**3. Beneficial interaction between grasses and bacteria**

Soil bacteria are capable of presenting beneficial effects on cultivated grasses. Several mech‐ anisms make bacteria to promote cultivated grasses, providing significant benefits to the plants, mainly regarding nutritional aspects.

#### **3.1. Beneficial interaction between grasses and nitrogen fixing bacteria**

About 78% of the Earth's atmosphere gases are composed of N<sup>2</sup> . This gas is neither good nor harmful to mankind. On the other hand, there are in the soil bacteria capable of transforming atmospheric nitrogen (N<sup>2</sup> ) into nitrogen assimilable by plants (NH<sup>3</sup> + ). The enzyme of N‐fixing microorganisms that catalyzes the conversion of N into NH<sup>3</sup> + is named *nitrogenase*. This enzyme is sensitive to oxygen, requiring molecules of iron (Fe), molybdenum (Mo), and vanadium (V) in its structural components [13], besides being an energetically expensive enzyme, requiring two molecules of ATP for each electron [14].

can produce phytostimulatory substances such as auxins [5, 7], cytokinins [6], and gibberel‐

Analytical Interpretation of the Beneficial Interaction Between Microorganisms and Grasses

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17

It is currently known that rhizobia promote plant growth in interactions with grasses, such as rice [5, 26, 27], barley [28], maize [29], Tanzania grass, and Pensacola [30]. Thus, rhizobia can not only symbiotically fix atmospheric N associated with legumes but they also present a great potential to be exploited as direct promoters of compatible yield increases when inad‐

The main phytostimulatory substances produced by rhizobia are the hormones present in aux‐ ins [5, 7], cytokinins [6], and gibberellins [7, 21]. The production of abscisic acid [31], lipochitool‐ igosaccharides (LCO) [28, 32], lumichrome [33], aminocyclopropane carboxylic acid deaminase

Among all auxin syntheses, the indole‐3‐acetic acid (IAA) is the most studied and the most produced by bacteria [36]. The IAA is mainly presented in the formation of lateral roots and root hair that increase the plant's nutrients absorption [5]. Different metabolic pathways for IAA biosynthesis have already been identified in bacteria [37], being that two main metabolic pathways, indole‐3‐acetamide (IAM) and indole‐3‐pyruvate (IpyA), depend on tryptophan [38]. Probably the IAA biosynthesis pathway in rhizobia is the indole‐3‐acetonitrile (IAN) [39].

Tryptophan has been found in root exudates. Kravchenko et al. [40] quantified the trypto‐ phan exudation by aseptic tomato and radish roots. Tomato seedlings released 2.8–5.3 ng of tryptophan per plant daily, whereas radish seedlings released 190–390 ng of tryptophan per plant per day. In the same study, the authors conducted experiments in soil pots, where they inoculated both cultures with a *Pseudomonas* plant growth‐promoting rhizobacteria and observed that radish root mass increased by 36% in inoculated plants, while proven ineffi‐ cient in tomatoes. The authors state that the beneficial effect of inoculation on radish plants can be explained by the fact that the rhizobacteria produced the plant growth stimulating

In an experiment conducted in a growth chamber, Silveira [41] studied the effect of inocu‐ lation of five *Rhizobium leguminosarum* bv. *trifolii* strains, and their ability to promote rice growth in cultivar IAC103 in nutrient solution. Considering the accumulation of dry mass, plants inoculated with SEMIA235 and SEMIA250 strains were superior compared to the con‐ trol treatment. The production of IAA by these strains was low, which can be the key to a great plant stimulation. Barazani and Friedman [42] have also reported that deleterious rhizo‐ bacteria produced high levels of IAA. However, with plant growth‐promoting rhizobacteria,

Biswas et al. [5] conducted laboratory and greenhouse studies to test the ability of rhizobia to promote plant growth in two rice cultivars. The studied rhizobia were assessed for the IAA production using the colorimetric method, which was positive for supernatant cultures for all rhizobia tested, ranging from 1.6 to 2.8 µg mL−1. The best responses to inoculations were obtained with *R. leguminosarum* bv. *trifolii* strain E11 and *Rhizobium* sp. strain IRBG74, which presented early stimulation in the plant growth, resulting in an increase in grain and straw

lower yields could be obtained during the same incubation period.

[34], and riboflavones and vitamins [35] produced by rhizobia have also been reported.

lins [7, 21], which directly favor the yield of cultivated plant species.

equately inoculated in succession/rotation cultures systems.

hormone IAA.

yields during the plant's maturity.

During the 1970s, Döbereiner's findings discovered that bacteria *Azospirillum* and *Herbaspirillum* could endophytically fix N in cultivated grass tissues [15]. There are currently commercial products based on *Azospirillum*, with bacteria selected for maize, wheat [15], and sugarcane [16]. This environmentally friendly process of N‐fixing decreases the consumption of mineral N fertilizers, reducing the cost for small farmers, since the demand of industrial N fertilizers with significant consumption of fossil fuels decreases [17].

Besides the endophytic grass fixing, *Azospirillum* and *Herbaspirillum* bacteria can also endo‐ phytically fix N in other plants, as in several monocotyledons and dicots such as herbs, shrubs, and trees [18]. When not associated with other leguminous plants [15], these free‐living nitro‐ gen‐fixing bacteria in the soil are considered optional associative N fixers [19].

Other plant growth promoters include *Azospirillum*, producing phytostimulatory substances, such as the indolyl acetic acid (IAA), gibberellic acid (GA), abscisic acid (ABA), and ethylene [20].

There is also a group of bacteria, named rhizobia, that symbiotically fix the atmospheric N for family *Fabaceae*. Unlike free‐living fixers, rhizobia can fix N only when associated within plant root nodules. In the N‐fixing symbiosis in leguminous plants belonging to the family *Fabaceae*, the rhizobia receive photo‐assimilated carbohydrates and, in exchange, they offer N, which is obtained as N<sup>2</sup> and transformed into NH<sup>3</sup> . The *nitrogenase* complex consists of two proteins: Fe‐protein and MoFe‐protein [3]. Thus, the metabolic exchanges between rhizobia and plants take place in structures called nodules, where the *nitrogenase* is protected from the atmospheric oxygen, due to the presence of leghemoglobin's hemeprotein, presented in high concentrations in active nodules, and fixed to oxygen.

Although they do not directly contribute to the grass nutrition, the symbiotic relationship between legumes and these symbiotic N‐fixing bacteria in root nodules promotes the contribution of N to the soil, which will contribute to the nutrition of grasses after the crop cycle of the legume through cultural residues decomposition. There are important reports in the literature on the benefits of grasses grown after legumes interacting with symbiotic N‐fixing bacteria [5, 21, 22]. Currently, among the 13 symbiotic N‐fixing bacteria, including the genera *Rhizobium*, *Mesorhizobium*, *Bradyrhizobium*, there are the subclasses α‐*proteobacteria* and β‐*proteobacteria*, with two genera belonging to the *Burkholderiales*, and a genus *Pseudomonas* subclass γ‐*proteobacteria* [23].

#### **3.2. The production of phytostimulatory substances by rhizobia**

The previous studies including rhizobia as grass growth promoters were driven by empirical findings in which specific rice plants cultivated in succession to clover produced more when compared to a cultivation without succession under the same soil, climate, fertilization, and management conditions, and this increment was not only related to residual N [21].

It could be proven that rhizobia are able to penetrate the grass tissue through fissures and root insertions [24–26]. In the intraradicular environment, as well as in the rhizosphere, rhizobia can produce phytostimulatory substances such as auxins [5, 7], cytokinins [6], and gibberel‐ lins [7, 21], which directly favor the yield of cultivated plant species.

microorganisms that catalyzes the conversion of N into NH<sup>3</sup>

with significant consumption of fossil fuels decreases [17].

concentrations in active nodules, and fixed to oxygen.

two molecules of ATP for each electron [14].

16 Grasses - Benefits, Diversities and Functional Roles

which is obtained as N<sup>2</sup>

+

is sensitive to oxygen, requiring molecules of iron (Fe), molybdenum (Mo), and vanadium (V) in its structural components [13], besides being an energetically expensive enzyme, requiring

During the 1970s, Döbereiner's findings discovered that bacteria *Azospirillum* and *Herbaspirillum* could endophytically fix N in cultivated grass tissues [15]. There are currently commercial products based on *Azospirillum*, with bacteria selected for maize, wheat [15], and sugarcane [16]. This environmentally friendly process of N‐fixing decreases the consumption of mineral N fertilizers, reducing the cost for small farmers, since the demand of industrial N fertilizers

Besides the endophytic grass fixing, *Azospirillum* and *Herbaspirillum* bacteria can also endo‐ phytically fix N in other plants, as in several monocotyledons and dicots such as herbs, shrubs, and trees [18]. When not associated with other leguminous plants [15], these free‐living nitro‐

Other plant growth promoters include *Azospirillum*, producing phytostimulatory substances, such as the indolyl acetic acid (IAA), gibberellic acid (GA), abscisic acid (ABA), and ethylene [20]. There is also a group of bacteria, named rhizobia, that symbiotically fix the atmospheric N for family *Fabaceae*. Unlike free‐living fixers, rhizobia can fix N only when associated within plant root nodules. In the N‐fixing symbiosis in leguminous plants belonging to the family *Fabaceae*, the rhizobia receive photo‐assimilated carbohydrates and, in exchange, they offer N,

proteins: Fe‐protein and MoFe‐protein [3]. Thus, the metabolic exchanges between rhizobia and plants take place in structures called nodules, where the *nitrogenase* is protected from the atmospheric oxygen, due to the presence of leghemoglobin's hemeprotein, presented in high

Although they do not directly contribute to the grass nutrition, the symbiotic relationship between legumes and these symbiotic N‐fixing bacteria in root nodules promotes the contribution of N to the soil, which will contribute to the nutrition of grasses after the crop cycle of the legume through cultural residues decomposition. There are important reports in the literature on the benefits of grasses grown after legumes interacting with symbiotic N‐fixing bacteria [5, 21, 22]. Currently, among the 13 symbiotic N‐fixing bacteria, including the genera *Rhizobium*, *Mesorhizobium*, *Bradyrhizobium*, there are the subclasses α‐*proteobacteria* and β‐*proteobacteria*, with two genera

The previous studies including rhizobia as grass growth promoters were driven by empirical findings in which specific rice plants cultivated in succession to clover produced more when compared to a cultivation without succession under the same soil, climate, fertilization, and

It could be proven that rhizobia are able to penetrate the grass tissue through fissures and root insertions [24–26]. In the intraradicular environment, as well as in the rhizosphere, rhizobia

belonging to the *Burkholderiales*, and a genus *Pseudomonas* subclass γ‐*proteobacteria* [23].

management conditions, and this increment was not only related to residual N [21].

**3.2. The production of phytostimulatory substances by rhizobia**

gen‐fixing bacteria in the soil are considered optional associative N fixers [19].

and transformed into NH<sup>3</sup>

is named *nitrogenase*. This enzyme

. The *nitrogenase* complex consists of two

It is currently known that rhizobia promote plant growth in interactions with grasses, such as rice [5, 26, 27], barley [28], maize [29], Tanzania grass, and Pensacola [30]. Thus, rhizobia can not only symbiotically fix atmospheric N associated with legumes but they also present a great potential to be exploited as direct promoters of compatible yield increases when inad‐ equately inoculated in succession/rotation cultures systems.

The main phytostimulatory substances produced by rhizobia are the hormones present in aux‐ ins [5, 7], cytokinins [6], and gibberellins [7, 21]. The production of abscisic acid [31], lipochitool‐ igosaccharides (LCO) [28, 32], lumichrome [33], aminocyclopropane carboxylic acid deaminase [34], and riboflavones and vitamins [35] produced by rhizobia have also been reported.

Among all auxin syntheses, the indole‐3‐acetic acid (IAA) is the most studied and the most produced by bacteria [36]. The IAA is mainly presented in the formation of lateral roots and root hair that increase the plant's nutrients absorption [5]. Different metabolic pathways for IAA biosynthesis have already been identified in bacteria [37], being that two main metabolic pathways, indole‐3‐acetamide (IAM) and indole‐3‐pyruvate (IpyA), depend on tryptophan [38]. Probably the IAA biosynthesis pathway in rhizobia is the indole‐3‐acetonitrile (IAN) [39].

Tryptophan has been found in root exudates. Kravchenko et al. [40] quantified the trypto‐ phan exudation by aseptic tomato and radish roots. Tomato seedlings released 2.8–5.3 ng of tryptophan per plant daily, whereas radish seedlings released 190–390 ng of tryptophan per plant per day. In the same study, the authors conducted experiments in soil pots, where they inoculated both cultures with a *Pseudomonas* plant growth‐promoting rhizobacteria and observed that radish root mass increased by 36% in inoculated plants, while proven ineffi‐ cient in tomatoes. The authors state that the beneficial effect of inoculation on radish plants can be explained by the fact that the rhizobacteria produced the plant growth stimulating hormone IAA.

In an experiment conducted in a growth chamber, Silveira [41] studied the effect of inocu‐ lation of five *Rhizobium leguminosarum* bv. *trifolii* strains, and their ability to promote rice growth in cultivar IAC103 in nutrient solution. Considering the accumulation of dry mass, plants inoculated with SEMIA235 and SEMIA250 strains were superior compared to the con‐ trol treatment. The production of IAA by these strains was low, which can be the key to a great plant stimulation. Barazani and Friedman [42] have also reported that deleterious rhizo‐ bacteria produced high levels of IAA. However, with plant growth‐promoting rhizobacteria, lower yields could be obtained during the same incubation period.

Biswas et al. [5] conducted laboratory and greenhouse studies to test the ability of rhizobia to promote plant growth in two rice cultivars. The studied rhizobia were assessed for the IAA production using the colorimetric method, which was positive for supernatant cultures for all rhizobia tested, ranging from 1.6 to 2.8 µg mL−1. The best responses to inoculations were obtained with *R. leguminosarum* bv. *trifolii* strain E11 and *Rhizobium* sp. strain IRBG74, which presented early stimulation in the plant growth, resulting in an increase in grain and straw yields during the plant's maturity.

*Bradyrhizobium japonicum* rhizobia isolated from soybean roots, *Azorhizobium caulinodans* iso‐ lated from *Sesbania rostrata*, *Rhizobium* NGR234 isolated from *Lablab purpureus*, *Sinorhizobium meliloti* isolated from *Medicago sativa*, *R. leguminosarum* bv. *viceae* Cn6, and *R*. *leguminosarum* bv. *viceae* strain 30 isolated from *Vicia faba* could infect and colonize sorghum and *Setaria* roots [43]. Considering that this distinct group of rhizobia isolated from different legumes can colo‐ nize these two grasses, the authors suggest that the infection of nonlegumes by rhizobia is more likely due to natural conditions than imagined. There was an increase in the growth of inoculated sorghum and *Setaria*, as well as an increase of P in the sorghum. According to the authors, this may have occurred due to the induction of bacteria as phosphate transporters from the plasma membrane of sorghum root cells.

*Alcaligenes*, *Rhodococcus*, and *Rhizobium* [34, 51]. In addition, some bacteria of *Rhizobium japonicum* (*B japonicum*) species synthesize phytotoxic antibiotics, aminoethoxyvinylglycine, and rhizobitoxin, which inhibit the formation of ethylene in plants [52]. The ethylene is a plant growth inhibitor, therefore bacteria that regulate its production can indirectly stimulate the plants and may be associated with the cell development, cell extension and the postponement

Analytical Interpretation of the Beneficial Interaction Between Microorganisms and Grasses

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19

*S. meliloti* can produce lumichrome [33]. The application of lumichrome in nanomolecular concentrations promoted the growth of legumes and grasses [43]. According to Ref. [48], the lumichrome stimulated the photosynthetic index of maize on the first and second day after application. Gouws [53] reported an increase in the root biomass of *Lotus japonicus* and tomato when treated with lumichrome. According to the author, the treatment with lumichrome caused complex changes in the gene expression of *L*. *japonicus* and tomato, being mainly affected the genes associated with the transcription regulation and ribonu‐ cleic acid (RNA) signaling, synthesis, degradation, proteins modification, and plant stress responses. The mechanism by which lumichrome promotes the plants growth still needs

Other microorganisms, such as *Azospirillum* spp. [54, 55], *Acetobacter diazotrophicus* [56], *Herbaspirillum seropedicae* [56], *Klebsiella pneumoniae* [55], *Pseudomonas syringae* [57], and *Paenibacillus polymyxa* [58], also produce phytostimulatory substances and are also related to

Siderophores are iron‐chelating compounds, nutrients that limit the microbial population growth in the soil's environment. Fe must be present as Fe2+, and many microorganisms such as bacteria and fungi have developed mechanisms to chelate Fe3+ through the production of

Siderophores are Fe sequestrants of high affinity and low molecular weight. Among the sid‐ erophores known, pyoverdine and enterobactin are secreted by microorganisms in response

under ion‐deficiency conditions by fungi and bacteria in order to incorporate this mineral into

Because of their great ability to compete for the cell metabolism, microorganisms producing sider‐ ophores are capable of suppressing the growth and development of pathogenic microorganisms that inhabit the rhizosphere, thus indirectly contributing to the health of cultivated species of plants, such as grasses. Some rhizobacteria of the *genera Pseudomonas* can produce iron‐chelating compounds, present in low concentrations in the rhizosphere, and thus suppressing the pres‐

entering the cell without reducing Fe3+ [60]. Thus, siderophores can capture Fe3

in solution [59]. The siderophores are iron‐chelating compounds,

+

produced

of the fall of leaves and fruits [52].

**3.3. Other phytostimulating‐producing bacteria**

siderophores before being transformed into Fe2+.

+

**3.4. Siderophore‐producing bacteria**

to the low availability of Fe3

the cell metabolism [61].

ence of pathogens near the roots [62].

the stimulation of grasses and other nonleguminous species.

to be clarified.

Gibberellins (GAs), phytohormones produced by rhizobia, stimulate stem growth [7, 21], whose effect is mostly observed in grasses, vegetables, and ornamental plants [44]. Important effects of GAs are evident during plant growth, especially on stem elongation, with increased leaf growth and xylem differentiation [45]. At determined GA content, the higher or lower IAA level means the optimal level [46]. Therefore, a certain balance between GA and IAA is essential for the maximum growth rate.

Erum and Bano [7] quantified the production of IAA and GA by rhizobia, using high pressure liquid chromatography (HPLC). The rhizobia, isolated from soil in northern Pakistan, located at 940–3090 m above sea level, produced phytohormones, and the GA production was about 10–30 times higher than the production of IAA. There was a positive and increasing correla‐ tion between the GA/IAA ratio produced and this altitude. According to the authors, the IAA and GA concentration gradient may represent a decrease of natural resources, such as radia‐ tion intensity, soil moisture, and soil nutrients.

Although cytokinins are produced by rhizobia [6], they have been little studied as it is difficult to detect and quantify them. Cytokines stimulate cell division (cytokinesis), being produced in the plant's root and transported through the xylem to the plant. The levels of auxin and cytokinins are inversely correlated in the plant [47]. Other phytoestimulators produced by rhizobia, the lipochitooligosaccharides (LCO), also known as Nod factors, are responsible for the morphoge‐ netic changes in legume roots during nodulation [48]. They have also stimulated the germina‐ tion of maize, rice, beet, and cotton, under laboratory, greenhouse, and field conditions [32].

Although the key role of LCO produced by rhizobia in nodule formation is clear, other mor‐ phogenetic activities in plants were attributed to LCOs, including the stimulation of genes in the cell division cycle and stimulation of mitotic divisions in protoplasm cultures of legumes and nonlegumes [49].

Miransari and Smith [28] tested the effect of LCO extracted from *B. japonicum* and gibberel‐ lin on barley seed germination. In the treatment with 10−5 M of gibberellin, there was 18% increase in the seedling germination compared to the control treatment, whereas in the treat‐ ment with 10−6 M of LCO, the increase represented 44%.

Some rhizobia can lower the level of ethylene excreted by the plants by forming the amino‐ cyclopropane carboxylic (ACC) acid deaminase, an enzyme that breaks ACC, a precursor of ethylene [50]. This enzyme was found in rhizospheric bacteria of the genus *Pseudomonas*, *Alcaligenes*, *Rhodococcus*, and *Rhizobium* [34, 51]. In addition, some bacteria of *Rhizobium japonicum* (*B japonicum*) species synthesize phytotoxic antibiotics, aminoethoxyvinylglycine, and rhizobitoxin, which inhibit the formation of ethylene in plants [52]. The ethylene is a plant growth inhibitor, therefore bacteria that regulate its production can indirectly stimulate the plants and may be associated with the cell development, cell extension and the postponement of the fall of leaves and fruits [52].

*S. meliloti* can produce lumichrome [33]. The application of lumichrome in nanomolecular concentrations promoted the growth of legumes and grasses [43]. According to Ref. [48], the lumichrome stimulated the photosynthetic index of maize on the first and second day after application. Gouws [53] reported an increase in the root biomass of *Lotus japonicus* and tomato when treated with lumichrome. According to the author, the treatment with lumichrome caused complex changes in the gene expression of *L*. *japonicus* and tomato, being mainly affected the genes associated with the transcription regulation and ribonu‐ cleic acid (RNA) signaling, synthesis, degradation, proteins modification, and plant stress responses. The mechanism by which lumichrome promotes the plants growth still needs to be clarified.

#### **3.3. Other phytostimulating‐producing bacteria**

Other microorganisms, such as *Azospirillum* spp. [54, 55], *Acetobacter diazotrophicus* [56], *Herbaspirillum seropedicae* [56], *Klebsiella pneumoniae* [55], *Pseudomonas syringae* [57], and *Paenibacillus polymyxa* [58], also produce phytostimulatory substances and are also related to the stimulation of grasses and other nonleguminous species.

#### **3.4. Siderophore‐producing bacteria**

*Bradyrhizobium japonicum* rhizobia isolated from soybean roots, *Azorhizobium caulinodans* iso‐ lated from *Sesbania rostrata*, *Rhizobium* NGR234 isolated from *Lablab purpureus*, *Sinorhizobium meliloti* isolated from *Medicago sativa*, *R. leguminosarum* bv. *viceae* Cn6, and *R*. *leguminosarum* bv. *viceae* strain 30 isolated from *Vicia faba* could infect and colonize sorghum and *Setaria* roots [43]. Considering that this distinct group of rhizobia isolated from different legumes can colo‐ nize these two grasses, the authors suggest that the infection of nonlegumes by rhizobia is more likely due to natural conditions than imagined. There was an increase in the growth of inoculated sorghum and *Setaria*, as well as an increase of P in the sorghum. According to the authors, this may have occurred due to the induction of bacteria as phosphate transporters

Gibberellins (GAs), phytohormones produced by rhizobia, stimulate stem growth [7, 21], whose effect is mostly observed in grasses, vegetables, and ornamental plants [44]. Important effects of GAs are evident during plant growth, especially on stem elongation, with increased leaf growth and xylem differentiation [45]. At determined GA content, the higher or lower IAA level means the optimal level [46]. Therefore, a certain balance between GA and IAA is

Erum and Bano [7] quantified the production of IAA and GA by rhizobia, using high pressure liquid chromatography (HPLC). The rhizobia, isolated from soil in northern Pakistan, located at 940–3090 m above sea level, produced phytohormones, and the GA production was about 10–30 times higher than the production of IAA. There was a positive and increasing correla‐ tion between the GA/IAA ratio produced and this altitude. According to the authors, the IAA and GA concentration gradient may represent a decrease of natural resources, such as radia‐

Although cytokinins are produced by rhizobia [6], they have been little studied as it is difficult to detect and quantify them. Cytokines stimulate cell division (cytokinesis), being produced in the plant's root and transported through the xylem to the plant. The levels of auxin and cytokinins are inversely correlated in the plant [47]. Other phytoestimulators produced by rhizobia, the lipochitooligosaccharides (LCO), also known as Nod factors, are responsible for the morphoge‐ netic changes in legume roots during nodulation [48]. They have also stimulated the germina‐ tion of maize, rice, beet, and cotton, under laboratory, greenhouse, and field conditions [32].

Although the key role of LCO produced by rhizobia in nodule formation is clear, other mor‐ phogenetic activities in plants were attributed to LCOs, including the stimulation of genes in the cell division cycle and stimulation of mitotic divisions in protoplasm cultures of legumes

Miransari and Smith [28] tested the effect of LCO extracted from *B. japonicum* and gibberel‐ lin on barley seed germination. In the treatment with 10−5 M of gibberellin, there was 18% increase in the seedling germination compared to the control treatment, whereas in the treat‐

Some rhizobia can lower the level of ethylene excreted by the plants by forming the amino‐ cyclopropane carboxylic (ACC) acid deaminase, an enzyme that breaks ACC, a precursor of ethylene [50]. This enzyme was found in rhizospheric bacteria of the genus *Pseudomonas*,

from the plasma membrane of sorghum root cells.

essential for the maximum growth rate.

18 Grasses - Benefits, Diversities and Functional Roles

tion intensity, soil moisture, and soil nutrients.

ment with 10−6 M of LCO, the increase represented 44%.

and nonlegumes [49].

Siderophores are iron‐chelating compounds, nutrients that limit the microbial population growth in the soil's environment. Fe must be present as Fe2+, and many microorganisms such as bacteria and fungi have developed mechanisms to chelate Fe3+ through the production of siderophores before being transformed into Fe2+.

Siderophores are Fe sequestrants of high affinity and low molecular weight. Among the sid‐ erophores known, pyoverdine and enterobactin are secreted by microorganisms in response to the low availability of Fe3 + in solution [59]. The siderophores are iron‐chelating compounds, entering the cell without reducing Fe3+ [60]. Thus, siderophores can capture Fe3 + produced under ion‐deficiency conditions by fungi and bacteria in order to incorporate this mineral into the cell metabolism [61].

Because of their great ability to compete for the cell metabolism, microorganisms producing sider‐ ophores are capable of suppressing the growth and development of pathogenic microorganisms that inhabit the rhizosphere, thus indirectly contributing to the health of cultivated species of plants, such as grasses. Some rhizobacteria of the *genera Pseudomonas* can produce iron‐chelating compounds, present in low concentrations in the rhizosphere, and thus suppressing the pres‐ ence of pathogens near the roots [62].

#### **3.5. Phosphate solubilizing bacteria**

Together with N and K, P is one of the required macronutrients for the cultivation of grasses, whose content concentration is always lower than N and K. However, it is commonly neces‐ sary to use a great amount of phosphate fertilizers in agricultural crops, because in spite of the soils contain a large amount of P their availability to the plants is very little as P tends to form very low solubility compounds in the soil [63].

it in a long term. There are currently commercial products based on genus *Trichoderma* strains, properly registered in the Brazilian Ministry of Agriculture, Livestock, and Food Supply (MAPA) that are indicated for the controlling of diseases caused by phytopathogenic agents, such as *Rhizoctonia*, *Fusarium*, and *Sclerotinia* [72]. Harman [4] and Machado et al. have described the benefits of *Trichoderma* inoculation on grass yield, observing an increase in

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21

Soil microorganisms are able to influence the establishment and yield of grasses by means of sev‐ eral mechanisms. The nutrients cycling by soil microorganisms, the biological nitrogen fixation by associative bacteria, phytohormones production by soil bacteria, and the acquisition of phosphorus by mycorrhizal fungal hyphae networks are just some examples of direct mechanisms of beneficial interaction between soil microorganisms and cultivated grasses. As examples of indirect mecha‐ nisms, we can mention the suppression of pathogens by mechanisms of predation or competition, as we also discussed. Given this wide range of mechanisms presented by microorganisms for the benefit of cultivated grasses and consequently of the human benefit, it is imperative that these mechanisms are well studied to be inserted in systems of conservationist agriculture, which must obtain the maximum agronomic yield of the crops, allied to the rational use of natural resources.

2 College of Agronomy, Institute of Educational Development from Passo Fundo, Brazil

[1] Gans J, Wolinsky M, Dunbar J. Computational improvements reveal great bacterial diversity and high metal toxicity in soil. Science. 2005;**309**:1387‐1390. DOI: 10.1126/

[2] Bashan Y, Holguin G. *Azospirillum*‐plant relationships: Environmental and physiologi‐ cal advances. Canadian Journal of Microbiology. 1997;**43**:103‐121 DOI: 10.1139/m97‐015

[3] Taiz L, Zieger E, editors. Fisiologia Vegetal. 3rd ed. Porto Alegre: Artemed; 2004. p. 719

[4] Harman GE. Myth and dogmas of biocontrol changes in perceptions derived from research on *Trichoderma harzianum* T‐22. Plant Disease. 2000;**84**:377‐393. DOI: 10.1094/

maize and black oat yields, respectively.

**6. Final considerations**

**Author details**

**References**

Rafael Goulart Machado

1 Emater‐RS/ASCAR, Brazil

science.1112665

PDIS.2000.84.4.377

Address all correspondence to: rgoulartmachado@gmail.com

Phosphorus is an essential element to grasses, since it is necessary and irreplaceable for the com‐ position of ribonucleic acids (RNA) and deoxyribonucleic acids (DNA), responsible for the trans‐ mission of the genetic code to the plants, protein production, and other essential compounds for the plant structure and seedling production. Grasses absorb soil P as H<sup>2</sup> PO<sup>4</sup> − and HPO<sup>4</sup> 2−, just like other plant species; thus, insoluble phosphates like tricalcium phosphate (Ca<sup>3</sup> (PO<sup>4</sup> ) 2 ) make this nutrient unavailable to the plant. Some of the soil bacteria are important in the process of dissolving these insoluble solutions, facilitating the access to this essential nutrient.

Inorganic phosphate‐solubilizing microorganisms excrete inorganic acids and protons asso‐ ciated to these acids, which directly dissolve the insoluble phosphate, or chelate the cations with the phosphate anion [64]. Among phosphate‐solubilizing bacteria, *Burkholderia* [65], *Bacillus*, and *Penicillium* strains [66] have been reported.

## **4. Mycorrhizae**

Mycorrhizal fungi are associated with roots of plants and play an important role in the soil phosphorus cycling as extensions of the root system, increasing the absorbing area of the root and the absorption rate of phosphorus. The mycorrhizal association does not substitute phos‐ phate fertilization, but efficiently increases the use of phosphorus or an added compound through fertilization [67]. Grasses such as maize, sorghum, wheat, rice, and cultivated forage grasses may have their roots naturally colonized by mycorrhizal fungi [68].
