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Revista mexicana de ciencias agrícolas

versión impresa ISSN 2007-0934

Rev. Mex. Cienc. Agríc vol.7 no.1 Texcoco ene./feb. 2016



Production of vegetable seedlings with Azospirillum sp. and foliar spray with bee honey

Wendy Cruz Romero1 

Juan Manuel Barrios Díaz1  § 

Maria de las Nieves Rodríguez Mendoza2 

David Espinoza Victoria2 

Juan Luis Tirado Torres2 

1Benemérita Universidad Autónoma de Puebla-Facultad de Ingeniería Agrohidráulica. Av. Universidad S/N. San Juan Acateno, Teziutlán, Pue. C.P. 73965. Tel. y Fax (231)3122933. (;

2Colegio de Postgraduados-Campus Montecillo. Carretera México-Texcoco km 36.5. 56230, Montecillo, Texcoco, Estado de México, México. (;


With the goal of proposing biotechnology for the sustainable production of vegetable seedbeds, broccoli (Brassica oleracea. Italica Group), onion (Allium cepa L.), lettuce (Lactuca sativa L.), and tomato (Solanum lycopersicum L.) seedlings were evaluated as nutrition alternatives, inoculated with 7A and AMRp10 strains of Azospirillum and foliar spray with 2% bee honey (AFMA) to determine the effect on height, leaf area, stem diameter, dry weight, SPAD units and bulb diameter (onion). The experiment was done in greenhouse conditions using a completely random design and the experimental units used were commercial seedbeds with a mixture of peat moss and pearlite as a substrate. The results indicate that the foliar spray with 2% bee honey significantly increased the height (13%), foliar leaves (38%) and dry weight (30%) of broccoli seedlings. In lettuce seedlings, the height and the leaf area were greater with A. AMRp10 in 18 and 98%, respectively. Furthermore, height increased 23% in tomato seedlings with A. AMRp10. On the other hand, with the inoculation of A.7A, SPAD units increased 7% in the broccoli seedlings when compared to the AFMA treatment and the stem diameter increased 11% compared with A. AMRp10. The leaf area of the tomato seedlings also increased 52% with regards to the A.AMRp10. In this research, the inoculation of the 7A strain of Azospirillum and foliar spray with bee honey showed to have developing effects on plant growth; therefore they constitute a promising and feasible alternative for the production of vegetable seedlings.

Keywords: Azospirillum; bee honey; bio-fertilizer; microbial inoculant; seedbed


Con el objetivo de proponer biotecnologías para la producción sustentable de almácigos de hortalizas, fueron evaluadas como alternativas de nutrición de plántulas de brócoli (Brassica oleracea var. Itálica), cebolla (Allium cepa L.), lechuga (Lactuca sativa L.) y tomate (Solanum lycopersicum L.), la inoculación con cepas 7A y AMRp10 de Azospirillum y la aspersión foliar de miel de abeja 2% (AFMA), determinando su efecto en la altura, área foliar, diámetro de tallo, peso seco, unidades SPAD y diámetro de bulbo (cebolla). El experimento se realizó bajo condiciones de invernadero empleando un diseño completamente al azar y utilizando como unidades experimentales almácigos comerciales con una mezcla de peat moss y perlita como sustrato. Los resultados indican que la aspersión foliar de miel de abeja 2% incrementó significativamente la altura (13%), área foliar (38%) y peso seco (30%) de las plántulas de brócoli, en las plántulas de lechuga la altura y área foliar fueron mayores que con A.AMRp10 en 18 y 98%, respectivamente, además, en las plántulas de tomate la altura aumentó 23 %, también con respecto a A.AMRp10. Por otra parte, con la inoculación de A.7A, en las plántulas de brócoli se incrementaron 7% las unidades SPAD respecto al tratamiento AFMA y 11% el diámetro de tallo en comparación con A.AMRp10, pero también el área foliar de las plántulas de tomate fue 52% mayor con respecto a A.AMRp10. En esta investigación, la inoculación con la cepa 7A de Azospirillum y la aspersión foliar de miel de abeja, demostraron que tienen efectos promotores del crecimiento vegetal, por lo tanto constituyen una alternativa promisoria y viable para la producción de plántulas de hortalizas.

Palabras clave: Azospirillum; almácigo; biofertilizante; inoculante microbiano; miel de abeja


Presently, it is important to continue researching sustainable strategies and techniques for the production of vegetable seedbeds that help to improve their quality, strength and adaptability. Seedlings need to have well-developed roots and be easily adaptable to the stress conditions caused by transplantation, and at the same time the excessive use of agrochemicals needs to be reduced.

A continuously developed biotechnology involves the use of microorganisms identified as plant growthpromoting rhizobacteria (Vessey, 2003), among which the Azospirillum genus is one of the most studied (Hernández et al., 2001); they are classified as diazotrophic microorganisms and are associated endophytically or rhizospherically with grains and grasses from different regions of the world. Five species have been described (De Bashan et al., 2007) and different strains have been used as commercial bio-fertilizers in several countries, including Mexico, due to their ability to stimulate plant growth and increase the yield of the cultures in different environments and edaphic conditions (Di Barbaro et al., 2005). Several studies have reported their ecology, physiology and genetic features (Tilak et al., 2005). Thus, these species constitute a nutritional alternative for cultures, stimulating the balance of the agro-ecosystems (Reganold et al., 1990) by restoring the physical, chemical and biological properties of the ground (Newman and Reynolds, 2005) and they contribute to the sustainable production of food (Abiven and Recous, 2007).

On the other hand, the effect of bee honey on some growth and development variables, such as in tomato seedlings, has also been investigated. An increase in the strength of the plants has been reported, reflected in the increase of height, stem diameter, leaf area and stimulation of the formation of the secondary xylem in less time (Villegas-Torres et al., 2001). In the cultivation of mango, the incidence and severity of floral malformation known as “witch’s broom” (Donald et al., 2002) has been reduced. And, in ornamental plants such as Lilium (Betancourt-Olvera et al., 2005) and Tulip (Rodríguez-Mendoza et al., 2011) it has favored height, stem diameter, shelf life and resistance to the flattening of leaves, which are important parameters that determine the quality of the flower to be cut.

Based on the foregoing, the objective of the research was to evaluate foliar spray with bee honey and inoculation of Azospirillum (7A and AMRp10) in the growth of broccoli (Brassica oleracea Italica Group) cv. Legacy, onion (Allium cepa L.) cv. Victoria, lettuce (Lactuca sativa L.) cv. Salinas and tomato (Solanum lycopersicum L.) cv. Río Grande seedlings.

Materials and methods

The study was done in a greenhouse with dimensions of 7.0 m wide by 18.0 m long, in a tunnel formation with a metallic structure covered in polyethylene, located in the Colegio de Postgraduados, Montecillo Campus, in Texcoco, State of Mexico. The plant materials used were: broccoli (Brassica oleracea Italica Group), onion (Allium cepa L.), lettuce (Lactuca sativa L.) and tomato (Solanum lycopersicum L.). For the growth of the seedlings, seed trays with 200 cavities were used and a mixture of peat moss and pearlite was used as a substrate in a volume ratio of 3:2. In each one of the established cultures, four treatments were evaluated: a) inoculation with Azospirillum 7A (A.7A); b) inoculation with Azospirillum AMRp10 (A. AMRp10); c) foliar spray with 2% bee honey (AFMA); and, d) control treatment, without inoculation and without AFMA.

The bacterial strains of Azospirillum, 7A (isolated from the corn culture from the state of Puebla) and AMRp10 (isolated from the rhizoplane of creole corn from the state of Tlaxcala) were provided by the culture collection of the Centro de Investigaciones en Ciencias Microbiológicas of the Benemérita Universidad Autónoma de Puebla (BUAP). The bacterial suspension used was prepared from an isolated colony in the middle of a liquid NFB culture without agar (Day and Dobereiner, 1976), with 107 cells mL-1 of inoculum employed and determined by the McFarland scale (McFarland, 1907). Inoculation was done after the seedlings sprouted, adding 0.1 ml of the bacterial suspension to the base of the stem.

The foliar spray with bee honey for the aforementioned treatment used commercial honey (Carlota®). Every seven days from the emergence of the seedlings, diluted honey in water was applied with a 2% concentration in a weight: volume relation (Rodríguez-Mendoza et al., 2011). The seedbeds were sprayed two times a day in the following manner. After the sowing, irrigation was done with pH distilled water adjusted to 5.5 with sulfuric acid (H2SO4) 1N and sodium hydroxide (NaOH) 1N. Then, after the emergence of the seedlings and during a period of 15 days, they were irrigated with the nutritional solution proposed by Steiner (Steiner, 1980) and diluted 50%. Finally and until concluding the seedbed stage, irrigation was done with the Steiner solution in its original concentration.

Evaluated variables

30 days after sowing (DAS), the following were determined in the broccoli, lettuce and tomato seedlings: the chlorophyll content of leaves located in the upper part at the same height and position was measured with Minolta’s SPAD-502® portable meter, considering the average of three readings per plants, (Rodríguez-Mendoza et al., 1998); the height of the plant was measured from the basal part until the apical meristem; the leaf area was obtained with a Li-Cor Li-3000A® integrator (Ruíz-Espinoza et al., 2007); the diameter of the stem in the broccoli and tomato seedlings was measured with a Vernier caliper; and, the dry weight of the seedling was determined after having washed the plant samples with distilled water and drying them on a stove with forced air circulation at 70 °C during 72 h (Alcántar-González and Sandoval-Villa, 1999). The evaluation of the onion seedlings was done 45 DAS, considering the aforementioned variables and measuring the diameter of the bulb using a digital electronic Vernier.

Statistical analysis

The experimental unit was comprised of 50 seedlings, among which 15 seedlings of each repetition (four in total) were considered for the measurement of the responses. The treatments were distributed under a completely random design. For the analysis of variance, measurement comparison (LSD, p= 0.05) and correlation between variables, the ANOVA and CORR procedures from the statistical computational package SAS (Statistical Analysis System) version 8.0 (SAS, 1999) were used.

Results and discussion

Growth of the broccoli seedlings (Brassica oleracea Italica Group)

In broccoli seedlings, foliar spray with bee honey (AFMA) had a significant effect (p≤ 0.05) on the height, foliar area and dry weight (Table 1), variables that were positively correlated (Figures 1a and 1b). The height of the plant increased by 13% when compared to the control sample and 16% when compared to the treatments inoculated with Azospirillum. The foliar area increased 38% compared to the control sample and 54% compared to A.7 and A.AMRp10. The dry weight of the seedlings increased 30% compared to the control sample and 37% compared to A.7A and A.AMRp10.

Table 1. Growth of broccoli seedlings (Brassica oleracea Italica Group) 30 DAS sprayed with 2% bee honey (AFMA) and inoculated with Azospirillum 7A (A.7A) and Azospirillum AMRp10 (A.AMRp10) strains. 

Tratamiento Altura (cm) Diámetro de tallo (cm) Unidades (SPAD) Área foliar (cm 2 ) Peso seco (g)
Testigo 12.97 b* 0.27 ab 49.97 ab 24.73 b 0.27 b
AFMA 14.65 a 0.28 ab 47.34 b 34.2 a 0.35 a
A.7A 12.82 b 0.3 a 50.73 a 21.76 b 0.25 b
A.AMRp10 12.33 b 0.27 b 48.29 ab 22.73 b 0.26 b
CV (%) 5.46 7.03 4.33 10.41 13.68
DMS 1.11 0.03 3.28 4.14 0.06

Figure 1. Correlation 30 DAS with the average of the treatments evaluated between: a) y= height (cm) and x= foliar area (cm2) and b) y= dry weight (g) and x= foliar area (cm2), of broccoli seedlings (Brassica oleracea Italica Group). 

On the other hand, A. 7A caused a 7% increase in the SPAD units compared to AFMA and the diameter of the stem also increased 11% compared to the other strain evaluated (A.AMRp10). In general, there was no significant effect on the growth of the broccoli seedling, which is consistent to what was reported by Boddey et al. (1986), who obtained unsatisfactory results in the cultures evaluated with homologous strains of Azospirillum. In this regard, Smith and Goodman (1999) indicate that the genotype of the organisms involved plays an important role in the formation of the association between microorganisms and plants, determining the biological result of the association.

Growth of onion seedlings (Allium cepa L.)

In onion seedlings, the only variable that presented a response to the evaluated treatments was the SPAD units and the maximum value was obtained with the control sample, which surpassed A.7A and A.AMRp10 by 54% (Table 2). This response was due to the tubular shape of the leaf which makes the transmittance of light difficult (Westerveld et al., 2003). In addition, in this stage of development the leaves are very thin and the cell of the SPAD meter, with dimensions of 2 x 3 mm (Schepers et al., 1998), probably did not cover it in its entirety showing measurements that were different and that were reflected on the highest coefficient variation of the evaluated cultures.

Table 2. Growth of onion seedlings (Allium cepa L.) 45 DAS sprayed with 2% bee honey (AFMA) and inoculated with Azospirillum 7A (A.7A) and Azospirillum AMRp10 (A.AMRp10) strains. 

Tratamiento Altura (cm) Diámetro de tallo (cm) Diámetro de bulbo (cm) Unidades (SPAD) Área foliar (cm 2 ) Peso seco (g)
Testigo 19.88 a* 0.29 a 0.44 a 31.74 a 7.15 a 0.07 a
AFMA 21.92 a 0.3 a 0.44 a 24.79 ab 16.46 a 0.08 a
A.7A 22.63 a 0.31 a 0.46 a 23.08 b 9.28 a 0.11 a
A.AMRp10 20.98 a 0.28 a 0.42 a 18.12 b 7.84 a 0.11 a
CV (%) 11.33 6.93 11.44 20.55 13.95 40.44
DMS 3.73 0.04 0.07 7.73 2.2 0.05

In this experiment, onion seedlings averaged 21.35 cm in height, 0.30 cm in stem diameter, 0.44 cm in bulb diameter, 10.18 cm2 in foliar area and 0.09 g in dry weight. Pulido et al. (2003) obtained a seedling height of 6 to 18 cm and a root longitude of 8 to 10 cm in seedbeds of cv. Red Creole inoculated with Azospirillum brasilense. On the other hand, Veiga de Vicenzo and Tessarioli Neto (2003) report a height in onion seedlings of 18.2 cm at 32 DAS in a controlled environment and with a supply of N, indicating that the ideal height for transplantation is 15 cm and 0.37 cm for the bulb diameter, all lower values than the ones obtained in this experiment (21.35 cm and 0.44 cm, respectively). These same authors also reported 0.13 g/dry weight plant, a slightly higher value than the one obtained in this study (0.09 g/plant). For this culture and in a similar manner to the broccoli seedlings, the treatments inoculated with Azospirillum did not have a differentiated effect on the growth variables.

In this regard, Alexandre and Zhulin (2001) state that the success of the colonization of Azospirillum in the plants depends on the process known as chemotaxis, which consists of the strong attraction between the BPCV and plant roots, through their own root exudates such as malate, succinate and fructose. Díaz-Zorita and Fernández-Canigia (2008) indicate that there have been several studies that show the benefits of inoculation with Azospirillum on the growth and production of different cultures, but its extensive use is limited by the alleged inconsistency of the results obtained and the variability has been attributed to the interaction with handling (fertilization, protection and structure of the culture) and environmental factors (type of soil).

Growth of lettuce seedlings (Lactuca sativa L.)

The height and the foliar area of lettuce seedlings were positively and negatively affected (p≤ 0.05) by AFMA and the strains A.7A and A.AMRp10, surpassing them by 18 and 78%, respectively (Table 3). Chutichudet and Chutichudet (2009) reported the height of seedlings at 32 DAS being 7.97 to 10.84 cm for cv. Grand Rapids, values that are similar to the average registered in this study (8.83 cm). On the other hand Kleiber et al. (2013) reported that the effect of benign organisms on the cv. Clotilde seedlings was reflected in 28.55 cm2 of foliar area 40 DAS; this was an inferior value to the one obtained with the AFMA treatment of our experiment (39.55 cm2). According to Betancourt-Olvera et al. (2005), honey acts as an enhancer for plant growth as it contains a high quantity of carbohydrates, a presence of hormones, vitamins, minerals, amino acids, proteins and other organic constituents.

Table 3. Growth of lettuce seedlings (Lactuca sativa L.) 30 DAS sprayed with 2% bee honey (AFMA) and inoculated with Azospirillum 7A (A.7A) and Azospirillum AMRp10 (A.AMRp10) strains. 

Tratamiento Altura (cm) Unidades (SPAD) Área foliar (cm 2 ) Peso seco (g)
Testigo 8.98 ab* 32.47 a 29.85 ab 0.22 a
AFMA 9.51 a 32.05 a 39.55 a 0.15 ab
A.7A 8.74 ab 30.11 a 24.39 b 0.14 ab
A.AMRp10 8.07 b 31.42 a 20.00 b 0.11 b
CV (%) 9.72 6.62 25.85 31.68
DMS 1.32 3.21 11.33 0.07

On the other hand, same as in the broccoli and onion cultures, the treatments inoculated with Azospirillum did not have a clear or significant effect on the growth variables evaluated; in fact, the dry weight of the seedling obtained with the control was significantly greater (50%) than the one obtained with A.AMRp10. This response is frequently associated with the inefficiency of the bacteria to consistently colonize the rhizosphere of the plants (Hatzinger and Alexander, 1994), which could be a characteristic of the PGPR and an important condition for the selection of the microbial inocula used as bio-fertilizer (Lugtenberg et al., 2001). The colonization of the rhizosphere by bacteria is a complex process originated by the combination of several mechanisms that affect certain aspects of mineral nutrition, the metabolism of carbon and the root development of the plants (Díaz-Vargas et al., 2001); among these mechanisms is the production of components that enhance plant growth, prompting an increase in the number and longitude of the root hair (Bacilio-Jimenez et al., 2001). No effect from the treatments was presented in the SPAD units and the general average was 34.88, which is superior to what was reported by Santos et al. (2010) for seedbeds of lettuce 41 DAS using different organic substrates (16.3 to 21.5 SPAD units).

Growth of tomato seedlings (Solanum Lycopersicum L.)

In tomato seedlings, the height and the foliar area were significantly affected (p≤ 0.05) by the treatments (Table 4). The height increased 23% with AFMA in respect to A.AMRp10. Villegas-Rodríguez et al. (2001) reported the following for tomato seedlings cultivated in hydroponics and with foliar spray with 2% bee honey: increases of more than 100% in their height when compared to plants irrigated solely with Steiner solution at 50%. The height of the seedling obtained in our study with AFMA (22.3 cm) is consistent with the statements of Markovic et al. (1997) who indicated that in order to ensure the success of the transplantation in the field the seedling should be 20 to 30 cm tall.

Table 4. Tomato seedlings growth (Solanum lycopersicum L.) 30 DAS sprayed with 2% bee honey (AFMA) and inoculated with Azospirillum 7A (A.7A) and Azospirillum AMRp10 (A.AMRp10) strains. 

Tratamiento Altura (cm) Diámetro de tallo (cm) Unidades (SPAD) Área foliar (cm 2 ) Peso seco (g)
Testigo 20.09 ab* 0.31 a 35.35 a 41.58 ab 0.39 a
AFMA 22.23 a 0.31 a 32.76 a 40.35 ab 0.47 a
A.7ª 20.37 ab 0.3 a 36.52 a 47.16 a 0.43 a
A.AMRp10 18.11 b 0.29 a 34.89 a 30.93 b 0.37 a
CV (%) 11.02 5.24 7.1 18.95 20.54
DMS 3.42 0.02 3.81 11.68 0.13

On the other hand, Terry et al. (2001) did not observe any significant effect from the inoculation with Azospirillum brasilense SP-7 on the height of tomato seedlings, reporting an average of 20 cm. Furthermore, they stated that in the initial stage of the plant growth there was no effective identification between the microorganisms and the plants inoculated to be able to express some sign of response. The height of the treatments inoculated with the Azospirillum strains used in this work (19.24 cm average) is superior to the one reported by Hernández and Chailloux (2004) for seedlings inoculated with Azospirillum lipoferum and Azospirillum brasilense and also to the one reported by Sánchez-López et al. (2012) in a study done with the Sofía cv. and inoculated with PGPR of the Enterobacter sp., Pseudomonas sp. and Bacillus sp. genera.

The foliar area increased 52% with A.7A when compared to A.AMRp10. It has been reported that when a strain of Azospirillum prompts the growth of plants, as in this case, it is mainly due to the formation of indole-acetic acid (IAA) which is produced by its inoculation (Tien et al., 1979); this metabolite enhances cellular division and the differentiation of tissue, consequently increasing the biomass (Spaepen et al., 2007). In this study, the foliar area was significantly correlated to the dry weight (r= 0.71, Figure 2a). In fact, Ribaudo et al. (2006) found a higher content of IAA and ethylene in plant tissues of tomato seedlings inoculated with Azospirillum brasilense FT326 when compared to those that had not been inoculated.

Figure 2. Correlation 30 DAS with the average of the evaluated treatments between: a) y= diameter of the stem (cm) and x= dry weight (g) and b) y= foliar area (cm2) and x= dry weight (g), of tomato seedlings (Solanum lycopersicum). 

The diameter of the stem, SPAD units and dry weight of the tomato seedlings did not significantly vary among treatments (p> 0.05). The average stem diameter was 0.31 cm, which is in accordance to the ranges reported by Hernández and Chailloux (2004) and Terry et al. (2000) for tomato seedlings inoculated with PGPR of the Azospirillum genus. In this same regard, Preciado Rangel et al. (2002) state that the diameter of the stem is an indicator of the strength of the seedlings as it directly reflects the accumulation of photosynthates, which can be subsequently transferred to the locations where there is demand. The average SPAD units was 34.88, which is an inferior value to the one indicated by Rodríguez-Mendoza et al. (1998) who reported 56.11 SPAD units 45 days after the transplantation, but this was due to fertilizations done to the leaves and soil with nitrogenous sources.

The average dry weight of the seedlings was 0.42 g/plant and there was a significant correlation with the diameter of the stem (Figure 2b). Even when in this study the increase of biomass was not affected by the treatments, there are works where the inoculation with Azospirillum strains helped tomato seedlings, such is the case for Carletti et al. (1994) who reported increases of up to 76% in the dry weight of the stem with A. lipoferum. Hadas and Okon (1978) also found significant increases in the longitude and dry weight of the root, dry weight of the aerial part and the total foliar area. In this same regard, Parra and Cuevas (2001) indicate that the mechanism through which Azospirillum influences the development and productivity of the plants is not clear, explaining the ability to fix atmospheric N in the soil through an increase in the nitrate reductase enzyme activity which stimulates the assimilation of nitrate by the non-inoculated plants.


Even when increases were not generalized in regards to height, foliar area, dry weight, SPAD units and stem diameter of the broccoli (Brassica oleracea Italica Group), lettuce (Lactuca sativa L.) and tomato (Solanum lycopersicum L.) seedlings, the spraying of 2% bee honey and the inoculation of the 7A strain of Azospirillum are good options for the sustainable production of vegetable seedlings, making use of their action mechanisms which promote plant growth. Their use is therefore promising and feasible.

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Received: July 2015; Accepted: January 2016

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