Revista Facultad Nacional de Agronomía - Medellín ISSN: 0304-2847 [email protected] Universidad Nacional de Colombia Colombia

Osorio Vega, Nelson Walter A REVIEW ON BENEFICIAL EFFECTS OF RHIZOSPHERE ON SOIL NUTRIENT AVAILABILITY AND PLANT NUTRIENT UPTAKE Revista Facultad Nacional de Agronomía - Medellín, vol. 60, núm. 1, 2007, pp. 3621-3643 Universidad Nacional de Colombia Medellín, Colombia

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A REVIEW ON BENEFICIAL EFFECTS OF RHIZOSPHERE BACTERIA ON SOIL NUTRIENT AVAILABILITY AND PLANT NUTRIENT UPTAKE

Nelson Walter Osorio Vega 1 ______

ABSTRACT

This paper is a review of the benefits of rhizosphere bacteria on plant nutrition. The interaction between plant and phosphate-solubilizing- bacteria is explained in more detail and used as model to illustrate the role that rhizosphere bacteria play on soil nutrient availability. Environmental conditions of rhizosphere and mycorrhizosphere are also discussed. Plants can release carbohydrates, aminoacids, lipids, and vitamins trough their roots to stimulate microorganisms in the soil. The soil volume affected by these root exudates, aproximately 2 mm from the root surface, is termed rhizosphere. Rhizosphere bacteria participate in the geochemical cycling of nutrients and determine their availability for plants and soil microbial community. For instance, in the rhizosphere there are organisms able to fix N 2 forming specialized structures (e.g., Rhizobium and related genera) or simply establishing associative relationships (e.g. Azospirillium, Acetobacter). On the other hand, bacterial ammonifiers and nitrifiers are responsible for the + - conversion of organic N compounds into inorganic forms (NH 4 and NO 3 ) which are available for plants. Rhizosphere bacteria can also enhance the solubility of insoluble minerals that control the availability of phosphorus (native or applied) using for that organic acids or producing phosphatases that act on organic phosphorus pools. The availability of sulfur, iron and manganese are also affected by redox reactions carried out by rhizosphere bacteria. Likewise, chelating agents can control the availability of micronutrients and participate in mechanisms of biocontrol of plant pathogens. Due to these and other benefits on plant growth, some rhizosphere bacteria have been called Plant Growth Promoting Rhizobacteria (PGPR). The benefits of PGPR have also been obtained, and even enhanced, in presence of mycorrhizal fungi. Some authors have employed the term “mycorrhizosphere” to describe the part of the soil affected by these interactions.

Key wordswords: rhizosphere, plant growth promoting rhizobacteria, phosphate solubilizing microorganisms, nutrient cycling. ______

RESUMEN

EFECTOS BENEFICOS DE RIZOSFRIZOSFÉÉRICASÉÉRICAS EN LA DISPONIBILIDAD DE NUTRIENTES EN EL SUELO Y LA ABSORCIÓN DE NUTRIENTES POR LAS PLANTAS

Este artículo se constituye en una revisión de los beneficios de bacterias rizosféricas sobre la nutrición vegetal. La interacción entre planta y bacterias solubilizadoras de fosfato es explicada en

1 Profesor Asociado. Universidad Nacional de Colombia, Sede Medellín. Facultad de Ciencias. A.A. 3840, Medellín, Colombia.

Recibido: Octubre 26 de 2006; aceptado: mayo 8 de 2007.

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 Osorio Vega, N.W. mayor detalle y usada como modelo para ilustrar el rol que algunas bacterias de la rizosfera juegan en la disponibilidad de nutrientes en el suelo. Las condiciones ambientales de la rizosfera también se discuten con detalle. Los beneficios de estas bacterias han sido obtenidos, y mejorados, en presencia de hongos formadores de micorrizas. Algunos autores han acuñado el termino “micorrizosfera” para describir la parte del suelo afectada por estas interacciones. Las plantas pueden liberar carbohidratos, aminoácidos, lípidos y vitaminas, entre otros, a través de sus raíces y estimular con ello la actividad y el número de microorganismos del suelo que las rodea. Este volumen de suelo afectado por tales exudados, aproximadamente 2 mm desde la superficie de la raíz, es llamado rizosfera. Las bacterias rizosfericas participan en el ciclo geoquímico de nutrientes y determinan su disponibilidad para las plantas y la comunidad microbial del suelo. Por ejemplo, en la rizosfera algunas bacterias fijan N 2 simbiótica o asociativamente, otras son importantes en la conversión del nitrógeno de compuestos orgánicos a + - formas inorgánicas (NH 4 y NO 3 ) disponibles para las plantas. También es relevante la habilidad de algunas bacterias rizosféricas para disolver fosfatos insolubles (nativo y aplicado) a través de ácidos orgánicos, mientras que otras son más activas en la liberación de fosfato de compuestos orgánicos mediante enzimas fosfatasas. Por otro lado, la disponibilidad del azufre, hierro, manganeso es afectada por reacciones bioquímicas de oxido-reducción llevadas a cabo por bacterias de la rizosfera. De la misma manera, agentes quelatantes liberados por estas bacterias controlan la disponibilidad y absorción de micronutrientes y participan en el biocontrol de patógenos de plantas. Debido a estos beneficios sobre la nutrición y el crecimiento vegetal estas bacterias rizosfericas han sido llamadas “rizobacterias promotoras del crecimiento vegetal” (PGPR, por sus siglas en inglés).

Palabras claves: rizosfera, rizobacterias promotoras del crecimiento vegetal, microorganismos solubilizadores de fosfato, ciclo de nutrientes. ______

Rhizosphere . The rhizosphere is the bulk soil (S), for which the “R/S ratio” is region of soil that is immediately near employed (Atlas and Bartha 1997). The to the root surface and that is affected rhizosphere effect is higher for bacteria by root exudates (Kennedy 1999); it followed by fungi (Table 1) and even was described for first time by Lorenz higher for some functional groups of Hiltner 1904. There are different types bacteria (e.g., ammonifiers, denitrifiers). of substances that diffuse from the roots By contrast algae exhibit more number and that stimulate the microbial activity, in the bulk soil than in the rhizosphere. such as carbohydrates (sugars and The type of plant can also affect the oligosaccharides), organic acids, vitamins, R/S ratio, which can be associated with nucleotides, flavonoids, enzymes, hor- the amount and type of root exudates mones, and volatile compounds (Prescott, (Table 2). Harley and Klein 1999). There are also differences between the The result is a dense and active microbial population density at the root surface population that interacts with the roots (rhizoplane) and the rhizosphere. and within it. The rhizosphere effect on Although on the rhizoplane there are the soil microbial population can be numerous microorganisms only 4-10 % measured comparing the population of its total surface area is in physical density (colonies forming units, CFU) contact with soil microorganisms between the rhizosphere soil (R) and the (Bowen 1980). Differences in the type

3622 Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 A review on beneficial effects..... of soil were not found in the literature, Gilbert, Handelsman, and Parke 1994 but some soils or media that exhibit pointed out that a lower R/S effect is severe constrains for microbial growth associated with suppressive soils for (e.g., acidic and Al-rich soils that root pathogens, in that sense the abundant in the tropics) can exhibit R/S microbial activity of non-rhizosphere ratio higher for bacteria and other microorganisms can also play an microorganisms. On the other hand, important role in plant disease control.

Table 1. Number of microorganisms (CFU g -1 soil) in the rhizosphere (R) of wheat (Triticum aestivum L.) and bulk soil (S) and their R/S ratio.

Microorganisms Rhizosphere soil Bulk soil R/S ratio Bacteria 1,2 x10 9 5,3 x10 7 23 Actinomycetes 4,6 x10 7 7,0 x10 6 7 Fungi 1,2 x10 6 1,0 x10 5 12 Protozoa 2,4 x10 3 1,0 x10 3 2 Algae 5,0 x10 3 2,7 x10 4 0,2 Ammonifiers 5,0 x10 8 4,0 x10 6 125 Denitrifiers 1,26 x10 8 1,0 x10 5 1260 (Modified from Gray and Williams 1971).

Table 2. Number of bacteria (CFUx10 6 g -1 soil or root dry mass) in the rhizoplane and rhizosphere of different plants, and in the bulk soil (S) and their R/S ratio

Plant species Rhizoplane Rhizosphere Bulk soil R/S ratio Red clover ( Trifolium pratense ) 3844 3255 134 24 Oats ( Avena sativa ) 3588 1090 184 6 Flax ( Linum usitatissum ) 2450 1015 184 5 Wheat ( Triticum aestivum ) 4119 710 120 6 Maize ( Zea mays ) 4500 614 184 3 Barley ( Hordeum vulgare ) 3216 505 140 3 (Rouat and Katznelson 1961).

This lower R/S effect seem to be rhizosphere varies with the plant and involved in the experiments of Zhang, the soil, but it is widely accepted Dick, and Hoitink 1996 who found less that it covers at least 2 mm from the severity of “root rot” (caused by Pythium rhizoplane. Some authors have ultimum and P. aphanidermatum ) and shown that the influence can be at “leaf-anthracnose” ( Colletotrichum orbi- least up to 10 mm (Table 3). The culare ) of cucumber plants grown in diversity of microorganisms is also compost-rich medium (suppressive) than variable, close to the rhizoplane those grown in sphagnum peat there is a diverse community but as (conducive). The extent of the the distance from the rhizoplane

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 3623 Osorio Vega, N.W. increases the diversity is lower. associated with the concentration of Papavizas and Davey 1961 found carbon in the soil solution (root similar effects on rhizosphere actino- exudates), which decreases from the mycetes and fungi, this seems to be rhizoplane (Yeates and Darrah 1991).

Table 3. Number of bacteria at increasing distances from the root surface (Paul and Clark, 1996).

Distance (mm) CFUx10 9 cm -3 soil Morphological types 0-1 120 11 1-5 96 12 5-10 41 5 10-15 34 2 15-20 13 2

The release of root exudates can be dense microbial population. Conse- affected by several factors in the plant, quently, the concentration of CO 2 is soil and environment. According to high. These conditions create an ambient Bowen and Rovira 1999, plants can anaerobic, and reduction reactions are released between 10-30 % of photo- favored. It is evident from the Table synthates through the root system. 1 where the denitrifiers (anaerobic Whipps and Lynch 1986 reviewed this bacteria) had a higher R/S ratio (1260) subject and found that a same factor facilitating the reduction of some (e.g., water stress, low soil pH, chemical elements such as nitrogen, sulfur, iron applied to foliage) produced increase or and manganese. decrease in the release of organic compounds in different plants. Roots also The rhizosphere pH is usually lower secret polysaccharides mucilage and loses than the bulk soil in 1-2 units. Several cap cells detached from the root tip mechanisms are responsible of this when it grows through the soil (McCully effect: (i) production of CO 2 by respiration 1999), releasing thus more carbonaceous processes, (ii) pump of H + in nutrient compounds into the rhizosphere. uptake by plant and microbes, (iii) release of organic acids by roots and microbes, The physical-chemical conditions that (iv) Organic matter decomposition, and predominant in the rhizosphere are (v) N 2 fixation by the useful to understand the role that plays Rhizobium -legume (Marschner 1997). microorganisms, particularly bacteria The effects can also vary with the soil on soil nutrient availability. The con- buffer capacity and the type of plant centration of oxygen in the rhizosphere involved. Acid conditions favor the is very low due to the high demand of solubilization of soil minerals (e.g., oxygen required for the respiration of calcium phosphates) (Bowen and carbonaceous compounds and the highly Rovira 1999). The characteristics of the

3624 Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 A review on beneficial effects..... rhizosphere vary with plant species and yield by different ways. The acronym soil conditions. The rhizosphere of PGPR has been widely used to group flooded rice exhibits an environment these microbes (Bowen and Rovira more aerobic than the bulk soil. The 1999). Recently, Bashan and Holguin aerenquima tissue of rice plants 1998 proposed the division of PGPR in permits the transport of O 2 to the roots two classifications: Biocontrol-Plant and its release into the rhizosphere Growth Promoting Bacteria (Biocontrol- (Marschner 1997). This facilitates the PGPB) and PGPB. These authors affirm oxidation of Fe and Mn that given the that this separation is important in reductive conditions of flooded soils order to differentiate the mechanisms tend to increase their availability up to employed by these bacteria to promote levels that become toxic for plants. the growth of plants. Biocontrol-PGPB are strictly those bacteria that Mycorrhizosphere . Most land plants form participate in the biocontrol of plant a symbiotic association with soil fungi pathogens while PGPB are bacteria that called (myco= fungus, rhiza= has other functions different to root) (Sylvia 1999). The mycorrhizal biocontrol (e.g., nutritional, hormonal). association favors water and nutrient Also they suggested replace the term uptake, particularly P, Cu and Zn; soil rhizobacteria for simply bacteria, structure development and stability, and because some bacteria can promote biological control of plant pathogens the plant growth but they are not (Marschner and Dell 1994). It is recog- inhabitants of the rhizosphere. nized that the mycorrhizal association is a natural strategy that most plants have This paper deals with rhizosphere bac- developed in their evolution process since teria whose effects are associated with their establishment on the earth’s surface plant nutrition. Although Bashan and (Paul and Clark 1996). Holguin’s proposal is interesting, it is very difficult to separate the effects of The fungal hypha is practically an both categories.... extension of the root system that increases the volume of soil explored Nitrogen fixation ... Nitrogen is one of the (Brady and Weil 1999). The mycorrhizal most limiting plant nutrients for plant hypha also release carbonaceous com- growth (Havlin et al . 1999). Some pounds into the surrounding soil for- rhizosphere bacteria have the ability to fix ming a niche called “mycorrhizosphere” N2 into organic forms that can then be (Rambelli 1973, Linderman 1988). It is used by plants. The rhizosphere condi- important differentiate between two tions favor the N 2 fixation because it is niches. Usually, the benefits of carried out by heterotrophic bacteria that rhizosphere microorganisms are increase use organic compounds as source of in presence of the mycorrhizal symbiosis. electrons for the reduction of N 2. Promi- nent among these microorganisms are

Plant growth promoting rhizorhizo---- the N 2 fixers of the genera Rhizobium, bacteria (PGPR)(PGPR). ... Rhizosphere bacteria Bradyrrhizobium, Mesorhizobium, Allo- can enhance the plant growth and crop rhizobium, Sinorhizobium , and Meso-

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 3625 Osorio Vega, N.W. rhizobium that form symbiosis with the interior of nodules avoiding thus legumes. In this case the concen- competition of other microorganisms tration of O 2 is regulated by (Graham 1999). They are perhaps the hemoglobin and the supply of most studied interaction between carbonaceous compounds occurs in plant and bacteria.

Rhizosphere (1-2 mm) Mycorhizosphere

C Rhizoplane C H+ Root + H Mycorhizosphere bacteria

Rhizosphere Mycorrhizal hypha bacteria (b) (a)

Figure 1. Schematic illustration of rhizosphere (a) and mycorhizosphere (b).

Another N 2 fixer is Azotobacter paspali, diazotrophicus has the advantage of a which grows in the rhizosphere of supply of carbon without microbial tropical grasses, such as Paspalum competition and apparently can tole- notatum c.v. batatais and Digitaria rate high concentration of O 2 than species, with which exhibit certain other bacteria. Sugarcane can derive as degree of specificity (Zuberer 1999). much as 100-150 kg N ha -1 from this Although fixation of 5-25 kg N ha -1 association. year -1 are widely accepted, values as high as 90 kg N ha -1 year –1 have been One of the most studied associative reported. Acetobacter diazotrophicus is a symbioses is that formed by Azospirillum

N2 fixer that can grow inside of the root spp. and roots of numerous grasses, tissue (‘endorhizosphere’) of sugarcane, including important cereal crops (Okon including vascular tissues where can 1994, Chanway 1997). Increases in the achieve number of 10 6 cells g -1 of these plant growth and yield by 5-30 % have tissues. For its particular location, A. been reported. The benefits seem to be

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due to the stimulation of nutrient inoculation with free-living N 2 fixers, such uptake, production of plant growth as Azospirillium and Azotobacter , are regulators (auxins, giberrellins, and uncertain. Successful results have been cytokinins), rather than to N 2 fixation. obtained when these rhizosphere Bashan, Rojas and Puente 1999 and bacteria are combined with plants Carillo-Garcia et al . 2000, have reported that have high efficiency in the that cactus species inoculated with A. (C 4 plants), thus the C brasilense improved their establishment supply for these heterotrophic and development in desert soils. bacteria might be satisfactory.

Other non symbiotic N 2 fixing bacteria Manganese. The availability of man- Azotobacter chrococcum , Bacillus ganese (Mn) in the rhizosphere is polymyxa , and Clostridium pasteurianum affected by two major factors: redox had increased seedling vigor of corn, condition and pH (Bohn, McNeal and wheat, and tomato and promoted O’Connor 1985). In oxidized soils earlier flowering of tomato (Rovira manganese is present in its oxidized 1963). Perhaps the response was also form, Mn 4+ , in the low-soluble due to hormonal effects and not to N 2 mineral Pryolusite. Some rhizosphere fixation. bacteria ( Bacillus, Pseudomonas, and Geobacter ) can reduce oxidized Mn 4+ Positive responses in plant growth to Mn 2+ , which is the chemical form with N 2 fixers can be expected in soils that is metabolically useful for where N supply is limited. For plants. The reaction is as follows: instance, desert soils (Aridisols in the + - 2+ U.S. soil taxonomy; Buol et al . 1997) MnO 2 + 4H + 2e ↔ Mn + 2H 2O (1) have very low organic matter and lack available water that restricts In this reaction two points are important, plant growth. The positive results of the reduction of Mn requires electrons Bashan, Rojas, and Puente 1999 and and protons. Electrons are supplied by Carillo-Garcia et al. 2000, support the decomposition of carbonaceous this affirmation. Other types of soils compounds and protons can be supplied (e.g., ash volcanic soils) with low N by the proton excretion system of root supply could be conducive for N 2 cells (Marschner 1997). Consequently, fixers. Similarly, eroded soils that the activity of Mn-reducers is highly have lost the soil organic matter favored in the rhizosphere. Applica- from their surface or that have been tions of organic matter also can favor burned soils can be rehabilitated for the reduction of Mn (Hue, Vega and plant growth using rhizosphere N 2 Silva 2001). In alkaline soils where Mn fixers. When legumes are employed usually is insoluble the rhizosphere the inoculation with their symbiotic effect is beneficial, but in acidic soils with partners ( Rhizobium species or abundance of Mn-minerals (e.g., related genera) can improve the Wahiawa soil in the Oahu Island, Hue establishment of plants. In the cases et al . 1998) excessive reduction of Mn of non-legumes, the results of the can induce Mn toxicity in sensitive plants.

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 3627 Osorio Vega, N.W.

Arines, Porto and Vilarino 1992, found reduce the availability of Mn 2+ for that the mycorrhizosphere can reduce the fungal pathogens limiting its ability to activity of Mn-reducers and favor the Mn attack roots. oxidation, which can be favorable for the management of Mn-rich soils. Iron . The dynamics of iron in the rhizosphere is very similar to that of Mn plays an important role in the manganese (Bohn, McNeal, and resistance of plants to plant disease. O’Connor 1985). Soil Fe is present in Mn, as well as Cu, is required for the oxidized forms Fe 3+ as a component of synthesis of lignin, which increase the the structure of insoluble minerals resistance of the root tissues to the Goethite (FeOOH) or hematite (Fe 2O3) penetration of pathogens, consequently (Lindsay 1979). Rhizosphere bacteria Mn-deficient plants are more susceptible (Bacillus, Pseudomonas, Geobacter, to the attack of plant pathogens. Alcaligenes, Clostridium, and Entero- Gaeumannomyces graminis , like many bacter) can reduce Fe 3+ to Fe 2+ , the other soilborne pathogenic fungi, is a form required by plants. Electrons and powerful oxidizer of Mn that impairs the protons are available in the rhizosphere lignification of root at infection sites and consequently iron is reduced, (Graham and Webb 1991). however it can be reprecipitated (Mullen 1999). The reactions of reduction are as Effective rhizosphere Mn-reducers follows: (e.g., Pseudomonas sp.) could have FeOOH + 3H + + e - ↔ Fe 2+ + 2H O (2) beneficial effects not only on plant 2 + - 2+ nutrition but also on biocontrol of Fe 2O3 + 6H + 2e ↔ 2Fe + 3H 2O (3) pathogens (Marschner 1997). Under Fe-deficiency, rhizosphere bac- In addition, roots and rhizosphere bacteria teria, particularly fluorescent Pseudo- can produce chelating-agents (phenolic monas , produce chelating agents (side- compounds, organic acids) that form rophores) that form soluble complexes soluble complex with Mn and other with Fe 2+ and that are available for these elements avoiding the reprecipitation of bacteria (Marschner 1997). Scher 1986, Mn (Marschner 1997). found in Fusarium -suppressive soils that Pseudomonas putida produced a In contrast, in flooded soils where the siderophore that sequestered iron. The availability of Mn 2+ can be high, the Mn- complex siderophore-Fe can only be used oxidization by rhizosphere bacteria would by P. putida but no by Fusarium, which favor plant growth. Rice roots release O 2 requires iron to synthesize enzymes that in the rhizosphere avoiding Mn-toxic degrade the plant cell walls. However, effects. On the other hand, Mn-oxidizing when Fe-EDTA (an iron fertilizer) was bacteria in the rhizosphere of plants applied, the biocontrol was lost because grown in M-deficient soils can play an Fusarium could use this fertilizer. important role in plant disease control (Gilbert, Handelsman and Parke 1994). A strong Fe-chelating agent, EDDA By reversing reaction (1), these bacteria enhanced the effect of P. putida . Van

3628 Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 A review on beneficial effects.....

Peer et al . (1990) found similar lignin (Marschner 1997). Lignification effects with EDDHA. Again, mecha- of wall cells is a common response of nisms related with nutritional effects plants when are challenged by plant participate in the biocontrol of plant pathogens. Iron deficiency plants can be pathogens. On the other hand, iron is more vulnerable to plant pathogens. In a component of heme groups in Table 4 the rhizosphere effects on pH catalase and peroxidaes enzymes, and the availability of Fe, Mn and Zn which are required in the synthesis of are presented.

Table 4. Soil pH and micronutrient availability (DTPA-extractable, µmol kg -1 soil) in bulk soil and rhizosphere of white lupin ( Lupinus albus ).

Bulk soil Rhizosphere soil

pH (H2O) 7,5 4,8 Iron 34 251 Manganese 44 222 Zinc 2,8 16,8 (Dinkelaker, Romheld and Marschner 1989).

Solubilization of phosphates by (Whitelaw, 2000), but this point is quite rhizosphere bacteria. In recent years, controversial. great attention has been dedicated to study the role that soil microorganisms The mechanisms involved in the play in the dynamics of phosphate (P), microbial solubilization of P are the particularly those able to solubilize production of organic acids and the insoluble P forms (Rao 1992). These release of protons to the soil solution microorganisms are bacteria and fungi (Kim, McDonald and Jordan 1997). that inhabitant the rhizosphere (Barea Inoculation with phosphate solubilizing and Azcon 1975, Bowen and Rovira rhizosphere bacteria (PSRB) and other 1999). Most soil bacteria can solubilize soil microorganisms, such as arbuscular insoluble phosphates, particularly mycorrhizal fungi (AMF), might active are those that belong to the enhance even more the benefits of this genera Pseudomonas, Enterobacter P solubilization. and Bacillus as well as some soil fungi, Penicillium and Aspergillus (Domey and Why to study PSRBPSRB??.??... One of the Lipmann 1988, Patgiri and Bezbaruah most important problems in tropical 1990, Rao 1992, Rokade and Patil agriculture is the low-soil-phosphate 1993, Whitelaw 2000). Some re- (P) availability. Many of the tropical searchers prefer to use fungal P- soils are highly weathered and have a solubilizers arguing that bacterial high P fixation capacity that makes strains can lost their ability to solubilize their management more difficult P after several cycles of in vitro culture (Sanchez 1976). Sanchez and Logan

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1992, estimated that 1018 million ha in soil P from the soil solution, where the tropics have a high P fixation roots directly take up plant nutrients capacity. In tropical America there are (Barber 1995). Such reactions consist 659 million ha affected, 210 in in the sorption of phosphates on the Africa, and 199 in Asia (Figure 2). solid surface of soil colloids and in The term “P-fixation” is used in the precipitation of phosphates with reference to a series of complex some cations in the soil solution reactions that remove bioavailable (Havlin et al . 1999).

Tropics

Area dominated by P deficient soils

Figure 2. Phosphate-deficient soils in the world (adapted from Van Wambeke 1976).

Phosphate sorption is caused mainly The precipitation of P in acidic soils occur by the presence of crystalline or non- with active forms of aluminum (Al 3+ , 2+ + 2,,3+ crystalline hydrous-oxides of iron and Al(OH) , Al(OH) 2 ) and iron (Fe ). In aluminum in highly weathered soils of calcareous soils, P is sorbed on the humid regions and acid savannas surface of calcium carbonate (Mattingly (Mattlingly 1975). Allophane (a non- 1975) or precipitated with calcium (Ca 2+ ) crystalline aluminum-silicate) and (Bohn, McNeal and O’Connor 1985). humus-Al/Fe complexes are the res- The predominance of these mecha- ponsible of the P sorption in soils nisms depends on the degree of soil derived from volcanic parent materials weathering and soil pH. In past decades, (Schwertmann and Herbillon 1992, several strategies have been employed Shonji, Nanzyo and Dahlgren 1993). to reduce the P fixation. These consist of

3630 Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 A review on beneficial effects..... use of high rates of P fertilizers, selection Many organic acids are effective in of fertilizers, time and method of solubilizing soil phosphates, these acids application, combination with amend- are produced by rhizosphere micro- ments and other fertilizers, use of soil organsims (Marschner 1997). Bolan et al . tests, etc. (Engelstad and Terman, 1994, studied the influence of the 1980). However, the efficiency of P addition of organic acids on high P-fixing fertilizers is still low (5-10 %) (Havlin et al . soils. These acids decreased the P sorp- 1999). Currently, there are environmental tion on the clay surfaces, favored the concerns in regard to the high levels of P solubilization of rock phosphate, and fertilization (Brady and Weil 1997). Rock increased dry matter of ryegrass phosphates (apatite) are fertilizers amply (Lolium rigidium ) and plant P uptake. recommended for soils with high P Hue 1991, found similar results in the fixation capacity because other more availability of P when added organic soluble sources are quickly fixed. acids on tropical soils in Hawaii and However, rock phosphates are extremely concluded that the efficiency of P insoluble, particularly in alkaline soils, and fertilizers might be enhanced if these a little more reactivity is always desired are added with organic acids or, more (Hammond and Leon 1992, Chien and practically with green manures or Hammond 1978). animal wastes.

Mechanisms of P solubilization by Kim, McDonald and Jordan 1997, point rhizosphere bacteriabacteria.. Several mecha- out that the production of organic acid nisms have been proposed to explain was the major mechanism involved in the P solubilization by PSRB, they are the solubilization of hydroxyapatite associated with the release of (rock phosphate) by the PSRB organic and inorganic acids, and the Enterobacter agglomerans , but other excretion of protons that accom- mechanisms might be involved. Under + panies to the NH 4 assimilation in vit ro conditions, the pH of the (Kucey 1983, Roos and Luckner1984, growth medium has decreased as a Abd-Alla 1994, Illmer, Barbato and result of the release of organic acids by Schinner 1995, Asea, Kucey and PSRB. Some of the organic acids Stewart 1988, Whitelaw 2000). In commonly found are gluconic acid (Di- addition, the release of phosphatase Simine, Sayer and Gadd 1998, Bar- enzymes that mineralize organic P Yosef et al . 1999), oxalic acid, citric compounds has been also suggested as acid (Kim, McDonald and Jordan 1997), another mechanism involved (Stevenson lactic acid, tartaric acid, aspartic acid 1986). Azam and Memon 1996, affirm (Venkateswarlu et al . 1984). These that Nitrosomonas and Thiobacillus acids are the product of the microbial mobilized inorganic phosphates by metabolism, mostly by oxidative respira- producing nitric and sulfuric acid. tion or by fermentation of organic carbon Equally, phosphates may be released sources (e.g., glucose) (Atlas and Bartha from solid compounds by carbonic acid 1997, Prescott, Harley and Klein 1999). formed as a result of the decomposition Such biological reactions occur in the of organic residues (Memon 1996). rhizosphere where carbonaceous com-

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 3631 Osorio Vega, N.W. pounds are used by PSRB and the the surface of soil colloids. He and Zhu phosphate released is taken up by the 1997, 1998 demonstrated that sorbed roots or mycorrhiza symbiosis. phosphates on the surfaces of kaolynite, goethite, montmorillonite and amor- When PSRB are inoculated to neutral or phous Al-oxides were displaced by mi- alkaline soils, the acid production crobial activity presumably using organic decreases the rhizosphere pH, favoring acids. thus the solubility of calcium phos- phates and apatites. If the activity of Experiences with PSRBPSRB.... The inocu- H+ increases in the reactants of the lation with Bacillus megatherium var. reactions (4) and (5), these reactions phosphaticum in Russian soils (Mollisols) proceed. In addition, the sequestering has been the best known reference of of Ca by organic anions favors the massive use of PSRB (Stevenson 1986). reactions. However, trials carried out in many locations demonstrated little consistency, (Dicalcium phosphate) CaHPO + H + ↔ 4 which it is not surprising due to the H PO - + Ca 2+ (4) 2 4 diversity of factors involved. In fact, + (Hydroxyapatite ) Ca 5(PO 4) 3 (OH) + 4H similar contradictions may be found in 2- 2+ ↔ 3HPO 4 + 5Ca + H 2O (5) the response of crops where P fertilizers have been applied (Sumner 1987). In In acid soils, the minerals variscite and some cases, the inoculation with known strengite control the solubility of phos- PSRB has enhanced the plant growth phate (Lindsay 1979). The presence of without affecting plant P uptake. Freitas, organic acids propitiates the formation of Banerjee and Germida 1997, found that complexes with Al and Fe ions, which in the inoculation with the PSRB’s Bacillus turn facilitates the dissolution of these thuringiensis, B. brevis, B. megatherium, minerals. If Fe 3+ and Al 3+ are sequestered B. polymyxa, B. sphaericus and via chelation with organic anions the Xanthomonas maltophila increased the reactions 6 and 7 proceed to the right. growth and yield of canola ( Brassica However, this point is controversial napus ), but they did not increase the because the reduction in soil pH might plant P uptake. PSRB can also release also solubilize other iron and aluminum substances that promote root growth minerals that would reprecipitate again such as hormones, enzymes, antibiotics; phosphates to form newly strengite and enhance availability of other nutrients variscite (Lindsay 1979). (e.g. Mn and Fe), and exert biocontrol of

-2 plant pathogens (Rao 1992, Premono et (Strengite) FePO 4.2H 2O ↔ HPO 4 + 3+ - al . 1994, Toro et al . 1996, Bashan and chelate-{Fe }+ OH + H 2O (6) Holguin 1998, Azcon and Barea 1996, -2 Kopler, Lifshitz and Schroth 1988, (Variscite) AlPO 4.2H 2O ↔ HPO 4 + 3+ - Frankenberg and Arshad 1995). The chelate-{Al }+ OH + H 2O (7) efficiency of PSRB has been questioned On the other hand, organic anions because: (i) organic substances required produced by PSRB can also compete for these microorganisms are scarce in with phosphates for fixation sites on non-rhizosphere microsites, (ii) antago-

3632 Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 A review on beneficial effects..... nism and competition with other micro- there is a great opportunity to satisfy organisms in the rhizosphere, and (iii) low their C requirement and deliver phos- translocation of solubilized phosphates phates into the soil solution (Figure 3). through soil because they can be again Kim, Jordan and McDonald 1998 a, b, refixed by soil components (Tinker 1980, studied the effect of individual and dual Bolan 1991, Azcon and Barea 1996). inoculation of Enterobacter agglomerans (PSRB) and Glomus etunicatum (AMF) on Mycorrhizosphere and PSRB . There are tomato growth and P uptake. They found several advantages with the combined that there was a synergistic effect when use of arbuscular mycorrhizal fungi (AMF) both microorganisms were inoculated and PSRB. First, mycorrhizal plants can (Table 5). release a higher amount of carbonaceous substances into their rhizosphere (‘my- Alkaline phosphatase activity was higher corrhizosphere’) than nonmycorrhizal in the treatment with G. etunicatum as plants (Rambelli 1973, Linderman well as the combination G. etunicatum + 1988). Second, the extensive net E. agglomerans. There was higher P con- formed around the roots by the centration in the rhizosphere and higher mycorrhizal hyphae can efficiently oxalic acid production when both micro- facilitate the uptake of phosphate organisms were concurrently inoculated. released by PSRB, avoiding thus its In this experiment glucose was applied as refixation. As long as the PSRB remain in an energy source to increase the release the rhizosphere (or mycorrhizosphere), of organic acids by PSRB.

Table 5. Effects of E. agglomerans (PSRB) and G. etunicatum (AMF) inoculation on tomato plant growth and P uptake (75 days after inoculation).

Treatments Shoot dry weight (g Root dry weight (g Total P (g plant -1) plant -1) plant -1) Shoots Roots Control 42,21 4,29 116,46 11,9 PSRB 48,49 5,10 125,26 13,6 AMF 47,62 5,57 120,94 13,4 PSRB + AMF 54,56 6,77 134,41 16,7 LSD ( P<0,05) 1,96 0,53 9,85 NS (Kim Kim, Jordan and McDonald 1998 a).

Similar synergistic effects have been effects were also reported with P. found in sunflower ( Helianthus annuus ) striata and Bacillus polymyxa (Mohod, with the triple inoculation of Azotobacter Gupta and Chavan 1991); in chili chroococcum, Penicillium glaucum and (Capsicum annuum ) with G. fasciculatum Glomus fasciculatum (Gururaj and or G. macrocarpum and P. striata Mallikarjunaiah 1995); in cotton with (Sreenivasa and Krishnaraj 1992); in the inoculation of Pseudomonas striata wheat with P. putida, P. aeruginosa and and Azospirillum sp. (Prathiba, Alagawadi P. fluorescens in combination with G. and Sreenivasa 1995); in rice favorable clarum. Gaur et al . 1990 found the

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 3633 Osorio Vega, N.W. same type of response in wheat with P. and Agrobacterium radiobacter , with striata and G. fasciculatum . In other G. fasciculatum and Gigaspora experiment with wheat, Gaur et al . margarita , the greatest plant growth 1990 obtained positive results with the was obtained when these microbes combination of two PSRB, P. striata and fertilizers were added.

Mycorrhizosphere

Root Organic carbon

Uptake PSRB - H2PO 4

Organic acids

Added Native AMF hypha

Soil P

Figure 3. Diagram presentation of the solubilization of phosphates in the mycorrhizosphere and the mycorrhizal P uptake.

PSRBPSRB--AMF--AMF and rhizobiarhizobia. ... Kopler, In soybean the combination of Lifshitz and Schroth 1988 found more Bradyrhizobium japonicum , P. fluorescens legume-Rhizobium nodulation when and G. mosseae have given equally also added Pseudomonas spp. Sturz et good results (Shabayey, Smolin and al . 1997 found that the nodulation of Mudrick 1996). Such results are likely Rhizobium leguminosarum b.v. trifolii due to a higher P uptake promoted by was promoted on red clover ( Trifolium the PSRB and AMF, which may satisfy pratense ) when it was co-inoculated the high P requirements of the sym- with Bacillus insolitus , B. brevis or biotic N 2 fixing process (Azcon and Agrobacterium rhizogenes. Similar re- Barea 1996, Young, Chen and Chao sults were obtained with the inoculation 1990). of G. mosseae and Azorhizobium caulinodans in Sesbania rostrata Apparently, there is a certain degree of (Rahman and Parsons 1997). specificity among the PSRB, AMF and P

3634 Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 A review on beneficial effects..... source. Toro, Azcon and Herrera 1996 citrate synthetase in the TCA cycle of a studied the effect of the combination of strain of Pseudomonas aeruginosa (a AMF ( Glomus spp. ) and eight PSRB on the known PSRB). This gene was then growth and P nutrition of a tropical transferred to tobacco cells of plants that legume, kudzu ( Pueraria phaseoloides ). not exhibit Al tolerance. Transgenic plants PSRB were isolated from an Oxisol and were produced high amounts of citric were characterized by their ability to acid and citrate and grew in solutions solubilize rock phosphate, iron phosphate with high concentration of Al. The and aluminum phosphate. In general, process was successfully replicated with when kudzu-Rhizobium -AMF were co- papaya plants. Although these ex- inoculated with PSRB there was an periments were oriented to enhance the increase in the plant growth, yield and Al tolerance of these plants, it is directly nutritional status. However, such syner- associated with the mechanisms pro- gism was not observed in all combi- posed for the solubilization of soil nations. For instance, Azospirillum sp., phosphates. Bacillus sp., and Enterobacter sp. had a higher effect when were co-inoculated Currently, the fungal inoculum Penicillium with G. Mosseae. Pseudomonas sp. and bilaii is commercially available in North an unidentified isolate had a better America with the name of Provide TM , performance when were combined with which has been successfully tested to G. fasciculatum . On the other hand, Fe- enhance plant P uptake of several phosphate solubilizers were more plants (Whitelaw 2000). Little research effective alone, while Al − and rock on phosphate solubilizers has been phosphate-solubilizers performed better carried in tropical soils that usually when were concurrently inoculated with exhibit a higher P fixation capacity than AMF. temperate soils. Recently, Osorio and Habte (unpublished) isolated several Germide and Walley 1996, pointed out phosphate solubilizers including bac- that is also possible to observe no teria from the rhizosphere of L. effects or even unfavorable effects with leucocephala naturally grown in three PSRB inoculation. This seems to be Hawaiian soils (Tantalus, Wahiawa and caused by alteration in the rooting Kaena soil series). The most effective P patterns (root distribution and root solubilizer was a fungus identified as length), reduction in the AMF coloni- Mortierella sp., which in turn was the zation of roots. Baas 1990 affirms that most efficient producer of acidity in an multiple inoculation of microorganisms in vitro test , several effective PSRB were might cause competition among them also isolated (not yet identified). for rhizosphere exudates and with the host plant for the uptake of available P. It is uncertain if many of the me- chanisms proposed for the PSRB Prospective research on PSRBPSRB.... In a operate at the same level of effec- series of elegant experiments, De la tiveness in diverse soils with variable Fuente and Herrera 1999, isolated the mineralogy. PSRB have also been used gene that codes the overproduction of in the industry of P fertilizers. Usually

Rev.Fac.Nal.Agr.Medellín.Vol.60,No.1.p.3621-3643. 2007 3635 Osorio Vega, N.W. rock phosphates are slightly acidulated acids decrease the rhizosphere pH with inorganic acids to increase its favoring the solubility of precipitated P reactivity (Chien and Hammond 1978), forms. Organic anions can also compete or used as raw material to produce or even replace phosphate sorbed on the more soluble fertilizers for which surfaces of soil clays, they also can strong acids are added (Young and chelate Al and Fe avoiding thus the Davies 1980). It is an expensive process precipitation of phosphate. due to the high cost of inorganic acids. Bar-Yosef et al . 1999 found that Pseudomonas cepacia , a known PSRB, ACKNOWLEDGEMENTACKNOWLEDGEMENTSSSS was very efficient to oxide glucose and to produce gluconic and 2-keto- The author thanks Dr. Anne Alvarez and gluconic acids in a reactor containing Dr. Francoise Robert from the University rock phosphate. Once the acids were of Hawaii, HI, USA, and Dr. Mauricio dissociated, protons reacted with rock Marin Montoya from the Universidad phosphate and released phosphate Nacional de Colombia, Sede Medellín for ions that were then precipitates with reading the manuscript. Ca to form soluble fertilizers (super- phosphates). Thus, PSRB yield benefits not only in their natural niche, the REFERENCES rhizosphere, but also in other environments. Abd-Alla, M. H. 1994. Use of organic phosphorus by Rhizobium legumino- sarum biovar viceae phosphatases. In: CONCLUSIONS Biology and Fertility of Soils. Vol. 18, no. 3; p. 216-218. Phosphate solubilizing rhizosphere bac- teria has a high potential to be used in Arines, J.; Porto, M. E. and Vilariño, A. the management of P deficient soils. 1992. Effect of manganese on vesicular- PSRB may be co-inoculated with AMF arbuscular mycorrhizal development in red generating synergistic effects on plant clover plant and soil Mn-oxidizing bacteria. growth and P uptake. The compatibility In: Mycorrhiza, Vol. 1, no. 3; p. 127- between PSRB and AMF seems to have 131. certain degree of specificity, for which is recommended to investigate what Asea, P. E. A.; Kucey, R. M. N., and are the more effective combinations. The Stewart, J. W. B. 1988. Inorganic mechanisms of P solubilization by PSRB phosphate solubilisation by 2 Penicillium are associated with the production of species in solution culture and soil. In: Soil organic and inorganic acids, proton Biology and Biochemistry. Vol. 20; p. 459- excretion, and phosphatase activity. 464. Organic acids are produced by the oxidation of carbonaceous originated in Atlas, R. and Bartha, R. 1997. Microbial the rhizosphere, from the soil organic ecology. New York: Addison Wesley matter or added as manure. Organic Longman. 694 p.

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