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Increases in N2 Fixation in Bean Crop

Increases in N2 Fixation in Bean Crop


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By Roldán Torres G. (1), Eleia M. Soria A. (1), Carlos Pérez N. (2), Juliana García I. (3)

Increases in the Biological Fixation of Atmospheric N2 in Bean (Phaseolus Vulgaris L.) Cultures Through Combined Inoculation of Diazotrophic Bacteria.

Summary

The present work was carried out with the objective of evaluating the effect of the combined inoculation of Rhizobium leguminosarum biovar. phaseoli and Azotobacter chroococcum (strain Mb-9), in the cultivation of common bean (Phaseolus vulgaris L.), together with the study of two inoculation doses of the Rhizobium biopreparation. Six treatments resulting from the microbial combinations and the Rhizobium biopreparation without combination were analyzed, taking as reference a treatment with mineral fertilization and a control. The Rhizobium doses were at a rate of 70 and 150 g kg.-1 of seed, while the Azotobacter dose was at a rate of 400 ml kg.-1 of seed. The fixation parameters, the main components of the yield and the agricultural yield of the different treatments were evaluated, in addition to an economic-environmental analysis to determine the feasibility of the fertilization methods. The results showed a significant increase with respect to all the variables evaluated with the use of microbial combinations, highlighting the dose of Rhizobium at a rate of 150 g combined with Azotobacter, which significantly increased the yield compared to inoculation with Rhizobium at a rate of 70 g and the control, and did not differ statistically with mineral fertilization. Therefore, it is recommended, according to the high levels of P2O5 and K2O in this soil, to use the combined inoculation of Rhizobium and Azotobacter as a fertilization alternative at a rate of 150 g kg-1 of seed, implying increases in yields, reduction in production costs and contribution to environmental sanitation.

Introduction.

In the developed world, agriculture depends to a great extent on the use of chemical fertilizers and pesticides to maintain its high agricultural productions, without taking into account the terrible damages that these can cause, either affecting the global nitrogen cycle, polluting groundwater and surface and increasing levels of atmospheric nitrous oxide (N2O) and CO2, which are considered powerful greenhouse gases (Anonymous, 2001).

The use of synthetic nitrogen in the last 40 years has increased from 3.5 million to 80 million tons, both in developed and developing countries, increasing its production costs to more than $ 20 billion USD annually. However, the natural processes of biological fixation of N2 (BNF) play an important role in the activation of sustainable agricultural systems due to their environmental benefit, such is the case of the application of bacteria belonging to the genus Rhizobium to legume crops ( Anonymous, 2001).
Burdman et al. (1998) report that of the different biological systems capable of fixing atmospheric N2, the Rhizobium-legume symbiosis constitutes the largest amount contributed to the ecosystem and to food production.

Among the species that establish symbiotic relationships with this bacterium is the common bean (Phaseolus vulgaris L.), which is the most important legume for human consumption worldwide, especially in underdeveloped countries; but at the same time, it is the species with the lowest nodulation and fixation capacity for atmospheric N2 (Burdman, 2000; Peña-Cabriales, 2000; Quintero, 2000). It is obvious that increasing the use and improving the management of N2 biologically fixed by this legume is an important goal for agriculture for both humanitarian and economic reasons.
The objective of this work is:

* Analyze the effects of the combined inoculation of Rhizobium leguminosarum biovar. phaseoli and Azotobacter chroococcum in N2 fixation and performance of common beans (Phaseolus vulgaris), as well as the study of two inoculation doses of the commercial Rhizobium biofertilizer.

Materials and methods.

The work was developed in areas belonging to the Agricultural Development Center of the FAR, in the municipality of Santo Domingo, in the period from January 23, 2001 to April 16 of the same year, using the Güira variety of black beans.

The characteristics of the soil in this area correspond to the typical reddish-brown Fersialitic classification, which presents an organic matter content of 2.95%, pH of 7.2 and P2O5 and K2O content of 43.02 and 32.72 Meq 100 g-1 respectively, a depth effective 51-90 cm and 2-4% humification.
24 plots of 25 m2 (5 x 5 m) were planted, using an experimental design in random blocks with 4 replications.

Treatments:

1. Inoculation with Rhizobium leguminosarum biovar. phaseoli at a rate of 150 g kg-1 of seed (Pérez, 2001).

2. Inoculation with Rhizobium leguminosarum biovar phaseoli at a rate of 150 g kg-1 of seed and Azotobacter chroococcum at a rate of 400 ml kg-1 of seed (Stancheva et al., 1995).

3. Inoculation with Rhizobium leguminosarum biovar phaseoli at a rate of 70 g kg-1 of seed.

4. Inoculation with Rhizobium leguminosarum biovar phaseoli at a rate of 70 g kg-1 of seed and Azotobacter chroococcum at a rate of 400 ml kg-1 of seed.

5. Mineral fertilization.

6. Witness (absolute).

The commercial Rhizobium biopreparation was used, which is carried out in the Provincial Soil Laboratory of the Villa Clara province, which was inoculated to the seed 24 h before sowing, using sucrose as an adhesive substance (Martínez, 1986). The Azotobacter biopreparation was carried out in the Microbiology laboratory of the Faculty of Agricultural Sciences of the UCLV, which had a bacterial concentration of 108 cfu ml-1, using the Mb-9 strain. The inoculation of this was carried out by immersing the seed previously inoculated with Rhizobium in the Azotobacter biopreparation for 15-20 minutes before sowing.

The dose of mineral fertilization applied was that recommended by the technical instructions, at a rate of 4 t cab-1 (0.75 kg per plot), of the complete formula 9-13-17. The application of this was carried out 15 days after sprouting.
The cultural attentions were those foreseen for the implantation of the crop according to the technical instructions.

Evaluations.

* Fixation parameters at 30 days, where samples of 20 plants were taken per plot (FAO, 1995).
- Number of total nodules.
- Number of active nodules.
- Fresh weight of nodules (g).
- Dry weight of nodules (g).

* Yield components at 80 days, samples were taken from 10 plants per plot (FAO, 1995).
- Number of pods per plant.
- Number of grains per plant.
- Number of grains per pod.
- Fresh weight of pods per plant (g).
- Fresh weight of grains per plant (g).
- Dry weight of 100 grains (g).
* At 84 days the harvest was carried out, subsequently analyzing the yield (t ha-1) of the different variants evaluated.

An economic analysis of the agricultural yield results was carried out to determine the effectiveness of the different fertilization variants evaluated and their influence on environmental contamination.
For the analysis of the fixation parameters, the data were processed using the SPSS statistical package, using the GLM (General Linear Model) Multivariate and Dunnett's test. The analysis of the data for the components of yield and agricultural yield were processed using the statistical package Statgraphics plus, through the GLM and Dunnett's test.

Results and Discussion.

The analysis of the fixation parameters is one of the main evaluations carried out in legume crops to measure and estimate the effectiveness of inoculation and nitrogen fixation (FAO, 1995).

As can be seen in table No 1 when analyzing the number of nodules per plant, there is a tendency to increase these in both combined inoculation treatments, with significant differences compared to the rest of the treatments analyzed. Regarding the inoculation with Rhizobium only, both at 150 g (1) and 70 g (3), there were no significant differences between these values, which indicates that the dose of the biopreparation can be reduced in this soil; but differences were observed when comparing them with the mineral fertilization treatment (5) and the control without inoculation (6). The latter, in all the parameters evaluated, differed significantly between both, and with lower values ​​than the other treatments. It is worth noting the number of nodules observed in the uninoculated control, although lower than the inoculated treatments, highlights the abundance and effectiveness of the autochthonous strains in this type of soil.

Table 1. Analysis of the fixation parameters.

TREATMENTS

TOTAL NODULES

PER PLANT

ACTIVE NODULES

PER PLANT

FRESH WEIGHT

OF NODULES (g)

DRY WEIGHT

OF NODULES (g)

1

26.54 b

15.76 b

0.129 bc

0.0411 b

2

33.67 to

24.17 a

0.165 to

0.0563 to

3

26.20 b

11.29 c

0.131 b

0.0438 b

4

31.71 to

14.35 b

0.144 ab

0.0496 ab

5

12.27 d

2.26 d

0.456 d

0.0114 d

6

20.29 c

9.97 c

0.104 c

0.0311 c

IT IS

2.072

1.489

0.013

0.004

Unequal letters in the columns differ for p <0.05.

When analyzing the active nodules per plant, this parameter of great importance, since it represents the effectiveness of the inoculation, it can be observed how the combined inoculation at 150 g (2) had the best absolute value with significant differences compared to the rest of the treatments, followed by the values ​​obtained by inoculation combined at 70 g (4) and inoculation with Rhizobium at 150 g (1), which did not differ statistically. Treatments 3 and 6 did not differ significantly, showing the effective infectivity of the native soil strains and the possible competitiveness with the inoculum strain. González and Lluch (1992) report that inocula prepared with very effective strains in N2 fixation have been shown to be unable to form a significant proportion of nodules in the field due to competition with autochthonous strains.
In the treatment where mineral fertilization was applied, what was stated by Vitousek and Matson (1993), cited from Anonymous (2001), can be corroborated; Montes (1999) and Caba et al. (2001) who point out that the presence of mineral nitrogen in the medium inhibits the formation of radical nodules and the activity of the nitrogenase enzyme.

The fresh weight of the nodules had a similar behavior to the results obtained in the variables previously analyzed, observing how the co-inoculation treatments resulted in the best values, statistically surpassing the controls. In this parameter, the effectiveness of the autochthonous strains of the soil can also be seen, as there are no significant differences between the uninoculated control and the inoculation with Rhizobium at 150 g kg.-1.
Like active nodules, the dry weight of the nodules is a parameter that has a great influence on the effectiveness of inoculation and N2 fixation. In these results, treatments 2 and 4 are evidenced as better values, which did not differ significantly between the two, although it is observed that treatment 4 had no significant difference with respect to treatments 1 and 3; but yes when comparing them with treatments 5 and 6.
Taking into account the global results of the behavior of the treatments against the fixation parameters, it can be observed that the combined inoculation with Rhizobium leguminosarum biovar phaseoli at a rate of 150 g kg.-1 of seed and Azotobacter chroococcum, was the treatment with the best values statistically, which can be given by the compatibility between the treated bacterial strains, the synergism between them and the adequate proportion of diazotrophs in the rhizosphere of the plants, causing an early colonization of the root hairs by Rhizobium, facilitated by the excretion of substances stimulators of plant growth produced by Azotobacter that directly influence the stimulation of the root system of the plant, as well as creating favorable conditions for infection by Rhizobium and increased nodulation. All these factors together will increase the availability of nutrients for diazotrophs and macrosymbionts and therefore favorable associative relationships will be established for the increase in N2 fixation.
These results coincide with those analyzed by Rodelas (2001) by stating that the inoculation of Rhizobium leguminosarum biovar viceae in combination with strains of Azotobacter and Azospirillum that promote plant growth, beneficially modifies both the concentration and the nitrogen content in the plants, in addition to have a favorable effect on nodulation and nitrogenase activity. Similarly, Burdman et al. (1997) state that when inoculating Azospirillum combined with Rhizobium leguminosarum biovar phaseoli in common beans, there was an increase in the total number of nodules and the fixation of atmospheric N2, in addition to an early nodulation.
These results are closely related to the interactions established between the treated strains, in this way it is suggested that the increases in nodulation and N2 fixation are caused by the ability of the genus Azotobacter to produce phytohormones and vitamins, such as acid Indoleacetic acid, gibberellic acid, cytokinins, thiamine, pantothenic acid, nicotinic acid and biotin, which intervene directly in plant development and bring about an elongation and conditioning of the root to facilitate infection by Rhizobium and subsequent nodulation (González and Lluch, 1992; De Troch, 1993; Baldini, 1997; Mayea et al., 1998; Caba et al., 1999; Rodelas, 2001).
In addition to these substances, the genus Azotobacter is capable of solubilizing phosphates, making them assimilable both by plants and by rhizospheric microorganisms, and in this way they contribute to creating favorable conditions for a good nodulation by Rhizobium. The conditions of low phosphorus availability reduce N2 fixation due to specific effects on the initiation and growth of the nodule and nitrogenase activity (González and Lluch, 1992; Montes, 1999).
Regarding the dose of inoculants, the one used at a rate of 150 g kg-1. of seed was the one with the best results, which shows that when there is an adequate bacterial concentration on the surface of the root hairs of the plants and in the rhizosphere, there will be a greater infection and proliferation by diazotrophs and therefore better results in nodulation (Pérez, 2001).
The yield components express a measure of the behavior of the different variants evaluated on the development and morphological parameters in this legume. In table No 2 it can be seen how with respect to the yield components, there were only statistical differences in terms of the number of pods per plant, number of grains per plant and number of grains per pod, parameters of great influence on yield.

Table 2. Analysis of the performance components.

About-

mentions

Do not give

pods

per plant

Weight of

pods by

plant (g)

Do not give

grains per

plant

Fresh weight

grain

(g)

Dry weight

of 100

grains (g)

Do not give

grain

per pod

1

5.62 b

3.91

21.07 b

2.84

12.80

3.92 to

2

6.77 to

4.81

26.47 to

3.64

13.04

3.92 to

3

5.10 b

3.42

18.62 b

2.47

12.84

3.40 b

4

5.90 ab

3.92

22.52 ab

2.77

11.37

3.79 to

5

6.00 ab

4.24

23.20 ab

3.15

12.79

3.98 to

6

5.20 b

3.62

20.22 b

2.65

12.45

3.84 to

IT IS

0.363

0.365

1.589

0.280

0.457

0.124


Unequal letters in the columns differ for p <0.05

Regarding the number of pods and number of grains per plant, it is observed that treatments 2, 4 and 5 did not differ statistically between them, as well as no differences between treatments 1,3,4,5 and 6, being the co-inoculation at 150 g, the only treatment that differed significantly with respect to variants 1,3 and 6. When analyzing the number of grains per pod, it was observed that treatments 1, 2, 4, 5 and 6 did not have significant differences, but they did when compared with the treatment of inoculation with Rhizobium at 70 g, which obtained the lowest absolute value.

These results coincide with those analyzed in the fixation parameters, since there is a low concentration of bacteria in the rhizosphere of the plants and the possible competition with the autochthonous strains of the soil due to the colonization of root hairs, the fixation of N2 and at the same time the growth and development of plants.

Analyzing the results of treatments 2 and 4 in comparison with those obtained in treatment 3 and the rest of the variants, the potentiation of the stimulation through the combined inoculation on the various variables evaluated is corroborated, an aspect that coincides with that proposed by Torres (2000), when studying the effect of the combined inoculation of Rhizobium leguminosarum biovar phaseoli and Azotobacter chroococcum (strain Mb-9) in two varieties of common bean (ICA Pijao and CIAP-7247), where it obtained a notable increase in the components of the yield (total biomass per plant, No. of pods per plant, No. of grains per plant, fresh weight of the grains and dry weight of 100 grains) compared to the inoculation with Rhizobium alone and to the control treatment.

Graph No 1 represents the yields obtained by the different treatments analyzed. It is worth highlighting the low production of grains in all the evaluated variants, mainly due to the irrigation deficit in the critical period of the crop, which brought with it a notable reduction in yields. However, it can be seen how treatment 2 obtained the best result, although without significant differences with treatments 4, 1 and 5; an increasing trend is observed in 24.47, 21.98 and 9.22% respectively with these treatments. Besides being the only variant that had significant differences with treatments 6 and 3, which obtained the lowest values, having increases with respect to these of 32.27 and 43.97% respectively.

Graph 1. Yield Analysis (t ha-1).

The behavior of the combined inoculation treatment at a rate of 150 g is explained by the synergistic and compatible relationships that these bacteria develop, as well as the bacteria-bacteria-plant interaction that is established, causing positive effects on the growth and performance of the plants. (Rodelas, 2001). In this association, the genus Azotobacter is capable of producing phytohormones and vitamins that favorably influence the growth and development of the root system, in addition to increasing the availability of assimilable mineral nutrients for the plant, enhancing both the proliferation of Rhizobium and the fixation of N2. Similar results are those obtained by Rodelas et al. (1999) when coinocular strains of Rhizobium leguminosarum biovar viceae Z. 25 (CECT 4585) and Azotobacter chroococcum H. 23 (CECT 4435) in Vicia faba, showing an increase in the total content per plant of phosphorus (P), potassium (K ), calcium (Ca), magnesium (Mg), manganese (Mn), zinc (Zn), copper (Cu), boron (B) and iron (Fe) in the fraction corresponding to the aerial part of the treated plants. In this sense, Burdman et al. (1996) state that inoculation with Rhizobium etli TAL 82 and Rhizobium tropici CIAT 899 in the common bean crop significantly increases the number of grains per plant, while co-inoculation with Rhizobium leguminosarum biovar phaseoli and Azospirillum brasilense strain Cd has resulted with higher yield increases than with Azospirillum inoculation alone. Likewise Burdman et al. (2000) state that the combined inoculation with Rhizobium leguminosarum biovar phaseoli and Azospirillum brasilense significantly increases the yield of common beans under limited conditions of water and nitrogen, pointing out that field experiments have shown increases in yields of 15 to 30% in coinoculated legumes. , values ​​higher than those obtained with the application of Rhizobium alone.

The results of the inoculated treatments have a close correlation with those obtained in the fixation parameters and the performance components, due to the fact that there is a greater fixation of N2 and increased levels of this element in the plants, it contributes to improving nutrition. vegetable bringing with it the increase in the production of grains per plant.

When analyzing the result of treatment 4, which did not differ with the control without inoculation and the rest of the treatments, it could be mainly caused by the low concentration of rhizobia in the inoculant, an effect very similar to what happened in treatment 3, in which both the concentration of microsymbionts and the influence of competitiveness with autochthonous strains, resulted in a significant reduction in yield. According to González and Lluch (1992), in order to achieve an effective combined inoculation of N2-fixing bacteria, an adequate cell relationship must be taken into account, since the random proportion can cause negative effects on nodulation and plant development. In both treatments where doses of Rhizobium were applied at a rate of 70 g, there were no significant differences; but an increase of 25.82% can be noted in the co-inoculation treatment with respect to the inoculation with Rhizobium alone.Regarding the treatment with mineral fertilization, it can be observed how this did not have significant differences with treatments 1, 4, 6 and 2, however , the latter presented a higher value than said treatment, for which it is recommended, taking into account the high levels of P2O5 and K2O present in this type of soil, the reduction of the application of mineral fertilizers. In this way, the yield would be increased by 9.22% on average and the production costs would be reduced. These results are in correspondence with those cited by Arcocha et al. (1994) by pointing out that it is possible to replace nitrogen fertilization by inoculation with Rhizobium in the cultivation of green beans, where the yield increased by 4478 kg.ha-1 of green beans in relation to the nitrogen fertilization treatment. Likewise, Huerta et al. (2001) when studying the yields of different common bean genotypes, found that some genotypes had the same yields when inoculated with Rhizobium as when fertilized.

Table No 3 shows the economic analysis carried out to produce 1 cab. of common bean from the fertilization variants, for which the traditional mineral fertilization was taken as a reference in contrast to the biological fertilization with Rhizobium and Azotobacter at a rate of 150 g kg.-1 of seed. It is noteworthy that the obtaining of mineral fertilizers by our country is carried out through imports, either of the fertilizer formulas, as well as of the raw material for its preparation, being necessary the investment of large sums of freely convertible currency for its acquisition or production, making the production process more expensive.

Table 3. Economic analysis of the fertilization methods for 1 cab.

Variants

performance

(qq cab-1)

cost

($)

Income from

Sales ($)

Net profit

($)

Biological

83.26

2 115.79

29 141

27 025.01

Mineral

75.59

14 867.80

26 456.50

11 588.70

Benefits

7.76

12 751.81

2 684.50

15 436.3

When analyzing the costs of both fertilization methods, a lower value is appreciated with the use of biological fertilization, which reduced this indicator by $ 12,751.81 compared to mineral fertilization, which shows the cost benefit of biological methods and saving inputs through this practice (Annexes 4). In the income from sales to Acopio, it is observed that with the use of biological fertilization a benefit is obtained for increases in production of $ 2,684.50 with respect to mineral fertilization. The net benefits represent the profits obtained through the different variants evaluated, for This means that by reducing production costs and increasing sales profits, there will be an increase in profits, observing a difference of $ 15,436.31 in the biological treatment when compared to the mineral.

The benefits of the application of biological fertilizers are not only appreciated in economic terms, but also the harmful effects of nitrogen fertilization on the absorption, assimilation and availability of different nutrients such as phosphorus (Montes, 1999), as well as the eradication of both atmospheric pollution as well as groundwater and the water table, this environmental impact being much more necessary than the economic impact.

Conclusions.

1. The application of Azotobacter chroococcum enhances the action of Rhizobium with respect to the efficiency of N2 fixation in common bean cultivation.

2. Co-inoculation significantly increases the number of active nodules, N2 fixation, the main components of yield and agricultural yield compared to the inoculation of Rhizobium alone and the control treatment.3. The optimal dose for Rhizobium inoculation is 150 g kg.-1 of seed.

Recommendations.

1. Study the possible application of Azotobacter only in this type of soil, due to the abundance and effectiveness of the autochthonous Rhizobium strains in this area.

2. Inoculate the common bean seed (Phaseolus vulgaris L.) with the combination of 150 g kg -1 of Rhizobium inoculant seed with 400 ml kg-1 of Azotobacter seed.

Bibliography.

1.- Anonymous. 2001. Biological Nitrogen Fixation. Agency for International Development. In: (http://www.nap.edu/readingroom/books/bnf/chapter1.html).
2.- Arcocha, G. E. and Ruíz, V. J. Inoculation against chemical fertilization in green beans (Phaseolus vulgaris). II Workshop on biofertilization in the tropics. November 16-18. Havana. Tropical Crops 15 (3). 1994: 73.
3.- Baldini, Y. Recent advances in BFN with non-legume plants. Soil Biology Biotechnology. 29 (5). 1997: 911-922.
4.- Bauer, T. Nitrogen Fixing Microorganisms: Rhizobiaceae family. In: (http://www.microbiologia.com.ar/suelo/rhizobium.html).
5.- Burdman, S .; Kigel, J. and Okon, Y. Effects of Azospirillum brasilense on nodulation and growth of common bean (P. vulgaris L.). Soil Biology Biochemistry 29 (5/6). 1997: 923-929.
6.- Burdman, S .; Vedder, D .; German, M .; Itzigsohn, R .; Kigel, J .; Jurkevitch, E. Legume crop yield promotion by inoculation with Azospirillum. In C. Elmerick, A. Kondorsi, and W. Newton. Eds. Biological Nitrogen Fixation for the 21st Century. 1998: 609-612.
7.- Burdman, S .; Hamaoui, B. 2000. Improvement of legume crop yields by co-inoculation with Azospirillum and Rhizobium. The Otto Warburg Center for Agricultural Biotechnology. The Hebrew University of Jerusalem, Israel.
8.- Caba, J. M .; Luque, C .; Mirapleix, M. J .; Gresshoff, P. M. and Ligero, F. 1999. Differential sensitivity of nodulation to ethylene in soybean (Glycine max) cv. Bragg and a supernodulating mutant. In: (http://www.cartuja.csic.es/SEFV99/abstracts/nuticion/p.3-29.html).
9.- Caba, J.M .; Poveda, J.L. Control of nodulation in legumes: Implication of phytohormones. In: (http://193.146.205.198/sefin/Ligero.html).
10.- De Troch, P. 1993. Bacterial surface polisaccharides in relation: a genetic and chemical study of Azospirillum brasilense. Dissertations of Agriculture. p 238.
11.- FAO. 1995. Technical manual of symbiotic nitrogen fixation. 125 pp.
12.- González, J. and Lluch, Carmen. 1992. Nitrogen Biology. Plant-Microorganism Interaction. Ed. Rueda. Madrid. Spain.
13.- Huerta, J .; Escalante, J. A .; Castellanos, J. Z .; Robles, R. and Flores, J. A. Biomass and grain production in common beans (Phaseolus vulgaris L.) as a function of nitrogen fertilization and inoculation with Rhizobium leguminosarum biovar phaseoli. In: (http://zea.chapingo.mx/somefi/RFM/20-1-es.html#Art4).
14.- Mayea, S .; Carone, Margarita; Novo, R .; Boado, Isabel; Silveira, E .; Soria, Miguelina; Morales, Yolanda and Valiño, A. 1998. Agricultural Microbiology. Volume II. Felix Varela. pp 156-178.
15.- Montes, Leidi. Effect of phosphorus on the nitrogen nutrition of common beans (P. vulgaris). In: (http://www.cartuja.csic.es/SEFV99/abstracts/nutricion/s.3-6.html).
16.- Peña-Cabriales, J. Biological Nitrogen Fixation in Latin America. The contribution of isotopic techniques. IMPROSA, S.A. de C.V., Irapuato. Mexico. 120 pp.
17.- Pérez, C. Personal communication.
18.- Quintero, E. Monograph. Agrotechnical management of beans (P. vulgaris) in Cuba. UCLV. Cuba.
19.- Rodelas, María Belén; Gonzalez. J .; Martínez, M. V .; Pozo, C. and Salmeron, V. Influence of Rhizobium-Azospirillum and Rhizobium-Azotobacter combined inoculation on mineral composition of faba bean (Vicia faba L.). In: (http://link.springer-ny.com/link/service/journals/00374/bibs/9029002/90290165.htm).
20.- Rodelas, María Belén. Rhizobium-Azospirillum and Rhizobium-Azotobacter interaction. Effect on nodulation and symbiotic fixation of dinitrogen in Vicia faba. In: (http://193.146.205.198/sefin/Ecologia/Rodelas.html).(http://193.146.205.198/sefin/Ecologia/Rodelas2.html).
21.- Stancheva, I .; Dimitrov, N .; Kalayanova, N .; Dinev, N. and Ponsha, K. Improvement of nitrogen uptake and nitrogen content in maize (Zea mays L.) by inoculation with Azospirillum brasilense. Agrochimic XXXIX (5-6), Sep-Dec. nineteen ninety five.
22.- Torres, R. Combined inoculation of Rhizobium leguminosarum biovar phaseoli and Azotobacter chroococcum in the common bean crop (Phaseolus vulgaris L.). Science and Technology Event, UCLV.

(one). Faculty of Agricultural Sciences, UCLV. Highway to Camajuaní Km 5 1/2, Santa Clara, Villa Clara. Cuba. CP: 54830.
(2). Center for Agricultural Research, UCLV. CP: 54830.
(3). Agricultural Development Center of the FAR, AGROFAR. Santo Domingo, Villa Clara. E-mail: [email protected]


Video: Luis Herrera-Estrella Langebio Spanish Part 1: Plant nutrition and sustainable agriculture (June 2022).


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