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Cultivos Tropicales

versão impressa ISSN 0258-5936versão On-line ISSN 1819-4087

cultrop vol.42 no.3 La Habana jul.-set. 2021  Epub 30-Set-2021

 

Short communication

Effect of the inoculation of PGPR isolated from corn on the growth of this crop under controlled conditions

Reneé Pérez-Pérez1  * 
http://orcid.org/0000-0002-5144-212X

Simón Pérez-Martínez2 
http://orcid.org/0000-0001-7349-7036

Iván Almeida-Acosta3 
http://orcid.org/0000-0002-5187-5881

1Instituto Nacional de Ciencias Agrícolas (INCA), carretera San José-Tapaste, km 3½, Gaveta Postal 1, San José de las Lajas, Mayabeque, Cuba. CP 32 700

2Universidad Estatal de Milagros (UNEMI). Milagros, Provincia del Guayas, Ecuador

3Estudiante, Universidad Agraria de La Habana “Fructuoso Rodríguez Pérez”, carretera a Tapaste y Autopista Nacional, San José de las Lajas, Mayabeque, Cuba

ABSTRACT

The application of inoculants formulated based on plant growth promoting rhizobacteria in crops of agricultural interest such as corn, represents an ecological alternative to the use of chemicals in agriculture. On the other hand, the use of native strains for the inoculation of plants could represent an advantage over the use of alien strains and, therefore, improve crop production. Consequently, the present work aimed to evaluate the inoculation effect of 20 bacterial strains, isolated from the rhizosphere of corn and previously characterized, corresponding to the genera Stenotrophomonas, Pseudomonas, Rhizobium and Enterobacter, in the development of morphoagronomic variables of its own culture. For this, inoculants were prepared with each of the strains in liquid LB medium. The inoculation was carried out on the corn seeds sown in unsterilized Red Ferrallitic soil, at a rate of 300 μl of inoculum per seed. The experiment was established under controlled conditions of light, relative humidity, temperature and irrigation and it was determined: plant height, root length, aerial dry mass, root dry mass and concentration of total chlorophylls, 30 days after inoculation. The best results were obtained with treatments inoculated with Stenotrophomonas sp. INCA-FRr1, Stenotrophomonas sp. INCA-FRc24 and Rhizobium sp. INCA-FRc1. This study represents the basis for the conception of a new bioproduct destined for the fertilization of corn crop.

Key words: FBN; Stenotrophomonas; Rhizobium; nutrition; phytostimulation

INTRODUCTION

The soil houses a large number of living beings, mainly microorganisms. The genetic variety and the diversity of ecological niches of microbial populations have a high impact on soil functions and, especially, on plant growth and development 1. Interactions established between plant roots and edaphic microorganisms constitute a dynamic environment called rhizosphere 2, where the diversity and size of microbial populations is higher compared to uncultivated soil 3. These populations actively participate in the biogeochemical cycles of nutrients, mainly nitrogen and phosphorus, produce plant hormones, synthesize antibiotics, among other characteristics and, as a result, favor the establishment, nutrition and development of plants 4.

Corn is one of the most important cereals, from a nutritional point of view; also, it is the most cultivated and harvested worldwide, along with wheat and rice 5. Given the domestication process that this crop has undergone, it is necessary to use large amounts of fertilizers to obtain acceptable yields 6. Fertilization, especially the incorporation of mineral nitrogen to the crop, represents the highest cost of the production process 7; Furthermore, the irrational use of these inputs has a negative impact on the agroecosystem 8 and even on human health 9.

The manufacture and application of inoculants formulated with various microbial species is a well-known practice in agriculture. Currently, within the framework of sustainability, the search for new microorganisms with various properties that promote plant growth is an emerging line of research, since in certain circumstances, they can partially replace the use of pesticides and chemical fertilizers 10. The use of native strains as inoculants promote the ecological-sustainable management of agroecosystems and could improve crop production 11. The ability of native strains to interact positively with the resident edaphic microbiota and their adaptability to local climatic and agroecological conditions often enhances their performance compared to non-native strains 12.

The objective of this work was to evaluate the inoculation effect of 20 strains, characterized as PGPR, isolated from the corn rhizosphere, corresponding to four bacterial genera (Stenotrophomonas, Pseudomonas, Rhizobium and Enterobacter), on the growth of low corn plants. controlled conditions.

MATERIALS AND METHODS

Microbiological material

Twenty strains isolated from the rhizosphere of commercial corn cultivars 'Raúl' and 'Canilla' were used. These were previously identified and were characterized, based on their ability to perform BNF, solubilize phosphorus and potassium salts and inhibit mycelial growth of the pathogen Fusarium oxysporum13. The characteristics of the strains are shown in Table 1.

Table 1 Identification and qualitative characterization as PGPR of 20 strains from the rhizosphere of Zea mays L. cultivars 'Raúl' and 'Canilla' 

Strains Identification BNF Solubilization (PO4 -2) Solubilization (K+) Antagonism
INCA-FRr1 Stenotrophomonas sp. + + + +
INCA-FRr2 Pseudomonas sp. + + - +
INCA-FRr3 Pseudomonas sp. + + - +
INCA-FRr4 Pseudomonas sp. + + - -
INCA-FRr5 Pseudomonas sp. + + + -
INCA-FRr6 Stenotrophomonas sp. + + - -
INCA-FRr7 Stenotrophomonas sp. + + - +
INCA-FRr8 Pseudomonas sp. + + - +
INCA-FRr9 Pseudomonas sp. + + - -
INCA-FRr10 Rhizobium sp. + - - -
INCA-FRr11 Pseudomonas sp. + + - -
INCA-FRr12 Stenotrophomonas sp. + + - -
INCA-FRr13 Stenotrophomonas sp. + + - -
INCA-FRr16 Enterobacter sp. + + - -
INCA-FRc1 Rhizobium sp. + - - -
INCA-FRc4 Rhizobium sp. + - - -
INCA-FRc8 Rhizobium sp. + - - -
INCA-FRc16 Stenotrophomonas sp. + + - -
INCA-FRc19 Rhizobium sp. + - - -
INCA-FRc24 Stenotrophomonas sp. + + - +

Preparation of inoculants

Inoculants were prepared in Erlenmeyer flasks of 150 mL capacity, with 20 mL of liquid LB medium. These were inoculated with a roast of each strain, stored at 4 ºC in solid LB medium. The flasks were kept under shaking conditions on a thermostated orbital shaker at 150 rpm and 29 °C for 24 h. The optical density was adjusted by spectrophotometry to 0.5 (λ = 600 nm) in each inoculant.

Inoculation in corn plants under controlled conditions

Corn cultivar ‘Raúl’ seeds were used, from the seed bank of the Department of Genetics and Plant Breeding of the National Institute of Agricultural Sciences (INCA). These were superficially disinfected with 70 % ethanol for 5 min, 20 % sodium hypochlorite, for 10 min and six consecutive washes with sterile distilled water. Then, they were placed superficially in pots with 700 g of Leached Red Ferralitic soil, not sterilized, at the rate of two seeds per pot. The inoculation was carried out with 300 μl of inoculum on each seed, establishing 20 treatments and a non-inoculated control. Five days after inoculation, the less developed or non-germinated seedling was extracted from each pot, keeping one plant per pot. The test was maintained for 30 days under controlled conditions of photoperiod (12 h light/12 h darkness), temperature (day/night 26/22 °C) and relative humidity (70 %). Irrigation was carried out every three days for all treatments, including the control, with a modification of the Hoagland nutrient solution (5 gL-1 KH2PO4, 27 g L-1 MgSO4.7H2O, 0.14 g L-1 H3BO3, 0.15 g L-1 CuSO4.5H2O, 0.008 g L-1 (NH4) 6Mo7O24.6H2O, 0.06 g L-1 ZnSO4.7H2O, 0.2 g L-1 MnSO4.4H2O, 1.87 g L-1 Fe-EDTA (6%)), from which the nitrogenous salts were removed. Subsequently, height (cm), root length (cm), aerial dry mass (ADM) (g), radical dry mass (RDM) (g) and total chlorophyll content (SPAD)

Diseño y análisis estadístico Statistical design and analysis

Eight replications per treatment were established and a completely randomized design was used. Variable values that were determined were subjected to the Bartlett normality test and the Kormogorov-Smirnov homogeneity of variance test. Subsequently, a simple classification analysis of variance was applied, using the Tukey mean comparison test for p <0.05. The SPSS Statistic program (ver. 21) was used for the statistical processing of the data. The experiment was carried out in triplicate.

RESULTS AND DISCUSSION

Inoculation in corn plants under controlled conditions

At 30 days after inoculation, statistical differences were observed between the growth indicators evaluated in each of the treatments (Table 2).

The treatments with the best results corresponded to the plants inoculated with the INCA-FRr1 and INCA-FRc24 strains, identified as Stenotrophomonas, in addition to INCA-FRc1, identified as Rhizobium. These treatments presented statistically superior values to the control in four of the five variables evaluated, which could be related to the mechanisms of plant growth promotion that they present.

Table 2 Inoculation effect of bacterial strains on the growth of corn plants cultivar 'Raúl', under controlled conditions 

Strains Height (cm) Root Length (cm) ADM (g) RDM (g) Total chlorophylls (SPAD)
INCA-FRr1 65.34 a 38.60 ab 0.63 abc 0.53 a 19.14 d
INCA-FRr2 57.90 abcd 35.79 abc 0.70 a 0.45 abc 28.56 abc
INCA-FRr3 61.64 abc 35.04 abc 0.66 ab 0.42 abc 25.96 bc
INCA-FRr4 59.52 abcd 35.82 abc 0.55 adcd 0.36 abc 27.59 abc
INCA-FRr5 58.26 abcd 34.40 abc 0.60 abcde 0.43 abc 29.26 abc
INCA-FRr6 53.40 de 38.34 ab 0.51 bcde 0.40 abc 33.38 a
INCA-FRr7 55.32 bcd 41.98 a 0.58 abcd 0.51 a 23.94 cd
INCA-FRr8 52.14 de 34.38 abc 0.49 bcde 0.41 abc 26.75 bc
INCA-FRr9 63.76 ab 30.60 c 0.64 abc 0.49 a 19.35 d
INCA-FRr10 56.04 abcd 32.70 bc 0.55 abcd 0.53 a 26.44 bc
INCA-FRr11 57.30 abcd 32.00 bc 0.48 cde 0.44 abc 28.43 abc
INCA-FRr12 60.04 abcd 35.04 abc 0.52 abcde 0.48 ab 28.01 abc
INCA-FRr13 54.08 cde 37.90 ab 0.50 bcde 0.38 abc 28.86 abc
INCA-FRr16 61.53abc 35.06 abc 0.67 ab 0.44 abc 24.22 cd
INCA-FRc1 64.90 a 37.20 ab 0.66 abc 0.50 a 18.74 d
INCA-FRc4 57.24 abcd 37.92 ab 0.56 abcd 0.40 abc 23.25 cd
INCA-FRc8 44.66 f 34.80 abc 0.34 f 0.36 abc 33.83 a
INCA-FRc16 64.80 a 37.18 ab 0.52 bcde 0.39 abc 29.74 abc
INCA-FRc19 53.40 de 30.90 bc 0.44 de 0.28 c 29.08 abc
INCA-FRc24 43.89 f 37.84 ab 0.63 abc 0.52 a 33.66 a
Control 51.24 e 29.60 c 0.39 ef 0.31 bc 18.70 d
Standard error 0.794 0.593 0.012 0.015 1.793

The mean of each treatment and the standard error for each measured variable are represented.

Equal letters in the same column do not differ significantly (Tukey p <0.05, n = 8)

Treatments with the strains Pseudomonas sp. INCA-FRr9 Stenotrophomonas sp. INCA-FRr12 and Stenotrophomonas sp. INCA-FRc16. The genera Stenotrophomonas, Pseudomonas and Rhizobium, are reported as natural, rhizospheric and endophytic microbiota of various crops including corn 14-16. Previous works ensure the phytostimulant effect of these microorganisms on different crops of agricultural interest, both legumes and non-legumes 17-20.

Plant height does not tend to increase much more than the non-inoculated controls, after applying some biological treatment 21; however, the results show significant increases of up to 27.5 % between the INCA-FRr1, INCA-FRc1 and INCA-FRc16 strains, with respect to the non-inoculated control. Different tests of inoculation of Rhizobium and Stenotrophomonas in corn result in a slight increase in the length of the plants, in comparison with the results obtained in this investigation 21-24. On the other hand, the root length was favored in the plants inoculated with these same treatments, in addition to the INCA-FRc24 and INCA-FRr7 strains. According to the literature, inoculation with different species of Rhizobium enhances an increase in root length, root number and root dry mass in corn plants 22. In the case of inoculation with Stenotrophomonas, significant increases in root development have not been reported in previous research 24-26; however, the best results in this trial correspond to treatment with Stenotrophomonas sp. INCA-FRr7, which presented an increase in root length of 41.8 %, above the control treatment.

The strains that contributed the most to the development of the aerial dry mass were Pseudomonas sp. INCA-FRr2, Pseudomonas sp. INCA-FRr3 and Enterobacter sp. INCA-FRr16, which presented increases of up to 79.5% compared to the control. Similar results are reported in the literature for some species of Enterobacter and Pseudomonas, which are mainly attributed to BNF and phytohormone production 27,28. Regarding the radical dry mass, increases of up to 71 % were obtained, with respect to control plants in the INCA-FRr1, INCA-FRc1 and INCA-FRc24 treatments, mainly. Some authors suggest that the growth and development of morphoagronomic variables in corn is caused by a sum of factors and not by individual values obtained in vitro29. Others affirm that the products from BNF contribute in high percentages to the total biomass development of maize and highlight the role of auxins as the main causes of the increase in root and aerial biomass 30.

On the other hand, the highest concentrations of total chlorophylls were obtained, again, in treatments inoculated with Rhizobium and Stenotrophomonas, highlighting the INCA-FRr6, INCA-FRc8 and INCA-FRc24 strains, with an increase of 81 %, above the control. The chlorophyll content in plant is closely related to its nutritional status 31 and, particularly, to the nitrogen content as an essential component of this biomolecule 32. Various investigations estimate a direct relationship between the production of chlorophylls and the supply of nitrogen to the plant, based on obtaining higher concentrations of total chlorophylls, as the dose of mineral nitrogen in the soil increases 32,33. Thus, one of the important factors that indicates the efficiency of nitrogen fertilization is the content of photosynthetic pigments in leaves, since the proteins of the Calvin cycle and of the thylakoids represent most of the foliar nitrogen 21.

Taking into account that all the strains used had the ability to perform BNF, it could be said that this aspect favored the production of total chlorophylls. However, plants inoculated with the INCA-FRr1 and INCA-FRc1 strains showed the lowest values of this variable, which contrasts with the rest of the variables, in which both treatments stood out positively. This could suggest that perhaps, BNF was not the main plant growth promotion mechanism used by these strains.

In this research, the soil used came from the same region from which the inoculated strains were isolated; furthermore, it was not sterilized for the trial, so there should be no significant changes in the resident microbiota 34. Indeed, the microbial populations present in this soil must have influenced the plant growth promoting activity of the inoculated strains, either by enhancing or inhibiting it. Therefore, it could appreciate that there is compatibility and synergism between the INCA-FRr1, INCA-FRc1 and INCA-FRc24 strains and the resident edaphic microbiota. On the other hand, mineral fertilizer was not applied to the treatments, which could influence the expression of plant growth promotion mechanisms presented by inoculated strains, especially BNF.

It has been shown that a deficiency in nitrogen compounds in the medium stimulates the synthesis of the enzymatic complex Nitrogenase, responsible for BNF 35. In this case, the low content of organic matter present in the Red Ferrallitic soils 36, the nitrogen elimination of compounds from the Hoagland nutrient solution and the lack of mineral fertilizer, could enhance conditions for the expression of nitrogen-fixing activity of these strains. On the other hand, and without ruling out the fundamental role of this element in the growth of plants, especially corn, it is possible that these microorganisms present other mechanisms to promote plant growth that have not been determined in this work. It should also be noted that the genera Stenotrophomonas and Rhizobium, the most outstanding in this trial, despite their diazotrophic character, in non-legume plants are better known for their phytostimulant capacity than for the contribution of BNF 21-24,37,38. For these reasons, it would be convenient to carry out a more complete characterization of the strains studied.

CONCLUSIONS

  • The inoculants made up of Stenotrophomonas sp. INCA-FRr1, Stenotrophomonas sp. INCA-FRc24 and Rhizobium sp. INCA-FRc1, presented significant increases with respect to the non-inoculated control in a greater number of variables. Although increasing nitrogen availability through BNF is essential for plant growth, there could be other mechanisms that contribute to it significantly. For this reason, it is necessary to delve into other characteristics that promote plant growth that these strains could present.

  • The INCA-FRr1, INCA-FRc1 and INCA-FRc24 strains are promising inoculants for a new phase of experimentation under semi-controlled and field conditions.

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Received: October 14, 2019; Accepted: March 29, 2021

*Author for correspondence: riny@inca.edu.cu

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