Synergistic Interactions of PGPR and AM Fungi in Enhancing Crop Productivity – A Winning Microbial Combination
Gomathy Muthukrishnan1, Sabarinathan Kutalingam Gopalasubramaiam1*, Priya John2, Ananthi Karuppaiah3 and Dilip Saikia4
1Agricultural College and Research Institute, Tamil Nadu Agricultural University, India
2Navsari Agricultural University, India
3Agricultural College and Research Institute, Vazhavachanur, India
4Silapathur College, India
Submission: April 25, 2024; Published: May 10, 2024
*Corresponding author: Sabarinathan Kutalingam Gopalasubramaiam, Agricultural College and Research Institute, Tamil Nadu Agricultural University, India, Email ID: sabarinathan@tnau.ac.in
How to cite this article: Gomathy M, Sabarinathan K G, Priya J, Ananthi K, Dilip S. Synergistic Interactions of PGPR and AM Fungi in Enhancing Crop Productivity – A Winning Microbial Combination. Int J Environ Sci Nat Res. 2024; 33(3): 556365. DOI: 10.19080/IJESNR.2024.33.556365
Abstract
Synergistic interactions between Plant Growth Promoting Rhizobacteria (PGPR) and Arbuscular Mycorrhizal (AM) fungi have been increasingly recognized as crucial contributors to enhancing crop productivity and sustainability. PGPR and AM fungi form mutualistic relationships with plants, promoting nutrient uptake, enhancing stress tolerance, and stimulating growth. Their combined application has shown remarkable effects on various crops, including increased nutrient acquisition, improved water-use efficiency, and enhanced resistance to biotic and abiotic stresses. This review explores the mechanisms underlying the synergistic interactions between PGPR and AM fungi and their implications for sustainable agriculture for improving crop productivity and reducing the environmental impact of conventional agricultural practices.
Keywords: Arbuscular Mycorrhizal fungi; PGPR; Mechanisms; Plant growth promotion
Introduction
Microbes that live in soil ecosystems are always closely associated with various plant systems; this relationship is known as a phytomicrobiome and the plant that is associated with microbes is called a holobiont [1,2]. Such relationship due to plant microbe interactions not only regulates microbial community but also plays vital role in the soil biogeochemical cycling. Microbes can survive in various environments including harsh conditions. They preferred to survive in the soil as it is rich in nutrients. The most suitable region for microorganisms in soil is the rhizosphere region where the nutrient availability is more and favourable for development of microorganisms [3]. It is a high nutrient zone where the presence of organic acids, amino acids, sugars, enzymes are more [4]. Plant growth-promoting rhizobacteria (PGPR), a group of microorganisms that live in the rhizosphere, are the main catalysts for enhancing soil fertility and nutrients, which produces amazing results in the area when compared to the bulk soil [5,6]. The bioformulation that contains good PGPR strains which helps in control of the plant pathogens and to increase the crop production. AM fungi also play a pivotal role in agriculture. AM fungi can explore larger volume of soil where plant roots cannot access and bring nutrients to the crop. AM fungi also help the plants to overcome biotic and abiotic stress of the environment. Combined inoculation of both PGPR and AM fungi can do marvelous tasks and helps for sustainable crop production. The present review article elucidates the synergistic interaction of PGPR and AM fungi for sustainable productivity.
PGPR
Root-releasing compounds have an impact on both microorganisms and plant growth. According to Uren [7], the root exudates, also known as rhizodeposits, contain phenolics, carbohydrates, fatty acids, amino acids, organic acids, sterols, putrescine, vitamins, and growth regulators that either attract or repel microorganisms. Rhizobacteria releases a variety of stimulants that help plants to absorb water and nutrients. It can directly assist plants for assimilation of nitrogen and phosphorus and alter the level of hormone and decrease population of bacterial pathogens [8]. Recent research showed that the growth of plants and productivity increased through the application of PGPR various conditions. In recent days more number of nonpathogenic rhizobacteria were monitored which improves the growth through the release of phytohormones such as auxins and cytokinin, siderophore production, act as biocontrol agent and promotes the induced systemic resistance of the host plant [9]. Both seed inoculation and foliar spray of B. megaterium PB50 significantly improved the plant growth under osmotic stress, protected plants from physical drought through stomatal closure, and improved carotenoid, total soluble sugars, and total protein content [10]. The production of phytohormones, such as indoleacetic acid (IAA), gibberellic acid (GA), abscisic acid (ABA), and cytokinin, hydrogen cyanide, siderophore and antagonistic activity against the foliar pathogens Pyricularia oryzae and Helminthosporium oryzae were evaluated and found as PGPR strains excelled well and showed its maximum potential [11].
Arbuscular Mycorrhizal Fungi (AMF)
AM fungi are one among the endomycorrhiza where the hyphae of the fungus not only grow inside the root of the plant, but penetrate the root cell walls, cortical cells and become enclosed in the cell membrane and forms arbuscles. The mutual association provides the plants to resist against many biotic and abiotic stresses through the metabolic pathways and increases the yield of crops by improving soil health, helps in uptake of nutrients and managing salt, moisture and nutrient stress in the environment. In plants, the AMF works against wide range of hosts through multi approach viz., change in root morphology, change in nutrition, activation of defense mechanisms, competes for colonization and photosynthates. AMF is considered as plant wealth/treasure in agriculture by the scientific community. In rice, various biotic stresses diminish the crop productivity mainly pathogens, insects etc., Among pathogens, soil borne diseases/pathogens were mainly managed by competing for nutrients and host whereas, other pathogens are managed mainly due to the interaction with host which stimulates/produces various plant growth hormones and chemicals such as strigolactones etc. Due to its multifaceted potential, AMF can be used as one of the tools for sustainable rice production. AMF play a vital role in nutrient management by providing rice with essential nutrient in its available form without superfluous application of fertilizers.
Mechanisms of PGPR
Antibiotic production
Antibiotic producing microorganisms are used directly in agricultural fields to fight against pathogenic microorganisms near plants or root surfaces. PGPR are the main antibiotic producing microorganisms and their secretions act as another method to chemical fertilizers and protect the plants from pathogens. They secrete lytic enzymes, bacteriocins and antibiotics [12] which kill or inhibit the pathogens. Bacillus and Pseudomonas produce antibacterial and anti-fungal agents such as subtilin, sublancin, TasA and subtilosin A that were ribosomal origin products and non-ribosomal peptide products namely, iturin, bacilysin, bacillaene, mycobacillin, Difficidin, chlorotetain, rhizocticins, lipopeptides, fengycin and surfactin [13].
Hydrolytic enzymes production
Biological control methods that incorporate enzymeproducing PGPRs have the potential to be a viable alternative to synthetic chemical methods, not only for effective plant pathogen management but also for the developement of a pollution-free environment. In host rhizosphere, a wide variety of PGPRs shows hyperparasitic activity against pathogens through secretion of several hydrolytic enzymes viz., proteases, lipases, cellulases, chitinases and 𝛽-1,3 glucanases, which disturb the cell wall of bacterial and fungal pathogens by acting on glycolytic linkages of prokaryote and eukaryote cell wall [14]. The lytic enzymes like lysozyme are bactericidal, fungicidal and nematicidal in nature. Extracellular enzymes viz., chitinases, 𝛽-1,4- glucanases, proteases, cellulases and xylanases secreted by PGPRs Bacillus sp. B. thuringiensis, B. atrophaeus and B. subtilis strain inhibit mycelial growth of fungal pathogens viz., Fusarium oxysporum, F. solani, R. solani, Botrytis cinerea [15,16].
Competition for niche
Rhizosphere region act as an important interphase between roots of plants and microorganisms, elucidated by different inorganic acids exudates by root surface i.e., sugars, vitamins, amino acids, organic acids, nucleosides, phenolic compounds and phytosiderophores. These nutrients act as chemical attractants for motile bacteria to migrate towards roots surface, providing niche to a diverse range of microorganisms, including pathogenic microbes [17]. In the rhizospheric region, competition for nutrients and physical occupation sites is an indirect mechanism utilized by competitive PGPRs against pathogenic microbes that depend on external sources [18].
Release of root exudates
Roots are able to release various chemical substances into the soil and it is known as root exudates. Roots regulating the soil microorganisms and change the physio-chemical properties of the soil and reduce soil plant pathogens. Root exudates are released by plants in two different forms. One through passive and the another through active secretions. The exudates are more in organic acids, amino acids, terpenoids, phenolic compounds, polyacteylenes, flavonoids, alkaloids, sugars, tannins, and secondary metabolites. Roots can secrete various types of proteins along with [19,20] higher molecular weight substances called as rhizo deposition that are released into the soil by plant roots that serve as nutritional source for rhizospheric microorganisms. Root exudates vary among the plant species, age and associated compounds [21].
Quorum sensing
Quorum sensing is an intercellular communication mechanism between bacteria, which is controlled by gene expression combined with cell concentration and facilitated by the diffusion of certain signal molecules such as N-acylhomoserine lactones (AHLs). It regulates expression of several phenotypes contributing bacterial pathogenesis in Psuedomonas syringae, Pectobacterium atrosepticum, Dickeya solani, Erwinia amylovora, Ralstonia solanacearum, Agrobacterium tumefaciens. In the rhizosphere region, certain PGPRs resists bacterial infections by adopting quorum-interrupting methods that interfere quorum sensing through enzymatic degradation of AHLs molecules, this mechanism is known as quorum quenching (QQ) and the PGPRs are known as QQ bacteria [22].
Siderophores production
Siderophores are less molecular weight (500-100Da) iron scavengers, that chelate iron from the environment and transport Fe3+ into microbial cell providing advantage to PGPR microbes [23]. When siderophores are released into the environment, they solubilize the iron and create an iron-siderophore complex that moves through the diffusion process until it reaches the cell membrane receptors of bacteria, where active transport takes place after recognition [24]. Bacterial siderophores are classified into four major classes they are phenol catecholates, carboxylate, pyoverdines and hydroxamates [25].
Indirect mechanisms
Induced resistance is defined as an improvement of the plant’s defense system against a broad spectrum of pathogens and pests that is acquired after appropriate stimulation. The induced resistance produced by an inducing substance upon infection by a pathogen is called Induced Systemic Resistance (ISR) or Systemic Acquired Resistance (SAR) [26]. The induction of systemic resistance by rhizobacteria is referred to as ISR, whereas that by other substances is called SAR [27]. Once resistance is induced it will afford non-specific protection against pathogenic microorganisms as well as against several insects and nematodes.
Systemic acquired resistance
The expression of phytohormones, which suppress invasive species, is the result of a number of actions triggered by pathogen or insect exposure. During SAR, resistance reactions occur in the non-infected parts starting from the infection site. At the place of attack, the plants respond to pathogen infection through the cell wall modification, production of phytoalexins, production of pathogenesis related (PR) proteins and activation of programmed cell death or hypersensitive reaction (HR) [28]. Plants use a variety of cues, including the sense of touch [29].
Mechanisms of AM fungi in enhancing crop growth
a) Changes in root growth and morphology: AM colonization induces notable changes in root system morphology, altering the dynamics of pathogens and modifying microbial populations, with the possible stimulation of microbiota components with antagonistic activity toward certain root pathogens. Different production of exudates in AMF roots can influence the microbiota composition.
b) Changes in host nutrition: the increased nutrient uptake resulting from AM symbiosis makes the plant more vigorous and consequently, more resistant, compensating for the loss of root biomass or function caused by pathogens.
c) Competition for colonization sites and photosynthates: both the AM fungi and root pathogens depends on host photosynthates, and they compete for the carbon compounds reaching the root. However, AM fungi have primary access to photosynthates, and the higher carbon demand may inhibit pathogen growth.
d) Activation of defense mechanisms: with AM colonization, the host plant produces a great number of phytoalexins, enzymes of the phenylpropanoid pathway, chitinases, b-1,3-glucanases, peroxidases, pathogenesis-related (PR) proteins, callose, hydroxyproline-rich glycoproteins (HRGP) and phenolics that can act in biological control.
e) Solubilization of minerals: Acidification of the rhizosphere due to organic acids secretion by the AM fungi makes the minerals to be available to the crops as solubilization and mobilization of minerals happens in the rhizospheric region [30].
f ) Sequestration of heavy metals: AM fungi inoculated plants produce lot of biomasses compared to uninoculated control plants [31]. Moreover, AM fungal hyphae release a super glue called glomalin that has the ability to sequester carbon and heavy metals [30].
Synergistic interaction of PGPR and AM fungi
Many researchers have noticed the synergistic interaction of PGPR and AM fungi and found a promising synergy between both the organisms on various plants. In Avena sativa, inoculation of Glomus intraradices and Acinetobacter sp showcased augmented growth even under hydrocarbon stress [32]. Devarajan et al. (2021) [33] noticed the combination of PGPR strains enhanced the drought tolerant nature of rice crop. [34] elucidated the role of Burkholderia on Sedum alfredii in heavy metal contaminated soil. Combination of endomycorrhizal mix and Pseudomonas species improved the nutrient uptake and growth of Zea mays [35]. Similarly iron absorption was maximum in Sorghum bicolor due to the AM fungi and PGPR [36]. In addition to that increased plant height was attained due to the synergistic influence of Funneliformis mosseae and PGPR inoculation [37]. Combination of these bacteria and fungus do wonders in remediation of contaminated sites making them as a promisible candidate to work under stress conditions [38]. This can address all types of soils with nutrient deficiencies and other contaminations and can able to go up to the level of bio fortification.
Changes in plant growth with colonization of PGPR and AM fungi
a) For phosphorous/nutrients acquisition from the soil: Helps in acquiring nutrients which are available in the soil by increasing the surface area with the mycelia.
b) Increased resistance to foliar pathogens: By triggering the defense mechanisms inside the host plant.
c) Increased drought and salt tolerance
d) Increased nutrient transfer from soil to the plants: By increasing the surface area with the help of mycelia and uptakes the nutrients through solubilization process.
e) Local resistance and systemic resistance to root pathogens: Because of the competition for colonization at the site of infection
f ) Soil health improvement, increased resistance to heavy metal toxicity: By fertilizing the soil, soil texture improves over the period of time.
g) Production of Plant Growth-Regulating Substances by the PGPR and AM fungi which provides induced systemic resistance and plant growth hormones. Through this systemic resistance is inhabited in host plants against plant pathogens, insect pests etc.
h) Combined inoculation of PGPR and AM fungi enhances the growth and yield of green gram than individual inoculation alone [39].
Conclusion
Through deeper understanding of the underlying mechanisms driving the positive interactions between PGPR and AM fungi could pave the way for more targeted and efficient applications. Efficient selection of PGPR and AM fungi untap the synergistic potential for specific plant types and environmental stress conditions. Deep insight into these associations further unlocks the hidden secrets in agricultural crops paving the way for sustainable agriculture.
References
- Bulgarelli D, Oter RG, Munch PC, Weiman A, Droge J, et al. (2015) Structure and function of the bacterial root microbiota in wild and domesticated barley. Cell Host & Microbe 17(3): 392-403.
- Smith DL, Gravel V, Yergeau E (2017) Editorial: Singalling in the phytomicrobiome. Frontriers in Plant Science 8: 611.
- Ahmed ST, Sweeney ST, Lee JA, Sweeney NT, Gao FB (2009) Genetic screen identifies serepin5 as a regulator of the toll pathway and CHMP2B toxicity associated with frontotemporal dementia. Proceeding of National Academic Science USA 106(29): 12168-12173.
- Ahemad M (2012) Implications of bacterial resistance against heavy metals in bioremediation: a review. Journal of Institute of Integrative Omics and Applied Biotechnology, pp. 39-46.
- Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: A review. Annals of Microbiology 60: 579-598.
- Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica (Cairo): 963401.
- Uren NC (2007) Types, amounts and possible functions of compounds released into the rhizosphere by grown plants. In: Pinton R, Varanini Z, Nannipieri P (Eds.), The rhizosphere, biochemistry and organic substances at the soil plant interface. Boca Raton, FL: Taylor Francis group, pp. 1-21.
- Walker TS, Bais HP, Grotewold E, Vivanco JM (2003) Root exudation and rhizosphere biology. Plant Physiology 132(1): 44-51.
- Van Loon LC (2007) Plant responses to plant growth-promoting rhizobacteria. European Journal of Plant Pathology 119: 243-254.
- Arun Kumar Devarajan, Sabarinathan KG, Gomathy M, Kannan R, Balachandar D (2020) Mitigation of drought stress in rice crop with plant growth‐promoting abiotic stress‐tolerant rice phyllosphere bacteria. Journal of Basic Microbiology 60(9): 768-786.
- Devarajan AK, Truu M, Gopalasubramaniam SK, Muthukrishanan G, Truu J (2022) Application of data integration for rice bacterial strain selection by combining their osmotic stress response and plant growth-promoting traits. Frontiers in Microbiology 13: 1058772.
- Leclère V, Béchet M, Adam A, Guez JS, Wathelet B, et al. (2005) Mycosubtilin overproduction by Bacillus subtilis BBG100 enhances the organism's antagonistic and biocontrol activities. Applied and Environmental Microbiology 71(8): 4577-4584.
- Sherathia D, Dey R, Thomas M, Dalsania T, Savsani K, et al. (2016) Biochemical and molecular characterization of DAPG-producing growth promoting rhizobacteria (PGPR) of groundnut (Arachis hypogea L.) Legume Research 39(4): 614-622.
- Santoyo G, Urtis-Flores CA, Loeza-Lara PD, Orozco-Mosqueda MDC, Glick BR (2021) Rhizosphere colonization determinants by plant growth-promoting rhizobacteria (PGPR). Biology 10(6): 475.
- Ni M, Wu Q, Wang J, Liu WC, Ren JH, et al. (2018) Identification and comprehensive evaluation of a novel biocontrol agent Bacilus atrophaeus JZB120050. Journal of Environmental Science and Plant Health Part B 53(12): 777-785.
- Jamali H, Sharma A (2020) Biocontrol potential of bacillus subtilis RH5 against sheath blight of rice caused by Rhizoctonia solani. Journal of Basic Microbiology 60(3): 268-280.
- Vacheron J, Desbrosses G, Bouffaud ML, Touraine B, Moenne-Loccoz Y, et al. (2013) Plant growth-promoting rhizobacteria and root system functioning. Frontiers of Plant Science 4: 356.
- Olanrewaju OS, Ayangbenro AS, Glick BR, Babalola OO (2019) Plant health: feedback effect of root exudates-rhizobiome interactions. Applied Microbiology and Biotechnology 103(3): 1155-1166.
- Stintzi A, Browse J (2000) The Arabidopsis male-sterile mutant, opr3, lacks the 12-oxophytodienoic acid reductase required for jasmonate synthesis. Proceedings of National Academy of Sciences, USA 97(19): 10625-10630.
- Stotz HU, Pittendrigh BR, Kroymann J, Weniger K, Fritsche J, et al. (2000) Induced plant defense responses against chewing insects. Ethylene signaling reduces resistance of Arabidopsis against Egyptian cotton worm but not diamondback moth. Plant Physiology 124(3): 1007-1018.
- Uren NC (2000) Types, amounts, and possible functions of compounds released into the rhizosphere by soil-grown plants. In The Rhizosphere; CRC Press: Boca Raton, FL, USA, pp. 35-56.
- Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proceedings of National Academy of Sciences 97(7): 3526-3531.
- Rajkumar M, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends of Biotechnology 28(3): 142-149.
- Ahmed E, Holmstrom SJ (2014) Siderophores in environmental research: roles and applications. Microbial Biotechnology 7(3): 196-208.
- Saha M, Sarkar S, Sarkar B, Sharma BK, Bhattacharya S, et al. (2016) Microbial siderophores and their potential applications: a review. Environmental Science and Pollution Research 23(5): 3984-3999.
- Hammerschmidt R, Kuć J (1995) Induced Resistance to Disease. Kluwer Academic Publishers, Dordrecht.
- Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizosphere bacteria. Annual review of phytopathology 36(1): 453-483.
- Sticher L, Mauch-Mani B, Métraux AJ (1997) Systemic acquired resistance. Annual review of phytopathology 35(1): 235-270.
- Hilker M, Meiners T (2010) How do plants “notice” attack by herbivorous athropods? Biological Reviews 85(2): 267-280.
- Gomathy, M, Sabarinathan, KG, Sivasankari, D, Pandiyarajan, P (2018) Arbuscular mycorrhizal fungi and glomalin–Super glue. International Journal of Current Microbiological and Applied Sciences 7(7): 2853-2857.
- Gomathy M, Sabarinathan KG, Thangaraju M, Subramanian KS, Sivashankari Devi T, et al. (2011) The effect of mycorrhizae inoculated maize root exudates in alleviation of chromiumtoxicity in chromium polluted environments. Insight Microbiology 1(2):20–30
- Xun F, Xie B, Liu S, Guo C (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environmental Science and Pollution Research 22(1): 598-608.
- Devarajan AK, Muthukrishanan G, Truu J, Truu M, Ostonen I, et al. (2021) The Foliar Application of Rice Phyllosphere Bacteria induces Drought-Stress Tolerance in Oryza sativa (L.). Plants 10: 387.
- J Guo, X Lv, H Jia, L Hua, X Ren, et al. (2020) Effects of EDTA and plant growth-promoting rhizobacteria on plant growth and heavy metal uptake of hyperaccumulator Sedum alfredii Journal of Environmental Sciences 88: 361-369.
- Dhawi F, Datta R, Ramakrishna W (2015) Mycorrhiza and PGPB modulate maize biomass, nutrient uptake and metabolic pathways in maize grown in mining-impacted soil. Plant Physiology and Biochemistry 97: 390-399.
- Mishra V, Gupta A, Kaur P, Singh S, Singh N, et al. (2016) Synergistic effects of Arbuscular mycorrhizal fungi and plant growth promoting rhizobacteria in bioremediation of iron contaminated soils. International Journal of Phytoremediation 18(7): 697-703.
- Li H, Qiu Y, Yao T, Ma Y, Zhang H, et al. (2020) Effects of PGPR microbial inoculants on the growth and soil properties of Avena sativa, Medicago sativa, and Cucumis sativus seedlings. Soil and Tillage Research 199: 104577.
- Mokarram-Kashtiban S, Hosseini SM, Tabari Kouchaksaraei M, Younesi H (2019) The impact of nanoparticles zero-valent iron (nZVI) and rhizosphere microorganisms on the phytoremediation ability of white willow and its response. Environmental Science and Pollution Research 26(11): 10776-10789.
- Gomathy M, Sabarinathan KG, Subramanian KS, Ananthi K, Kalaiyarasi V, et al. (2021) Rhizosphere: Niche for microbial rejuvenation and biodegradation of pollutants. Microbial Rejuvenation of Polluted Environment Volume 1: 1-22.