MINI-REVIEW

The influence of plant growth-promoting rhizobacteria in planttolerance to abiotic stress: a survival strategy

Matthew Chekwube Enebe1& Olubukola Oluranti Babalola1

Received: 5 March 2018 /Revised: 29 June 2018 /Accepted: 6 July 2018 /Published online: 20 July 2018# The Author(s) 2018

AbstractAction is needed to face the global threat arising from inconsistent rainfall, rise in temperature, and salinization of farm landswhichmay be the product of climate change. As crops are adversely affected, man and animals may face famine. Plants are severelyaffected by abiotic stress (drought, salinity, alkalinity, and temperature), which impairs yield and results in loss to farmers and to thenation at large. However, microbes have been shown to be of great help in the fight against abiotic stress, via their biologicalactivities at the rhizosphere of plants. The external application of chemical substances such as glycine betaine, proline, andnutrients has helped in sustaining plant growth and productive ability. In this review, we tried to understand the part played bybioinoculants in aiding plants to resist the negative consequences arising from abiotic stress and to suggest better practices that willbe of help in today’s farming systems. The fact that absolute protection and sustainability of plant yield under stress challenges hasnot been achieved bymicrobes, nutrients, nor the addition of chemicals (osmo-protectants) alone suggests that studies should focuson the integration of these units (microbes, nutrients, chemical stimulants, and osmo-protectants) into a strategy for achieving acomplete tolerance to abiotic stress. Also, other species of microbes capable of shielding plant from stress, boosting yield andgrowth, providing nutrients, and protecting the plants from harmful invading pathogens should be sought.

Keywords Alkalinity . Climate change . Drought . Plant growth-promoting rhizobacteria . Rhizosphere . Salinity

Introduction

The unpredictability of the hydrological cycle has posed a se-rious challenge to farmers, horticulturists, and to the globalcommunity, concerning its effect inmeeting food needs ofman-kind and animals. The number of people to be fed is constantlyincreasing and food supplies are not meeting the demand.

In order to increase the quantity and quality of crops grown,agriculturists have intensified the use of open and groundwater sources for irrigation purposes, which has a correspond-ing salinization implication.

However, the use of bioinoculants (plant growth-promotingrhizobacteria) has been of great help in combating this abiotic-climate-induced change that limits the overall performance ofplants under stress (Alori et al. 2017a; Staudinger et al. 2016).

The use of biofertilizers to enhance successful adaptation andsurvival of plants will gear toward ensuring a sustainable cropyield and improvement of soil fertility and structure. This is agood approach to stress management (Alori et al. 2017a).These microbes through deaminase enzyme production(Saleem et al. 2015), nodulation (Masciarelli et al. 2014), andother physiological activities at the rhizosphere help the plantstolerate stress.

External (exogenous) introduction of beneficial chemicalsubstances as supplement has been used to improve resilience,yield, and tolerance of plants to the toxicity of these stress-imposed conditions, such as the application of caffeic acid(Klein et al. 2015), sodium polyacrylate (Hong et al. 2016),jasmonic acid (Khan et al. 2017), genistein (Hasanah andRahmawati 2012), chitosan (Bistgani et al. 2017), humic acid(Kasmani et al. 2013), gibberellic acid and other hormones(Shaddad et al. 2013), and molybdenum (Bouzid andRahmoune 2012). These chemicals aid the physiological per-formance and adaptation that manifest in a well-balancedmor-phological state of the plant growing in a stressful environ-ment. The stresses range from drought, salinity, alkalinity,pathogenic microbial attack to chemicals.

* Olubukola Oluranti BabalolaOlubukola.Babalola@nwu.ac.za

1 Food Security and Safety Niche Area, Faculty of Natural andAgricultural Sciences, North-West University, Private Bag X2046,Mmabatho 2735, South Africa

Applied Microbiology and Biotechnology (2018) 102:7821–7835https://doi.org/10.1007/s00253-018-9214-z

Abiotic stresses are stress conditions to plants arising fromthe environment. They are the non-living part of the ecosys-temwhose effect is felt by the living component of the system.Nature is balance sensitive, and at short supply or deviationfrom the normal occurrence of these conditions will create astress in the ecosystem and jeopardize the well-being of livingthings. Water, nutrients, salts, temperature, and pH are amongthe basic abiotic components of the agricultural ecosystemthat have an influence on plants.

These abiotic stresses not only affect plants but also affectmicrobes. In an effort to survive and prevail despite the stiffcompetition among microbes particularly at the rhizosphere,some microbes possessing the cellulase enzyme capable ofdissolving the cellulose cell wall of plant roots gain entranceinto the apoplast of plants, the cell wall interior as well as thevascular bundle—xylem, where they live and undergo normalmetabolic activities.

Although researchers have looked at various means of han-dling the stress inducers to enable plants to increase their sur-vival and performance, yet, little has been done on the inte-grative aspect of this enhancement strategy of protecting andempowering plants to resist and grow better under drought,salinity, or alkaline conditions.

This review aims to understand the influence of plantgrowth-promoting rhizobacteria in plant tolerance to abioticstress, and to suggest a new trend involving the application ofmicrobes, nutrients, nodule inducers, growth hormones, andosmo-protecting substances on growing plants (Fig. 1) ex-posed to abiotic stress, in order to achieve better performanceand adaptation of crops and to increase the overall return oninvestment/expenditure of farmers.

Sustainable agriculture—the influenceof climate change and human populationgrowth on crop yield

The two major challenges affecting crop production in thismodern time are climate change and escalation of human pop-ulation number. The two are interrelated; one influences theother. As the human population increases, the need for fuelenergy increases. Also, the need to generate heat for cookingfood leads to deforestation. These human activities elevate theconcentration of carbon dioxide in the atmosphere.

Climate change could result in an unregulated supply ofrain water which could either occur in excess or in prolongedshort supply. Whichever the case, crop production is affectednegatively. Extreme rain fall gives rise to erosion andflooding, while drought results in loss and poor performanceof crops. In a bid to boost crop productivity and yield and tocombat drought-induced stress, farmers resort to the use ofirrigation which adds salt to the soil.

Drought is a great cause of poor yield of crops leading tofood shortages.

Carbon dioxide increase, on the other hand, may aid thegrowth and nitrogen assimilation of plants. For example, al-though water limitation affects the clover plant’s fixation ofnitrogen, in the presence of a moderate supply of water, theplant could still perform excellently in the presence of carbon(IV) oxide and increased atmospheric heat (Lazzarotto et al.2010).

However, adequate nutrient management with respect toimproving the fertility of the soil could be an aid in solvingthe problem of climate change challenges on crops (St Clairand Lynch 2010) together with the use of rhizobacteria toboost crop production (Babalola 2010).

Population explosion also creates an urgent need for theestablishment of shelter, recreation centers, industrialization,urbanization, etc. to accommodate human activities, and thisaffects land availability for mechanized farming.

To sustain the nutritional need of the growing human pop-ulation, agricultural practices must be intensified, irrespectiveof short supply of rain water, environmental effects of the useof inorganic chemicals (fertilizers), and salinity issues. Thebiotechnological application of microbes may address the ris-ing problem and ensure sustainability in the provision of foodfor all. In addition, the use of biofuels in automobiles as wellas the practice of afforestation should be encouraged to helpcut down on greenhouse gas accumulation for effective con-trol of climate change. The use of electric automobiles shouldalso be incentivized.

Plant growth-promoting rhizobacteria—theredeemer of plants

Plant growth-promoting rhizobacteria are those indispensablemicrobes possessing the unique abilities of supporting directlyand indirectly the wellbeing of plants. These microbes, inorder to survive in the rhizosphere, expanded their biologicalactivities that influence the survival and growth of plants(Babalola 2010).

A number of these microbes with the enzyme machinerynecessary for the breakdown of the exudates of plants are ableto protect the plant from stress arising from water scarcity andsalt pollution. They produce a variety of substances such asdeaminase enzyme (Saleem et al. 2015), plant hormone–in-dole acetic acid (Gujral et al. 2013), siderophore (Stajkovic-srbinovic et al. 2014), PO42− solubilizing enzyme (Kumariand Khanna 2016), salicylic acid (Ekinci et al. 2014), andmicrobiocidal/biostatic enzyme (Moustaine et al. 2017).

Some of these microbes contribute to plants nutritionallyby trapping and integrating nitrogen into the plant via nitrogenfixation (Attitalla 2012). However, as a means of surviving thestiff competition for existence and dominance at the root

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environment, some microbes devise a means of burrowing/penetrating the tissues of plants and establish themselves asendophytes within the plant (Khan et al. 2016b), contributingnot only to the nutrition of the plant but also to enhancingplants’ survival rate and adaptation to their environment.

PGPR contribute to sustaining the intrinsic resistance ofplant to pathogenic and environmental challenges. Some ofthese organisms are excellent in biofilm formation and secre-tion of polysaccharide substances which confer stability toplants during stress (Kasim et al. 2016). As microbes contrib-ute significantly in biohydrometallurgy by the generation ofmetal-rich solution through the biological oxidation of sulfur-containing ore, they also play a role in the immobilization ofmetals or cations and render them non-bioavailable usingpolymeric substances and other chemicals they produced(siderophores etc.) (Fashola et al. 2015). Their presence cancontribute to the reduction in metal stress on plants whenapplied to them as bioinoculants. The growth and survival ofplants will not be possible without the help of these Bfarmers’friends^ living both within and around the plant surfaces.

A healthy plant is a product of a healthy relationship be-tween the plants and the growth-promoting microbes, whilean unhealthy relationship could be observed in the degradationof the physical and physiological wellbeing of the plant. PGPR

are the key players in the fight for sustainable plant develop-ment amidst stress conditions arising from climatic as well asmanmade activities. The classes of microbes belonging to thesegroup/genera are Micrococcaceae HW-2 (Hong et al. 2016),Bradyrhizobium (Masciarelli et al. 2014), Bacillus (Kasim etal. 2016), Microbacterium, Pseudomonas, Curtobacterium(Cardinale et al. 2015), Variovorax, Paenibacillus (Yolcu etal. 2011), Pantoea (Damam et al. 2014), and many others.

Drought stress in the reduction of plantperformance

Drought has been implicated in the reduction of plant meta-bolic and physiological activities. It reveals its effect in thedegree of biomass yield, growth, nodulation, and chlorophyllgreenness of plants. It is a major agricultural crop impairmentinducer and a global concern as it affects the supply and sus-tainability of food availability to people and livestock.Rainfall is the major source of water for growing crops/plants by farmers (in a subsistent agriculture) in many partsof the world. The gradual delay or low level of rainfall due tothe influence of climate adjustment to manmade activities isaffecting the biotic aspect of the ecosystem particularly green

Fig. 1 The interactions ofmicrobes, useful chemicals, andtheir overall influence in plantstress tolerance, growth, andproductivity

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plants which are the primary and major producers of foodupon which all life forms depend for meeting their daily nu-tritional needs.

The effect of drought is obvious, yet the microbesdomiciled at the root zone of plants, known as plant growth-promoting rhizobacteria, have proven to contribute to the tol-erance and quick adaptation and adjustment of plants todrought stress (Table 1) via supplementary production of phy-tohormones that induce root growth, thus allowing a betterwater absorption, production of deaminase enzyme responsi-ble for the disintegration of ACCmolecules, nitrogen fixation,and solubilization of P (Vurukonda et al. 2016a; Olanrewaju etal. 2017).

The survival and enhanced influence of endophytic mi-crobes toward poplar adaptation to water stress, for example,revealed that the presence of these organisms aided the phys-iological wellbeing of the plant and enabled it to tolerate waterscarcity in the soil. The result showed 28% increase in bio-mass (shoot and roots) as against the control (Khan et al.2016c).

The increase in root number and tissue mass promoted thewider reach of plant roots for water and nutrient absorption,

which enabled them to thrive in water scarce environments.This survival approach of plants is akin to the aid of microbialsymbionts capable of plant hormone production (indole aceticacid, gibberellin), which stimulate growth and the resultantstress annulment for better performance of the plant.

In line with the survival-induced strategy, the endophyteswill produce a poly-sugar substance known as trehalose, ca-pable of protecting biologically produced compounds andmolecules from breakdown during water induced osmotic ten-sion (Khan et al. 2016c).

It was observed that Ocimum basilicum L., the plant pop-ularly known as basil, had improved chlorophyll pigment con-tent and antioxidant activity under water-induced stress in thepresence of mixed rhizobacteria consortium—Pseudomonassp., Bacillus lentus, and Azospirillum brasilens (Heidari andGolpayegani 2012), which indicated the aid of microbes in thesynthesis of useful substances in the plant in spite of the pre-vailing stress challenges. Among the nitrogen fixers of atmo-spheric N to plants for its nutritional needs, Azospirillum is agood farmers’ friend that contributes in enriching the soil andenabling plants to thrive under abiotic stress. This microbe,which possesses a list of unique attributes such as auxin

Table 1 Contributions of microbes in the induction of drought tolerance by plants

Plant species Microbes Microbial enhanced plant productivity under stress References

Tomato Rhizophagus irregularisVariovorax paradoxus 5C-2

Enhanced photosynthetic rate, reduced lipid oxidation,and increased root water conductivity and oxidativephosphorylation in the plant

Calvo-Polanco et al. (2016)

Chickpea Pseudomonas putida MTCC5279 (RA) Reduced/controlled the expression of stress responsegene, maintained water content, osmolyte,membrane structure, and germination rate of theplant

Tiwari et al. (2016)

Maize Azospirillum spp. (Az19) Improve the growth and productivity of the plant underwater stress compared to the control

Garcia et al. (2017)

Wheat Piriformospora indica Enhanced adaptation of plant by promoting nutrientand water absorption, improved root growth,biomass, water, chlorophyll and modulate theactivities of antioxidant molecules

Hosseini et al. (2017)

Trifolium repens Rhizophagus intraradicesBacillus megateriumPseudomonas putida

A consortium of these microbes increased plantnutrient and water contents, reduced stomatalconductance and stress enzyme activities for betteradaptation to drought

Ortiz et al. (2015)

Wheat Azospirillum brasilense Sp245 Increased growth and expansion of xylem in thecoleoptile of inoculated plant for easy conduction ofwater

Pereyra et al. (2012)

Lavandula dentata Arbuscular mycorrhizal fungiBacillus thuringiensis

Co-inoculation enhanced plant growth, nutrientcontent, biomass, and reduction in lipid oxidation ofthe plant

Armada et al. (2016)

Maize Arbuscular mycorrhizal fungiBacillus thuringiensis

Improved nutrient content and water transport proteinas well as reduce lipid oxidation in the stressed plant

Armada et al. (2015a)

Brassica oxyrrhina Pseudomonas libanensis TR1Pseudomonas reactans Ph3R3

Enhanced growth, pigment and water content as well asphytoaccumulation of heavy metals in the plant

Ma et al. (2016)

Maize Pseudomonas putida (FBKV2) Encouraged root and shoot growth, dried biomassweight and reduced stomatal conductance in theplant

Vurukonda et al. (2016b)

Common Bean Rhizobium Promoted plant weight, nutrient content and increasedPhaseolus vulgaris yield

Yanni et al. (2016)

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production, deaminase enzyme production, siderophore–irontrapping substance, nitrogen fixation, exopolysaccharide, etc.,enables its associates (plants) to tolerate drought as well as saltdisturbances (Cruz et al. 2017a; Vacheron et al. 2015).

Azospirillum generates biocidal substances (bacteriocins,hydrogen cyanide, proteolytic enzymes, siderophores) capa-ble of destroying pathogen/invaders of plants and encouragesplants to tolerate abiotic stresses as well as living organismsinducing stress on plants. It could be regarded as a plantgrowth-promoting bacteria and is widely studied by re-searchers (Vacheron et al. 2015; Creus et al. 2010). The con-tribution of this organism in nutrient uptake by plant as well aswater-facilitated uptake is well documented. Therefore,Azospirillum and other microbes capable of enriching andunbinding trapped nutrients and making them available foreasy taking up by plants are called biofertilizer and they inturn depend on plant excretory products (root exudates) fortheir nutrition (Babalola 2010).

A closer look at the biosynthesis of siderophore byGordonia rubripertincta CWB2 suggests that gorA gene un-der expression in Escherichia coli produce GorA hydroxylaseenzyme (N-hydroxylatingmonooxygenase) which was able tohydroxylate the substrate putrescine (1, 4 diaminobutane) inthe presence of coenzyme (FAD and NADPH). Thehydroxamate is a crucial part in siderophore synthesis. It isresponsible for binding to irons and other metallic elements inthe rhizosphere (Esuola et al. 2016).

A screening study on rhizobacteria obtained from cactirhizosphere showed that the predominant isolate belongingto the Bacillus sp. exhibited amazing plant growth-promoting traits like the production of indole acetic acid,PO4

2− solubilization, and hydrogen cyanide and NH3 produc-tion. Bacillus has the attribute of producing exopolysaccharidesubstances that enable them to form biofilms and surviveharsh environments, and has contributed to the survival,growth, and performance of Zea mays L. seedlings leaf area,stem, and biomass shoot dry weight in a simulated water stressexperiment (Kavamura et al. 2013). This attribute of poly-sugar production by microbes strengthens the resistance ofinoculated plants to water stress inhibitory effects and thusensures their growth and survival in a water-deficient environ-ment (Nocker et al. 2012).

To understand the consequences of water deficiency onplant physiological condition and activities, groundnut plantswere subjected to water stress using a hydrocarbon com-pound—polyethylene glycol, which neither penetrated norposed any toxicity effect to the plant, rather it caused a de-crease in the plant RNA, chlorophyll composition, and watercontent shortfall in the plant. The observed effect is concen-tration based. The higher the concentration of the polyethyl-ene glycol, the higher the water stress effect it exerts on theplant and the higher the corresponding reduction effect ofRNA in the leaves and roots. This effect was observed in the

quantity of water content of the plant leaf (relative water con-tent). The drought interfered with chlorophyll a more than b(Meher et al. 2017). The production of oxygen radicals andhydrogen peroxide molecules are responsible for destructionof lipids and the breakdown of chlorophyll which leads toreduction and yellowing of the leaves (Meher et al. 2017).

In another experiment, a legume plant (Aspalathus linearis)was subjected to drought condition via withholding of watersupply to the plant. This led to an observable effect on thephotosynthetic rate of the plant by 40% reduction as well as61% reduction in stomatal conductance, as a consequences ofcontinuous closure of stomata to maintain intracellular watercontent and cut down on water loss from the leaves. This is oneof the strategies plants adopt to increase their efficiency in theuse of water during drought stress periods. Drought-inducedclosure of stomata has a direct connection with the reduction inplant assimilation and fixation of carbon (IV) oxide from theatmosphere. Inadequate supply of water directly impedes theprocess of photosynthesis in plants. Preferential developmentand growth of underground plant parts (roots) to shoot parts ofthe plant undergoing stress was also observed, which enabledthe plant to absorb more water from the inner layer of the earth(Lotter et al. 2014).

Although A. linearis is capable of forming a symbioticrelationship with rhizobium microbe, drought, on the otherhand, affected the nitrogen nutritional content of the plant asa result of its influence on the activities of the nodules and theN2 fixing enzyme (nitrogenase). This consequently makes theplant more dependent on the available nitrogen in the soil(Lotter et al. 2014).

Periodic or interval water supply through rain water to ricefarming has proven to contribute to water stress in rice plants.Rice, being a moderately water-loving plant, finds it difficult tocope with dryness arising from drought and requires a suitablemeasure for increasing the adaptability and productivity of theplant in a lowwater vicinity. The application of potassium saltsas nutrient (potassium chloride and potassium sulfate) could bea good measure in reducing water stress on rice plants.Potassium nutrient applied at a concentration of 120 kg perhectare was able to increase rice yield and the index of itsharvest within 15 days of water scarcity (Zain and Ismail2016). Potassium has a link with the efficiency of water useby the plant and improves it via the promotion of transpiration-pull-boost with the assistance of potassium ions which arecomponents of cell membranes mediating active transport ofnutrients as well as water into the rice plant.

The ease of water entry from the soil into the plant contrib-utes in canceling the potential damage of tissues by oxygenradicals during water-deficient condition. A 338% increase inproline concentration within the plant treated with K+ salt wasobserved (Zain and Ismail 2016).

The use of sugar beet fermented byAspergillus niger as soilamendment in the presence of bioinoculant Bacillus

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megaterium and a consortium of arbuscular mycorrhizal fungipromoted plant growth, biomass, nutritional content, and wa-ter level and reduced the conductance of stomata and the ac-tivities of enzymatic antioxidants in plants faced with droughtstress. The amendment boosted the effectiveness of the bacte-ria toward supporting the growth and productivity of thestressed plant (Armada et al. 2014).

The importance of water as a medium for transport andbiochemical reaction in a living system cannot beoveremphasized. A limited water environment interferes withthe smooth biochemical processes and interaction of mole-cules in the plant as well as its associated microbes in therhizosphere. The performance of Glycine max under droughtstress was increased in the presence of Bradyrhizobiumjaponicum and a nodulation stimulant—genistein. Genisteinas well as daidzein iso-flavone substances are capable of in-ducing response reaction of nodule gene expression inBradyrhizobium sp. These compounds are components of ex-udates from legume roots. Genistein treatment ofG. max seedtogether with a bioinoculant (B. japonicum) greatly encour-aged the resistance of soybean to drought stress and decreasedits detrimental effect on the formation of nodules by the mi-crobe (Hasanah and Rahmawati 2012).

The tolerance of plants to drought stress is dependent ontheir own genetic makeup. The physical manifestation ob-served in a plant is in direct correlation with the quality andquantity of the physiological activities taking place at thegene level. All biomolecules produced are the product ofgene expression. The easier the expression of genesencoding the biomolecules that protect the plant cellularcomponent from drought induced cellular destruction/dam-age, the more the viability and productivity of the plant at agiven stress condition. Different species of soybean under-going a 15-day vegetative growth under drought stress re-vealed that the electrolyte loss was more in plant tissuestressed for 10 days and above. The shoot dry matter orbiomass concentration decreased (by 79.18%) at the 10thday to 15th day of stress, while the root biomass or dryweight/root growth increased (by 100.96%). This meansthat drought promotes the accumulation of nutrient and pho-tosynthetic products at the root and stimulates its growthand development to maintain balance, adjustment, and sus-tainability of plant physiological adaptation to the stressproblem. Soybean species (SJ-4) possessing uniquegenetic/physiological characteristics performed better thanothers under drought stress and should be the crop of choicefor drought-predominant locations (Tint et al. 2011).

Also, two soybean species showed slight yield reduction of8 and 12%, respectively, as compared to when grown underconsistent water supply via irrigation. This implies that theyare good in tolerating drought as a result of their inherent delayin wilting and a corresponding elongation of fixation of car-bon dioxide in their leaves (Pathan et al. 2014).

In the same vein, the accumulation of amino acid (proline)in the leaves of tomato plant and increased value of the relativewater content of the leaves of the plant confer resistance todrought by tomato plant. Proline is responsible for sustainingthe movement of water molecules from a region of higherconcentration to that of a lower concentration in response toconcentration gradient between the plant and its environment.It helps the plant maintain its turgor intracellular pressure byfacilitating movement of available water from the soil into theroot of the plant (Jureková et al. 2011).

A non-bioinoculant phyto-drought-stress-mediated strate-gy involving the application of chitosan to a plant (thyme)undergoing drought stress helped to offset the effect ofdrought on the plant by 20% compared to the untreated con-trol which showed a decrease in dry matter of the plant by 54and 56% on the photosynthesis retardation of the plant underdrought stress (Bistgani et al. 2017). In the same manner, itencouraged the synthesis of essential oil in the thyme plant,reduced the degree of peroxidation, sustained the cell mem-brane conformation and function, and stimulated the accumu-lation of proline amino acid in the leaves of the plant by 20%(Bistgani et al. 2017). Being a polysaccharide, chitosan isgenerated from chitin alkalinization of N-deacetylation.These molecules are abundant in the outer skeletons of insects,fungi, and algae cell wall composition and are implicated insecondary metabolite production in plants when applied tothem (Lei et al. 2011).

A sainfoin plant inoculated with arbuscular mycorrhizalfungi exhibited 7.27, 4.21, and 2.40% increase for relativewater content, N2, and P leaves total content, respectively, atthe 40th day of the experiment. This fungus enabled the plantto adapt and survive during drought limitations by enhancingplant growth and protecting it from damage induced by stress(Jing et al. 2014). Generally, an external–internal symbioticrelationship by soil fungi (arbuscular mycorrhizal fungi) per-forms the same protective role as endophyte does to plants.There is a biomass increase as well as a decrease of Fusariumoxysporum infectivity of tomato plant inoculated withGlomusintraradices and Piriformospora indica irrespective of the nu-tritional content of the soil used (Cruz et al. 2017b). Also, theinvolvement of mycorrhizal fungi in nutrient dissolution/solubilization particularly as it concerns phosphorus gives cre-dence to its participation in the direct promotion of planthealth and productivity.

These microbes form a channel (protein transport chan-nel) for dissolution and absorption of solubilized PO4

2−

from the rhizosphere into the host plant in a mutualisticdependent relationship. They are generally used asbiofertilizers for immobilized nutrient dissolution via theorganic acids produced which are capable of reacting withthe compounds of trapped minerals and converting them tosoluble forms for easy assimilation by plants (Igiehon andBabalola 2017).

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The presence ofmycorrhizal fungi adds further surface areafor water and nutrient acquisition, thereby making the plantmore resilient and tolerant to the climate change-inducedstress. This notwithstanding, they also partake in structurebuilding, arrangement, and improvement of soil for properaeration and migration of water together with nutrients in thesoil, making the soil healthy and fertile (Igiehon and Babalola2017; Alori et al. 2017a). It is a known fact that fungi cansurvive and thrive well in a dry or semi-dry soil and stillperform their normal activities. This property is exploited byarbuscular mycorrhizal fungi in making an inoculated plantperform its activities under drought condition as the organismreaches out for more water within the soil where the roots ofthe plant can possibly not reach (Alori et al. 2017a).

In addition to fungi solubilizing PO42− bacteria, the en-

zymes (phytase, phosphatase) can produce organic acid(acetic acid, citric acid) and will be able to mineralize or sol-ubilize P via ionic interaction of the charged group in thesemolecules. These solubilizers of P play a part in the enrich-ment of soil fertility and supporting plant nutritional require-ments irrespective of the prevailing bioavailability or non-bioavailability of the nutrient in the soil. Though the level ofavailable P can determine the function of the microbes as itrelates to solubilization of P, the higher the available nutrients,the less the quest to solubilize already immobilized phospho-rus and vice versa. Microbes are the key players in the replen-ishment of P in the soil (Alori et al. 2017b; Zhu et al. 2011).

Also, bacterial inoculation of rice plant using Pseudomonasfluorescens promoted the intrinsic tolerance of rice plant todrought stress and encouraged the expression of abscisic acidsynthetic genes particularly at the stage of reproduction by theplant. This confers an induced systemic plant resistance todrought stress. It implies that microbes, especially the PGPRcolonizing the rhizosphere of plants, have an indirect as well asa direct role in enhancing the expression of genes by water-deficient plants through a process known as induced systemicresistance. Microbes in their various capacities have beenshown to aid plants in their tolerance to drought (Saakre etal. 2017; Bresson et al. 2013).

The symbiotic N2 fixers (Sinorhizobium meliloti andSinorhizobiummedicae), on the other hand, possess the abilityof protecting a legume (Medicago truncatula) from senes-cence of the leaves under drought stress (Staudinger et al.2016). The rhizobial inoculants aid in the delay of the processof senescence by promoting the accumulation of potassiumions, reduction in the protein mediating ethylene production,and induction of cytokinin production which inhibit senes-cence and accumulation of sugars and amino acids that aidedin the plant survival during stress.

Nodulated medicago plants recovered from drought stressfaster than the non-nodulated legumes as a result of the shiftsin the carbon partitioning from starch to sugars and thus theenhanced allocation of reserves to osmolytes during drought,

enabling to stay green with the ability of fast recovery afterrewatering (Staudinger et al. 2016).

Drought stress reduced relative water content and chloro-phyll and increased proline concentration of the plant (wheat)(Keyvan 2010). Obviously, drought affects root, shoot, yield,and overall performance of the affected plant. Yet at moderatewater scarcity or even severe conditions, the intrinsic qualityof the plant determines to a large extent its sensitivity or tol-erance to the drought condition. The osmotic adjustment andperformance of three barley plant species (yousof, fajr 30, andmorocco) was measured when theywere subjected to differentdrought treatments (moderate and severe). The results showedthat yousof species possesses a drought tolerance trait and wasable to have an increased root length to shoot length ratiounder severe stress conditions.

The test plants survived the water stress by employing anadjustment in the osmotic behavior of their root systems lead-ing to the accumulation of solutes such as proline in their cellsto maintain the cell structure and function during water scar-city. This adjustment in osmosis to sustain the turgidity of theplant cells directly influences the escalation level of photosyn-thesis and tissue growth of plant during drought stress(Afshari-Behbahanizadeh et al. 2014).

The symbiont (Bradyrhizobium sp.) aided the tolerance ofcowpea plant to water scarcity stress and boosted the qualityof NO3

− (nitrate) and amino acid (proline) in the inoculatedplant (Barbosa et al. 2013).

Groundnut inoculated by Bradyrhizobium under droughtconditions had a large quantity of amino acids which wasderived from the nitrogenase-catalyzed conversion of atmo-spheric N to NH4

+ ions necessary for amino acid and proteinformation in the plant (Delfini et al. 2010). The observed in-crease in protein level of legume-inoculated plants implied thatthese microbes aid in the supply of nitrogen via fixation in thepresence of the nitrogenase enzyme operating at the root nod-ules of the plant. Bioinoculation of legume plant with rhizobi-um has helped to encourage the development of many leaves inthe plant due to the greater number of root nodules in the plantroots that aid in nitrogen fixation (Ferreira et al. 2011).

The treatment of annual medic plant growing in sufficientwater (irrigated) and water-deficient (dry farming) systemswith a mixture of biofertilizer and chemical fertilizer in anintegrated fertilization practice encouraged the plant to effi-ciently adapt to the water-deficient condition and accumulateboth macro- and micronutrients in the tissues of the plantcompared to the use of chemical fertilizer alone. The applica-tion of bioinoculants and mineral fertilizer to a plant growingin a water-limiting environment is more (Table 2) effective inboosting plant productivity than in water-sufficient soil(Shabani et al. 2015).

The attenuation capacity of microbes to the negative effectsof drought on plant development was facilitated by the use of acombination of Azotobacter chroococcum and Pseudomonas

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fluorescence together with phosphorus fertilizer, and was ableto boost the inorganic P content of the plant (soybean) growingunder insufficient and abundant water content of the soil. TheN content of the leaves and root of the soybean plant wereincreased by 6 and 8% under water stress condition. The ab-sorption of phosphorus in the soybean plant under the influ-ence of bioinoculant increased by 16% (Vladimir 2012).

Although drought negatively affected plant developmentsuch as water content, chlorophyll of the leaves, and the dryweight of the root with a corresponding increase in the aminoacid proline and abscisic acid–osmoprotecting molecules, yetthe application of humic acid to the drought-stressed plant hasreversed the observed effect by decreasing the quantity ofproline and absicsic acid content of the treated plant, withresultant increases in chlorophyll content, dry weight of theroot, and water content of the pistachio plant during droughtstress circumstances (Kasmani et al. 2013).

However, from the above reviewed information, it is clearthat bioinoculants and the application of useful chemicals andamino acid could help plants avert the challenges of droughtconditions and aid in the promotion of a sustainable productionof crops especially in those regions prone to water scarcity(insufficient rain fall).

Salt-induced challenges on plant

The deleterious nature of sodium chloride and other salt com-pounds on the growth and development of plants particularly

in inducing water limitation stress and uncontrollable negativestomata closure cannot be overemphasized. This necessitatesthe application of an attenuation strategy to cancel the effect ofsalt on crops.

The co-inoculation of Pseudomonas and endomycorrhizaeon cowpea plant undergoing salt-induced stress showed a de-crease in the mycorrhizal infection of the plant. Treatment of6000 ppm sodium chloride in the presence of the fungi andbacteria increased the carotenoid concentration (0.449 mg/g).Also, osmolytes (proline and sugars) increased in the presenceof endomycorrhizae inoculation in the plant. Irrigation withtap water in the midst of endomycorrhizae and Pseudomonasfluorescens gave higher fresh and dry weight, pod length, seednumber, and protein content of the cowpea plant (Manaf andZayed 2015) compared to the one irrigated with salt water.

As part of microbial facilitated plant tolerance to salinity,biofilm formation is a suitable strategy which microbes em-ploy in enhancing barley plant tolerance to soil salinity. Thiswas observed in the aversion/reversal of the harmful effect ofsalt on a number of growth parameters such as seedling length,relative water content of the plant’s leaf as well as fresh anddry weight of barley plant. This biofilm formation strategy bymicrobes is actually a means of protecting themselves fromthe harsh conditions they found themselves in (short supply ofnutrient, ionic toxicity as well as water limitation inducedosmotic stress), enhancing survival within the presence ofthese limited resources by aggregating in masses (sessile com-partmentalization) of cells at both living and non-living sur-faces present at the root environment and contributing

Table 2 Plant drought stress tolerance mediated by synergy between microbes and soil amendment

Plant species Microbes Amendment Plant productivity and tolerance outcome References

Arundo donax Micrococcaceae HW-2 Sodium polyacrylate Microbial attributes of plant hormone,deaminase and siderophore productionand enhanced water retention capacity ofsodium polyacrylate promoted shootgrowth, biomass, and root of the plant

Hong et al. (2016)

Thymus vulgarisSantolina chamaecyparissusLavandula dentateSalvia officinalis

Enterobacter sp.Bacillus thuringiensisBacillus megateriumBacillus sp.

Fermented agrowaste The amendment enhanced nutrient uptakevia bacterial stimulated activities forproper nutrient absorption by plants andstomatal conductance during droughtstress

Armada et al. (2015b)

Pinus halepensis Azospirillum brasilensePantoea dispersa

Olive-mill waste The treatment and the inoculants promotedthe carbohydrate and microbial biomasscarbon as well as soil nutrient andconsequently increased growth, watercontent and nutrient uptake by the plant

Mengual et al. (2014a)

Lavandula dentata L. Bacillus megateriumEnterobacter sp.Bacillus thuringiensisBacillus sp.

Composted sugar beet It increased biomass shoot dry weight, root,and nutrient content of the plant. Theamendment increased the concentrationof bioavailable phosphorus and nitrogenin the plant rhizosphere

Mengual et al. (2014b)

Cistus albidus L. Azospirillum brasilensePantoea dispersa

Olive residue Increased dry root, shoot weight, organiccarbon, soil enzymes, and microbialbiomass carbon

Schoebitz et al. (2014)

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indirectly to tolerance ability of the plant to stress (Kasim et al.2016; Qurashi and Sabri 2012).

Bacillus amyloliquefaciens (SQR9) contributed to maizesalt tolerance by enhancing its chlorophyll production levelvia colonizing and interacting with the plant roots. It also aidsin the exclusion of sodium from the plant root, and stimulatesthe production of sugars and antioxidant within the tissues ofthe maize plant (Chen et al. 2016). This implies that a sensitiveplant could become tolerant to salt stress in the presence of abioinoculant.

This unique contribution to the wellbeing of the plant(Table 3) could be ascribed to its ability to produce indoleacetic acid, solubilize phosphorus, colonize the plant root,and produce enzyme deaminase (ACC-deaminase) capableof maintaining optimum biological function of the plant inthe midst of stress inducers.

With a shift in perspective, it was understood that opportu-nistic pathogens of humans can aid in plant tolerance to saltstress. The organism Methylobacterium mesophilicum couldefficiently colonize and dominate the root rhizosphere regionof three plants (cucumber, tomato, and paprika) under thestudy at salt concentration as high as 6% and possess thecapability of phytohormone (IAA) production together withfungicidal enzyme production that contributes to the growth,protection, and tolerance of the plant to biotic and abioticstress (Egamberdieva et al. 2015b).

Sensitive crops have remarkable reduction in viability andperformance when challenged with salt stress as compared totolerant species, following the observed accumulation of pro-line and reduced leaf area in a sensitive wheat plant comparedto a tolerant plant. However, the application of synthesizedphyto-hormone (gibberellic acid) on salt-stressed wheat plantshas resulted in adequate adaptation of two wheat plant speciesto salt-influenced stress and improved its yield (Shaddad et al.2013).

Moreover, the efficiency of microbial exopolysaccharideformation and the formation of biofilm during environmentalstress at the plant rhizosphere is a contributory factor towardplant adjustment to salinity or salt-induced osmotic shock.The polysaccharide molecules produced by microbes in abid to protect themselves from desiccation and ionic toxicityhave a charged part which reacts with dissociated sodium ionsand chelates them. This reduces the toxicity and abundance ofthese ions in the rhizosphere, making the soil suitable for rootproliferation (Arora et al. 2010).

The quest for a better way to reduce or alleviate stressinducers has led researchers to investigate the use of non-biological methods such as the external application of micro-nutrient Mo (molybdenum) as an additive to plants facingsalinity stress. Whenmolybdenumwas applied to a bean plant(Phaseolus vulgaris) subjected to salt stress, the plant was ableto maintain its chlorophyll composition and tissue compo-nents. Mo being a unique player (cofactor) in cellular enzyme

biosynthesis and activities enhanced the formation of chloro-phyll and maintenance of adequate cellular function (Bouzidand Rahmoune 2012).

The critical evaluation of the microbial community of Astertripolium L. showed the predominance of gram-positive bac-teria residing in the root of the halophyte, while gram-negativebacteria exist more in the rhizosphere and bulk part of the soil.The isolated organism exhibited the ability of forming 1-aminocyclopropane-1-carboxylate deaminase, indole aceticacid, etc. that contribute to the survival and tolerance of theplant to salt-induced stress and toxicity (Szyma’nskaa et al.2016).

It was noted that rhizosphere bacteria of a desert-adaptedplant (Suaeda fruticosa) fromKutch Desert has a unique strainof bacteria (Bacillus licheniformis strain A2), which solubi-lized phosphate, produced indole acetic acid, siderophore etc.,and contributed to 31% groundnut height and 43% biomassincrement of the plant and 24 and 28% rise when grown in50 mM sodium chloride supplemented soil (Goswamia et al.2014).

Another non-biological stress alleviation technique showedthat caffeic acid was able to aid the plant (soybean) toleratesalt stress. The applied caffeic acid stimulated the NO (nitricoxide) composition of the nodules, which has a direct relation-ship with the induction of cyclic guanine monophosphate re-sponsible for controlling reactive oxygen radicals produced inthe stressed plant. Caffeic acid helps to shield nitrogenaseenzyme and leghemoglobin of the soybean root nodules fromthe destructive effect of sodium and chloride ions, therebyadding to the growth of the plant by enabling the symbiontsto fix nitrogen adequately to meet plant nitrogen requirements.Caffeic acid has also been implicated in chlorosis suppressionof treated plants undergoing salinity-induced stress (Klein etal. 2015; Wang et al. 2011).

On the other hand, it was demonstrated that sodium chlo-ride impedes the uptake of potassium ions by Broussonetiapapyrifera plant, resulting in high sodium to potassium ratio.Sodium ion equally decreased the calcium, magnesium, andphosphorus content of the plant root system and caused aninduced ion imbalance in the plant rhizosphere. Bio-activeenzymes responsible for controlling oxygen radicals (catalase,peroxidase, superoxide dismutase) were also decreased by theinhibitory effect of the high salt concentration in the plantenvironment. Protein content of the plant was also affectedas observed in the appearance and disappearance of proteinbands in the plant samples analyzed (Zhang et al. 2013). Plantgrowth-promoting rhizobacteria inoculated on wheat plantpromoted its root and shoot growth and the weight of the freshtissue component of the plant. The observed rates of plantgrowth were from 62.2 to 78.1% in the presence of thebioinoculant (Orhan 2016). This could be attributed to theproduction of phyto-hormone by the microbes. Stress-adap ted bac te r i a (Pseudomonas pu t ida R4 and

Appl Microbiol Biotechnol (2018) 102:7821–7835 7829

Pseudomonas chlororaphis R5) capable of producing planthormone (IAA) at the rhizosphere of inoculated cotton plantsubjected to salt stress completely averted salinity stress oncotton plant (Egamberdieva et al. 2015a). This was also foundin cotton plant inoculated with Klebsiella oxytoca (Rs-5) thatresulted in the increase in seed germination (15.40%), growth,and overall tolerance of cotton to salinity stress (Wu et al.2014).

A newly identified rhizobacteria (Ochrobactrumintermedium) possessing the survival ability of changing itsmembrane phospholipid composition when subjected to stresscondition and also producing indole acetic acid, siderophores,

deaminase enzyme, and utilization of nitrate happens to im-prove the growth (root and shoot) of groundnut plant subject-ed to salt stress better than a well-known classifiedBradyrhizobium sp. (C145) accepted as a suitable groundnutinoculant by the Argentine INTA organization. The organismalso performed better in the production of biofilm thanBradyrhizobium and recorded high tolerance to 300 mmolsodium chloride and higher temperature (Paulucci et al. 2015).

Soil additives containing a variety of organic matter (poul-try droppings, olive plant waste, rice straw, molasses) and aconsortium of microbes known as Beffective microbe^ (bacte-ria, yeast, photosynthetic bacteria, actinomycetes, etc.),

Table 3 The unique contributions of microbes to salinity tolerance by plants

Plants Microbes Microbial influenced plant productivity and salinitytolerance

Reference

Chili Bacillus spp.Alcaligenes spp.Proteus spp.Aneurinibacillus aneurinilyticus

Significantly increased root and shoot length more thanthe control

Patel et al. (2017)

Rice Enterobacter sp. Promoted the growth of rice seedling and reducedethylene production and antioxidant enzymeactivities in the plant

Sarkar et al. (2018)

Rice Bacillus sp. Aided the alleviation of salt stress by increasing thebiomass and growth of rice seedling via productionof indole acetic acid and deaminase enzyme

Misra et al. (2017)

Festuca arundinacea Enterobacter ludwigii Membrane transport protein in the microbe that controlsodium and hydrogen ion movement across bacteriacell and the production of plant hormone, phosphatesolubilization, nitrogen fixation contribute towardsthe growth, tolerance, and plant productivity

Kapoor et al. (2017)

Alfalfa Halomonas mauraEnsifer meliloti

Increased the weight of shoot dry weight, yield, andwater content of the plant

Martinez et al. (2015)

Rice Thalassobacillus denorans (NCCP-58)Oceanobacillus kapialis (NCCP-76)

Inoculated plant was observed to have increasedgermination ability, root and shoot growth, protein,and chlorophyll contents as well as nutrient contentswith reduced sodium ion accumulation in the plant

Shah et al. (2017)

Rice Bacillus pumilus Enhanced plant growth and decreased theaccumulation of sodium ions without having aneffect on boron accumulation in the leaf tissues

Khan et al. (2016a)

Oat Klebsiella sp. It boosted plant growth, water content, dry shoot, androot weight of inoculated plant

Sapre et al. (2018)

Wheat Bacillus subtilis Enhanced salicyclic acid content of the plant, leaf watercontent, and reduced proline and malondialdehydecontent of the plant for better induction of systemicresistance

Lastochkina et al. (2017)

Barley Hartmannibacter diazotrophicus The production of deaminase enzyme enhancedpercentage root and shoot dry weight and growth ofthe plant

Suarez et al. (2015)

Canola Enterobacter cloacae HSNJ4 Enhanced canola tolerance via promotion of planthormone content of the plant and reduced ethyleneand malondialdehyde content. Root, shoot, andchlorophyll contents were improved

Li et al. (2017)

Sunflower Rhizophagus irregularisChryseobacterium humi ECP37Ochrobacterium haematophilum ZR3-5

Improved biomass and nutritional content of the plantas well as antioxidant response in the plant andlowered sodium ion content in the plant

Pereira et al. (2016)

LettuceRadishChinese cabbage

Arthrobacter scleromae SYE-3 Increased all the plant shoot length and leaf number inlettuce by 45.1%

Hong and Lee (2017)

7830 Appl Microbiol Biotechnol (2018) 102:7821–7835

collectively regarded as bokashi, have proven to be effectivein shielding Mandarin tree (citrus plant) from salt stress andimproving its productivity, and the nutritional content of thefruit, and also in enhancing the rhizosphere microbial commu-nity count and population (El-Hamied 2014). The bokashitreatment has aided greatly in the salted soil fertility improve-ment and protection of the plant from osmotic salt-inducedstress (El-Hamied 2014).

In a salt toxicity alleviation study, microbial species knownas Kocuria erythromyxa EY43 and Staphylococcus kloosiiEY37 were found to be very potent in increasing straw-berry plant growth, chlorophyll, mineral content, and fruityield. The organism was able to inhibit the absorption oftoxic ions (sodium and chloride ions) from the plant rhi-zosphere making a salinity-sensitive strawberry plant in-sensitive and tolerant to the condition of salt stress(Karlidag et al. 2013). The integration of endophytic bac-teria (Sphingomonas sp. LK11) with applied jasmonic ac-id synergistically improved the overall tolerance of tomatoplants (wild type and mutant species) to salinity. Thecombined applied microbe–jasmonic acid enhanced rootand shoot growth of the plant, brought about proper reg-ulation of glutathione content of the plant, and enabled itovercome the detrimental effects of salinity. It was notedthat the microbial-jasmonate treatment lowered the intra-cellular abscisic acid level of the plants (Khan et al.2017).

Although application of nutrients or minerals is an al-ternative measure to curbing salinity stress, introductionof excess of these nutrients will result in phytotoxicityinstead of phytoenhancement and will necessitateremediation.

Three hundred percent growth in barley plant growing insalt-containing soil was recorded when inoculated withCurtobacterium flaccumfaciens which did not fully expressthe attributes of plant growth promotion in pure culturegrowth medium. This organism, being relatively new in thisbranch of study, was originally associated with the infectionand destruction of crops but was now found to protect plants(barley) from salt stress better than the well-known microbesexhibiting excellent characteristics of plant growth promotionsuch as Microbacterium natoriense and Pseudomonasbrassicacearum (Cardinale et al. 2015).

Rhizobium naturally adapted to desert environments hasbeen shown to perform well in establishing nodules onthe root of legumes at a high level of salt–soil contentand to contribute to growth and better performance ofthe legume (Sobti et al. 2015). Also, an endophytic bac-teria (Bacillus subtilis LK14) isolated from the plant(Moringa peregrina) bark possesses high indole aceticacid production capacity and ACC-deaminase was ableto improve the growth and development of tomato plantseedlings (Khan et al. 2016b).

Microbial facilitated survival of plants under saline tensionis dependent on microbial production of deaminase enzyme(1-aminocyclopropane-1-carboxylate deaminase) responsiblefor degrading the plant product known as aminocyclopropane-1-carboxylate, the precursor of the plant hormone (ethylene)(Adams and Yang 1979; Dong et al. 1992; Honma andShimomura 1978; Glick et al. 2007). This hormone is respon-sible for the interference of root development when chal-lenged with stress substances that induce elevated level ofethylene production and is well documented by Tak et al.(2013).

Chickpea plant affected by an increase in salinity was res-cued by co-inoculation with two deaminase enzyme-producingmicrobes (Mesorhizobium MBD26 and Rhizobacteria RHD18) with an observed nodulation capacity of 49 nodules perplant, 201 mg weight of nodules, 12.28 mg per plant nitrogen,and a rise in 31.2% of the above the soil plant part dry weight(shoot dry weight). The result was further increased to 53 nod-ules and 116.9% grain produced, with N2 level spanning be-tween 9.59 and 27.36 mg per plant investigated (Chaudharyand Sindhu 2017).

The production of deaminase by rhizobacteria, on the otherhand, encouraged the root growth of velvet beans undergoingdrought stress by catalyzing the disintegration of 1-aminocyclopropane-1-carboxylate to generate nutrients forthe microbes and in turn create a shortage of the ingredient(ACC) necessary for the production of ethylene. This helpedto limit the action of this hormone (Saleem et al. 2015). Theinoculation of Bradyrhizobium japonicum together withBacillus amyloliquefaciens enabled better nodule formationon the soybean roots by the B. japonicum and resulted in betterfixation of nitrogen and plant viability (Masciarelli et al. 2014).

Alkalinity stress in phyto-retardation

Apart from stress induced by sodium chloride, sodium carbon-ate (Na2CO3) and sodium hydrogen carbonate (NaHCO3) alsoconstitute a problem to crops. They are implicated in the for-mation of alkaline soil that results in elevated soil pH andinterferes with the bioavailability of phosphorus, iron, copper,manganese, and zinc resulting in induced nutrient deficiencyand osmotic stress capable of interfering with the proper bio-logical function of the plant (Chen et al. 2011). The high pHhas its own inhibitory challenges on non-alkaliphilesinhabiting the rhizosphere. It also interferes with their biolog-ical activities as well as physiological functions of the plant.

However, fertility issues of alkaline soil could be handledby the application of bioinoculants. These microbes amelio-rate the alkalinity effect on plant by supporting increase in thenumber of nodules formed. They boost nitrogenase enzymeactivities for efficient nitrogen fixation and improve mycor-rhizal dominance in the root of faba bean inoculated with

Appl Microbiol Biotechnol (2018) 102:7821–7835 7831

Rhizobium leguminosarum and mycorrhizal fungi. The teamwork between the two organisms promoted faba bean produc-tivity and resistance to alkalinity stress (Abd-Alla et al. 2014).

Conclusion

The reality of abiotic stress in reducing the availability of foodfor the growing human population is obvious. The tempera-ture of the atmosphere is rising and deviation or instability inrainfall is frequently observed in our environment today. Thiscreates a tension in the sustainability of farming practice forfood production. And as human beings devise an alternative tocombat these challenges by adopting irrigation methods, sa-linity becomes the end product of this alternative practice.This also affects plants negatively.

Significant effects of plant tolerance to abiotic stress arethat it will result in promoting yield and production of cropsto feed humans and livestock. This can be achieved via thesearch, selection, and engineering of plant species capable ofresisting salinity and drought stress.

The use of plant growth-promoting rhizobacteria will go along way in supporting the plant to develop both intrinsic andextrinsic ability to tolerate stressful conditions and sustainyield. An integrated abiotic stress management strategy ofco-integration of external application of proline, caffeic acid,nutrients, synthetic plant hormones, and microbes (PGPR)could aid greatly in ensuring continuous and efficient agricul-tural practices that will manage the stress and boost the yieldof crops.

Acknowledgments M.C.E. is supported by the NRF-TWAS/AfricanRenaissance Doctoral Scholarship. This work is based on the researchsupported by the National Research Foundation of South Africa (GrantsRef: UID81192, UID95111; OOB).

Funding The study was funded by the National Research Foundation ofSouth Africa (Grants Ref: UID81192, UID95111; OOB) and the SouthAfrica’s National Research Foundation/The World Academy of ScienceAfrican Renaissance Scholarship (NRF-TWAS/African RenaissanceDoctoral Scholarship).

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict ofinterest.

Ethical approval This article does not contain any studies with humanparticipants or animals performed by any of the authors.

Open Access This article is distributed under the terms of the CreativeCommons At t r ibut ion 4 .0 In te rna t ional License (h t tp : / /creativecommons.org/licenses/by/4.0/), which permits unrestricted use,distribution, and reproduction in any medium, provided you give appro-priate credit to the original author(s) and the source, provide a link to theCreative Commons license, and indicate if changes were made.

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