Introduction
Livestock production in pastures demonstrates the resilience of tropical
forage grasses, however, their sustained exposure to stressful conditions
compromises their physiology (Li et al. 2009), limiting productivity and
reflecting in poor livestock management practices. The stress imposed on plants
can be alleviated using sustainable tools, among which biological inputs play a
significant role, improved the tolerance of plants to physiological
disturbances caused by factors biotics and abiotic (Colla et al. 2015).
Among the bio inputs available
in the market, microbiological inoculants composed of fungi or strains of
rhizobacteria are utilized in diverse agriculture crops and frequently denominated
as plant growth-promoting microorganisms (PGPM) (Brazil 2020). Their primary
function is to enhance plant growth and provide protection against biotic and
abiotic stresses (Souza et al. 2015). These microorganisms can engage in
mechanisms ranging from biological nitrogen fixation, phosphorus solubilization,
resistance to soil pathogens, and an increase in root surface area (Bashan et
al. 2012; Yasmin et al. 2016; Majeed et al. 2022), thereby
providing plants with increased nutrient and water uptake.
Plant growth-promoting
mechanisms, mediated by rhizobacteria and mycorrhizal fungi, demonstrate significant
potential for optimizing plant development (Nadeem et al. 2014; Rouseaux
et al. 2020; Dawood et al. 2023). These microorganisms can
establish a synergistic relationship between themselves and between species of
plants, maximizing their effectiveness in promoting the growth of host plants.
Studies have shown that fungal structures function as a communication route for
bacteria, facilitating their penetration into the epidermis of the root tissue,
while the production of phytohormones by these bacteria favors the colonization
and mycelial growth of mycorrhiza (Ruíz-Sánches et al. 2011;
Villarreal et al. 2016). However, it is important to highlight that
antagonistic interactions can arise due to competition for nutrients and other
resources essential for the survival of these microorganisms in the
rhizosphere. The success or failure of co-inoculation is intrinsically linked
to the physiological stage of the host, the time of infection, and the
divergent nutritional demands between fungi and rhizobacteria (Biró et al.
2000).
Considering the global panorama
with climate and extreme events (Feller and Vaseva 2014), growing demand for
food and the responsibility for sustainable pasture production (Guimarães et
al. 2022); the use of microbial inoculants in grass species present in
pastures, such as Megathyrsus maximus (Jacq.) BK Simon and SWL Jacobs
(syn. Panicum maximus Jacq.) emerge as a viable alternative to increase
sustainability in the cultivation of agronomically important plants. However,
studies are needed to clarify and validate the use of bioinoculants in
pastures, aiding in the better adaptation of forage crops in challenging
scenarios. The present study was aimed to evaluate the effect of single and dual
inoculation with R. intraradices and A. brasilense on initial
growth, root characteristics and chemical composition of aerial part of Mombasa
grass.
Materials and Methods
Experimental details
Experiments were performed in the greenhouse of the Department of Rural
and Animal Technology, State University of Southwest Bahia, Itapetinga, Bahia
(15º 14' S, 40º 14' W), during October–January of the years 2020–2021. Weather
data during the experimental period were obtained using a digital
thermo-hygrometer. The average maximum and minimum temperature values were 39.4
ºC and 20.4ºC, respectively, and the maximum relative humidity was 84% and
minimum was 20%.
The soil used in the experiment
was collected at a depth of 0–20 cm and subjected to physical and chemical
analysis at the Department of Agricultural and Soil Engineering, State
University of Southwest Bahia. The soil analysis demonstrated the following
result: Sandy-loam textured, clay 9%, silt 35.5%, sand 55.5%, pH (water) 6.3,
phosphorus (ion-exchange resin extraction method) 15 mg.dm-3,
potassium 0.97 cmolc.dm-3, calcium 1.5 cmolc.dm-3,
magnesium 1.6 cmolc.dm-3, H + Al 1.1 cmolc.dm-3, sum of
bases 4.1 cmolc.dm-3, effective cation exchange capacity 4.2
cmolc.dm-3, total cation exchange capacity 5.2 cmolc.dm-3,
base saturation 79%, organic matter 7 g.dm-3.
Treatments and experimental design
Mombasa grass was evaluated in four different treatments consisting of
(i) a non-inoculated group (Control), (ii) inoculation with Azospirillum
brasilense, (iii) inoculation with Rhizophagus intraradices and (iv)
co-inoculation with A. brasilense and R. intraradices. The
experiment was randomized according to completely randomized design with four
replications, totaling 16 experimental units (plastic pots), with a capacity of
12 L and, which were filled with 10 kg of soil. To maintain the soil close to
the water retention capacity in 30% (Souza et al. 2020), all pots were
weighed every day and water was added as needed.
According to the recommendations
of the Soil Fertility Commission of Minas Gerais State (Ribeiro et al.
1999), there was no need for liming. Only phosphorus and nitrogen were used
after the uniformity cut, with basal fertilization being carried out for
establishment with 50 kg ha-1 of P2O5 and 50
kg ha-1 of nitrogen in the form of urea and simple superphosphate
respectively.
Application of PGPM and sowing of seeds
Before planting and inoculation, seeds were surface disinfected by
immersion in 3% sodium hypochlorite for 3 min, followed by four consecutive rinses
in water and air drying. For inoculation with A. brasilense, a
commercial product containing Ab-V5 and Ab-V6 strains was used, with a
guarantee of 2 x 108 CFU mL-1, with a recommendation of
100 mL of inoculant for 5 kg of seeds, which were homogenized and dried in the
shade for 30 min. For inoculation with R. intraradices, a commercial
inoculant was used with a guarantee of 20,800 propagules g-1, using
120 g ha-1 added to the planting hole immediately after sowing; the
co-inoculation treatment used a combination of the previously mentioned forms
of inoculation. Five seeds were sown per unit experimental and 15 days after
the emergence, seedlings were thinned to four plants per pot.
The microbial inoculants used in
this study are registered with the Ministry of Agriculture, Livestock and
Supply for commercialization in Brazilian territory. Commercial product
containing A. brasilense strains registration number: 22902 10000-0;
Commercial product containing R. intraradices registration number:
PR-93923-10074-1.
Parameters analyzed
When the plants completed 30 days after emergence, a cut of
uniformization was realized at a height of 20 cm, and fertilization with
phosphorus and nitrogen was performed. After cutting to standardize the
experimental units, monitoring of the regrowth of Mombasa grass began, with
evaluation during two periods of 28 days.
For evaluation, two tillers per
pot were marked with colored ribbons and evaluated every 3 days. The following
were determined by measurements of individual leaves and tillers: leaf
appearance rate (LAR, leaves tiller-1 day-1); phyllochron
(PHY, leaves tiller-1 day-1); leaf elongation rate (LER,
cm leaves tiller-1 day-1); leaf senescence rate (LSR, cm
tiller-1 day-1); number of living leaves per tiller
(NLL), final leaf length (FLL, cm leaf-1); tiller density (TD), and
final plant height (FPH, cm).
At the end of each evaluation
period, the SPAD (Soil Plant Analytical Division Value) index was read using a
SPAD 502 Plus device at times of highest solar incidence, with readings taken
in the middle third of two completely expanded leaves within each experimental
unit. Then, the same leaves used to read the SPAD index were collected for
extraction of photosynthetic pigments (Chlorophyll a, Chlorophyll b,
Total chlorophyll and Carotenoids), which were cut, excluding the central vein,
weighed 0.2 g, stored in 5 mL of dimethyl sulfoxide, and kept for 72 h in the
dark. Afterwards, readings were taken on the spectrophotometer at wavelengths
of 665, 649 and 480 nm and quantified according to Wellburn (1994), with results
expressed in µg.g-1 fresh
mass.
After collecting the material
for chlorophyll, a cut was made 20 cm from each experimental unit. The
harvested material was identified, weighed, and taken to a forced air
circulation oven at 65°C for pre-drying for 72 h, then weighed again, thus
calculating the biomass production of the area (g.pot-1). The
material was then ground in a Willey-type knife mill with a 1 mm sieve to carry
out bromatological composition, where the contents of dry matter (DM, method
INCT-CA G-003/1), mineral matter (MM, INCT-CA method M-001/1), crude protein
(CP, INCT-CA method N-001/1) and neutral detergent fiber (NDF, INCT-CA method
F002/1) and acid detergent fiber (ADF, method INCT-CA F-004/1) according to
methodologies described by Detmann et al. (2021), being carried out in
the University’s Bromatological Analysis Laboratory.
The experimental units were dismantled after the
second cut, and the roots were removed and washed in running water. The volume
of the root system was estimated using a cylindrical vessel with graduations,
recording the water displacement after immersion of the roots. The root system
was then dried in an oven at 65°C until constant weight and then weighed to
obtain the root dry weight.
Statistical analysis
The data obtained were grouped and analyzed as the average of two
experimental cutting. The dataset was analyzed by one-way analysis of variation
(ANOVA), when significant differences were detected; means were compared with Tukey’s
test at the 5% level, by using SAS software OnDemand for Academics.
Results
Morphogenic and structural characteristics
Different
inoculation treatments displayed diverse responses on development and growth of
Mombasa grass. LAR, LER, PHY and NLL (P <
0.001 for all) were greater with A. brasilense and R.
intraradices inoculated single, whereas PHY and NLL (P < 0.001 for both) were higher in non-inoculated plants and
co-inoculation. Compared to the non-inoculated plants, the plants treated by
co-inoculation or single inoculation with R. intraradices and A.
brasilense represents 83% significantly higher leaf senescence rate (P < 0.001). On the other hand, the
variables FLL, TD and FPH were not significant (P = 0.200, P = 0.082
and P = 0.080 respectively), presenting averages of 39.44 cm leaf-1,
16.62 tillers and 59.06 cm, respectively (Table 1).
Photosynthetic pigments
Chlorophyll a concentration and SPAD index value were influenced by the
treatments tested (P < 0.001 for
both) being 26 and 22%, respectively, greater when inoculated with microorganisms
than in the non-inoculated plants. No differences were found for chlorophyll b,
total chlorophyll, and carotenoids (P
= 0.090, P = 0.075 and P = 0.165),
with averages of 31.58 µg.g-1
of fresh biomass, 211.19 µg.g-1
of fresh biomass and 23.25 µg.g-1
of fresh biomass, respectively (Table 2).
Productive parameters
The production of fresh and dry biomass (Fig. 1) was significantly
greater (P < 0.001 for both) in
the presence of A. brasilense, with respective values of 21.25 g. pot-1
and 5.86 g.pot-1. The other treatments were equivalent for these
variables, not differing from each other or from the non-inoculated plants,
with averages of 18.37 g.pot-1 of fresh biomass (P = 0.270)
and 5.05 g.pot-1 of dry biomass (P
= 0.124).
Bromatological characteristics
Inoculation with A. brasilense resulted in greater averages for
MM and CP contents (P = 0.001 and P = 0.010) than the
non-inoculated plants treatment, with percentage increases of 5.25 and 13.41%,
respectively. Conversely, for variables DM, NDF and ADF no effects were
observed for any inoculation (P = 0.572, P = 0.165 and P = 0.362
respectively), with an average of 27.55, 67.12 and 33.36% respectively (Table 3).
Root evaluation
Plants inoculated with A. brasilense and co-inoculated showed
greater averages for root system volume (average of 74 mL) and root dry weight
(average of 134.46 g) (P < 0.001), with a percentage increase of 29
and 18%, respectively, in relation to the non-inoculated plants (Table 4).
Table 1: Morphogenic and structural
characteristics of Mombasa grass inoculated with plant growth-promoting
microorganisms
|
Items |
Control |
A. brasilense |
R. intraradices |
Co-inoculation |
CV% |
|
LAR |
0.23b |
0.32a |
0.36a |
0.27b |
8.75 |
|
PHY |
4.32a |
3.04b |
3.01b |
3.82a |
9.73 |
|
LER |
3.07c |
4.72b |
5.56ab |
3.57cb |
17.25 |
|
LSR |
1.32a |
0.92b |
0.65b |
0.60b |
23.91 |
|
NLL |
5.00b |
7.15a |
7.17a |
5.66b |
8.64 |
|
FLL |
41.41 |
39.65 |
36.10 |
40.61 |
10.07 |
|
TD |
16.25 |
15.25 |
17.75 |
17.25 |
17.92 |
|
FPH |
59.50 |
59.75 |
60.25 |
56.75 |
8.66 |
LAR: Leaf appearance rate (tiller leaves-1
day-1); PHY: phyllochron (tiller leaves-1 day-1);
LER: Leaf elongation rate (cm leaves tiller-1 day-1);
LSR: leaf senescence rate (LSR, cm tiller-1 day-1); NLL:
number of living leaves (per tiller); FLL: final length of leaves (cm.leaf-1);
DFV: leaf life span (days); NP: tiller density; FPH: final plant height (cm);
CV: coefficient of variation; Means within lines followed by different letters
differ by Tukey’s test at 5% probability
Table 2: Concentration of
chlorophylls, carotenoids (µg.g-1 of fresh mass) and SPAD index of
Mombasa grass inoculated with plant growth-promoting microorganisms
|
Items |
Control |
A. brasilense |
R. intraradices |
Co-inoculation |
CV% |
|
Chlorophyll a |
152.66b |
184.60ab |
188.45ab |
192.76a |
9.69 |
|
Chlorophyll b |
38.87 |
29.85 |
24.12 |
33.48 |
26.78 |
|
Total chlorophylls |
191.51 |
214.45 |
212.58 |
226.24 |
8.33 |
|
Carotenoids |
28.58 |
23.81 |
23.82 |
16.82 |
38.72 |
|
SPAD |
16.17b |
19.38a |
19.00a |
20.90a |
5.98 |
CV: coefficient of
variation; Means within lines followed by different
letters differ by Tukey’s test at 5% probability
Table 3: Chemical composition of
Mombasa grass inoculated with plant growth-promoting microorganisms
|
Items |
Control |
A. brasilense |
R. intraradices |
Co-inoculation |
CV% |
|
DM |
27.66 |
27.69 |
27.65 |
27.23 |
5.65 |
|
MM |
7.81c |
8.22a |
7.86b |
7.96b |
7.74 |
|
NDF |
65.54 |
68.96 |
68.45 |
65.54 |
4.39 |
|
ADF |
32.11 |
34.58 |
34.54 |
32.23 |
8.66 |
|
CP |
5.74b |
6.51a |
6.11ab |
6.17ab |
5.26 |
DM: dry matter; MM:
mineral matter; NDF: neutral detergent fiber; ADF: acid detergent fiber; CP:
crude protein; CV: coefficient of variation. Means within lines followed by different letters
differ by Tukey’s test at 5% probability
Table 4: Root
characteristics of Mombasa grass inoculated with plant growth-promoting
microorganisms
|
Items |
Control |
A. brasilense |
R. intraradices |
Co-inoculation |
CV% |
|
Root volume |
59.40b |
77.00a |
60.60b |
71.00ba |
13.44 |
|
Root dry weight |
113.53b |
130.84a |
115.75b |
138.08a |
23.05 |
CV: coefficient of
variation; Means within lines followed by different letters differ by Tukey’s
test at 5% probability
%20410-416_files/image002.png)
Fig. 1:
Shoot fresh and dry weight of the aerial part of Mombasa grass inoculated with
plant growth-promoting microorganisms. Means followed by different letters, for
each items analyzed, differ by Tukey’s test at 5% probability (Coefficient of
variation for shoot fresh: 10.60%; Coefficient of variation for Shoot dry:
5.32%)
Discussion
The benefit of using plant growth-promoting microorganism has been
reported by several authors, contributing positively to crop development with
improvements in nutrient absorption, resistance to pathogens, and root
development (Souza et al. 2011; Goswami et al. 2016; Fukami et
al. 2018). In this study, we present results of morphogenic,
bromatological, and biomass production characteristics in Mombasa grass,
assessed under controlled conditions using commercial inoculants applied in
seeds.
Seed inoculation with the
microbial inoculant employed has improved various morphogenic parameters of
Mombasa grass, leading to a greater leaf appearance rate and a lower
phyllochron value, while also increasing the number of live leaves (Table 1).
The ability of A. brasilense strains to produce and modulate the level
of endogenous phytohormones like auxins, gibberellins and cytokinins (Cassán et
al. 2020) and arbuscular mycorrhizal fungi R. intraradices to assist
in water and nutrient absorption (Begum et al. 2019), can stimulate the
proliferation and elongation of plant cells, root elongation and stimulating
the differentiation of meristematic tissues (Glick 2014; Souza et al.
2017), reflected in the improvement of the morphogenic characteristics. This
indicates that the inoculants used can activate mechanisms that influence the
generation and development of new leaves, resulting in a greater flow of
tissue, increased interception efficiency, and enhanced conversion of luminous
energy by Mombasa grass.
Considering combined or isolated
inoculation, remarkable results were observed for the SPAD index and
chlorophyll a (Table 2), translating into greater photosynthetic
efficiency and consequently increased biomass production. Our findings confirm
the hypothesis that the use of plant growth-promoting microorganisms results in
greater nitrogen assimilation by plants compared with the non-inoculated plants;
this underscores the positive impact of using these microorganisms in enhancing
plant growth and nutrient assimilation processes.
The strategy of isolated
inoculation with A. brasilense increased the dry biomass production of
the aboveground part of Mombasa grass, representing a percentage increase of
approximately 19% compared with the non-inoculated plants. Microbial
bioinoculants have numerous positive functions associated with the absorption
of essential elements for plant development. A. brasilense has the
ability to synthesize auxins that stimulate development and improve the root
system (Hungria et al. 2021; Guimarães et al. 2023), optimizing
nutrient absorption by adding improvements in photosynthetic activity through
the efficient assimilation of these elements, which favors productive capacity.
This signifies potential benefits
for productive systems that rely on pasture renewal techniques. Positive gains
in the biomass production of forage grasses associated with A. brasilense
have been reported, as seen in species such as U. ruziziensis (Hungria et
al. 2021), Mulato II grass (Rouseaux et al. 2020), Mombassa and Zuri
grasses (Guimarães et al. 2023). These findings highlight the promising
impact of microorganism-based strategies in enhancing biomass yield, which is
particularly relevant for sustainable pasture management practices.
Improvement in forage quality is
another crucial aspect of productive systems associated with microbial
inoculant. The plant microorganism association can optimize fertilizer
utilization through enhanced absorption de soil nutrient. The anticipation is
that such advancements will contribute to more sustainable agricultural practices
by promoting efficient nutrient use, thereby mitigating the environmental
impacts associated with livestock production.
The results confirm the viability
of using bioinoculants in the bromatological characteristics of Mombasa grass
subjected to seed inoculation, as evidenced by the mineral content and crude
protein values. This is particularly noticeable with the use of A.
brasilense, which is characterized by a percentage increase of 5.25 and
13.41%, respectively, compared with non-inoculated plants. These improvements
are attributed to the benefits of enhanced root growth, leading to increased
nutrient absorption. The findings underscore the positive impact of seed
inoculation with A. brasilense on the nutritional composition of Mombasa
grass, highlighting its potential in optimizing the mineral and protein content
of forage crops.
Strains of A. brasilense
possess the capacity to synthesize phytohormones, primarily indole-3-acetic
acid (IAA), which aids in root growth and optimizes the absorption of nutrients
and water (Fukami et al. 2018; Cassán et al. 2020). Arbuscular
mycorrhizal fungi, such as R. intraradices, can result in positive plant
development. These fungi grow within the cortex cells and extend their hyphae
into the soil, forming a mycelial network that acts as an extension of the
roots, optimizing the absorption of water and nutrients (Smith and Read 2008).
Therefore, plants with heavier roots and a larger root volume may indicate the
potential for soil exploration, optimizing the absorption of essential elements
for their development, which can contribute to the establishment and
sustainability of the system.
Conclusion
These results suggested that single inoculation of A. brasilense
or R. intraradices improved the initial growth of Mombasa grass. Data
further revealed that dual inoculation with these microorganisms cooperated
synergistically to stimulate root development and improved nutritional status.
Therefore, the use of this microbial inoculant as an alternative is capable of
optimizing the initial growth of Mombasa grass for sustainable production.
Acknowledgements
The authors thank the State University of Southwest Bahia and The Coordination
of Improvement of Higher Education Personnel for their assistance and financial
support with number of process 88887.611572/2021-00.
Author Contributions
HSS: Formal analysis, Conceptualization, Data curation, Investigation,
Methodology, Project administration, Resources, Validation, Writing – original
draft. TMV, NVS, ICD, BEFS, EMVP, JASJ and TPRS: Investigation, Methodology,
Visualization. NTC: Writing – review and editing. DDF, RRJ and FAT:
Supervision, Validation, Writing – review and editing. All the authors have
read and agreed to the submitted version of the manuscript.
Conflicts of Interest
No potential conflict of interest was reported by the authors.
Data Availability
Data presented in this study will be available on a fair request to the
corresponding author.
Ethics Approval
Not applicable to this paper.
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