© The Authors, 2023, Published by the Universidad del Zulia*Corresponding author: wceiroc@gmail.com
Keywords:
Biostimulation
Bioassays
Microorganisms
Yield
Autochthonous microorganisms as an alternative for biofertilization of Nicotiana tabacum L.
Microorganismos autóctonos como alternativa de biofertilización de Nicotiana tabacum L.
Microorganismos autóctones como alternativa para biofertilização de Nicotiana tabacum L.
Lianet Brizuela-Fuentes
1
Ramón Jaime Holguín-Peña
2
Elio Macías Nuñes
1
Wilson Geobel Ceiro-Catasú
3
*
Rev. Fac. Agron. (LUZ). 2022, 40(3): e234023
ISSN 2477-9407
DOI: https://doi.org/10.47280/RevFacAgron(LUZ).v40.n3.01
Crop production
Associate editor: Dra. Lilia Urdaneta
University of Zulia, Faculty of Agronomy
Bolivarian Republic of Venezuela
1
Department of Agronomy, Faculty of Agricultural Sciences,
University of Granma, Bayamo, PO Box 21, C.P. 85100,
Granma, Cuba.
2
Phytopathology Laboratory, Agriculture in Arid Zones
Program. Centro de Investigaciones Biológicas del Noroeste,
Mar Bermejo 195. Colonia Playa Palo de Santa Rita. C.P. 23070.
La Paz, B.C.S., Mexico.
3
Postdoctoral, Phytopathology Laboratory, Agriculture in Arid
Zones Program, Centro de Investigaciones Biológicas del
Noroeste, La Paz, Baja California Sur, Mexico; Postdoctoral
in Agricultural and Environmental Sciences, University of San
Carlos of Guatemala.
Received: 26-02-2023
Accepted: 02-06-2023
Published: 27-06-2023
Abstract
Tobacco is a crop of economic importance in tropical countries;
it generates signicant income in small agricultural areas. Within the
agrotechnical activities that are carried out on this plant, biofertilization
with Autochthonous Microorganisms (AM) represents a viable option for
production with low inputs. Therefore, the objective of the research was to
determine the biofertilizer eect of AM on black tobacco cv. Havana-2000.
The experiment was carried out on a farm located in Los Cayos, Yara,
Granma, Cuba, during the period November-February/2021. For this, the
yield variables and the components were measured in the eld. Statistical
processing was performed using ANOVA and principal component analysis.
The AM recorded four groups of microbes: bacteria (7x10
12
CFU.mL
-1
)
Lactobacillus sp. and Rhodopseudomonas sp., the fungi (3x10
11
CFU.mL
-1
)
Trichoderma sp., Aspergillus sp. and Penicillium sp., the yeasts (2x10
11
CFU.mL
-1
)
Saccharomyces sp. and Candida sp. and the actinomycete Streptomyces sp.
(1x10
10
CFU.mL
-1
). In the eld, the AM biostimulated between 15 - 82 %
of the yield and the components, achieving the best results at the dose of
36 L.ha
-1
. Finally, the importance of using AM as an organic alternative for
tobacco biofertilization is demonstrated.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2023, 40(3): e234023. July-September. ISSN 2477-9407.
2-6 |
Resumen
El tabaco es un cultivo de importancia económica en países
tropicales, genera ingresos signicativos en pequeñas áreas agrícolas,
dentro de las actividades agrotécnicas que se realizan a esta planta,
la biofertilización con Microorganismos Autóctonos (MA) representa
una opción viable para la producción con bajos insumos. Por ello, el
objetivo de la investigación fue determinar el efecto biofertilizante de
MA
sobre el tabaco negro cv. Habana-2000. El experimento se realizó
en una nca ubicada en Los Cayos, Yara, Granma, Cuba, durante el
período noviembre-febrero/2021. Para ello, se midieron las variables
del rendimiento y los componentes en campo. El procesamiento
estadístico se realizó mediante ANOVA y análisis de componentes
principales. Los MA registraron cuatro grupos de microbios: las
bacterias (7x10
12
UFC.mL
-1
) Lactobacillus sp. y Rhodopseudomonas
sp., los hongos (3x10
11
UFC.mL
-1
) Trichoderma sp., Aspergillus sp. y
Penicillium sp., las levaduras (2x10
11
UFC.mL
-1
) Saccharomycessp.
y Candidasp. y el actinomiceto Streptomycessp. (1x10
10
UFC.mL
-1
).
En campo, los MA bioestimularon entre 15-82 % el rendimiento y
los componentes, lográndose los mejores resultados a la dosis de 36
L.ha
-1
. Finalmente, se demuestra la importancia de usar MA como una
alternativa orgánica de biofertilización del tabaco.
Palabras clave: bioestimulación, bioensayos, microorganismos,
rendimiento.
Resumo
O tabaco é uma cultura de importância econômica em países
tropicais, gera renda signicativa em pequenas áreas agrícolas,
dentro das atividades agrotécnicas que são realizadas nesta planta,
a biofertilização com Microorganismos Autóctones (MA) representa
uma opção viável para produção com baixos insumos. Portanto, o
objetivo da pesquisa foi determinar o efeito biofertilizante do MA
em tabaco preto cv. Havana-2000.O experimento foi realizado
em uma fazenda localizada em Los Cayos, Yara, Granma, Cuba,
durante o período novembro-fevereiro/2021. Para isso, as variáveis
de desempenho e os componentes foram medidos em campo. O
processamento estatístico foi realizado por ANOVA e análise de
componentes principais. O MA registrou quatro grupos de micróbios:
bactérias (7x10
12
UFC.mL
-1
) Lactobacillus sp. e Rhodopseudomonas
sp., os fungos (3x10
11
UFC.mL
-1
) Trichoderma sp., Aspergillus sp. e
Penicillium sp., as leveduras (2x10
11
UFC.mL
-1
) Saccharomyces sp.
e Cândida sp. e o actinomiceto Streptomyces sp. (1x10
10
UFC.mL
-1
).
No campo, o AM bioestimulou entre 15-82 % a produtividade e os
componentes, obtendo os melhores resultados na dose de 36 L.ha
-1
.
Por m, demonstra-se a importância do uso da MA como alternativa
orgânica para a biofertilização do tabaco.
Palavras-chave: bioestimulação, bioensaios, microrganismos,
rendimiento.
Introduction
The cultivation of tobacco (Nicotiana tabacum L.) is part of the
culture of many peoples, as well as, constitutes a crop of economic
importance in tropical countries. In Cuba, it represents a strategic
line within the economy, since it generates the largest income in the
agricultural sector and is considered a cultural tradition. Cuban cigars
have a high quality and great acceptance in the international market,
due to the exotic organoleptic characteristics of the aromatic leaves
(Ceiro-Catasú et al., 2021).
Black tobacco is considered native to Cuba, it is identied
by having a unique aromatic pattern and its cured leaves show a
dark coloration. This type of tobacco is used to obtain layers for
the elaboration of Cuban cigars and strong cigarettes. Among the
cultivars that are established on the island, Havana-2000 has excellent
advantages in terms of its edaphoclimatic adaptability, tolerance to
pests and diseases; as well as it has a potential yield of 2.33 t.ha
-1
, and it
adapts well to the forms of covered cultivation, sun-curing (involves
simply drying the leaves uncovered in the sun) and with indirect
sunlight (Sosa-Sánchez et al., 2022).
Historically, autochthonous microorganisms (AM) have been
used as biofertilizers in tobacco-producing areas, these promote plant
growth, can activate plant defense mechanisms and adaptability to
edaphoclimatic conditions (Ceiro-Catasú et al., 2023; Reinaldo,
2020; Cables-Labrada and Escalona, 2013). Among the most
studied microorganisms are mycorrhizae, bacteria, fungi, yeasts, and
actinomycetes, which stand out for practical agronomic use (Ulacio
et al., 1997).
Currently, AM are considered compatible with sustainable and
low-input agriculture, because their active ingredient is made up
of autochthonous microbial species of four main groups: bacteria,
yeasts, fungi, and actinomycetes, which are characterized by the
biofertilizer eect, biostimulant of growth, activator of plant defenses
and improvers of physical properties, soil chemistry, and biology
(Ramírez et al., 2022; Viera-Arroyo, 2020).
In particular, the bacterial species Lactobacillus plantarum, L.
casei, Rhodopseudomonas palustris, and Rhodobacter sphaeroides
act on the synthesis of amino acids, nucleic acids, bioactive
substances, and carbohydrates, as well as in the degradation of soil
organic matter and as antagonists of pathogens (Xu et al., 2020).
Yeasts (Saccharomyces cerevisiae and Candida utilis) synthesize
hormones and enzymes involved in active cell division in plants, while
their secretions are helpful substrates for feeding other saprophytic
microorganisms (Hernández-Fernández et al., 2021; Nadeem et al.,
2010).
Certain fungal species such as Aspergillus oryzae, Penicillium
sp., Trichoderma sp., and Mucor hiemalis, are considered key in the
transformation and degradation of organic remains, provide nutrients
to plants and synthesize secondary metabolites and antibiotics that
regulate phytopathogen populations in the soil (Tanya-Morocho
and Leiva-Mora, 2019). Actinomycetes (Streptomyces albus and S.
griseus) are involved in the decomposition of soil organic residues
and have an antagonistic eect on phytopathogenic species (Mamani
et al., 2022).
For this reason, autochthonous microbial species are key to the
production of biofertilizers at the local level. Meanwhile, certain crop
residues contain sucient nutrients to articially reproduce microbes
of agronomic interest. In tropical agricultural areas, non-commercial
fragments of cassava root (Manihot esculenta Crantz) remain in
the eld during harvest and have nutritional importance for the
elaboration of AM, due to their adequate contents of carbohydrates,
proteins, dry matter, and minerals, which can be used as nutritive
substrates for the reproduction of AM (Rivas et al., 2022; Ramírez-
Marrache et al., 2019).
Considering the above, the objective of the research was to
determine the biofertilizer eect of the AM on black tobacco cv.
Havana-2000 in open eld conditions.
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Brizuela-Fuentes et al. Rev. Fac. Agron. (LUZ). 2023 40(3): e234023
3-6 |
Materials and methods
Location of the experiment, type of soil and its preparation
The research was carried out on the farm “La Poderosa”, located
at coordinates 20°18’33.75”N and 76°49’20.95”W. This farm
belongs to the farmer Eurelvis Hernández Mascapa, associated with
the Credit and Services Cooperative “José Arteaga” in the town of
Los Cayos, Yara municipality, Granma province, Cuba. The research
was conducted during the period November-February/2021. The
predominant soil was a Fluvisol of medium consistency, with at
relief, without the presence of obstacles, with a loam-clay texture,
MO content of 1.3 %, and a pH of 7. The preparation was carried out
with animal traction, using the minimum tillage and the following
tasks: breaking (25 cm), tiller (20 cm), and furrowing to a depth of
25 cm.
Autochthonous microorganisms and their characteristics
The AM were prepared on the farm with well water of optimum
quality (electrical conductivity (EC): ≤0.8). In 200 L of water, three
components were incorporated for the formulation: mineralogical
(NaCl, 200 g), microbiological (microbial inoculant from the farm,
200 g of mulch + soil at a ratio of 0.5: 1
v
/
v
and nutritious (400 g of
nutritious paste, made from the cooking of residues of Manihot
esculenta root harvest. Once the three components were added to the
vessel, they were homogenized, hermetically sealed, and left to
ferment in the dark for 72 h at room temperature (25 ± 3 °C).
The AM recorded the following characteristics: pH 6.6,
EC: 1.4, and total microbial populations of bacteria 7x10
12
CFU,
fungi 3x10
1
1
CFU, yeasts 2x10
11
CFU, and actinomycetes 1x10
10
CFU; they were quantified by conventional techniques (Da Silva
et al., 2018). The present genera of bacteria, fungi, yeasts, and
actinomycetes were determined in the laboratory of
Agricultural Microbiology, University of Granma, Cuba, by
morphological characterization (Saif et al., 2021; Condori-Pacsi,
2019; Kim et al., 2018; Martínez et al., 2015; Trujillo and
Hernández, 2015; Allende et al., 2013; Cardona, 2011; Said et al.,
1999).
Determination of the biofertilizer effect of the autochthonous
microorganisms on yield variables and components on
black tobacco plants cv. Havana-2000 in the open field
Planting was done manually on November 22, 2021, and
the crop was established at a traditional distance of 0.90 m x
0.30 m. Fertilization with ammonium nitrate at a dose of 100
kg.ha
-1
was used throughout the experimental area. The cultural
practices of identification, hilling, pruning, irrigation, and pest
management were carried out according to the Technical
Instructions (Espino et al., 2012).
Evaluations
They were performed 50 days after transplanting and before the
start of harvest, 25 plants were randomly evaluated for each treatment.
The variables evaluated were: the number of leaves (CH), measured
by direct leaf count for each plant, leaf length (LH in cm), the central
leaf (thin center) was measured from the petiole to the apex with a
millimeter ruler, leaf width (AH in cm), measured by the central
part of the leaf, and yield (R in t.ha
-1
) was obtained on a dry basis for
each treatment and was estimated per hectare.
Treatments, experimental design, and statistical processing
The AM were applied ten days after transplantation at a rate of
0, 12, 24, and 36 L.ha
-1
, these doses were considered the treatments
of the experiment. A 4x4 randomized block design (four blocks x
treatments) was used. The blocks had an area of 90 m
2
with 333 plants
each, subdivided into four plots (22.5 m
2
) where the treatments were
established. An ANOVA and Tukey’s test, p≤0.05 were used, while
a principal component analysis was performed among the group of
variables studied. The data set met the Shapiro-Wilks normality test,
processed with the InfoStat package (StatSoft, 2017).
Results and discussion
Microbiological characterization of autochthonous
microorganisms
Four groups of microbes were evidenced in the AM. The bacteria
were the most abundant 7x10
12
CFU.mL
-1
, with the registration of
two genera Lactobacillus sp. and Rhodopseudomonas sp., followed
by fungi with 3x10
11
CFU.mL
-1
, with three genera Trichoderma sp.,
Aspergillus sp. and Penicillium sp. Yeasts 2x10
11
CFU.mL
-1
were
counted, with two genera Saccharomyces sp. and Candida sp., while
the lowest amount of microbes corresponded to the actinomycete
Streptomyces sp., with 1x10
10
CFU.mL
-1
. Among the bacteria,
Lactobacillus sp., presented the largest population (63 %), compared
to Rhodopseudomonas sp. (37 %). Trichoderma sp. (46 %) was the
most abundant fungus. Saccharomyces sp. (88 %) was the yeast with
the highest presence within the AM and Streptomyces sp. (100 %) was
the only actinomycete counted (table 1).
Table 1. Microbiological populations characterization contained
in the MA.
Microorganisms Genera present
Total
populations
(CFU.mL
-1
)
Percentage
(%)
Bacteria
Lactobacillus sp.
(Lactic acid)
Rhodopseudomonas sp.
(Photosynthetic)
7x10
12
63
37
Fungi
Trichoderma sp.
Aspergillus sp.
Penicillium sp.
3x10
11
46
40
14
Yeasts
Saccharomyces sp.
Candida sp.
2x10
11
88
12
Actinomycetes
Streptomyces sp.
1x10
10
100
The mixed culture of these benecial microbes under optimal
conditions of water quality, electrical conductivity, pH, nutrients, and
mineralogical content, constitute the main basis for multiplication
and exponential growth, which was achieved in the present research.
Tlais et al. (2023) reported that AM are characterized by the synthesis
of secondary metabolites with an eect on biostimulation of plant
growth and yield. The foregoing indicates that microorganisms
and substances derived from their metabolism constituted the main
bioactive ingredients of AM (Pereira et al., 2019).
Determination of yield and its components in black
tobacco plants cv. Havana-2000 treated with autochthonous
microorganisms in eld conditions
The analysis of the yield variables and their components showed
signicant dierences between the treatments (Tukey, p≤0.05). The
largest number of leaves was achieved with the dose of 36 L.ha
-1
(7.95), followed by the dose of 24 L.ha
-1
(7.15) and the lowest values
were obtained in the treatment with the lowest dose (6.35) and in T0,
where the biofertilizer was not applied (5.95). The length of leaves
showed signicant dierences between treatments (Tukey, p≤0.05).
The longest length was achieved with the dose of 36 L.ha
-1
(33.97
cm), followed by 24 L.ha
-1
(28.81 cm) and 12 L.ha
-1
(26.21 cm),
while the lowest value was recorded at T0 (20.87 cm) (table 2).
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Rev. Fac. Agron. (LUZ). 2023, 40(3): e234023. July-September. ISSN 2477-9407.4-6 |
The width of leaves showed signicant dierences between
treatments (Tukey, p≤0.05). The highest width was achieved with the
dose of 36 L.ha
-1
(19.87 cm), followed by 24 L.ha
-1
(16.01 cm) and
12 L.ha
-1
(14.25 cm), while the lowest value (10.95 cm) was recorded
at T0. Agricultural yield showed signicant dierences between
treatments (Tukey, p≤0.05). The highest value was achieved with 36
L.ha
-1
(0.78 t.ha
-1
), followed by the dose of 24 L.ha
-1
(0.66 t.ha
-1
) and
12 L.ha
-1
(0.59 t.ha
-1
), while the lowest value was recorded at T0 (0.51
t.ha
-1
) (table 2).
Table 2. Quantity, length, width of leaves and yield in tobacco
plants cv. Havana-2000 treated with MA under eld
conditions.
Treatments (L.ha
-1
) CH LH (cm) AH (cm) R (t.ha
-1
)
0 5.95 a 20.87 a 10.95 a
0.51 a
12 6.35 a 26.21 b 14.25 b
0.59 b
24 7.15 b 28.81 c 16.01 c
0.66 c
36 7.95 c 33.97 d 19.87 d
0.78 d
CV 6.15 6.02 7.45 9.23
CH: leaves number, LH (cm): leaves length, AH (cm): leaves width, R (t.ha
-1
):
yields, CV: variation coecient.
There was evidence of biostimulation of the number of leaves
between 6.72 and 33.61 % with AM compared to T0. This result is
in the range recorded by Calero-Hurtado et al., (2019), who reached
16.66% biostimulation in tobacco cv. SS-2006 with the combined
application of AM and the Biobras-16 biostimulant at 64 days
after transplantation. Taking into account that the leaves constitute
the agricultural product of tobacco, it is considered that their
quantity, length, width, and mass, are the most important variables
on yield (Jiménez, 2021). Calero-Hurtado et al., (2019) showed a
greater length of the central leaves of tobacco cv. SS 2006 with the
combined treatment AM and the Biobras-16 biostimulant, reaching a
biostimulation of 11.32 %.
On the other hand, it was demonstrated biostimulation of the
width of leaves between 30.13-81.46 % with AM compared to T0.
In this regard, the width of the central leaves of tobacco cv. SS 2006
with a combined treatment of AM and the Biobras-16 biostimulant,
achieved a biostimulation of 15.32 % (Calero-Hurtado et al., 2019).
This value was lower than that recorded in the present study. In this
regard, although it was not possible to verify scientic results on the
agricultural yield of tobacco with the use of AM, it was known that
an agroecological alternative based on green manures (Zea mays L.,
Vigna unguiculata (L.) Walp, Canavalia ensiformis (L.), Sesamum
indicum L. and Sorghum vulgare Pers., managed to boost the yield
between 15-20 % of the cv tobacco. Havana-92, on a dierentiated
eutric uvisol soil, in areas of the “Camilo Cienfuegos” Agricultural
Production Cooperative, located in the town of Bueycito, Buey Arriba
municipality, Granma province, Cuba (Nieto-Martínez et al., 2007).
The greater size observed in length and width of the leaves is
related to the antioxidant activity of bacteria (Lactobacillus sp.
and Rhodopseudomonas sp.) on plants. These are characterized
by enhancing the processes of photosynthesis and accumulation
of carbohydrates such as trehalose and ranose, these organic
compounds improve cellular osmotic regulation and plasma
membrane integrity, enabling greater growth and tolerance of plants
to stress (Naamala et al., 2022; Hsu et al., 2021).
The biostimulation of yield and its variables was probably due
to the integrated benecial action of AM which are characterized
by being antagonists of phytopathogenic species, by mechanisms of
antibiosis, parasitism, and induced systemic resistance. Likewise, the
AM increase photosynthesis, the absorption of water and nutrients,
aspects closely related to an increase in yield and its components
(Tanya-Morocho and Leiva-Mora, 2019).
Trichoderma sp., Aspergillus sp., and Penicillium sp. In interaction
with yeasts and actinomycetes in the plant rhizosphere induce the
production of amino acids, organic acids, hormones, vitamins and
sugars, substances used by plants for the biostimulation of growth,
development and yield processes (Elnahal et al., 2022; Feijoo, 2016).
The above, constitute scientic arguments that could inuence the
biostimulation of performance in black tobacco cv. Havana-2000.
The principal component analysis explained that 99.00 % of the
variability in the observations was due to component one, while the
sum of the two components revealed 90.60 % of the total variability
of the model. It was evidenced that the dose of 36 L.ha
-1
achieved the
greatest association with the variables plant height (AP) and yield
(R), followed by 24 L.ha
-1
(gure1).
Figure 1. Biplot model between the variables that make up the
yield in black tobacco cv. Havana-2000 treated with
the autochthonous microorganisms in eld conditions.
Treatments: 0; 12; 24 and 36 L.ha
-1
. CH: Number of leaves,
AP: Plant height (cm), R: Yield (t.ha
-1
), AH: Leaf width
(cm), and LH: Leaf length (cm).
Ceiro-Catasú et al. (2023) recently reported the results of a
principal component analysis in Glycine max (L.) Merrill, biofertilized
with AM in eld conditions in eastern Cuba, where they observed that
the variables seeds per plant, length of plants, yield, mass of seeds
and pods per plant, were associated with the dose of 36 L.ha
-1
of AM,
while seeds per pod showed a greater association with 24 L.ha
-1
.
Which showed as a tendency, an increase in yield at the highest dose
of AM.
Conclusions
The autochthonous microorganisms register four groups of
microbes: bacteria (7x10
12
CFU.mL
-1
) Lactobacillus sp. and
This scientic publication in digital format is a continuation of the Printed Review: Legal Deposit pp 196802ZU42, ISSN 0378-7818.
Brizuela-Fuentes et al. Rev. Fac. Agron. (LUZ). 2023 40(3): e234023
5-6 |
Rhodopseudomonas sp., fungi (3x10
11
CFU.mL
-1
) Trichoderma sp.,
Aspergillus sp., and Penicillium sp., yeasts (2x10
11
CFU.mL
-1
) Saccharomyces
sp. and Candida sp. and an actinomycete (1x10
10
CFU.mL
-1
) Streptomyces
sp. While, the agricultural yield and components in black tobacco
cv. Havana 2000 was boosted between 15-82 % with the AM.
This indicates that the use of AM is an organic alternative for crop
biofertilization in tropical areas.
Acknowledgment
To the project “Contributions from Science, Technology, and
Innovation to Tobacco Development in Granma”, nanced by the
‘‘Empresa de Acopio Benecio y Torcido del Tabaco de Granma’’
(EABTTGRA), Bayamo, Cuba. This work was part of a research
of the Postdoctoral in Agricultural and Environmental Sciences,
School of Postgraduate Studies, Faculty of Agronomy, University
of San Carlos of Guatemala. Likewise, thanks to the ‘‘Secretaría de
Relaciones Exteriores’’ (SRE, Mexico) and the ‘‘Agencia Mexicana
de Cooperación Internacional para el Desarrollo’’ (AMEXCID) for
the granting of the Excellence Scholarship for Foreigners 2022, Fol
No: 0BG634313122.
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