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Review

Multi-Omics Approaches in Plant–Microbe Interactions Hold Enormous Promise for Sustainable Agriculture

by
Umesh Kumar
1,†,
Subhisha Raj
2,†,
Arathi Sreenikethanam
2,†,
Rahul Maddheshiya
3,
Seema Kumari
4,
Sungsoo Han
5,
Krishan K. Kapoor
6,7,
Rakesh Bhaskar
5,*,
Amit K. Bajhaiya
2,* and
Dharmender K. Gahlot
8,9,*
1
Department of Zoology, MNS Government College, Bhiwani 127021, India
2
Algal Biotechnology Lab, Department of Microbiology, Central University of Tamil Nadu, Neelakudy, Tamil Nadu 610005, India
3
Department of Zoology, School of Sciences, IFTM University, Moradabad 244102, India
4
Department of Zoology, Dronacharya Government College, Gurugram 122001, India
5
School of Chemical Engineering, Yeungnam University, Gyeongsan 38541, Republic of Korea
6
Department of Microbiology, CCS Haryana Agricultural University, Hisar 125004, India
7
Department of Bio & Nano Technology, Guru Jambheshwar University of Science & Technology, Hisar 125001, India
8
Department of Molecular Biology, Umeå University, 901 87 Umeå, Sweden
9
Umeå Centre for Microbial Research (UCMR), Umeå University, 901 87 Umeå, Sweden
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Agronomy 2023, 13(7), 1804; https://doi.org/10.3390/agronomy13071804
Submission received: 31 May 2023 / Revised: 30 June 2023 / Accepted: 1 July 2023 / Published: 6 July 2023
(This article belongs to the Special Issue Role of Plant Growth-Promoting Microbes in Agriculture)
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Abstract

:
Plants do not grow in isolation; they interact with diverse microorganisms in their habitat. The development of techniques to identify and quantify the microbial diversity associated with plants contributes to our understanding of the complexity of environmental influences to which plants are exposed. Identifying interactions which are beneficial to plants can enable us to promote healthy growth with the minimal application of agrochemicals. Beneficial plant–microbial interactions assist plants in acquiring inaccessible nutrients to promote plant growth and help them to cope with various stresses and pathogens. An increased knowledge of plant–microbial diversity can be applied to meet the growing demand for biofertilizers for use in organic agriculture. This review highlights the beneficial effects of soil–microbiota and biofertilizers on improving plant health and crop yields. We propose that a multi–omics approach is appropriate to evaluate viability in the context of sustainable agriculture.

1. Introduction

The Green Revolution in the 1960s led to an increase in the yield of crops with the application of agrochemicals such as chemical fertilizers, insecticides, fungicides, and herbicides on most agricultural lands. One of the major challenges for the 21st century is shifting to environmentally sound and sustainable crop production; enhanced agricultural production is necessary to provide sufficient food to meet the increased demand arising from the population growth. Improving and enhancing agricultural production via various viable methods is a possible solution to this problem. One of these methods, which is globally being practiced today, is utilizing chemical fertilizers and pesticides to enhance agricultural yields. However, this poses a significant threat to our health and environment upon overuse. Such an over-application of agrochemicals in farming has led to severe consequences on the physio-chemical properties of soil and the associated microbial population (Figure 1). Along with these, plant-attacking pathogens with a varying genetic composition demand more efficient and environment-friendly strategies in agricultural production. In their natural habitat, almost every plant is colonized by a diversity of microbial species [1,2,3]. These microorganisms play a crucial role in both soil and plant health and positively affect plant growth and yield. A good percentage (1–35%) of microbes isolated from plant-related habitats exhibited pathogen-resistant activities along with direct assistance in plant growth and development. Microbial species that have co-evolved with their hosts, together forming holobionts, can also confer resistance to diseases. As they have co-evolved together, the plants’ metabolism and their associated microbes are interlinked to a great extent. They support each other to maintain the normal functioning of the holobionts [1,4]. For example, arbuscular mycorrhizal fungi (AMF) and plant-growth-promoting microorganisms (PGPM) are tolerant to a variety of stresses, such as drought, excessive salinity in the soil, and the presence of heavy metals. Thus, the co-evolved microorganisms support good plant health even in stressful environments [5]. A recent report on biofertilizers, namely on combinations of PGPM and AMF, highlights their significance as eco-friendly and cost-effective tools to boost both soil health and plant yield [6]. Such investigations can yield useful insights that can enhance plant fitness and boost crop yields.
Plant microorganisms equipped with degradation pathways and metabolic capabilities assist in the efficient degradation of organic/inorganic pollutants and thus reduce their associated phytotoxicity [7]. More so, plants and their associated microbes are responsible for the secretion of various compounds with chelating, acidifying, degradative, solubilization, or reductive properties. These organic/inorganic compounds and their properties can help in accelerating metal immobilization. Microbes in an association can enhance the phytoremediation process by controlling the metal accumulation in plants and improving plant growth. For example, root endophytes equipped with a metal resistance/sequestration system can efficiently decrease metal phytotoxicity [8,9]. Various studies have demonstrated the phytoremediation activities of arbuscular mycorrhizal fungi and various plant-growth-promoting rhizobacteria on heavy-metal-containing soil and water [10]. Hence, the development and application of biofertilizers can boost plant health and crop yield in stressful environmental conditions. Soil microorganisms contribute to this in a sustainable cycle of soil health, plant health, and increased crop yield with no harmful impact on the ecosystems. Safety, decomposability, efficiency, better control, and fewer adverse effects on the environment are some of the features of microbial biofertilizers (microbial inoculants). These properties make them more apt and feasible than that of conventional chemical fertilizers in sustainable agriculture [2]. This review highlights the impact of soil microbiota on plant health and crop yield and how biofertilizers enhance soil microbiota, resulting in improved crop yields. We propose that a multi-omics approach is best suited to evaluating the benefits of microbial diversity and biofertilizers on soil and plant health, as well as crop yield.

2. Impact of Excessive Consumption of Agrochemicals and Abiotic Parameters on Soil Microbiota–Plant Interactions

Agrochemicals, including chemical fertilizer application, are currently necessary to enhance crop yields. Their excessive application reduces both soil properties and soil microbiota–plant interactions and contributes to environmental pollution [11,12,13,14] (Figure 1). Even though the usage of agrochemicals in the form of readily available chemical fertilizers and pesticides can give rapid and visible results in biomass improvement and pest resistance in various crops, they can pose a serious threat to the health of living organisms and their ecosystem [2]. It was found that certain agrochemical treatments in agriculture had a negative effect on about half of the naturally occurring microbes in the soil; among them were identified to be plant-specific microbes involved in nitrogen fixation and nutrient acquisition by plants. A significant reduction in microbial enzymes responsible for nitrogen fixation was observed when the plants were treated with certain pesticides and fungicides [15]. These chemicals can alter soil factors such as moisture, pH, organic matter content, and temperature, modifying soil microbes’ physiological and biochemical activities. Thus, it causes a harmful impact on their diversity and number [16]. Although the continuous use of chemical fertilizers increases nutrient availability in soil, it can upset the natural balance between plants for food sources such as below-ground nutrients versus above-ground photosynthesis [17]. It has been reported that the reduction in microbial diversity in nutrient-rich soil with an adequate water content was primarily due to the competition of flora for light sources [14,18]. Moreover, changes in soil pH from the excessive consumption of chemical fertilizers (i.e., ammonium sulfate) are less beneficial to microbial richness and diversity (Figure 1) when compared with organic fertilizers or manures, suggesting long-lasting harmful effects of chemical fertilizers [19]. Similarly, applying chemical fertilizers in soil can generate nutrient channels, thus causing nutrient gradients affecting the soil microbial density. For instance, chemical fertilizers such as ammonium sulfate and urea application created a nitrogen gradient in soil, which significantly impacted the diversity and population of the microbes [20].
Root exudates secreted by various plant roots consist of low-molecular-weight and high-molecular-weight organic compounds. The nature of these rhizo-deposits depends on the environmental conditions, and they are plant-species-specific. These molecules provide a readily available carbon source to the soil microbes [21]. In the long run, high-throughput sequencing and 13C foot-printing demonstrated that the consumption of conventional agrochemicals has reduced the reliance of microbes on plant-derived carbon due to chemically induced stresses between plants and soil [22]. Previously, it has been indicated that the relationship between plants and soil microbiota could be altered by changing the symbiotic relationships between plants and associated AMF [23]. In addition, the consumption of nitrogen fertilizers can also affect the species richness and diversity of AMF by increasing nutrient levels in the soil, thus affecting their inter-relationship [24]. Consequently, the modulation in plant–microbe interactions induced by the consumption of chemical fertilizers might also be related to the time duration of plant growth. Many studies on this impact on plant–microbe interactions have been carried out over short timescales [11,22,25,26,27]. Studies over longer time periods are required to monitor soil–microbiota and plant–interactions where organic soil improvement has been applied. Organic methods of soil improvement and plant fertilization are increasingly being applied [28]. The use of nitrogen-fixing bacteria in modern agricultural practices as a plant growth promoter has become an effective and eco-friendly strategy to cut down the need for conventional, inorganic, nitrogenous fertilizers [29].
In addition, along with chemical fertilizers, naturally occurring abiotic parameters or stresses can also impact the soil microbes associated with plants. Even though it is already known that abiotic stresses such as drought, salinity, flood, extreme cold, or hot temperatures can alter plant metabolism or physiology adversely, an extensive study on the effects of these stresses on plant–microbial interactions still needs to be conducted. The impact of these parameters on the interactions can be influenced by the intensity and time interval of the stress exposure, plant, and microbe species involved, and other related environmental variables [30,31,32]. Therefore, the relationship between abiotic stresses and the plant–microbe interaction is complex yet fascinating.
One of the most prominent abiotic stresses is salinity/salt stress, which can alter soil’s physical and chemical properties with which the plants and microbes associate. Some studies showed a decline in the bacterial population and diversity in salt-sensitive plants’ rhizosphere compared to that of salt-tolerant plants. This indicates that specific bacterial communities help in salinity tolerance, and the genus Pseudomonas was the most abundant among them. Microbes can protect plants from salt stress by altering phytohormones signaling, water and ions intake, and the soil characteristics associated with the plants. Thus, salt stress can alter the microbial structure both below and above the ground, and the genotype of the respective plant also influences this [33,34,35].
Another critical abiotic stress associated with plants is water scarcity/drought. Studies have proved that water scarcity can influence microbial diversity and population in the rhizosphere and endosphere of plant roots. It has been demonstrated that despite a reduction in microbes under drought stress, there was an increase in the Actinobacteria population under the same condition from the roots down to the soil among various plant species [36,37,38]. Similarly, it has been shown that there was an alteration in the population of arbuscular mycorrhizal and ectomycorrhizal fungi, which assist plants in obtaining sufficient nutrients and water [39,40].
Besides salt and water stress, another interesting abiotic stress that can alter the plant–microbe relationship is temperature (both high and low) stress. As environmental temperature variations can impact soil moisture and pH, they can also affect the holobiont. As drought stress is associated with high temperatures, the same actinobacterial enrichment can be observed in plant roots and soil under hot temperatures. Certain microbes can help plants to tolerate high temperatures by reducing Reactive Oxygen Species (ROS) production and improving nutrient and water absorption [41,42,43]. Likewise, certain plant–microbe interactions help plants to battle cold temperatures by escalating starch and carbohydrate storage and metabolism [44,45].
In summary, research shows that the use of chemical fertilizers, pesticides, and certain natural abiotic stresses can significantly impact the structure and diversity of plant-associated microbes and their relationship.

3. Soil Microbiota—An Ecological Engineer

Population growth is a major challenge for humankind. How can we produce sufficient food in a sustainable manner? Reliance on artificial, chemical fertilizers is incompatible with the need to develop sustainable agricultural practices which are equally focused on maintaining soil health and improving crop productivity. For a growing population, conventional agricultural practices are unsustainable. Moreover, it is a challenging task for both farmers and the policy makers to satisfy increasing food demands. On the other hand, the overuse of agrochemicals, i.e., pesticides, and chemical fertilizers has led to a reduction in microbial diversity in soil, consequently reducing crop productivity [46]. They also had detrimental effects on human health and the environment [3]. To overcome these challenges, the use of biofertilizers, i.e., plant-growth-promoting microorganisms (PGPMs), and AMF offers a sustainable alternative [47,48] (Figure 2, Table 1). These plant–microbial interactions offered by PGPMs can mostly result in beneficial outcomes, which can be in the form of stress tolerance, hormone(s) production and balance; pathogen(s) resistance and suppression; and nutrient and water acquisition [49]. Moreover, microbes associated with seeds can significantly influence plant health by positively affecting seed germination and development, thus enhancing crop productivity [50]. The co-inoculation of mycorrhizae with plant-growth-promoting rhizobacteria ameliorates the negative effect of biotic stress and induces resistance against phytopathogens through promoting growth attributes [6,51].
However, some microbes and their interaction can have a negative effect on plants– causing harmful diseases. Thus, an extensive study on these complex interactions will help in establishing sustainable agriculture through crop improvement [49].
Despite these various advantages of plant-associated microbial communities, they are not always optimal to meet the increasing demand associated with a growing population. This continues to be one of the primary causes for farmers to use chemical fertilizers, which show visible differences in crop yield irrespective of their harmful effects on soil and the environment. As this has been a repeated practice for several generations of the plant, now, they have partially lost their ability to associate with beneficial microbiota in the soil. To restore soil fertility and microbial relationship, it is necessary to resume native farming practices [52]. According to the theory of ecological communities, there are four processes that can alter the plant-associated microbiota. These are selection, dispersal, speciation, and ecological drift. The rhizosphere gains new microbial species because of dispersal and speciation, but microbial species are lost as a result of selection and ecological drift. If these processes are properly understood, these can be used to purposefully engineer the soil–microbiota for the enhanced productivity of the plant [53]. It is a well-known fact that the plant-associated microbiome is responsible for several structural advantages which contributes to an improved phenotype conferring pathogen resistance. Therefore, another strategy which can be included in microbiome engineering is the generation of synthetic microbiome in which selected microbial strains with desired functions can be combined [54]. Up until now, there have been many microbiome engineering studies performed on model plants, particularly on Arabidopsis thaliana, but more efficient research on commercially important plants is necessary to practically meet the rising demands.

4. PGPM Boost Plant Growth and Productivity

Beneficial microorganisms like PGPM are observed among the rhizospheric fungi and bacterial communities. These microbes have been considered eco-friendly and cost-effective means to control plant pathogens by inducing defense responses– activating cellular components, cell wall reinforcement, and the production of secondary metabolites. Flavobacterium spp., Pseudomonas spp., Bacillus spp., Enterobacter spp., Streptomyces spp., Clostridium spp., and Serratia spp. are some microbial communities included under PGPM that can improve agricultural productivity [55,56,57]. Plant hormones such as Jasmonates, Ethylene, and Salicylic acid play a vital role in defense signaling [55,56], solubilizing phosphates, and regulating the production of plant pathogens [58]. Moreover, rational dosages of distillery effluent evaluated on the productivity of chickpea crop and on the augmented soil-rhizobia (in clay pots) has demonstrated that irrigation water combined with a low concentration (100 m3 ha−1) of distillery effluent enhanced plant growth and improved soil biochemical properties as well as root-associated rhizobia [59]. PGPM can directly facilitates plant growth and development through positive regulatory mechanisms and processes (Figure 2, Table 1). In addition, PGPM inoculants enhanced the accessibility and absorption of essential plant nutrients such as nitrogen, phosphorous, zinc, and potassium in various crops, which are crucial for plant growth [60]. They aid nutritional uptake and enhance nutrient availability via the solubilization of minerals, N2-fixation, the mineralization of organic compounds, and production of several plant hormones [61]. Atmospheric N2-fixing PGPM inoculation rejuvenates growth-promoting activities and disease management and balances the N2 level in plants [62,63]. Plant-species-specific PGPM helped certain crops to withstand abiotic stresses such as drought, salinity, flooding, and low temperature [60]. It was also discovered that these PGPM were able to induce a positive impact on plant growth in certain crops, even under chemically stressed, high organo-phosphate pesticide conditions, indicating that these microbes can reduce the toxicity induced by the accumulation of such chemicals [64].
The augmentation of phosphorus-solubilizing microbes, Mesorhizobium ciceri and M. mediterraneum, isolated from chickpea nodules [65], could be used in biofertilizer formulations to enhance soil health. Several other PGPM that solubilize organic and inorganic soil metals could boost plant growth/yield. This in-built aptitude of PGPM has been recognized in biofertilizer formulations and could contribute to the development of sustainable agricultural practices (Table 1). In addition, the employment of microbial antagonists to compete with plant pathogens has been suggested as more beneficial to plant and soil health than the application of chemical pesticides. For example, PGPMs such as Bacillus and Pseudomonas spp. inhibit the growth of harmful microbes by producing antibiotics (Table 1). The use of PGPM antibiotics to combat several plant pathogens offers a promising prospect of biocontrol mechanisms as demonstrated by studies of PGPM antibiotics for over two decades [66]. Thus, the exploitation of beneficial PGPM inoculants as biofertilizers can be considered a more environment-friendly and sustainable approach to improve crop production.

5. Mycorrhizal Fungi Boost Plant Growth and Productivity

Mycorrhizae are the association between plant-roots and fungi. This symbiotic relationship has been identified in about 90% of all land plants. A dramatically larger root web in association with mycorrhizae permits the plant to obtain additional moisture and nutrients (Figure 2). This is particularly important in phosphorus uptake, one of the crucial nutrients for plant growth. A symbiotic relationship between plant-roots and fungi can play a vital role in the tolerance to drought and salinity stress. Arbuscular mycorrhizal fungi (AMF), which are symbiotic mycorrhizal fungi, have a key role in the uptake of nutrients in plants by increasing the absorption-surface-area of host plant-root systems. They also provide an opportunity for enhanced interaction with other soil microbes, thereby influencing plant development [67]. Therefore, these AMFs that modulate the hormonal balance and thus the physiology of respective plant are excellent examples of such symbiotic relationships. They also improve the efficiency of photosystem-II and photosynthetic products under low-water conditions [68]. For example, Trichoderma harzianum promotes root growth even in water-deficient conditions in rice crops [69,70].
Several studies on Medicago truncatula suggest mycorrhizal symbiosis has a more substantial impact on the plant microbiome. This is indicated by the mycorrhizal fungi contributing to formation of fungal mantle around the roots [71,72]. The fungal mantle enhances soil health and metabolites in the roots’ vicinity. Consequently, bacteria accumulate in the hyphal networks. Additionally, when mycorrhizae colonize the roots of a plant, it is known to provide a safeguard against several plant diseases (Figure 2).
A relatively recent study on the adaptation of plants to environmental fluctuations suggests that plants can adapt, interact, modify, and select specific microbial communities to reduce the harmful effects of different stresses, a phenomenon known as a ‘Cry for Help’ [4,73,74,75,76]. In particular, these AMFs were also shown to promote salinity tolerance in various crops via different mechanisms such as improving soil conditions and the biochemical and physiological properties of the host-plant and enhancing nutrient acquisition. They can dilute toxic ion(s) accumulation and their adverse effects by increasing the water absorption capacity of plants by improving their root hydraulic conductivity, thus maintaining an osmotic balance [77]. A study conducted on chickpea indicated that a co-inoculation of plant-growth-promoting bacteria and arbuscular mycorrhizal fungi resulted in an increased yield even under water-deficit conditions [78]. Therefore, the adjustment of these interactions between plants and microbes could represent a positive option to mitigate the adverse effects of climate change on food crops. In this framework, microbiome engineering has recently emerged as a promising approach in order to promote positive interactions between soil-microbiota and a cognate host-plant [54,79,80,81,82,83].

6. Multi-Omics—An Integrated Approach for a Better Insight into Soil-Microbiota–Plant Interactions

The rise of Omics approaches enables the investigation of microbial diversity and plant–microbe interactions across diverse ecological communities (Figure 3). Discovering complex microbial communities in various environments is one of the significant challenges as it has been possible to characterize only a tiny fraction of microbes as of now. This ‘Omics’ science derived from an integrative analysis concept helps to unravel complex plant–microbe interactions at the molecular level [49]. To fully understand the complex communication between plant(s) and the associated microbes, multi-omics strategy has the potential role to explore the molecular mechanisms and interpret the functionality behind these interactions which have an impact on the growth and development of plants [84]. In order to acquire a thorough understanding of the intricate interactions between plant(s) and the linked microbes, multi-omics approaches in plant–microbe interactions entail the simultaneous study of several omics data sets, such as epigenome, metabolome, proteome, transcriptome, and genomes. This integrated method of multi-omics enables the identification of significant molecular markers, regulatory networks, and metabolic pathways involved in host–microbe interactions [85]. There are still some gaps in our understanding of this aspect of plant–microbiome interactions, but more studies have recently begun to look at additional microbiome properties, such as activity and functional capability, by using an omics strategy.
In addition, the process of finding and describing the precise gene(s) or genomic area(s) that support complex traits in plants, such as disease resistance, yield, or quality, is known as quantitative trait loci (QTLs) [86]. Researchers can prioritize specific genes within the QTLs and suggest putative causative gene(s) that might be responsive to the observed trait variations. Furthermore, omics data can direct functional validation research such as gene-expression analyses, gene-editing (such as CRISPR/Cas9), or transgenic methods to confirm the function of candidate gene(s) in trait expression [87]. Therefore, it is conceivable to increase their expression in superior semi-dwarf kinds and obtain a high yield in an environmentally benign way by employing CRISPR/Cas9 technology to alter the promoter regions.
A widely used omic technique is ‘metagenomic’ in which the genomic analysis of environmental samples is carried out; however, in other important techniques such as ‘meta-transcriptomic’ and ‘meta-proteomic’, the analysis of expressed genes and the analysis of the proteins included in the biomass are conducted, respectively. Moreover, in another approach known as metabolomic, tiny molecules synthesized by microbes based on their genome information are analyzed [88,89]. Studying endophyte–plant interactions can be completed effectively using metabolomic. To validate a study by linking the genotype and phenotype, metabolomic is typically used in conjunction with other omics approaches. The above-mentioned metagenomic analysis using the next-generation sequencing method demonstrated that only about 5% of bacteria are culturable by methods available today, signifying that many microbes, especially bacteria, are still unknown, and their functions are not yet identified [90]. The 16S rDNA sequencing from the plant leaf surfaces also showed that environmental factors influence the microbial community composition more than that of the plant species. Along with the assignment of functional traits to microbes, these metagenomic studies also revealed several viruses without any pathogenic effects that are also associated with plants. However, this area was not much explored. Similarly, techniques such as meta-transcriptomic and meta-proteomic can be utilized to predict the microbial communities associated with the plant(s) along with their functions and activities. These techniques have proved their efficiency in studying microbial bioremediation as well [91,92,93].
To identify key markers and apply them in plant-breeding to develop more productive and climate-resistant plant cultivars, multi-omic data must be integrated into biological networks. The data measured are analyzed and integrated using multivariate statistics in multi-omic [94]. Integrated multi-omics approaches are revealing the composition of microbiomes these days [95]. Scientific advancements [96,97,98,99], especially genome sequencing, can help to characterize valuable features for both plants and their associated soil- microbiota. These omics studies will help to identify the roles of various genes, metabolites, proteins, and nucleic acids involved in these plant–microbial interactions. This information can be later utilized to modify or strengthen these interactions [100]. For example, the genome sequencing of a number of endophytic bacteria, microbes which colonize plant tissues, has brought insight into several ingrained beneficial traits, such as N2-fixation, quorum sensing, biofilm formation, iron uptake, and metabolism. This suggests the endophytic bacterial-lifestyle is well-equipped to survive in an iron-limiting environment and can competently sequester iron (when needed) from other microbes, including from plant-pathogens [101].
Moreover, understanding how plants and microorganisms change their metabolic profile in reaction to each other is made easier by metabolomic. It can indicate changes in secondary metabolites such as phytoalexins or antimicrobial chemicals produced by plants in response to microbial infections as well as primary metabolites such as sugars, amino acids, and organic acids. The identification of the metabolites exchanged between plant roots and mycorrhizal fungi aids nutrient uptake and transportation. Furthermore, it can provide evidence on the synthesis and release of signaling molecules such as phytohormones, alkaloids terpenes, or microbial signaling molecules (such as quorum sensing molecules). These compounds are key players in orchestrating plant–microbial interactions that preferentially appeal to microbiomes that may improve plant resilience [95,102,103].
Research has been conducted extensively on Echinacea purpurea and A. thaliana to better understand their microbiomes and how these microbiomes contribute to the growth and reproduction of host plants [104]. An important part of the root-specific metabolites are terpenoids which can accumulate as triterpene glycosides in plant tissues and form the mevalonate pathway [105]. It supports the formation of the Arabidopsis-based microbiota by regulating the growth of specific root bacteria [106]. Additionally, some metabolites (flavonoids, quorum-sensing molecules) are involved in the regulation of symbiosis between plants and microbes such as rhizobia, arbuscular mycorrhiza, and ectomycorrhiza. Legume plants need to produce distinctive flavonoids that bind to NodD proteins on the surface of rhizobia strains. Another metabolite is the drought-induced secretion of glycerol-3-phosphate (G3P), and in roots, with the help of actinomycetes microorganisms, plants can utilize G3P for their growth [36]. The supply of iron and phytosiderophores in the rhizosphere is decreased by stress, which is encouraged by actinobacteria. These bacteria could flourish in low-iron environments, which increases their ability to promote plant growth [107,108]. It is crucial to understand the molecular interactions and signaling pathways with metabolites to alter the structure and functionality of the microbiome in order to promote plant resilience. For metabolite identification, screening, and quantification, a variety of technologies and approaches are available, each with its advantages and disadvantages. For example, Spectrophotometric techniques are thought to be quick and economical for analyzing substances for fingerprints. Metabolites can be found using spectrophotometers at the appropriate wavelength. Another fingerprinting method is Fourier transform infrared (FTIR) spectroscopy, which can analyze thousands of samples each day of various metabolites without harming or wasting the samples [109,110].
Likewise, the genome analysis of diazotrophic Klebsiella pneumonia bacterium displays its aptitude to tackle harmful plant reactive oxygen species (ROS) by expressing several defensive enzymes, such as superoxide dismutases, putative catalases, peroxidases, reductases, etc. [111,112]. A multi-omics approach involving the integration of metabolomic, genomic, and volatilomic was proposed for a better understanding of the plant defense pathway (Salicylic acid pathway) and a combination of metabolomic and spectranomic for plant stress detection in 2020 [98].
A metagenomic analysis of endophytic bacteria from rice crops demonstrated several key features that are shared among endophytes which are crucial for establishing successful plant–microbe interactions [9,102]. By employing post-genomic approaches, for example, meta-transcriptomic, i.e., a global expression analysis of mRNA; meta-proteomic, i.e., a global expression analysis of proteins; and meta-proteogenomic (Figure 3), a deeper insight into plant-endophyte interactions can be harnessed by linking up the genomic information with the physiological attributes of plants. A meta-proteogenomic study on the microbial communities of the rice phyllosphere and rhizosphere demonstrated that despite the presence of nifH genes in both micro-environments, dinitrogenase reductase was exclusively identified in the rhizosphere [1,113]. If such approaches could be employed to study the endosphere of other plants or crops, along with synthetic-biology-enabled microbiome engineering [109], a significant exploration of soil microbiota–plant interactions would be feasible to promote more sustainable agricultural methods through the application of biofertilizers.
Overall, multi-omics strategies offer a potent arsenal for comprehending the intricate connections between plants, their genomes, and the environment. Utilizing this knowledge will enable the development and optimization of sustainable agricultural techniques that will improve output, resource efficiency, and responsibility toward the environment.

7. Conclusions and Prospects

The world population is increasing day by day, and so is the demand for food and other resources. Improving agricultural production by various means is a possible solution for the same. However, the utilization of chemical fertilizers and pesticides can have detrimental effects on human health and the environment. Therefore, an understanding of the role of plant–microbe interactions in the agriculture system is necessary to manage the soil-microbiota to achieve maximum benefits to plant- and soil-health, i.e., sustainable agriculture. There are many unanswered questions which remain within the field of soil- microbiota–plant interactions. Exploring these interactions can help to devise strategies to harness their full potential. Some of these interactions can improve plant growth and development via phytohormone production, defending pathogens, and escalating nutrient(s) absorption by plants. Unravelling molecular complexity can make a valuable contribution to operationalize these interactions which will result in improved soil health, good plant-health, and sustainable crop-yields, all of which are essential if the increasing world population is to be fed.
The application of multi-omics approaches in plant–microbe interactions can offer great potential for the future. The integration of multi-omics approaches, in which there will be a combination of experimental and computational techniques, can help to have a better understanding of plant–microbe interactions, revealing the specific microbial player(s) in the system. This will help in gaining a better understanding of the mechanisms of microbial interactions in plant growth, stress response, and disease resistance. However, the main challenge is selecting the most appropriate technology and methods suitable for the problem that needs to be solved. The limitation of databases is another challenge that needs to be addressed. If these techniques can unravel the mechanisms and potential of microbes in plant–microbe interactions, we will soon be able to engineer microbes for biofertilization and biocontrol. These genetically modified microbes will contribute to the establishment of agriculture-practices with less environmental impact. However, it is essential to evaluate them for biosafety and biosecurity before introducing these genetically modified microbes for public usage. One of the few factors preventing more people from using biofertilizers is an ignorance of improved application techniques for these fertilizers in the field. This technique will also contribute to offering protection against environmental contaminants.
Here, in this review, we have discussed the importance of soil-microbiota, their interaction with plants and how they impact their growth and productivity. We have also reviewed the modes in which these interactions are affected by chemical fertilizers and abiotic parameters. However, we know that the rise of omics approaches has enabled the investigation of microbial diversity and plant–microbe interactions across diverse ecological communities. Thus, here, we analyzed the different genomic (metagenomic) and post-genomic (meta-transcriptomic and -proteomic) approaches, which are being utilized to attain a better insight into soil-microbiota–plant interactions. We have explained each of the available omic techniques, and their purpose in understanding plant–microbe interactions at the molecular level. Furthermore, this review endeavors for an advancement in the multi-omics approaches (the integration of various omics techniques) that are used for the identification of biofertilizers and pesticides which affect soil-health, the soil-microbiota, crop- physiology and productivity by inducing biochemical cascades that control gene-expression profiles, fine-tune transcription factors, and crosstalk metabolism among the soil-microbiota. Therefore, in our opinion, multi-omics approaches could play an integral role in the identification of beneficial biofertilizers that can alter the structure of the soil-microbiome and the natural physiology of plants in a certain niche.

Author Contributions

D.K.G. and U.K. proposed the concept of manuscript; D.K.G., U.K., S.R. and A.S. wrote initial drafts of the manuscript with support (literature mining and occasional editing) from R.M., S.K., S.H. and K.K.K.; D.K.G., A.K.B. and R.B. refined the drafts and supervised the writing process. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

We acknowledge David Johnstone for critical reading and improving English of the manuscript. D.K.G. also acknowledges Umeå University, Sweden, for its learning environment and development opportunities for young researchers. S.R. would like to thank CSIR for her Ph.D. fellowship and A.S. would like to thank SERB for her Ph.D. fellowship. A.K.B. would like to thank SERB-SRG grant from the Govt. of India. S.R., A.S., and A.K.B. would like to thank the Dept. of Microbiology, Central University of Tamil Nadu, for the administrative support. S.H. and R.B. show gratitude to the Korean Institute of Planning and Evaluation for Technology in Food, Agriculture, and Forestry (IPET) through the High Value-added Food Technology Development Program, funded by the Ministry of Agriculture, Food and Rural Affairs (MAFRA; 321027-5).

Conflicts of Interest

Authors declare no conflict of interest.

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Figure 1. Application of agrochemicals in farming has led to severe consequences on the physio-chemical properties of soil and associated microbial populations. A conceptual model illustrating the deleterious effects of agrochemical-augmented soil on the diverse interactions in the plant rhizosphere and subsequent soil and plant health. N: Nitrogen; P: Phosphorus; K: Potassium; PGPM: Plant-growth-promoting microorganisms.
Figure 1. Application of agrochemicals in farming has led to severe consequences on the physio-chemical properties of soil and associated microbial populations. A conceptual model illustrating the deleterious effects of agrochemical-augmented soil on the diverse interactions in the plant rhizosphere and subsequent soil and plant health. N: Nitrogen; P: Phosphorus; K: Potassium; PGPM: Plant-growth-promoting microorganisms.
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Figure 2. The use of biofertilizers such as plant-growth-promoting microorganisms, and AMF offers a sustainable alternative. A representation of the possible interactions between plant, mycorrhiza and PGPM favoring plant growth. N: Nitrogen; P: Phosphorus; K: Potassium; PGPM: Plant-growth-promoting microorganisms; ACCD: 1-Aminocyclopropane-1-Carboxylate Deaminase.
Figure 2. The use of biofertilizers such as plant-growth-promoting microorganisms, and AMF offers a sustainable alternative. A representation of the possible interactions between plant, mycorrhiza and PGPM favoring plant growth. N: Nitrogen; P: Phosphorus; K: Potassium; PGPM: Plant-growth-promoting microorganisms; ACCD: 1-Aminocyclopropane-1-Carboxylate Deaminase.
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Figure 3. The rise of omics approaches enables the investigation of microbial diversity and plant–microbe interactions across diverse ecological communities. Diverse genomic (metagenomics) and post-genomic (meta-transcriptomics and -proteomics) approaches are being utilized to acquire a better insight into soil microbiota–plant interactions. For clarity, only a schematic depiction of each approach is shown. Descriptive technical and analytical plans for these approaches can be harnessed from elsewhere [70,71,72,73].
Figure 3. The rise of omics approaches enables the investigation of microbial diversity and plant–microbe interactions across diverse ecological communities. Diverse genomic (metagenomics) and post-genomic (meta-transcriptomics and -proteomics) approaches are being utilized to acquire a better insight into soil microbiota–plant interactions. For clarity, only a schematic depiction of each approach is shown. Descriptive technical and analytical plans for these approaches can be harnessed from elsewhere [70,71,72,73].
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Table
Table 1. Examples of recognized biofertilizers and their properties to empower sustainable agriculture.
Table 1. Examples of recognized biofertilizers and their properties to empower sustainable agriculture.
Biofertiliser and Their Biochemical PropertyEnriched Microorganism(s)Reference(s)
Nitrogen fixingRhizobium spp. and Frankia spp.[1]
Phosphorus solubilizingPseudomonas striata and Penicillium spp.[2,3]
Zinc solubilizingPseudomonas and Bacillus spp.[4,5]
Sulphur oxidisingAcidothiobacillus spp., Xanthobacter and Pseudomonas spp.[6]
Potassium mobilizingAspergillus niger, Bacillus spp.,
Acidothiobacillus spp., Burkholderia spp., Ferrooxidans spp., Paenibacillus spp. and
Pseudomonas spp.		[7,8]
Other plant-growth-promoting microbesAgrobacterium spp., Enterobacter spp., Streptomyces spp., Pseudomonas fluorescens and Xanthomonas spp.[9]
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Kumar, U.; Raj, S.; Sreenikethanam, A.; Maddheshiya, R.; Kumari, S.; Han, S.; Kapoor, K.K.; Bhaskar, R.; Bajhaiya, A.K.; Gahlot, D.K. Multi-Omics Approaches in Plant–Microbe Interactions Hold Enormous Promise for Sustainable Agriculture. Agronomy 2023, 13, 1804. https://doi.org/10.3390/agronomy13071804

AMA Style

Kumar U, Raj S, Sreenikethanam A, Maddheshiya R, Kumari S, Han S, Kapoor KK, Bhaskar R, Bajhaiya AK, Gahlot DK. Multi-Omics Approaches in Plant–Microbe Interactions Hold Enormous Promise for Sustainable Agriculture. Agronomy. 2023; 13(7):1804. https://doi.org/10.3390/agronomy13071804

Chicago/Turabian Style

Kumar, Umesh, Subhisha Raj, Arathi Sreenikethanam, Rahul Maddheshiya, Seema Kumari, Sungsoo Han, Krishan K. Kapoor, Rakesh Bhaskar, Amit K. Bajhaiya, and Dharmender K. Gahlot. 2023. "Multi-Omics Approaches in Plant–Microbe Interactions Hold Enormous Promise for Sustainable Agriculture" Agronomy 13, no. 7: 1804. https://doi.org/10.3390/agronomy13071804

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