**1. Introduction**

The world is at a point where we can no longer prevent all of the effects of climate change (because some of it is already here), but can only slow its further progress. The purpose of this paper is therefore to give the reader an understanding of why plant growth promoting organisms, or their products, are relevant, amidst climate change challenges, by showing how they can be used to mitigate the effects of climate change on crop production. The paper also highlights the various ways in which this approach can be used, and the role that inoculant formulation plays in maintaining the efficacy, durability and handling of microbial inoculants. The major drivers of climate change are human driven [1–3]. Burning of fossil fuels for energy, agriculture and industrialisation all contribute to emission of greenhouse gases (GHGs), such as: methane, carbon dioxide and nitrous oxide (N2O). Agriculture is a major contributor to greenhouse gas emissions [4,5], especially through the use of N based fertilizers, methane emissions from animals and animal manure, deforestation to acquire more land for crop production, etc. According to the intergovernmental panel on climate change (IPCC) report on GHG emissions, energy consumption contributes about 35%, agriculture, forestry and related land use 24%, industry 21% and transport 14% [6]. The greenhouse gases then trap heat radiating from the earth's surface, causing global warming. Unfortunately, climate change also adversely affects

agriculture [6,7], especially because, along with increases in global temperature, comes the increased prevalence of biotic and abiotic stresses that are detrimental to agriculture production, such as: pests, pathogens, nutrient deficiencies, salinity and weather extremes [1,8–10], some of which may encourage the further use of chemicals to correct, while there is little that can be done about others such as high temperatures and floods. Unmanaged, such factors affect plant growth and render arable land unproductive. This puts us in a challenging situation, especially because world population is growing so that there is a need to increase food production [5], both through increasing yield per unit area and reclaiming more land for crop production [11]. Therefore, while we strive hard to hold greenhouse gas emissions to 'bearable' levels, there is also a need for sustainable approaches that will ensure increased food production in the face of climate change. The use of agrochemicals has boosted crop productivity and contributed to food security, especially in developed countries. However, shortcomings related to their improper and continuous use, such as: increased greenhouse gas emissions (which is a major contributor to global warming), surface and ground water contamination, residual contamination of crop harvest, which poses health concerns to both humans and animals, as well as high costs related to their use. These circumstances have created a need for a more ecofriendly and sustainable approach for enhancing crop productivity in the face of climate change [11–13].

Several approaches have been suggested; the use of plant growth promoting microorganisms and compounds that they produce is perhaps the most promising [14]. The holobiont refers to plants and their associated microbes, which probably coexisted since the colonization of land by the first terrestrial plants [15–17]. This association is referred to as the holobiont [18], and it is dynamic, with the plant asserting a great influence on the nature of phytomicrobiome, especially in its rhizosphere [19], which is mainly attributed to the composition of their root exudates. The rhizosphere, endosphere and phyllosphere may be comprised of pathogenic, neutral and beneficial microbes, in relation to the plant [18,20]. Microbes that exert beneficial effects on the plant are termed plant growth promoting microorganisms (PGPM). These microbes may inhabit the rhizosphere, rhizoplane, phyllosphere, endosphere, etc. [19] For decades, PGPM such as rhizobia, mycorrhizae and plant growth promoting bacteria (PGPR, first defined by Kloepper and Schroth, in 1978) have been reported to enhance plant growth under stressed and non-stressed conditions. The use of microbial inoculants is an old practice [21] that has recently gained more prominence during the last three decades. Much research has been done on rhizobia, and currently a lot is being done on plant growth promoting rhizobacteria and PGPR derived compounds. The ability of microbes to suppress plant pathogens, as well as mitigate the effect of abiotic stress on plants, has been investigated by many researchers, and the findings are promising.

Although they occur naturally in the rhizosphere, and plant tissue, PGPM populations are often insufficient to induce desired effects, hence, it is recommendable to isolate them from their natural environments and multiply their populations before reintroduction into the soil or onto the plant as microbial inoculants [14]. Products in the form of microbe-produced compounds are currently gaining popularity among researchers, although they are less well known among farmers, in comparison to microbial cell inoculants, packaged as either single microbial strains or consortia, which have been commercialised for quite some time [21,22]. Microbe based inoculants are generally from the bacteria (such as Bacillus and Rhizobia) and fungi (especially Trichordema) subgroups [19,22,23], although some groups of archea have also been reported to enhance plant growth. Microbially produced compounds, such as lipochitooligosaccharides (LCO), as plant growth enhancers, on the other hand, are only gaining attention recently, which may explain their lesser availability on the agro-input market. Figure 1 below summarizes some of the mechanisms PGPM employ to mitigate the effects of biotic and abiotic stress on plants, which are later discussed in detail.

**Figure 1.** Mechanisms employed by plant growth promoting microorganisms (PGPM) to mitigate effects of biotic and abiotic stress on plants.

#### **2. PGPM as Enhancers of Soil Fertility**

For proper growth and development, plants need enough supply of essential macro (Nitrogen, Phosphorus, Potasium, Magnesium, Calcium, etc.) and micro (iron, manganese, boron, zinc, molybdenum, copper) nutrients. N, P and K are the most limiting as far as plant growth is concerned. Unfortunately, with climate change comes abiotic stresses like high temperature, drought and salinity, which influence the biogeochemical transformation of nutrients like P, K, and N, making them either available or less available for plant uptake [24–26]. While the lack of bioavailable macro and microelements is natural in the soil, it could be worsened by climate change. Nitrogen, phosphorus and potassium as the most plant growth limiting elements and their biogeochemical cycle, are affected by temperature and rainfall amongst other abiotic factors, which happen to be affected by climate change. Processes like decomposition, mineralisation, immobilisation, etc. are largely influenced by temperature and rainfall. Processes like soil erosion should also be noted, which is majorly due to run off and wind affect soil fertility as the nutrient rich topsoil is washed away.

Alkalinity affects the availability of Fe, Cu, Zn and Mn, while very low pH is associated with Al toxicity. Processes such as mineralization and nitrogen fixation are affected by moisture, temperature and pH, because they are driven by soil microorganisms like rhizobia, nitrifying bacteria, etc., and enzymes [24,26], which are also affected by abiotic stress. A study by DaMatta et al. [27] showed a decrease in leaf N content of *Co*ff*ea canephora* due to water stress. For PGPM technology to be relevant, amidst climate change, it is paramount that stress tolerant strains are identified and used. At the same time, the availability of these nutrients is essential, because they play a key role in minimizing the effects of other abiotic stresses like drought, salinity and high temperature on crops. The roles N, P, K, Ca, Mg and Fe play in the mitigation of abiotic stress have been reported by many researchers [27–33]. For instance, N and P have been reported to minimize the effects of drought stress [24–26,34,35]. K plays a major role in drought stress as well, since it is involved in the opening and closing of the stomata. Agricultural soils have been degraded due to continuous and intense cropping. Agricultural practices like continuous cropping, especially monocropping of non-leguminous crops, without application of fertiliser, is one way of depleting soils of nutrients [36]. This is a common practice of many smallholder farmers, especially in sub-Saharan Africa, due to the inaccessibility and cost of fertiliser [37]. Climate change is only further degrading the situation, because factors such as high temperatures, drought, flooding, salinity, extreme pH, etc. may cause changes in the physiochemical

properties of essential soil nutrients such as N, Fe, P and K, thereby limiting their mobility and/or affect their availability for plant uptake, while enhancing the accumulation of toxic elements such as aluminum (Al3+). The role of stress tolerant beneficial microbes in maintaining/increasing crop production amidst climate change challenges cannot be ignored. In order to reclaim land that has been abandoned due to inadequate nutrients for crop growth, considering the financial and environmental costs related to synthetic fertilisers, stress tolerant plant growth promoting organisms can be a cheaper and sustainable approach. With the need to reclaim more land for crop production, emphasis on enhancing soil fertility is inevitable, because nutrients can enhance plant tolerance to abiotic stress. Therefore, there is a need to address the issue using more sustainable approaches. With limited alternatives, and research output so far, microbial inoculants are a promising approach to enhance soil fertility, particularly in conjunction with the various challenges associated with climate change. Microbial inoculants may be defined as formulations comprised of microorganisms, such as bacteria and fungi, as the active ingredients, which once applied on plants, can enhance their growth [19,22,38]. They may also enhance plant quality through the increased concentration of essential nutrients such as proteins [14], and valuable metabolites such as flavonoids, phenolics, alkaloids and carotenoids [23]. Microbial inoculants may also enhance soil biodiversity and properties such as soil structure [22]. As biofertilizers, microbial inoculants enhance the availability and uptake of essential plant nutrients, such as: nitrogen, phosphorus, iron, zinc, and potassium [11–13], which, if lacking or available in inadequate quantities, could limit plant growth.

#### *2.1. Nitrogen Fixation*

Some free-living and symbiotic bacteria fix atmospheric dinitrogen into plant usable forms, initially ammonium, through biological nitrogen fixation. Symbionts such as *Rhizobia*, *Bradyrhizobium*, *Sinorhizobium*, *Frankia*, *Actinobacteria* and *Bukholderia* form specialized structures called nodules on their host plants, where they obtain nourishment and shelter, and in turn, fix nitrogen [38,39]. The process is referred to as symbiotic nitrogen fixation and it occurs in both legumes and non-leguminous plants, although that of legumes is the most studied. Communication in the form of molecular signals from both the microbe and host plant, as well as a complex of enzymes (e.g., nitrogenase) and genes (nif and/or symbiotic genes), are involved in the process of nitrogen fixation. On the other hand, free-living nitrogen fixing bacteria such as *Azotobacter* do not need to occupy plant tissue to fix nitrogen. Because of its high energy requirement, plants tend to prefer applied N fertilizer to biological nitrogen fixation (BNF), hence, for effectiveness, synthetic N should not be used along with biological nitrogen fixing organisms, because the plant may suppress the nitrogen fixing symbiosis. Where a starter dose of synthetic N is necessary, it should be applied cautiously, because high N supply can have an inhibitory effect on nodulation (nodule dry weight and number of nodules) and nitrogenase activity [24,40,41]. Arbuscular mycorrhizal fungi, through their hyphae, can enhance the acquisition of soil N by the plant [42], although there are wide variabilities as to the degree of this, whose causes are not yet known [22]. The efficiency and effectiveness of nitrogen fixing bacteria varies among and within plant species, and, in the agricultural context, are largely limited to members of the fabaceae family. Other crops can benefit from the symbiosis by including legumes in crop rotation regimes. There is also a need for more research on how to extend such modifications to non-leguminous plants. Approaches such as genetic engineering to enable non-legume nitrogen fixation and enhance effective communication with N fixing microorganisms can be further researched. Although genetic engineering is questionable, especially its ecological impact, some of the questions are likely from a lack of adequate information on the technology. Extensive research to address most of the questions can be very helpful.

#### *2.2. Phosphate Mobilisation and Solubilisation*

Although phosphorus is an abundant element in most soils, it frequently occurs in forms unavailable for plant use. The application of external sources of P fertiliser, such as single super phosphate, diammonium phosphate, etc., can help meet plants' P requirements, but this too may be

immobilised shortly after application, making it largely unavailable for plant uptake [43]. mobilization (chemical solubilization and mineralization), which results in plant available forms of the respective nutrients and solubilization, which is a more general term and does not necessarily result in readily plant available forms. For instance, the solubilization of organic P does not necessarily mean that the P is already plant available, as it may still be bound in unavailable organic forms (e.g., phytates). PGPM may enhance soil phosphorus availability for plant uptake through solubilisation and/or mobilisation of inorganic phosphorus. A PGPM may possess both or either mechanisms. The terms, phosphorus solubilisation and phosphorus mobilisation are often used synonymously by many researchers, although they are not necessarily the same thing. P solubilisation is the broader term, which may entail P mobilisation. Goldstein and Krishnaraj [44] described phosphate solubilising microorganisms as those that convert sparing soluble organic or mineral P, into soluble orthophosphate, in a way that significantly increases P availability to a specific plant or plant population within the microorganism's native soil ecosystem. The same author defined phosphate mobilising microorganisms as those that convert sparingly soluble organic or mineral P, into soluble orthophosphate P, in a way that significantly contributes to pool of available orthophosphate (Pi) in the native soil ecosystem. Phosphorus solubilising bacteria, such as: *Pseudomonas*, *Bacillus*, *Burkholderia* and *Rhizobium*, and some fungal species solubilise inorganic phosphates from sparingly soluble forms such as: tricalcium phosphate, dicalcium phosphate and aluminum phosphate, to forms such as hydrogen phosphate (HPO4 <sup>−</sup>2), or dihydrogen phosphate (H2PO4 <sup>−</sup>1), which plants can utilise [37,42–46] through the production of low molecular weight organic acid anions, such as gluconate, lactate, glycolate and oxalate. Phosphorus mobilisers, on the other hand, produce enzymes (such as phosphatase, phytase and phosphonoacetate hydrolase) that chelate cations, bind phosphates and dephosphorylate organic phosphates [22,24]. Dephosphorylation is catalyzed by hydrolase enzymes such as phosphonoacetate, which some PGPM can produce. For instance, ectomycorrhiza and ericoid mycorrhizal fungi produce extracellular acid phosphatases and phytases, which catalyse the mineralisation of P from organic complexes in the soil [42,47]. Other fungal species, such as *Aspergillus niger*, also produce organic acids which aid the process of P solubilisation [48,49]. Through the possession of hyphae, some mycorrhizae such as arbuscular mycorrhizae can deliver up to 80% of the phosphorus taken up by the host plant [27,40].
