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Idesia (Arica)

versión On-line ISSN 0718-3429

Idesia vol.35 no.2 Arica jun. 2017  Epub 13-Mayo-2017 

Sugarcane clones inoculated with five species of promoting growth plant bacteria


Clones de caña de azúcar inoculados con cinco especies de bacterias promotoras del crecimiento vegetal


Figueiredo Guilherme Grodzki Oliveira1*, Civiero Joño Carlos1, Romano Tales1, Bespalhok Filho Joño Carlo1, Daros Edelclaiton1

1 Department of Plant Science and Crop Protection, Federal University of Paraná, Rua dos Funcionários. Curitiba, Paraná, Brazil.* Corresponding author:;


The utilization of Plant Growth Promoting Bacteria (PGPB) in non-leguminous plants as sugarcane have been intensified along the last years targeting mainly the increase in productivity and the appeal for more sustainable agriculture. The genotypes selection that have closer affinity with PGPB strains may be the way to optimize sugarcane production and to boost sustainable agriculture in agroenergetics sector. In this way, the aim of the work was to test the response of five sugarcane clones and RB867515 cultivar with mix PGPB inoculation. The experiment was conducted in greenhouse for 45 days long in completely randomized design factorial 6x2, with six sugarcane genotypes, which five of them derived from previous PGPB works and the treatments were control and inoculated, being first one without PGPB application and the second one with 1-bud sett immersed in bacterial solution, evaluating shoot and roots of plants. The only significant variable was height of plants for all applying treatments, and genotypes were statistically different among them in all estimated parameters. There was treatment x genotype interaction, except the root morphologic analysis, of which only showed difference within genotypes. However, there was not standard response of inoculation among the genotypes, where clones 7 and 8 showed potential in PGPB studies, and the RB867515 was non-responsive to the in-oculation. Posterior tests are necessary with these genotypes evaluating bacteria population and late response of inoculated plants.

Key words: Saccharum spp., PGPB, root morphology, genotypes.


La utilización de bacterias promotoras del crecimiento vegetal (BPCV) en plantas no leguminosas como la caña de azúcar se ha intensificado en los últimos años, dirigiéndose principalmente al aumento de la productividad y para una agricultura más sustentable. La selección de genotipos que tienen una mayor afinidad con las cepas de BPCV puede ser la forma de optimizar la producción de caña de azúcar y fomentar la agricultura en el sector de agroenergía. El objetivo del trabajo fue analizar la respuesta de cinco clones de caña de azúcar y el cultivar RB867515 con la inoculación de una mezcla de cinco BPCV. El experimento se realizó en invernadero durante 45 días en diseño 6x2, con seis genotipos de caña de azúcar, cinco de ellos derivados de trabajos previos con BPCV. Los tratamientos fueron el control y inoculado, siendo el primero sin BPCV y el segundo con esquejes de una yema inmerso en solución bacteriana, evaluando brotes y raíces de plantas. La única variable significativa fue la altura de las plantas para todos los tratamientos aplicados, y los genotipos fueron estadísticamente diferentes entre ellos en todos los parámetros estimados. Hubo interacción tratamiento x genotipo, excepto el análisis morfológico de raíz, de los que solo mostró diferencias en los genotipos. Sin embargo, no hubo respuesta estándar de inoculación entre los genotipos, donde los clones 7 y 8 mostraron potencial en los estudios con BPCV, y el RB867515 no respondió a la inoculación. Posteriores pruebas son necesarias con estos genotipos evaluando la población de bacterias y la respuesta tardía de la planta inoculada.

Palabra clave: Saccharum spp., BPCV, morfología de la raíz, genotipo.


Sugarcane belongs to the family Poaceae that have great importance in the agriculture business. This crop is planted in 27 million hectares around the world. The planting is mainly restricted in the boundaries of the hottest regions on the Earth, where the most soils have low amounts of nutrients (FAO 2015; James 2004). The sugarcane development in limited soils could be explained by the cultivars adaptation with the environments, followed by affinity with soil's microorganisms, which includes the Promoting Growth Plant Bacteria (PGPB). The PGPBs supply nutrients to the plant through the soil, rhizosphere and even inside the plant, utilizing the mechanisms of Biological Nitrogen Fixation (BNF) or the production of other compounds that promot plant development, such as phytohormones and siderophores (Mehnaz, 2013, 2015).

According Boddey et al. (1991), those bacteria could contribute with 60-80% of total nitrogen amount constituent in superior plants. These values may represents about 200 kg N ha-1 year, justifying the sugarcane development in poor soils, in this way being projected an economy of fertilizers with the use of inocula of PGPB. On the other hand, the phytohormones produced by PGPBs promotes the growth of plants, mainly roots, elongating stalks and increasing chlorophyll content in leaves, affecting positively the productivity of sugarcane, as demonstrated by Marques Júnior et al. (2008), Oliveira et al. (2002) and Pereira et al. (2013).

Oliveira et al. (2002) when searching for inoculant to sugarcane, showed the contribution of PGPB mix in SP70-1143 sugarcane cultivar. They used five bacteria, among which: Gluconacetobacter diazotrophicus, Azospirillum amazonense, Burkholderia tropica, Herbaspirillum rubrisubalbicans and H. seropedicae. The benefits of these bacteria were demonstrated in others studies, such as production of phytohormones and BNF (Bastián et al., 1998; Fuentes-Ramírez et al., 1993; Mehnaz, 2013).

Bastián et al. (1998) studied the bacteria H. seropedicae and G. diazotrophicus, and observed the phytohormones Auxins and Gibberellins produced by them, corroborating the results obtained by Fuentes-Ramírez et al. (1993), whereupon visualized the potential of G. diazotrophicus (strain: PAl5), in Auxin production. The same strain was reported in the work of Oliveira et al. (2002). According Mehnaz (2015) the genus Azospirillum sp. has been a tool to inoculate plants because to the producing Auxin, Gibberellin, Cytokinin and Ethylene.

Even though the contribution of those bacteria to the sugarcane's growth, there is an interaction more specific between sugarcane genotypes and bacteria strains, enhancing the "promoting effect" (Lopes et al., 2012). Lopes et al. (2012) studying sugarcane families interacting with A. brasilense strains, opened possibilities to forward responsive clone selection in initial breeding phases.

Accordingly, the exploration of PGPBs in the sugarcane is becoming more directed to better association among genotype (commercial-use) and bacterium, linked also to the cultivating environment. Nonetheless, in a non-controlled environment, as field crops, have been demonstrated divergence in results with same genotype and bacterium, which obligate the research programs to find better association in initial phases of breeding (García et al., 2013; Muthukumarasamy et al., 2006; Lopes et al., 2012; Pereira et al., 2013; Schultz et al., 2014).

Thus, the aim of the present work consisted in test the response of five sugarcane clones and the cultivar RB867515 with the inoculation of a mixed PGPBs inoculum.

Materials and Methods

The experiment was conducted in greenhouse for 45 days long, in Crop Science Department of Federal University of Paraná-Brazil. PET recipients with 1-liter capacity were utilized to condition plants. One bud sett with 5 cm sectioned from apical part of stalk in a recipient was planted. The chronological age of the bud was 10 months, and was treated thermally in water-bath (52 °C for 30 minutes). The sets were acclimated for 48 hours with 35 °C.

The substrate Plantmax® autoclaved for 60 minutes, 1 atm and 120 °C was utilized. Its composition consists of pinus, vermiculite, simple superphosphate and potassium nitrate. The chemical composition is: pH (H2O) 5.47, 662.1 ppm P, 600 ppm K, 22.62 ppm Zn, 210.3 ppm Fe, 21.4 ppm Mn, 0.79 ppm Cu, 9.64 (cmolc dm-3) Ca2+, 3.65 (cmolc dm-3) Mg2+ and 0.24 (cmolc dm-3) Al3+.

The treatments were control (non-inoculated), consisting in 1-bud sett immerset in distilled water for 30 minutes; and other one inoculated treatment with 1-bud sett immersed in solution prepared with mixed bacteria for 30 minutes. The bacteria were: Gluconacetobacter diazotrophicus (BR11281), Azospirillum amazonense (BR11115), Burkholderia tropica (BR11366), Herbaspirillum rubrisubalbicans (BR11504) and H. seropedicae (BR11335). The bacteria came separately in liquid vehicle, containing 109 cells mL-1, and the solution prepared by mix of bacteria in distilled water in 1:100 ratio.

Five sugarcane clones with response to inoculation from Lopes et al. (2012) work were used (Table 1), and RB867515 was the standard cultivar. The experiment were in completely randomized factorial design (two treatments and six genotypes), with four replications. Two plants represented the parcel.

Table 1. Responsive clones to inoculation in previously study.

Adapted from Lopes et al. (2012).

The evaluation occurred 45 days after inoculation and the estimated parameters were height of plants (cm) (measured from the ground to +1 leaf, when sheath is visible), diameter (mm) (measured in the middle of stalk) and foliar area (cm2). Foliar area was estimated by Hermann and Cámara equation: AF=CxLx0,75x(N+2), where L is width of leaf +3, C is length of leaf +3, 0,75 is form factor and N represents the number of leaves with at least 20% of green area. The roots were scanned and evaluated by software WinRhizo (2004), and the parameters estimated: length (cm), projected area (cm2), diameter (mm) and volume (cm3).

The percentage (%) of relative content of water in roots, aerial part and organic reserve (1-bud sett) were realized, with follow equation: (FM-DM) x100xFM-1, where FM is the fresh mass and DM dry mass. After, the variables dry mass and fresh mass of aerial part and relative content of water were transformed to log10 (x). For normality was applied Shapiro-Wilk test to the variables analyzed. For parametric data was applied F-test and non-parametric data was applied Kruskal-Wallis test (H-test).

Results and Discussion

The respounds of the genotypes (G) according the variables analyzed were different. For F-test there was statistical difference to genotypes, however for treatments (T) there was difference only for the height, while the interaction G x T not showed difference for parameters estimated for roots, such as length, projected area, average diameter and volume (Figure 1, 2).

Figure 1. Height, diameter, foliar area, relative content of water (RCW) in organic reserve, RCW in root, RCW in aerial part analysis, in greenhouse condition, with clones 3,6,7,8 and 9, and RB867515 cultivar, inoculated and non-inoculated.

Figure 2. Roots scanned and analyzed with software WinRhizo, for treatments non-inoculated and inoculated, to the genotypes 3, 6, 7, 8, 9 and RB867515.


According data analyzed by H-test, the difference among genotypes was significant to all estimated parameters, in level of genotypes inside control treatment. For inoculated treatment, had no difference to relative content of water (RCW) in roots (Figure 1). The difference between each genotype confirms that sugarcane clones show single characteristics, confirmed in the study of Pereira et al. (2013).

The results in Figure 1 shows that treatment, according statistical analysis (F-test and H-test), had almost no influence in the development of sugarcane for studied conditions. Oliveira et al. (2002) evaluated 45 Days After Inoculation (DAI), as in this work, and the authors did not find difference between control and inoculated treatments with same five bacteria, to the dry mass of plants. The difference was observed after 200 DAI, being inoculated plants with better performance than control plants, probably due contribution and establishment of bacteria, suggesting that the reviews occurred also after that period.

Therefore the period evaluated could be an influence to the response to inoculation, on the other hand, even in greenhouse and autoclaved substrate, it is speculated in presence of other microorganism should happen competition with PGPB causing its less influence in this study. Other thesis concerns the nutrients in the Plantmax® that could affect the development and establishment of microorganisms. Otherwise, the nitrogen present in Plantmax®, may affect positively the PGPB-plants association, whereas in this case nitrogen associated to PGPB had tendency to enhance biometric variables (Gírio et al. (2015).

Civiero et al. (2014) observed in field, controlled condition in Rhizotron system for sugarcane, the inoculated treatment with mixed bacteria did not differ statistically from non-inoculated treatment, even plant cane or ratoon cane, mainly the variables for roots. The work was developed with soil from Paranavaí-PR, with different characteristics of substrate, which may contribute to competition in micro biota. According Marques Júnior et al. (2008) the better expression of H. seropedicae depends of thermal treatment application in sett, as applied in present study, preventing the competition with other microorganisms.

Gírio et al. (2015) found difference for inoculated treatment, in field experiment, to height, diameter of stalk, length of roots, dry and fresh mass of roots and aerial part. The inoculation with mixed bacteria according some studies could enable promoting of growth in initial phases, as occurred in the height of plants in present study, mainly due mechanisms like phytohormones production and BNF (Figure 1) (Oliveira et al., 2002; Pereira et al., 2013).

For height of plants, the inoculated treatment had not the better performance than non-inoculated only for the clone 9 and RB867515 (Figure 1). The clones 6, 7 and 8 showed positively tendency for inoculation. These three clones are from full-sib family, presented in the work of Lopes et al., (2012), which the family showed better performance when inoculated with A. brasilense, contributing to likely ability to the PGPB-clone interaction.

In PGPB's studies the height of plants have been suggested as one possible responsive variable to the inoculation. García et al., (2013) observed a gradual increase in the height of sugarcane plants of RB867515 inoculated with PGPB-mixed, as the results obtained by Gírio et al., (2015), going against the data results in present work, being explained

for the time of evaluation. In both studies, the evaluation occurred after 90 DAI. In field conditions in India with the CoSe92423 cultivar, the height of sugarcane plants was increased by G. diazotrophicus inoculation (Chauhan et al., 2013). Alexander (1973) explains the secondary effect of Gibberellin for the enhancing of height, bringing elongation of stalk, without affecting its mass.

The stalk diameter (SD) had no influence by treatments, although there was interaction G x T and influence when comparing different genotypes (Figure 1). SD is a variable with high heritability and used in large scale for sugarcane genotypes selection, estimating productivity in some cases. Therefore, less influence of inoculation on this characteristic (SD), should be explained due the SD is more restrictive to the genotype, being less involving by external or environmental influence. However, Chauhan et al. (2013) and Lopes et al. (2012) observed the PGPB-inoculated treatments increasing stalk diameter.

The tendency for positive response when PGPB are present, increasing Foliar Area (FA) is demonstrated in Figure 1. The RB867515 was the only genotype that have not followed this tendency. The final period of sugarcane represent the reduce of FA, when there is lesser vegetative stimulus and high incentive in sucrose accumulation in entire stalk, maturing sugarcane. The maturation of sugarcane and the consequent loss of senescence and leaf area are directly linked the possible drop in temperature and water restriction to the culture (Alexander, 1973; Pincelli and Silva, 2012).

Notwithstanding, every stress should reduce FA, which explains the reduced FA of RB867515. Once the PGPB signalizes as pathogen to plants until the balance establishment. After a period, the bacterial population tends to stabilize and inure with plant cooperation, turns the interaction (bacteria x genotype) before negative, to positive (Figure 1; Oliveira et al., 2002).

The Relative Content of Water (RCW) generally was superior in inoculated treatment in roots and aerial part. The RCW of sett organic reserve was worst in inoculated plants for clones 7, 8 and 9, representing further depletion of reserve, which moreover explains more RCW in those treatments in the roots and aerial part. On this account, the water is a vehicle to development of plants, mainly when there is elongation of cells by phytohormones action (Taiz and Zeiger, 2006). In this case, enhanced the characteristics of inoculated clones 7 and 8. The Clone 9 when inoculated invests its reserve to develop length of roots (Figures 1, 2). The utilization of organic reserve as soon as possible, promotes the investment of sugarcane plants in roots and leaves, anticipating events of biotic and abiotic stresses (Carneiro et al., 1995).

The Figure 2 shows the roots variables, and they have similar aspect when the treatments applied to the different genotypes. The clones 7, 8 and 9 presented better performance and clones 3 and 6 and RB867515 presented the worst performance. The three first clones bear more restrictive conditions, as biotic and abiotic stresses. The deeper roots development should be important for restriction hydric periods. In general, in optimal condition for cultivating, the roots of sugarcane develop until have more roots than necessary to plants, known as 'spare capacity', one way to prepare to stress conditions (Smith et al., 2005). According James (2004) the continuous production of new roots is essential to adjust sugarcane to environmental changes.

There was no difference for the treatments and genotypes for diameter of roots (DR), representing minor or no influence of inoculation on this characteristic. The DR is affected by age of plant, which aging of roots contributes to the increase of diameter, determinated by rusticity of some genotypes and its genetics (Vasconcelos, 2011).

Clones 6, 7 and 8 presented positively response when inoculated, focused in length and projected area of roots, of which have strict relation each other. There was volume increase when clone 8 was inoculated. This fact may be attributed by phytohormones action native of bacteria mix (Figure 2; Bastián et al., 2008; WinRhizo, 2004).

Those results increasing roots can be attributed to the secondary effect of the bacteria, producing exogenously phytohormones to the plant to be recovered for growth promotion. The phytohormones produced may be (e.g.) auxin and gibberellin (Bastián et al., 1998; Fuentes-Ramírez et al., 1993).

The G. diazotrophicus has great potential in sugarcane's roots promotion, mostly driven by its skill in produce auxin and BNF (Fuentes-Ramírez et al., 1993). Bastián et al. (1998), detected auxin and gibberellin present in medium content the bacteria H. seropedicae and G. diazotrophicus, confirming the potential to the growth promoting.

Auxin commonly known as growth hormone develops a key role to the roots' expansion, especially lateral roots, increasing projected area. The hormone impels H+-ATPase' synthesis, which acts in membrane level, initiating the relaxation of the cell wall and allowing elongation of the cells, thereafter the root, grows. To this process occurs

auxin has certain balance with other hormones, such as cytokinin and ethylene, regulating process as growth, vascular differentiation and gravitropism of the roots (Taiz and Zeiger, 2006).

Based on that balance, where inoculation had no result, it may suggest the hypothesis of hormonal imbalance, by the production of phytohormone from the bacteria involved in the process, inhibiting root development. Some studies demonstrate that great amount of auxin has effect inhibit on growth plant process, because the auxin can induce ethylene production (Taiz and Zeiger, 2006).

Otherwise RB867515 had no effect with inoculant (Figure 2), corroborating with Civiero et al. (2014). In field condition, with plant cane, Schultz et al. (2014), did not observe the influence of inoculation on this cultivar productivity. The difference appeared on second ratoon, indicating first the necessity to establishment of bacterial population.

Working with RB72454 female genitor of RB867515, Marques Júnior et al. (2008), observed positive response of cultivar in relation to root development when inoculated with H. seropedicae HRC 54, increasing length and projected area of roots compared to control treatment.

The positively response of some genotypes could be a relationship between strain of bacterium and sugarcane genotype or sugarcane families, such as Lopes et al. (2012), showed specificity with sugarcane family and Azospirillum spp. genus. This specificity was first related through B4362 cultivar and Herbaspirillum rubrisubalbicans, of which causes mottled stripe disease, nevertheless others cultivars have not shown that disease (Olivares et al., 1997; Oliveira et al., 2002; García et al., 2013; Pereira et al., 2013).


According results there were no similar response among the genotypes experienced with the five bacterial strains. The genotypes 7 and 8 showed tendency to positive response to inoculation, instead RB867515 cultivar presented negative response to PGPB. The morphologic characteristics of the roots were altered by inoculation, being a tendency to increase length, projected area and volume.

Therewith, there is a greater specificity between genotypes and PGPB, opening new possibilities to long term studies, with the purpose of identify the acting, as well as the populational fluctuation of those bacteria over the plantation period.

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Fecha de Recepción: 17 Marzo, 2017. Fecha de Aceptación: 27 Abril, 2017.

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