavorable conditions of growth and Funding was provided by the Consortium de Recherche et
is currently developing quickly and contributing to improvement Innovations en Bioprocédés Industriels au Québec (CRIBIQ),
of plant growth under stressful environmental conditions. grant number 2017-034-C30.
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The Roles of Plant Growth Promoting

TABLE 1 | Effectiveness of PGPM on plant growth under acidity stress.

Plant species Microbe Stress type Response of plant to microbe References

TABLE 2 | Effectiveness of PGPM on plants growth under alkalinity stress.

Plant species Microbe Stress type Response of plant to microbe References

synergistic contributions of inoculated symbionts to alkalinity Use of Acidifying Agents

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