Plant beneficial microorganisms

Types of PBM

PBM are known as microorganisms that can increase plant establishment, growth and development, and defend plants across disease and abiotic stresses. PBM mainly include PGPB, arbuscular mycorrhizal fungi (AMF), and rhizobia.

Plant growth-promoting bacteria

The most PBM present in soils are PGPB such as Azospirillum ,Azotobacter , Pseudomonas , and Bacillus , which are bacteria capable of inducing growth and development of plants and protecting plants against phytopathogens (Rocha et al. 2019b). PGPB increase plant tolerance to environmental stresses and facilitate plant growth through direct and indirect mechanisms. Direct mechanisms by PGPB include expanding root growth, fixation of atmospheric nitrogen (Bloch et al. 2020), solubilization of mineral nutrients (e.g., phosphate, potassium) (Adnan et al. 2020), and production of phytohormones (e.g., auxins, cytokinins, and gibberellins) (Sudewi et al. 2020), iron-chelating siderophores (Kramer et al. 2020), and organic acids. Indirect mechanisms can be neutralized or modify the harmful effects of plant pathogens by producing various antagonistic compounds, such as extracellular lytic enzymes, hyperparasitism, antibiotics, siderophores, and hydrogen cyanide (Emmanuel and Babalola 2020).Bacillus sp. such as B. amyloliquefaciens , B. subtilis , and B. sphaericus can breed resistance in plants against viral diseases (e.g., cucumber mosaic virus on tomato) (Kloepper et al. 2004).

Arbuscular mycorrhizal fungi

In agricultural and natural ecosystems, as biologically beneficial fungi, AMF can create an interaction of physical between plant roots and soils, which represent an essential part of agricultural ecosystems (Khan 2005). Nearly 90% of AMF can form symbioses with plant roots (Ortas and Bykova 2018, Paravar et al. 2022), contributing significantly to increasing plant uptake of macro and microelements in soils under environmental stress (Ghanbarzadeh et al. 2020) and to improving soil density to create a protective barrier from pathogens and enhance water acquisition (Rocha et al. 2019a). AMF can also protect crops against environmental stresses (Langeroodi et al. 2020). For instance, under drought stress, AMF may increase plant water uptake and turgor maintenance associated with osmotic balancing, and root hydraulic conductivity (Langeroodi et al. 2020, Zou et al. 2020). Overall, AMF play a beneficial role in producing metabolites such as essential oil (Pirzad and Mohammadzadeh 2018), fatty acids (Rahimzadeh and Pirzad 2019), phytohormones (Kadam et al. 2020), amino acids (Zhang et al. 2020), antioxidant enzymes (Piri et al. 2019, Zou et al. 2020), and adjusting plant physiological statuses such as carbon dioxide exchange amount (Thirkell et al. 2020), stomatal conductance (Boutasknit et al. 2020), photosynthetic pigments, proline content (Alam et al. 2019), and phenolic content (Bencherif et al. 2019). It has been demonstrated that AMF can enhance photosynthesis activities and stomatal movement by developing the root systems (Gholinezhad and Darvishzadeh 2021). Indeed, root colonization by mycorrhizal mycelium not only bolsters the root systems but also facilities the absorption of water and nutrient from larger soil volumes against drought stress (Paravar et al. 2021). Additionally, a raised nutrients uptake especially phosphorous by developing root system can provide the essential ATP and NADPH, which support oil and fatty acids biosynthesis (Rezaei-Chiyaneh et al. 2021). Some researchers reported that AMF can decrease the accumulation of ROS by increasing flavonoids, carotenoids, anthocyanins, and phenols under water deficit (Jerbi et al. 2022).
Other beneficial microorganisms are Trichoderma(Coninck et al. 2020) which can be applied as biological control generalists of plant diseases and pathogenic fungi with a well-shielded cropping system (Yang et al. 2017). They can control pathogens by absorption of released nutrients (known as mycoparasitism) (Kim et al. 2021), production of antibiotics (e.g., aldehydes, alcohols, ketones, hydrogen cyanide, and heterocyclic nitrogen) (Daryaei et al. 2016), and generation of degrading enzymes (e.g., crystalline cellulose-hydrolyzing enzyme and b-glucosidase) in the cell wall (Kthiri et al. 2020). Trichodermaspecies can colonize the rhizosphere at the critical “early germination” stage, contributing significantly to improving nutrient uptake and plant resistance to various stresses (e.g., heavy metal, salt, and drought stresses) (Lutts et al. 2016) and they can serve as usual fungi of soil and rhizosphere to replace chemical seed treatment (Kthiri et al. 2020).

Microbial consortia

Association between microorganisms and host plants can keep soil fertility and plant health, especially in low-input agriculture, which depends on biological prices than agrochemicals (Sessitsch and Mitter 2015). Indeed, in the microbial consortium, microbial species can perform synergistic interaction and give benefit each other. Some strains can maintain the non-producing strains against drought stress by producing secondary metabolites, such as exopolysaccharides (Lau et al. 2022). A study showed that microorganisms belonging to the roots of grapevine and olive plants can improve the growth of Orize sative L. This enhancement may be due to the extensive roots system and increased water uptake ability (Yoolong et al. 2019). In addition, it has been found that using humic acid and PGPR (B.megaterium andB. subtilis ) enhanced the plant height and yield compared with untreated control. Indeed, Humic acid and PGPR enhanced the photosynthesis process by promoting stomatal conductance and stomatal density, thereby, improving the yield (Ansari et al. 2019). Also, it has been reported that the application of PGPB and N-fixing bacteria caused the improvement of root growth and resilience of plants against environmental stresses, as well as decreased N losses (Dal Cortivo et al. 2017) PGPB can be used in the formation of ameliorating nodules in legumes when co-inoculated with rhizobia (Rocha et al. 2019a). It has been found that Bacillus polymyxa andAzospirillum brasilense increased root colonization byGlomus aggregatum , and promoted biomass and phosphorus amount of palmarosa grass grew under irresoluble inorganic phosphate source (Oliveira et al. 2017).

PBM inoculation on plant growth

Nutrients

Mixed or separate microorganisms can be inseminated within leaves, seeds, seedlings, roots, or soils. These inoculations cause the colonization of the rhizosphere or the inside of the plant, as well as, growth and toleration across abiotic stress stimulation (Lopes et al. 2021). PBM inoculation directly improves plant growth and productively, tolerance to abiotic stresses (e.g., drought, salt, and extreme temperatures) by increasing nutrient uptake, producing exopolysaccharides, osmoregulators, and antioxidants, regulating phytohormones (e.g., auxin, gibberellin, cytokinin, abscisic acid, and ethylene) (Lichtfouse et al. 2009) and/or indirectly protect plants against abiotic stresses by inducing systemic resistance, as well as producing siderophore and volatile metabolites (Abhilash et al. 2016). Due to the increase in reactive oxygen species (ROS) production, peroxidation of lipids, free radical accumulation and elevated ethylene production, plant growth is inhibited during drought stress. Hence, the above events resulted in cell death and decreasing in photosynthetic rates and chlorophyll content. Also, PBM inoculation can positively affect germination indices of seed, seedling and early growth characteristics, root development and improve crop biomass and productivity (Moradtalab et al. 2020, Sharma et al. 2012).
It has been proved that PBM can be used as biofertilizers to increase the stock of macro and micro-elements, boost plant growth and decrease the application of chemical fertilization (Ghanbarzadeh et al. 2020). Since the essential nutrients for plants mainly include nitrogen, phosphorus, and iron, among PBM selection tests, nitrogen fixation, phosphate solubilization, and siderophore production are widely investigated (Lopes et al. 2021). One of the essential macro-elements for synthesizing proteins and nucleic acids is nitrogen. It has been reported that PGPB strains such as Azospirillum ,Azotobacter , Achromobacter , Rhizobium andKlebsiella can fix biological nitrogen via decreasing nitrogen gas (N2) to ammonia (NH3) (Souza et al. 2015). Moreover, phosphorus is an urgent plant nutrient for growth, which participates as a structural ingredient of nucleic acids, phospholipids, and adenosine triphosphate (ATP) (Khan et al. 2009, Maleki Farahani et al. 2019). Some PGPB strains such as Rhizobium , Bacillus , Pseudomonas ,Azotobacter , and Azospirillium can dissolve phosphate and convert insoluble organic and inorganic phosphate into available plant form, which are called phosphate-solubilizing bacteria (PSB)(dos Santos et al. 2020;. Organic acids (gluconic or keto-gluconic acids) produced by PSB along with their carboxyl and hydroxyl ions chelate cations and reduce pH to release phosphorus (Sharma et al. 2013). Furthermore, PGPB act a main role in metabolic and biochemical pathways, especially for biological nitrogen fixation and photosynthesis (Richardson and Simpson 2011). It is known that large proportions of soil-phosphorus remain interlocked in various insoluble forms and are unavailable for plants. PBM can decrease soil pH through execration of organic acids such as gluconate, citrate, lactate, and succinate that leads to the acidification of the surroundings and microbial cells, therefore, phosphorus ions are released by substitution of H+ for Ca2+ (Martínez-Viveros et al. 2010). In addition, iron is one of the essential micro-elements for the biosynthesis of chlorophyll, photosynthesis, and respiration. As a chelator, siderophores have a great specificity to bind iron, continued by the transport and deposit of Fe3+ in bacterial cells (Dimkpa et al. 2009).Burkholderia , Enterobacter , Grimontella , andPseudomonas can be used as siderophore producers to promote plant nutrition and inhibit phytopathogens via sequestration of free environmental iron (Souza et al. 2015).

Phytohormones

Phytohormones are organic compounds that are responsible for plant development. PBM can modulate phytohormones, such as auxins, cytokinins, gibberellins, abscisic acid, ethylene, salicylic acid, brassinosteroids, jasmonates, polyamines, and strigolactones (Santner et al. 2009). A study reported the increased auxin and gibberellin in leaves of Zea maysinoculated by PGPB (Khan et al. 2016). The negative effects of drought, chilling, heat, or salinity stress can be alleviated by PBM inoculation via auxin production, gibberellin, cytokinin, ACC deaminase, abscisic acid strigolactones, and jasmonates (Khan et al. 2020). It has been demonstrated that PBM inoculation increased auxin concentration in plants and improved the growth of various plant species (e.g., Zea mays , Brassica juncia , Fagopyrum esculentum , andSaccharum officinarum ) by improving uptake of water and nutrient (Gouda et al. 2018). The auxin produced by PBM is a beneficial phytohormone that regulates cell division (Sarkar et al. 2017). PBM can improve plant-related parameters (e.g., seed germination, development of leaves, stem, flower and fruit) by enhancing gibberellin (Zerrouk et al. 2020). Under saline conditions, PBM inoculation can increase the concentrations of abscisic acid, jasmonates, and brassinosteroids in plants (Arora et al. 2020).

Exopolysaccharides

Microorganisms can form a productive biofilm on the root surface by producing exopolysaccharides (Banerjee et al. 2019). In this way, this mechanism causes the increase of water keeping in soil particles and maintains soil moisture in the rhizosphere. In addition, Streptococcus epidermidis can protect the cells of plant roots against osmotic stress and enhance environmental stress tolerance (Banerjee et al. 2019). It was suggested that Pseudomonas putida strain GAP-P45 as an exopolysaccharide producing bacterium can cause the biofilm formation on the root surface in Helianthus annuusseedlings and increase tolerance of seedlings against drought stress (Naseem et al. 2018). In addition, other studies have demonstrated that proline accumulation, sugars and free amino acids increased in plants inoculation by exopolysaccharides producing bacterium Pseudomonas aeruginosa andAzospirillum spp. under drought stress (Bano et al. 2013, Gusain et al. 2015, Rana et al. 2020).

Antioxidants

The PBM can enhance antioxidant enzymes activities such as ascorbate peroxidase (APX), catalase (CAT) and superoxide dismutase (SOD), and antioxidant non-enzymes such as glutathione (GSH), carotenoids, tocopherols, and phenolics to alleviate ROS accumulations that are caused by various stresses (Fazeli-Nasab et al. 2021, Gouda et al. 2018). Increased activity of CAT and APX due to inoculation of Cuminum cyminum seeds with Pseudomonas fluorescens and Trichoderma harzianum under drought stress conditions has been reported (Piri et al. 2019). Linum usitatissimum inoculation with P. fluorescens enhanced antioxidant enzymes such as CAT, APX, and GSH in storage conditions (Gafsi et al. 2006).

Osmoregulants

Against drought and salinity stresses, microbial inoculants can produce osmoregulants such as carbohydrates, proteins, amino acids lipids, proline, glycine betaine, and trehalose (Van Oosten et al. 2017). Osmoregulants induce the stabilization of protein and membrane structure under dehydration conditions, maintain osmotic balance across the membrane, and ensure protein correct folding under salinity stress (Sharma et al. 2012). It has been found that Burkholderia phytofirmans . can increase plant tolerance across low temperatures by modifying carbohydrate metabolism (Fernandez et al. 2012). Also,Pseudomonas fluorescens has been found to promote plant tolerance against water stress by enhancing catalase and peroxidase enzyme activities and proline accumulations (Saravanakumar et al. 2011).

Inoculation methods of PBM

Different methods of PBM inoculation on host plants can affect the survival and reproduction of microbes crowded into the rhizosphere and their ability to promote plant growth (Strigul and Kravchenko 2006). Due to the fact that the mobility of microorganisms in the soil is low, microbial inoculants should be placed in the vicinity of the rhizosphere. To spread microbial inoculants around the rhizosphere, nematodes can be used as a vector for their inoculation (Msimbira and Smith 2020). Except for inoculant density and methods of inoculation, the response of the plant to PBM inoculation and their colonization is also important for microbial functioning (Venturi and Keel 2016). After inoculation, the reduction of microbial population in the rhizosphere may be due to unadapted microorganisms to their new environment. However, root exudations play a critical role in microbial growth. Besides, biotic and abiotic factors can also affect the functional variety of microbial populations (Strigul and Kravchenko 2006). Microbial inoculation can be carried out with a single isolate or microbial consortia (e.g., co-inoculation). It was found that co-inoculation improves the efficiency of inoculation and plant development (Lopes et al. 2021). Different methods including seed, soil, root, and foliar inoculation are used to inoculate plants with PBM (Fig. 1; Table 1).
Table 1. Effects of different methods of PBM inoculation on plant growth