The role of rhizosphere microbes as phosphate solubilizing bio fertilizers in shallot: a review

Crops need nutrients to grow, develop, and produce yields, both in macro and micronutrients form. One of the essential macronutrients is phosphorus (P). Phosphorus is required by plants to produce plant biomass. Andisols are often used as agricultural lands in the highlands of the tropics. This soil type has high P retention and low available P. Andisol contains clay minerals with up to 97.8% P-retention. Therefore, this condition led to low P availability, but high total P in the soils. There was a tendency to increase the dose of inorganic fertilizers, especially P fertilizer in this area. A survey reported that shallot Andisol farmers applied P fertilizer about five times of shallot recommendation rate, however, the production has not increased, yet. The high rate of chemical fertilizers causes land degradation and environmental pollution. One of the solutions to increase phosphorus availability is by improving P solubility which increases P uptake by plants. Increasing P solubility is environmentally friendly and can be done by utilizing phosphate-solubilizing microbes which are often found in the plant rhizosphere. The use of phosphate-solubilizing microbes for plants today can be found in bio-fertilizers. This method could maintain soil health and give a good impact to the plant growth and production. This review would determine the use of phosphate-solubilizing microbes to manage P deficiency in Andisol soils. Some study cases about the effect of phosphate-solubilizing microbes on plant performances would also be addressed. Currently, it is hoped that farmers will begin to implement environmentally friendly agriculture by giving phosphate-solubilizing bio fertilizers to escalate available P and production.


Introduction
The shallot is a seasonal vegetable plant with an edible part of almost 90%.Shallots are widely used by Indonesian people as a spice for various types of dishes [1].Shallot cultivation has spread widely, at first it was only cultivated in the lowland areas [2,3] but spread to the highlands and almost all provinces in Indonesia.At present, shallots are a vegetable commodity with the largest area, with an area of 186,900 ha [4].Indonesia's shallot production in 2021 is 728.6 tons, with an import volume of 174 tons and an export volume of 26 tons.Along with the increasing population of Indonesia and the high rate of land conversion in shallot production centers, especially in Java, the productivity of shallots needs to be continuously increased to be able to meet increasing domestic demand [5].Increasing the productivity of vegetables can be done with the right cultivation techniques, one of which is the proper management of nutrients, namely through fertilization.
Plants need the essential nutrients (macro and micro) in their growth.Phosphorus (P) is needed in sufficient quantities to be able to the support plant growth [6], this causes using the inorganic phosphate fertilizers widely used by farmers for optimal crop production [7].The element P is plenty in the soil, but its availability is low because most of it is in an insoluble form.The P availability in the soil is only about 1/10 % of the total P for plants [8].Mehta et al [9] argued that although the reserves of P in soil are large, their availability is very low due to the fixation reaction process that occurs in the biogeochemical cycle.energy of phosphorus, suggesting an increase in the retention and fixation of phosphorus in these soils [22].This condition led to low P availability in Andisol soils.
Allophane is a prominent mineral with short-range-order (SRO) found in Andisols [24].The quantity of phosphate sorbed on allophane is greater compared to other minerals like goethite and ferrihydrite, potentially attributed to its unique surface properties.The adsorption mechanism involves rapid and robust binding of phosphate to defect sites, followed by feebler attachment and ultimately the interference of the allophane structure accompanied by the formation of aluminum phosphates (Alp) through precipitation [25].
Andisols originating from volcanic ash minerals possess a notable capacity to retain phosphorus (P), commonly referred to as P retention capacity (PRC).The PRC value of allophonic soils was correlated with acid ammonium oxalate extractable (Alox), while in non-allophonic soils the concentration of pyrophosphate-extractable Al (Alp) was correlated to the PRC value.Moreover, the relationship between organic matter (OM) and PRC was linked to the presence of organically bound aluminum (Al) in allophonic soils.This was due to the indirect influence of Alp on the PRC through the presence of OM [26].The effect of organic matter shows on the discharge of organic carbon that accounted for 40% and 83% of the absorbed phosphorus on a molar basis in two Andisol soils [27].
In nature, the phosphorus availability in Andisol is commonly low to medium.Marpaung et al [11] argued that the availability of P in Andisols in Berastagi, Karo regency, North Sumatra was medium at 10,70 ppm and the P-total was high at 279.45 mg 100 g -1 .Mindawati et al [28] argued that the Pavailability of Andisols in Cikole, Lembang, West Java was 8.5 cmol (+) kg -1 and the value increased due to tree plantation up to 13.4 cmol (+) kg -1 .Moreover, Sopha [29] reported that P-availability in Andisol soils was close correlated to soil pH.Andisol-Bayongbong soils had higher pH and Pavailability compared to Andisol-Pacet soils.Moreover, soils used for intensive horticulture enriched with horse manure had a lower phosphorus fixation, higher phosphorus availability and pH levels, and greater concentrations of exchangeable base cations like calcium, magnesium, and potassium as micronutrients like zinc, manganese, and copper [30].
Management of Andisols can be directed at reducing the high adsorbed P. Dissolving P in Andisol soil can be done in various ways including by utilizing rhizosphere microbes, namely phosphate solubilizing microbes, and applying organic matter.

Rhizospheric Microbes
Soil microbes are one of contributing actors to maintain and increase the soil biological, chemical and physical fertility.These organisms, including fungi, bacteria, archaea and protozoa, can bring many meaningful services in the soil ecosystem.They are involved in nutrient cycling, nutrient transformation, organic matter content decipherment, aggregation of soil, soil respiration, and the pathogens elimination, which is essential for sustainable agriculture and food production.Without these microbes, nutrients would remain locked up in organic matter and unavailable to plants, leading to nutrient deficiencies and reduced crop yields [31,32].
The interactions between soil microbes and plants are complex and reciprocal.In terms of chemical site, the available of nitrogen, potassium and phosphorus can be increased by the soil microbes' performance.They change organic matter into some essential available nutrients.In addition, soil microbes contribute to the soil physical fertility, for example, the structure of the soil, water-holding capacity, and stability.These microbes are required in the arrangement of soil aggregates too, by bounding the clusters of soil particles with microbial secretions and organic matter [33].In addition, soil microbes can fix atmospheric N, decay the plant residues and organic wastes, detoxify pesticides, plant disease and suppress the pathogens of soil-borne.
The rhizosphere is around plant roots which are the habitat for microorganisms and the exudation of plant roots [34].The rhizosphere region also has high microbial activity when compared to the nonrhizosphere region [35].The diversity of soil microorganisms in rhizosphere depend on some factors as well as, species of plant, stage growth of plant, and soil type [36].The nutrients availability in the rhizosphere which is needed by plants is undoubtedly influenced by the microorganisms' composition 1255 (2023) 012003 IOP Publishing doi:10.1088/1755-1315/1255/1/0120034 [37].The physiological activity of rhizosphere microorganisms contributes to the nutrient uptake, properties of soil, and growth significantly [38].
Soil microbes was found in the rhizosphere include fungi and bacteria.Rhizosphere fungi are capable to upgrade plant resistance to soil-borne and airborne diseases [39].Entophytic fungi are generally symbiotic with their host plants.This fungus provides some advantages to host plants, among others, by increase growth rates, and increase resistance to diseases, pests, and drought.Among the species of soil fungi, some benefit plants, and some act as plant diseases [40].
Fungi in the rhizosphere are classified as plant fertility-promoting fungi (bio fertilizers) because they have two main roles, i.e. cover plants against pathogens and increase the soil fertility.Rhizosphere fungi produce bioactive metabolites which be able support plant growth, namely Indole Acetic Acid (IAA).The phytohormone auxin is an IAA that is often found in nature and can be classified as exogenous and endogenous IAA. [41].The exogenous IAA which is produced by rhizosphere fungi are able to increase the plant growth by spurring the differentiation process in roots by generate the root hairs.Some of fungi that can generate the auxin are Aeschynomene, Collectrichum gloeosporioides, and Phanerochaete chysosporiumi.According to [42] Fungi can produce IAA as a secondary metabolite that acts as a growth regulator, for example, Penicillium sp [43].The results of the study [44] found Aspergillus, Penicillium, Mucor, and Trichoderma in the rhizosphere of the honey citrus plant.While research [45] on shallot cultivation found Aspergillus, Penicillium, Paecilomyces, and Trichoderma.
Bacteria also found in the rhizosphere.Indigenous bacteria from the genera Azotobacter, Bacillus, Acinetobacter, Pseudomonas, and Azospilium are some of the microorganism in the soil and also plants, which are often found at the roots and base of stems.Commonly, these four bacterial genera have been implemented as Plant Growth Promoting Rhizobacteria (PGPR) to enhance plant growth through their benefits on phosphate dissolution, nitrogen fixation, and phytohormone formulation [46,47,48]; and to reduce the disease attacks caused by soil pathogens [49,50,51].
Microbes that are commonly used as active ingredients in bio fertilizers are nitrogen-fixing microbes and phosphate solvents.Some of the bacteria identified to be able to fix N2 are Azotobacter sp., Azosprillum sp., and Beijerinckia sp.[52].Azotobacter is a free-living aerobic bacterium that is predominantly found in soil.Some research results show a positive effect of inoculation of Azotobacter sp. in various plants [53,54,56].Another study showed that Azotobacter is not only effective for nitrogen fixation but can also produce growth hormones, fungicides, and siderophores, and is able to dissolve phosphates [56].Phosphate-solubilizing microbes in the soil consist of fungi and bacteria.According to Chen et al [57], the types of phosphate-solubilizing bacteria that are able to dissolve P in soil are Achromobacter, Bacillus, Aerobacter, Enterobacter, Pseudomonas, Flavobacterium, and Rhizobium.Meanwhile, the types of phosphate-solubilizing fungi include Alternaria, Aspergillus, Rhizoctonia, Penicillium, and Fusarium [58].
In addition, vesicular-arbuscular mycorrhizal fungi (MVA) are also soil microorganisms that can help to increase plant growth too.MVA fungus has a very wide distribution, that is, almost 90% of plants are in symbiosis with MVA fungi.This fungus is able to provide nutrients for its host plants, especially phosphorus (P) and nitrogen (N) [59], and reduce plant abiotic stress [60,61].Hiesalu et al [62] also reported that there was a significant correlation between plant species richness and AM fungi associated with roots in grassland vegetation.

Phosphate solubilizing microbes
Phosphorus exists in a variety range of inorganic and organic forms; nevertheless, it is not available to plant due to adsorption, precipitation, or both [63].Phosphate solubilizing microbes produce substances such as organic acids, mineral acids, siderophores to solubilize insoluble phosphate minerals and release ions such as PO4 -3 , HPO3 -2 , and H2PO4 -1 [64,65,66].Insoluble phosphate can be dissolved and mineralized by bacteria, fungi, actinomycetes, and algae.The use of phosphate-dissolving microbes is an approach with the principles of sustainability and environmental friendly in managing P deficiency in agricultural soil [1,67].The fundamental process for dissolving phosphate minerals in soil is the creation of phosphatase enzymes and organic acids [68].
Organic phosphorus in soil was found predominantly as inositol phosphate or phytate [78].Organic phosphorus is also found in xenobiotics such as detergents, insecticides, antibiotics, and flame retardants.The majority of these organic molecules have a high molecular weight and are chemically robust.These molecules must be transformed into H2PO4 − , HPO4 -2 , and Pi for plant uptake [79].Phosphate solubilizing microorganisms secreting enzymes are involved in the phosphate mineralization process such as phosphatases and phytase [80,81,85].Acid phosphatases have been found to solubilize phosphate and some species of Burkholderia, Citrobacter, Enterobacter, and Pseudomonas produces this enzyme [82,83,84].Phytase is another enzyme involved in the mineralization of organic phosphorus.Pseudomonas mendocina, Aspergillus niger, Aspergillus terreus, produces phytase for solubilizing phosphate [85].More over according to Kalayu [67] Streptomyces spp.produce phosphoesterases, phosphodiesterases, phytases, and phospholipases.

The role of microbe's phosphate-solubilizing in soil and plants as bio fertilizer.
The accumulation of phosphorus occurs in intensive fields [86] such as shallot fields in Brebes [87].According to Penn and Camberato [88], the available of P fertilizer to plant only 25-30%, the rest becomes unavailable to plants.As the result, the P potential is high while the availability of P for plant is low [89].As well as impacts on the environment such as eutrophication and soil salinity [90].According to Walpola and Yoon [91], the potential P in agricultural land is able to maintain production for up to 100 years.On the other hand, the decreasing availability of P-source mining materials requires P-dissolving microorganisms capable of converting P potential to become available for plants.
Based on Istina et al [92] the indigenous phosphate solubilizing microbe Burkholderia gladiola and Penicillium aculeatum can increase the soils P nutrient content.The other phosphate solubilizing bacteria Bacillus sp, can dissolve phosphate qualitatively [93], which can escalate the nitrogen and phosphate availability of soils, are B. Subtilis, B. amyloliquefaciens, B. pumilus [94] and B. mycoides [68].Other bacteria in increasing N and P uptake in maize are Bacillus amyloliquefiniens [95].This is supported by Ulfiyati and Zulaika [93] to dissolve phosphate qualitatively using the Bacillus genus.
Phosphate solubilizing microbes are beneficial to soil growth and quality.Several studies stated that phosphate-solubilizing microbes used as biofertilizers and biocontrol for crops and soil improvements [96,97].
The availability of P increases through the application of organic acids and phytase enzymes which are able to dissolve soil P. Release of organic acids and phosphatase and phytase enzymes present in various soil microorganisms through increasing the solubility of insoluble phosphate compounds by phosphate solubilizing microorganisms especially phosphate solubilizing bacteria [100].

Plant growth promotor
Another advantages of phosphate solubilizing microbes is the ability to produce phytohormones such as production of siderophores, gibberellin acid (GA3) and Indole Acetic Acid (IAA), and antagonist against pathogens [98,101].Phytohormmones and siderophores can improve plant growth and production.It is powered by Kim et al [102] that the B. amyloliquefaciens strain excreted gibberellin and its phosphate solubilizing ability could contribute to increased plant growth.The bacteria which act as growth promoter of rhizobacteria adalah Bacillus cereus which is characterized by the growth of shallots [103].Bacillus and Paenibacillus spp.Is PGPR strains that produce IAA [104].
Plant P uptake is closely related to available in the soil.Plants are able to absorb available P and increase plant P uptake when available soil P is high [105].For example, the increase in the number and weight chickpea seeds is due to an increase in available P [106].Other evidence is an increase in height, fresh and dry weight of shoots, as well as the number of fruits compare to control due to application of phosphate solvent Burkholderia ambifaria and B. Tropica [107].Furthermore, the number of flowering shallots and seed weigh per plot increase through the application of PSB inoculation [108].In addition, phosphate-solubilizing bacteria can also increase organic matter and improve the absorption of element P [57].Pseudomonas sp.Wheat Increase growth and P avaibility [113] Pseudomonas aeruginosa Chili Increase growth and P avaibility [114] Pseudomonas fluorescens Bulbs of sugar beetroot Influence of metabolites of growth rate index [115] Aspergillus niger Aspergillus niger TMPS1 Wheat Improve soil P availability and promote plant growth [116,96] Aspergillus niger and Penicillium brevicompactum

Antibiotics
The role of phosphate solubilizing microbes apart from being a plant growth promoter also plays a role in the biocontrol of several phytopatogens in plants.Pathogens that can attack plants can reduce crop yields and reduce food quality, due to unhealthy plants growing and developing.Control that has been carried out so far by using chemicals that are careless has an unfavorable impact.One alternative is the use of biological agents as biocontrol in protecting plants from pathogens [120,121].Some of antibiotics produced by phosphate solubilizing microbes such as Streptomyces spp., Stenotrophomonas spp., Bacillus spp., and Pseudomonas spp., are fengycin, iturin, xanthobaccin, kanosamine, zwittermicin, oligomycin [122,123].According to Raaijmakers and Weller [124], Pseudomonas produces the antibiotic 2,4-diacetylphloroglucinol which is able to suppress phytopathogenic infestations through host induction and root colonization in wheat.Other bacteria that play a role in inhibiting the growth of mycelia in rice panicles are Bacillus amyloliquefaciens [125], Antagonist against the brown root rot pathogens is Tricoderma citrinoviride, T. viride, T. harzianum, and A niger [126], biocontrol of Salicaceae endophytes against soil-borne plant pathogens are Pseudomonas, Burkholderia, Curtobacterium, and Rahnella [127].
Bio fertilizer of P solvent is a fertilizer enriched with beneficial microorganisms and growth regulators which function to overcome land degradation [128,129], able to increase shallot production and activity phosphomonoesterase enzymes by increasing the population of bacteria in the rhizosphere [130].Penicillium, Pseudomonas, Flavobacterium, Bacillus, Micrococcus, Fusarium, Aspergillus, and Sclerotium are P-solvent microbes [131] which can be isolated from cassava and sunflower skin waste which produce the fungi Aspergillus flavus, A. niger, Enterobacter, and Burkholderia [132,133].Modification of rhizosphere through a combination of agronomy, nutrient management, use of organic and biological fertilizer, and regulation of rhizosphere processes can increase soil sustainability and nutrient efficiency [134].
The increase in plant dry weight and tuber production was able to reach 14 t/ha with the application of a combination of manure and biological fertilizers [135].Other research has shown an increase in the rate of germination, optimal growth, and production of shallots > 20 t/ha through the application of growth regulators in the form of organic fertilizers [136,137].According to Husein et al [138] that the use of bio fertilizers in Indonesia is increasing where ≥ 50% are available in agricultural shops in Bandung and Semarang.This shows that the big opportunity in the development of bio fertilizers has future market opportunities.

Conclusion
Phosphorus is required by plants to produce plant biomass.Andisols are often used as agricultural lands in the highlands of tropics.This soil type has high P retention and low available P. Andisol contain clay minerals with P-retention up to 97.8%, therefore, this condition led to low P availability.Increasing P solubility with environmentally friendly can be done by utilizing phosphate-solubilizing microbes which are often found in plant rhizosphere.In the rhizosphere area of plants are found many useful microbes, including the microbes of phosphate-solubilizing.Phosphate solubilizing microbes have a beneficial role for plants.The role of phosphate solubilizing microbes includes being able to dissolve phosphate bound in the soil such as Andisols into dissolved P thru the production the phosphatase enzymes and organic acids Phosphate solubilizing microbes are also capable of producing growth regulatory hormones which help plants to produce better growth and yields.Another role is that phosphate solubilizing microbes are also capable of producing antibiotics that are able to control pathogen attacks on plants so that plants become healthier.Using the microbes of phosphate-solubilizing in plants as biofertilizers has a very positive effect on maintain soil health, plant growth and yield which also supports sustainable agriculture.

Table 1 .
The role of phosphate solubilizing microbes on plant