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Terra Latinoamericana
On-line version ISSN 2395-8030Print version ISSN 0187-5779
Terra Latinoam vol.38 n.3 Chapingo Jul./Sep. 2020 Epub Jan 12, 2021
https://doi.org/10.28940/terra.v38i3.737
Special number
Agronomic response of sweet pepper (Capsicum annuum L.) to application of Bacillus subtilis and vermicompost in greenhouse
1
http://orcid.org/0000-0002-7448-6918
1
http://orcid.org/0000-0001-8314-6598
2
http://orcid.org/0000-0002-9489-4054
3
http://orcid.org/0000-0002-6906-4243
1Facultad de Ciencias Agrícolas-Xalapa, Universidad Veracruzana. Circuito Universitario Gonzalo Aguirre Beltrán, Colonia Zona Universitaria. 91090 Xalapa, Veracruz, México.
2Centro de Investigaciones Biológicas del Noroeste S.C. Av. Instituto Politécnico Nacional No. 195, Col. Playa Palo de Santa Rita Sur. 23096 La Paz, Baja California Sur, México.
3Departamento Académico de Agronomía, Universidad Autónoma de Baja California Sur. Carretera al Sur km 5.5., Col. El Mezquitito. 23080 La Paz, Baja California Sur, México.
The use of agrochemicals in sweet pepper (Capsicum annuum L.) cultivation has led to the search for fertilization alternatives, such as Bacillus subtilis and vermicompost, which are options to produce food without affecting the environment and human and animal health. Thus, the objective of this study was to evaluate the effect of incorporating Bacillus subtilis and vermicompost, individually or mixed, on the agronomic response of C. annuum L.) under greenhouse conditions. A completely randomized design with 15 replicates was used for each treatment where T1 = chemical fertilizer; T2 = B. subtilis; T3 = B. subtilis + chemical fertilizer; T4, T5, T6 = 280, 380, 570 g of vermicompost, respectively; T7, T8, T9 = B. subtilis + 280, 380, 570 g of vermicompost, respectively. At 90 days after sowing (DAS), the following variables were evaluated: height, stem diameter, number of leaves, buds, and flowers, leaf area, fruit production, and bacterial population (colony forming units, CFU). The sweet pepper plants with the highest dose of vermicompost (570 g) plus B. subtilis showed the greatest increase in all the variables evaluated, exceeding the plants with the chemical fertilizer only. The mixed application of B. subtilis + vermicompost can be an alternative for the production of C. annuum L. without having to use chemical fertilizers.
Index words: protected agriculture; leaf area; biofertilization; production
El uso de agroquímicos en el cultivo de chile dulce ha originado la búsqueda de alternativas de fertilización como Bacillus subtilis y lombricomposta, los cuales, son una opción para producir alimentos sin afectar al ambiente, salud humana y animal. El objetivo de este estudio fue evaluar el efecto de la incorporación individual y en conjunto de B. subtilis y lombricomposta sobre la respuesta agronómica de chile dulce bajo invernadero. Se utilizó un diseño completamente al azar con 15 repeticiones por cada tratamiento donde; T1 = plantas con fertilizante químico; T2 = B. subtilis; T3 = B. subtilis + fertilizante químico; T4, T5 y T6 = 280, 380 y 570 g de lombricomposta, respectivamente; T7, T8 y T9 = B. subtilis + 280, 380 y 570 g de lombricomposta, respectivamente. A los 90 días después de la siembra se evaluó: altura, diámetro del tallo, número de hojas, número de botones, número de flores, área foliar, producción de fruto y población bacteriana (UFC). Las plantas de chile dulce con la dosis más alta de lombricomposta (570 g) más B. subtilis presentaron los mayores incrementos en todas las variables evaluadas superando significativamente a las plantas con fertilizante químico. La aplicación en conjunto de lombricomposta y B. subtilis puede ser una alternativa para la producción de chile dulce sin tener que emplear fertilizantes químicos.
Palabras clave: agricultura protegida; área foliar; biofertilización; producción
Introduction
Despite the domestication of sweet pepper, which occurred in northeast and central-east Mexico, the number of haplotypes found in the Yucatan Peninsula suggest that its management and diversification occurred in such region of the Pre-Hispanic Mesoamerica (from central Mexico to Central America) (Pérez-Castañeda et al., 2015; Casas et al., 2019). The sweet pepper species with greater commercial demand because of their color, aroma, size, flavor, or pungency are C. chinense, C. frutescens, C. pubescens, and C.annuum. However, this last one is the most valuable at world level and thus sown in temperate, tropical and subtropical regions of Europe, Asia, Africa, and America (Aguirre-Mancilla et al., 2017; Kumar et al., 2018).
The fruit of C. annuum L., also known as bell pepper, is one of the horticultural products that are appreciated in several countries, of which the United States of America and Canada are the main markets where consumption was at least 992 thousand and 3 thousand tons (Mg), respectively (SAGARPA-SIAP, 2017). In Mexico, its consumption goes beyond being only a condiment and nutritional food since it has culturally turned out to be a symbol of national and international identity (Aguirre and Muñoz, 2015). The first world producer of C. annuum is China with 16 120 406 Mg harvested in a little more than 711 thousand ha and Mexico occupies second place with 2 732 635 Mg achieved on 7.4% of the total surface dedicated to the cultivation of this species of the Solanaceae family (SAGARPA-SIAP, 2017).
Despite the bell pepper is cultivated under different sowing systems, both temporal and irrigation, or ferti-irrigation, transplanting or direct seeding, open sky and protected agriculture, its yield per unit of sown surface is not the desired one, and its productivity may be increased by using state-of-the art technology (Nkansah et al., 2017; Yang et al., 2018).
According to Jaramillo et al. (2007), greenhouse cultivation is included within the protected techniques that promote favorable and optimal artificial or microclimate conditions (as incidental radiation, precipitation, temperature, and humidity) with the purpose of guaranteeing a desirable quality and production at harvest. With respect to the use of chemical fertilizers and their high economic and ecological costs, they are undoubtedly aspects that have caused the search for alternatives and new management strategies, which may reduce the application and use of contaminant supplies for plants, humans, water, soil, and the environment (Yuan et al., 2017; Verma et al., 2020). Faced with the use of chemical fertilization products on plants, growth promoting bacteria (PGPB) and the application of organic manure, such as vermicompost, have turned out to be options for the development of productive farming systems that promote reducing the use of chemical fertilizer and favoring sustainable production (Brar et al., 2019; Parastesh et al., 2019).
Bacillus subtilis is a bacterium considered within the PGPB because of its capacity to solubilize phosphorus (Prakash and Arora, 2019), produce siderophores (Rizzi et al., 2019), exert biological phytopathogen control (through parasitism, antagonism, antibiosis, and competence) (He et al., 2019; Cucu et al., 2020), and produce phytohormones (auxins, gibberellins, abscisic acid and ethylene) (Kudoyarova et al., 2019) that promote plant growth. This bacterium may provide an increase in agriculture productivity, decrease cultivation costs, and it does not cause contamination to the environment, which makes it a safe and sustainable alternative for cultivation production (Bhat et al., 2019).
Vermicompost is the process by which organic waste decomposes through the synergic action of earthworms and microbial communities (Ali et al., 2015); it also contains important nutrients for plant growth and productivity (Roychowdhury et al., 2017) and improves physical, biological and chemical properties in soil (Aksakal et al., 2016).
The application of PGPB and vermicompost may be an alternative to the use of chemical fertilizers, promoting cultivation growth and productivity sustainably. Therefore, this study evaluated the effect of incorporating B. subtilis and vermicompost, individually and jointly, on the agronomic response of C. annuum under greenhouse conditions.
Materials and Methods
This study was performed in a greenhouse located in the city of Xalapa, Veracruz, México, at 19° 33’ N and 96° 56’ W, at 1428 m a.s.l.
Substrate
A mixture of soil, sand, and pumice in a ratio of 2:1:1 (vol/vol) was made and disinfected with Bunema( (metam sodio 45%) at a dose of 100 mL m-2 (Terralia, 20181); subsequently, 5 kg black bags were filled with the substrate.
Bacterial concentration
The bacterium B. subtilis was provided by the Phytopathology Laboratory at Centro de Investigaciones Biológicas del Noroeste and cultured in trypticase soy broth (TSB) at 3% and 28 (C at 180 rpm for 48h. After that, the bacterial concentration was adjusted to a 1 ( 109 UFC mL-1using an ultraviolet visible (UV/Vis) spectrophotometer at 660 nm and absorbance of 1. The inoculation with B. subtilis was performed at transplanting by applying 3 mL on each plant root.
Vermicompost
A commercial vermicompost (TerraNova Lombricultores, Xalapa, Ver. MX), produced from coffee pulp, had the following characteristics: organic matter 84%, pH 7.4, organic phosphorus 0.108%, total phosphorus 0.25%, total nitrogen 3.99%, total potassium 2.14%, total calcium 1.72%, total magnesium 0.8%, C/N relationship 12.21, fulvic acids 10.5%, and humic acids 15.1%. The doses of 280, 380, and 570 g of vermicompost per plant was following the recommendation of López et al. (2012). The vermicompost was sterilized with Bunema( (metam sodium 45%) at a dose of 100 mL m-2.
Chemical fertilization
The following were applied per plant to the fertilized treatments: 12 g of diammonium phosphate (18-46-00) and 12-12-17 + 2 of MgO each 10 days after transplant (DAT) and the following leaf fertilizers: 7.2 g L‑1 of Nitrosol( every eight days (from day 20 to 40 DAT), 5 g L-1 of Syntek( and Ca-Bo every eight days (from day 40 to 90 DAT) (Agroscience, 2017).
Treatment description
At the moment of transplanting, each plant was inoculated with B. subtilis, chemically fertilized or with vermicompost. A completely randomized design was used with 15 replicates per treatment, where T1 = chemical fertilizer; T2 = B. subtilis, T3= B. subtilis + chemical fertilizer, T1 = chemical fertilizer; T2 = B. subtilis; T3 = B. subtilis + chemical fertilizer; T4, T5, T6 = 280, 380, 570 g of vermicompost, respectively; T7, T8, T9 = B. subtilis + 280, 380, 570 g of vermicompost, respectively. The plants were placed inside a greenhouse for 90 days.
Variables evaluated
At the end of the experiment the variables evaluated were plant height (cm), stem diameter (mm), leaf, buds, and flower number, leaf area (cm3), production (g), and colony forming units (CFU) by the method proposed by Glick et al. (1999).
Results and Discussion
Morphologic parameters
The bell pepper plants that were inoculated with the bacterium and different vermicompost doses showed a significant increase in height, stem diameter, leaf, bud, and flower number, and leaf area when compared with those treated with chemical fertilizer (Table 1). The inoculated plants with B. subtilis plus the high dosage of organic fertilizer reached an increase of 86% in height, 197% in stem diameter, 500% in leaf number, 200% in bud number, 187% in flower number and 462% in leaf area when compared with those of the chemical fertilizer treatment. The rest of the plant treatments with the bacterium or organic manure showed the highest values in all the morphological variables with respect to the fertilized plants.
Table 1: Morphological parameters of sweet chili plants inoculated with B. subtilis and vermicompost dose.
|
Treatment |
Description |
Height |
Stem diameter |
Number of leaves |
Number of buds |
Number of flowers |
Leaf area |
|
cm |
mm |
cm3 |
|||||
|
1 |
Chemical fertilizer |
16.03 a† |
4.1 a |
15 a |
19 a |
16 a |
127.24 a |
|
2 |
B. subtilis |
17.73 b |
5.3 b |
18 b |
22 b |
18 b |
154.07 b |
|
3 |
B. subtilis + chemical fertilizer |
19.49 c |
6.6 c |
22 c |
23 b |
18 b |
255.67 c |
|
4 |
286 g vermicompost |
21.24 d |
7.5 d |
45 d |
30 c |
20 c |
327.57 d |
|
5 |
381 g vermicompost |
23.54 e |
7.6 d |
51 e |
35 d |
23 d |
386.14 e |
|
6 |
571 g vermicompost |
24.88 f |
8.1 e |
61 f |
39 e |
24 d |
557.24 f |
|
7 |
B. subtilis + 280 g vermicompost |
26.39 g |
9.2 f |
77 g |
44 f |
32 e |
630.41 g |
|
8 |
B. subtilis + 380 g vermicompos |
28.19 h |
10.3 g |
78 g |
49 g |
33 e |
696.91 h |
|
9 |
B. subtilis + 570 g vermicompos |
29.97 i |
12.2 h |
90 h |
57 h |
46 f |
715.13 i |
† Different letter in the same column indicate significant differences (Fisher’s LSD test, P < 0.05).
The increase in morphological parameters of bell pepper with B. subtilis and vermicompost may be due mainly to two factors. The first one would be the content of the organic manure in macro and micronutrients (Maji et al., 2017) and growth promoters, such as auxins, gibberellins, cytokins, fulvic and humic acids (Goswami et al., 2017; Ravindran et al., 2019), which are used by the plants as energy sources or in their cell division and elongation processes, among others (Hanc et al., 2019). Furthermore, the application of vermicompost improves plant rooting, aeriation, water retention, and promotes microbial activity (Zhao et al., 2017; Gupta et al., 2019), mainly that of the PGPB (Viti et al., 2010; Espinosa-Palomeque et al., 2017).
The second factor is the capacity of B. subtilis to produce organic acids of low molecular weight that allow releasing soluble soil phosphorus; this macro-element is used by the plants for photosynthesis, energy, and carbon source degradation that allows them to reach greater plant growth (Wang et al., 2019). B. subtilis also produces indole-3-ascetic acid (IAA), which is a plant hormone that participates in cell division and elongation, tissue differentiation, and light and gravity responses (Wagi and Ahmed, 2019). In addition, the plant protection towards phytopathogens by the bacterium influences plant growth positively (Ndeddy and Babalola, 2016; Rizzi et al., 2019). Finally, the bacteria of the genus Bacillus have a high capacity of plant root adhesion and colonization, which produces a greater effect on their growth (Allard-Massicotte et al., 2016).
The application of vermicompost or B. subtilis has increased several morphological cultivation parameters, such as rice (Sharma and Garg, 2018), tomato (Durukan et al., 2019), barley (Jamily et al., 2019), lettuce (Lee et al., 2020), among others. In the particular case of bell pepper, the application of vermicompost or B. subtilis has promoted growth of several germplasms of this solanceae (Álvarez-Solís et al., 2016; Haghighi and Barzegar, 2018; Huang et al., 2020). Nonetheless, to our knowledge, this is the first report of the effect of different dosage of vermicompost plus B. subtilis on C. annuum cultivation.
Bell pepper production and colony forming units of Bacillus subtilis
Bell pepper production increased 364% in the plants inoculated with B. subtilis and the highest dosage of vermicompost compared with those chemically fertilized (Figure 1). An increase was observed in chili production as the plants inoculated with the bacterium were fertilized with higher vermicompost dosage. The mineral nutrient content in the organic manure, such as vermicompost and the supply of growth promoting substances and phosphorus solubilization by the PGPB, such as B. subtilis have an important role in plant productivity (Choudhary et al., 2019).
Columns with the same letter are statistically equal (Fisher’s LSD, P < 0.05).
Figure 1: Production (g) of sweet pepper fruit in plants inoculated with B. subtilis and vermicompost dose. Where: T1 = plants with chemical fertilizer, T2 = B. subtilis, T3 = B. subtilis + chemical fertilizer, T4 = 280 g of vermicompost, T5 = 380 g of vermicompost, T6 = 570 g of vermicompost, T7 = B. subtilis + 280 g of vermicompost, T8 = B. subtilis + 380 g of vermicompost and T9 = B. subtilis + 570 g of vermicompost.
The increase in the vermicompost doses applied to the plants allowed the populations of B. subtilis to increase in sweet pepper roots (Figure 2), accounting for a greater number of the bacterium CFU with the highest dosage of vermicompost. To this respect, Singh et al. (2012), Ammaan et al. (2019) and Maheshwari et al. (2019) mentioned that organic manure are important in increasing beneficial bacterial populations, which are a relevant factor in plant productivity. With respect to the plants chemically fertilized and inoculated with B. subtilis, the decrease of bacterial population might have been due to the negative effect of the fertilizer based on nitrogen and phosphorus, which decreased the microbial activity related to the biological nitrogen fixation or phosphorus solubilization. This process is significant when these nutritional elements are scarce in the plant rhizosphere (Nadeem et al., 2014; Chiquito-Contreras et al., 2017).
Columns with the same letter are statistically equal (Fisher’s LSD, P < 0.05).
Figure 2: Population of B. subtilis in roots of sweet pepper plants with vermicompost. Where: T1 = plants with chemical fertilizer, T2 = B. subtilis, T3 = B. subtilis + chemical fertilizer, T4 = 280 g of vermicompost, T5 = 380 g of vermicompost, T6 = 570 g of vermicompost, T7 = B. subtilis + 280 g of vermicompost, T8 = B. subtilis + 380 g of vermicompost and T9 = B. subtilis + 570 g of vermicompost.
Phytohormones and bacteria are not a contribution of chemical fertilizers toward plants; thus, organic technologies are important because of their multiple biological characteristics that allow improving their mineral nutrition, growth and productivity (Soni and Kapoor, 2019). The synergic effect exerted by the vermicompost plus the PGPB on yield increase has already been reported in several cultivations, such as tomato (Ojha et al., 2016), lettuce (Khosravi et al., 2018), cauliflower (Thakur et al., 2018), mustard (Beenish et al., 2019), among others.
Sustainability of the different agricultural systems should contemplate the use of organic manure, such as vermicompost and PGPB, such as B. subtilis because they are ecologically acceptable options to increase plant productivity, and with null impact to the environment and animal and human health compared to chemical fertilizers (Lim et al., 2016; Vejan et al., 2016).
Conclusions
The application of both, vermicompost and B. subtilis increased the morphological parameters and C. annuum plant production in greenhouse. The highest values were significantly quantified all the variables evaluated with the highest dosage of organic manure plus the bacterium, going beyond the plant treatment with chemical fertilization. The joint application of vermicompost and B. subtilis may be a sustainable alternative for bell pepper cultivation.
Acknowledgments
The authors are grateful to Lidia Martínez-Juárez for technical support and Diana Fischer for translation and edition.
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Recommended citation:
Lara-Capistrán, L., R. Zulueta-Rodríguez, B. Murillo-Amador, M. Romero-Bastidas, T. Rivas-García y L. G. Hernández-Montiel. 2020. Respuesta agronómica del chile dulce (Capsicum annuum L.) a la aplicación de Bacillus subtilis y lombricomposta en invernadero. Terra Latinoamericana Número Especial 38-3: 693-704. DOI: https://doi.org/10.28940/terra.v38i3.737
1Terralia. 2018. Bunema 55 GE-Metam Sodio 45%. https://www.terralia.com/agroquimicos_de_mexico/view_trademark?trademark_id=8341.
Received: October 09, 2019; Accepted: January 06, 2020
Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons
