Boron-zinc interaction in the absorption of micronutrients by cotton Received for publication: 22 July, 2017. Accepted for publication: 16 February, 2017 Doi: 10.15446/agron.colomb.v36n1.66539 1 Doutorado em Agronomia (Produção Vegetal), Universidade Federal da Grande Dourados (Brasil) 2 Doutorando em Ciências. Centro de Energia Nuclear na Agricultura – CENA/USP, Programa de Pós-graduação em Ciências, Piracicaba, SP (Brasil). 3 Doutorado em Ciencia do Solo. Universidade Estadual do Mato Grosso do Sul (UEMS) Aquidauana - MS. * Corresponding author: ericabb25@hotmail.com Agronomía Colombiana 36(1), 51-57, 2018 Boron-zinc interaction in the absorption of micronutrients by cotton Interacción boro-zinc en la absorción de micronutrientes por el cultivo del algodón Érica de Oliveira Araújo1*, Elcio Ferreira Dos Santos2, and Marcos Antonio Camacho3 ABSTRACT RESUMEN B-Zn interaction modifies the nutritional dynamics of cop- per (Cu), iron (Fe) and manganese (Mn) in cotton. The main objective of this research was to evaluate the effect of B and Zn concentrations on the absorption of Cu, Fe and Mn in cotton plants grown in a nutrient solution. A completely randomized experimental design with three replicates was performed, in a 4×5 factorial scheme, corresponding to four concentrations of B (0, 20, 40 and 80 µM L-1) and five concentrations of Zn (0, 1, 2, 4 and 8 µM L-1). At 115 days after emergence, the plants were collected, divided into roots, shoots and fruits, and chemically analyzed. The results allowed to conclude that the Cu content and total Cu in the fruit, total Cu in the roots, Cu efficiency, Fe content in the roots, Fe absorption efficiency, Mn content in the fruit, and Mn absorption efficiency of cotton are inf luenced by the concentrations of B in the solution. The interaction between B and Zn affected the total Fe in the roots, Fe content and total Fe content in the fruit, Fe transport efficiency, total Mn in the shoots and Mn transport efficiency. In addition, Zn acts differently according to the supply of B and vice versa. La interacción boro-zinc (B-Zn) modifica la dinámica nutricio- nal del cobre (Cu), hierro (Fe) y manganeso (Mn) en el cultivo del algodón. El objetivo del presente trabajo fue evaluar el efecto de concentraciones de B y Zn sobre la absorción de Cu, Fe y Mn por plantas de algodón creciendo en solución nutritiva. Se utilizó un diseño completamente al azar con tres repeticiones en un esquema factorial 4×5, siendo cuatro las concentraciones de B (0, 20, 40 y 80 µM L-1) y cinco las concentraciones de Zn (0, 1, 2, 4 y 8 µM L-1). A los 115 días después de emergencia las plantas fueron recolectadas, divididas en raíz, parte aérea y frutos, y sometidas a análisis químicos. Los resultados per- mitieron concluir que el contenido y el total de Cu en el fruto, el contenido de Cu en la raíz, la eficiencia de utilización de Cu, el total de Fe en la raíz, la eficiencia de absorción de Fe, el total de Mn en el fruto y la eficiencia de absorción de Mn son inf luenciadas por las concentraciones de B en la solución. La interacción B-Zn afectó el contenido de Fe en la raíz, el conte- nido y el total de Fe en el fruto, eficiencia de transporte de Fe, el total de Mn en la parte aérea y la eficiencia del transporte de Mn, Adicionalmente Zn actúa de manera diferente de acuerdo al suministro de B y viceversa. Key words: Gossypium hirsutum L., copper, iron, manganese, nutritional efficiency. Palabras clave: Gossypium hirsutum L., cobre, hierro, man- ganeso, eficiencia nutricional. al., 2012; Araújo et al., 2013). B is directly related to the me- tabolism of the ribonucleic acid (RNA), different functions of the plasmatic membrane and constitutes the structure of the cell wall and pectic substances associated with it, especially the middle lamella (Wimmer and Eichert, 2013). Zn is required in many active sites of different proteins, such as carbonic anhydrase and superoxide dismutase. The deficiency of this nutrient reduces the photosynthetic rate through the modification of the activity of enzymes involved in the process of carbon fixation (Broadley et al., 2007; Assunção et al., 2013). B-Zn interaction inf luences different metabolic processes of the plant, interfering with the mineral composition through the stimulation or inhibition of the absorption Introduction Cotton farming is one of the main activities of the Brazilian agribusiness. The increasing use of more productive variet- ies worldwide, with a higher nutrient demand, requires a better knowledge on the nutritional relationships in cotton (Rochester and Constable, 2015). In this context, a better knowledge of the nutritional dynamics is important for the establishment of an efficient fertilization program. Gossypium hirsutum L. – species of greatest use for cotton production in Brazil – is responsive to the application of micronutrients, especially in low natural fertility areas. Among the micronutrients, boron (B) and zinc (Zn) are the most limiting elements to achieve better yields (Araújo et http://dx.doi.org/10.15446/agron.colomb.v36n1.66539 52 Agron. Colomb. 36(1) 2018 of other nutrients (Baxter, 2009). These relationships are highly variable and may occur inside the cells or in the rhizosphere (Morgan and Connolly, 2013). The B-Zn interactions in cotton are correlated (Araújo et al., 2012) and the reduction in B absorption as a function of Zn is common. Besides cotton (Araújo et al., 2012), this result has already been observed for lemon (Rajaie et al., 2009), olive tree (Jasrotia et al., 2014) and wheat (Nasim et al., 2015). Thus, the effect of the B-Zn interaction on the absorption of these nutrients is evident. However, there is still limited information on the effect of B-Zn interaction in the absorption dynamics of other micronutrients, such as Cu, Fe and Mn. Many nutritional relationships have been observed between micronutrients (Baxter, 2009; Milner et al., 2013; Aibara and Miwa, 2014). These nutritional interactions have been cataloged as complex, with initial modification at a mo- lecular level, resulting in a variation of the absorption and mineral composition of the plants. Thus, the observed nutritional interaction depends on the availability of nutrients and on the analyzed plant species (Araújo et al., 2012; Araújo et al., 2013). Therefore, the need for studies that address the classic nutritional interaction between B and Zn, evaluating the absorption of Cu, Fe and Mn is evi- dent. Understanding the micronutrient interaction would enhance the use of fertilizers, reducing production costs. The hypothesis of this study is that the combinations of B and Zn in nutrient solution modify the total content and the efficiency of absorption, use and transport of Cu, Fe and Mn in cotton. Given the above, the main objective of this research was to evaluate the effect of B and Zn con- centrations on the absorption of Cu, Fe and Mn in cotton cultivated in nutrient solution. Materials and methods The experiment was conducted in an agricultural green- house of the Plant Production Sector of the State University of Mato Grosso do Sul (UEMS), in Aquidauana-MS, at the geographic coordinates 20º28’ S and 55º48’ W with an altitude of 174 m a.s.l. The experimental design was com- pletely randomized with three replicates, in a 4×5 factorial scheme, corresponding to four concentrations of B (0, 20, 40 and 80 µM L-1), applied in the form of boric acid, and five concentrations of Zn (0, 1, 2, 4 and 8 µM L-1), applied in the form of zinc sulfate. The experimental units consisted of plastic pots with 3 L capacity, filled with washed and sterilized quartz sand. Cotton seeds, cv. FiberMax 910, were placed to germinate on trays with moistened sand. Five days after emergence, when cotyledon leaves developed, three seedlings were transplanted to each experimental unit, where they received a complete and diluted (1/5) nutrient solution (Epstein and Bloom, 2006). At 28 days after emergence, thinning was performed leaving only one plant in each experimental unit. The nutrient solution application started according to each treatment, irrigating three times a day with deionized water. In the treatment solutions lacking a specific nutrient, the concentrations were identical to those of the complete solution, except for the absent nutrient. The nutrient solution showed the following composi- tion: 6.0 mL of 1 mol L-1 KNO3; 4.0 mL of 1 mol L-1 Ca(NO3)4·H2O; 2.0 mL of 1 mol L-1 NH4H2PO4; 1.0 mL of 1 mol L-1 MgSO4·7H2O; 1.0 mL of 0.2 mol L-1 Fe-EDTA; 1.0 mL of 0.05 mol L-1 KCl; 1.0 mL of 0.02 mol L-1 H3BO3; 1.0 mL of 0.002 mol L-1 MnSO4·H2O; 1.0 mL of 0.002 mol L-1 ZnSO4·7H2O; 1.0 mL of 0.0005 mol L-1 CuSO4·5H2O; 1.0 mL of 0.0005 mol L-1 H2MoO4 (85% MoO3). At 115 days after emergence, the plants were collected and divided into roots, shoots (stem and leaves) and fruits (boll). All the collected plant material was rinsed in a detergent solution at 3 mL L-1, running water, 0.1 mol L-1 HCl solution and deionized water, respectively. The samples were placed in paper bags and then dried in a forced-air oven at 65ºC for 72 h. After drying, the plant material was ground in a Wiley-type mill (Thomas Scientific, USA). The samples were subjected to nitric-perchloric digestion for the deter- mination of Cu, Fe and Mn contents in the different plant parts (Malavolta et al., 1997). The determination of Cu, Fe and Mn was used to calculate the absorption efficiency (mg g-1) = [total content of nutri- ent in the plant (mg)/root dry matter (g)] (Swiader et al., 1994); transport efficiency (%) = [(content of nutrient in the shoots (mg)/total content of nutrient in the plant (mg)) x 100] (Li et al., 1991); and use efficiency (g2 mg) = [(total dry matter produced (g))2/total content of nutrients in the plant (mg)] (Siddiqi and Glass, 1981). The results were statistically assessed with an analysis of response surface, using the statistical package SAS and adopting a 0.05 significance level. Initially, an analysis of variance was performed and, according to the significance of the F test, the study of polynomial regression was con- ducted (for cases with significant interaction), through the RSREG procedure. 53De Oliveira Araújo, Ferreira Dos Santos, and Camacho: Boron-zinc interaction in the absorption of micronutrients by cotton Results and discussion The interaction between the B and Zn treatments inf lu- enced the Fe content in the boll, total Fe in the roots and in the boll, total Mn in the shoots and transport efficiency of Fe and Mn (Tab. 1). There was a significant response (P<0.05) of B concentrations for Cu content in the boll, total Cu in the roots and in the boll, Fe content and total Fe in the roots, Mn content in the boll, Cu use efficiency and the efficiencies of absorption of Fe and Mn (Tab. 1). Zn doses in the solution did not affect individually any of the studied variables. Various studies indicate antagonistic relationship between Zn and cationic micronutrients, such as Cu, Fe and Mn. This interaction occurs due to the com- petition of the cations for the absorption sites (Broadley et al., 2007; Baxter, 2009; Assunção et al., 2013). This study did not find any antagonistic relationship between Zn and other cationic micronutrients (Fe, Mn and Cu), disagree- ing with the results reported by Rajaie et al. (2009), Aref (2011) and Lima Neto and Natale (2014) in other plant species. Hence, only B doses and the combined doses of B and Zn inf luenced the absorption of Cu, Fe and Mn in cotton (Tab. 1). Cu content and total Cu in the cotton fruit were in- f luenced by the B concentrations in the solution. The increase in B concentrations in the solution until 40 µM L-1 promoted a reduction in the Cu content and total Cu in cotton bolls (Figs. 1A, 1B). B doses higher than 40 µM L-1 increased Cu content and total Cu in the bolls. Aref (2011) observed an increment in the concentration of Cu in maize leaves with the increase in B concentrations in the planting substrate. Ahmed et al. (2011) observed a positive effect of B doses on Cu content and total Cu in different parts of cotton plants. However, the total Cu in cotton roots linearly decreases with the increment in B concentrations in the solution (Fig. 1C), agreeing with the results found by Esringü et al. (2002) who observed a rgjeduction of Cu concentration in strawberry roots with the increase in the supply of B reporting an antagonistic relationship between the nutrients. Cu use efficiency for the production of dry matter was positively inf luenced by the supply of B in the solution, so that the increase in B concentrations promoted linear increment in the Cu use efficiency of cotton plants (Fig. 1D). B is related to various biochemical processes in the plants; thus, its concentrations in the cultivation substrate may directly or indirectly affect the use of Cu by the plant (Malavolta, 2006; Wimmer and Eichert, 2013). TABlE 1. Summary of the analysis of variance: coefficient of variation and P-value for the effect of B, Zn and the B-Zn interaction for content, total and efficiency of absorption, transport and use of Cu, Fe and Mn. Parameters CV (%) P-values B Zn B x Zn Copper (Cu) Cu content in the shoots (g kg-1) 67.29 0.846 0.065 0.532 Cu content in the roots (g kg-1) 37.53 0.110 0.216 0.184 Cu content in the boll (g kg-1) 26.09 0.000* 0.468 0.119 Total Cu in the shoots (mg) 66.09 0.805 0.065 0.488 Total Cu in the roots (mg) 44.49 0.028* 0.476 0.053 Total Cu in the boll (mg) 32.30 0.000* 0.555 0.129 Absorption efficiency of Cu (mg g-1) 33.21 0.197 0.105 0.387 Transport efficiency of Cu (%) 42.92 0.560 0.159 0.173 Use efficiency of Cu (mg g-1) 32.17 0.013* 0.339 0.205 Iron (Fe) Fe content in the shoots (g kg-1) 28.92 0.209 0.364 0.173 Fe content in the roots (g kg-1) 32.57 0.003* 0.878 0.121 Fe content in the boll (g kg-1) 32.66 0.000* 0.078 0.000* Total Fe in the shoots (mg) 31.16 0.220 0.531 0.207 Total Fe in the roots (mg) 32.06 0.000* 0.646 0.005* Total Fe in the boll (mg) 41.74 0.000* 0.346 0.000* Absorption efficiency of Fe (mg g-1) 27.72 0.005* 0.800 0.253 Transport efficiency of Fe (%) 37.44 0.000* 0.830 0.009* Use efficiency of Fe (mg g-1) 31.32 0.054 0.578 0.186 Manganese (Mn) Mn content in the shoots (g kg-1) 14.73 0.060 0.103 0.053 Mn content in the roots (g kg-1) 28.83 0.057 0.491 0.469 Mn content in the boll (g kg-1) 19.53 0.000* 0.653 0.218 Total Mn in the shoots (mg) 18.69 0.000* 0.264 0.003* Total Mn in the roots (mg) 36.62 0.059 0.867 0.055 Total Mn in the boll (mg) 24.89 0.063 0.089 0.456 Absorption efficiency of Mn (mg g-1) 17.72 0.000* 0.131 0.592 Transport efficiency of Mn (%) 21.8 0.104 0.777 0.035* Use efficiency of Mn (mg g-1) 19.6 0.051 0.116 0.506 B: Boron; Zn: Zinc; CV: Coefficient of variation. *Significant by F test at P≤0.05. B concentrations in the solution promoted a significant increment in Fe content and total Fe in cotton roots (Figs. 2A, 2B). Similar results were obtained by Esringü et al. (2012) in strawberry, in which the Fe content in the roots increased with the concentration of 10 µM L-1 of B, decreas- ing at the concentration of 20 µM L-1 of B. These results suggest that B has certain affinity for Fe and that there may be a synergetic relationship between the nutrients. Rajaie et al. (2009) also observed significant increase in the concentration of Fe with the increment in B levels in Citrus aurantifolia. 54 Agron. Colomb. 36(1) 2018 Fe content and total Fe in the cotton fruit were signifi- cantly affected by the interaction between B and Zn in the solution. The increase in B concentrations in the solution promoted the reduction in Fe contents and total Fe in the fruit with the increment in Zn concentrations (Figs. 2C, 2D). Ahmed et al. (2011) reported that the Fe content, in different parts of the cotton crop, significantly increased with the increment in the applied levels of B. The increase in Fe concentration in the fruit with the increasing levels of B has also been reported in guava (Salvador et al., 2003) and in Citrus aurantifolia (Rajaie et al., 2009), disagreeing with the results obtained in the present study. There is a lack of available information about the inf luence of B on the absorption of other micronutrients, and the results vary according to the analyzed plant species. Fe absorption efficiency positively responded to the B supply in the solution, so that the increase in B concentra- tions promoted increment in the Fe absorption efficiency of cotton (Fig. 3E). Fe transport efficiency was affected by the interaction between B and Zn in the solution, demonstrating an antagonistic relationship between B and Zn at the highest concentrations of B, and a synergetic relationship at the highest concentrations of Zn (Fig. 3F). It is possible to observe an increment of 25% in the transport of Fe by the roots with the increase in Zn concentrations at 0 µM L-1 of B. The Mn content in the fruit decreased with the increment in B concentrations, until 40 µM L-1 of B, with an increase at the highest concentrations of the nutrient (80 µM L-1), the same behavior observed for Cu content and total Cu in the cotton fruit (Fig. 3A). Aref (2011), working with maize plants, observed that the Mn content was affected by B fertilization, with a reduction in leaf Mn content under these conditions. On the other hand, Esringü et al. (2012) observed an increment in leaf Mn content with the increase in B concentrations, until 10 µM L-1, with reduction at the highest B concentration (30 µM L-1). In contrast, the data of the present study indicate that Mn positively responded to B only at the highest concentra- tion of the nutrient. FIgURE 1. Content of Cu in the boll (A), total Cu in the boll (B), content of Cu in the roots (C) and Cu absorption efficiency (D) of cotton in response to different B concentrations in the nutrient solution. y=0.0012x2 - 0.0975x + 6.0805 R2 = 0.96 y=0.0135x2 - 0.0944x + 60.768 R2 = 0.99 y=-3.4018x + 685.25 R2 = 0.95 y=0.0074x + 1.106 R2 = 0.99 B (µM L-1) DC B (µM L-1) To ta l C u in th e bo ll (m g) B (µM L-1) To ta l C u in th e ro ot s (m g) 400 650 700 600 550 500 450 0 20 40 60 80 B (µM L-1) C u co nt en t i n th e bo ll (m g g- 1 ) BA 3.0 6.0 5.5 5.0 4.5 4.0 3.5 6.5 7.0 0 20 40 60 80 0 20 40 60 80 0 20 40 60 80 35 30 65 60 55 50 45 40 70 75 To ta l C u in th e ro ot s (m g) 1.0 1.7 1.8 1.6 1.5 1.4 1.3 1.2 1.1 55De Oliveira Araújo, Ferreira Dos Santos, and Camacho: Boron-zinc interaction in the absorption of micronutrients by cotton y=0.0494x2 - 5.1388x + 327.04 R2 = 0.47 Ŷ=3452.3927 + 66.0153B + 304.7927Zn - 4.5169B*Zn R2: 0.07 P<.0001 Ŷ=422.922 - 3.1126B - 0.2623Zn + 0.00063B*Zn R2: 0.82 P<.0001 Ŷ=3802.2387 - 30.3201B + 2.7300Zn + 0.001135B*Zn R2: 0.73 P<.0001 y=1.3307x + 432.01 R2 = 0.35 Ŷ=26.0591 - 0.08348B - 0.0468Zn + 0.00015B*Zn R2: 0.25 P<.0001 B (µM L -1) DC B (µM L -1) To ta l F e in th e ro ot s (m g) B (µM L -1) C on te nt F e in th e bo ll (m g g- 1 ) 100 350 400 450 300 250 200 150 0 20 40 60 80 B (µM L-1) Fe c on te nt in th e ro ot s (m g g- 1 ) BA 0 20 40 60 80 0 20 40 60 80 7000 6000 5000 4000 3000 8000 9000 To ta l F e in th e bo ll (m g) 400 600 550 500 450 350 300 250 200 B (µM L -1) FE B (µM L-1) A bs or pt io n ef fic ie nc y of F e (m g g- 1 ) 0 20 40 60 80 Tr an sp or t e ff ic ie nc y of F e (% ) 400 600 550 500 450 350 300 Zn (µ M L -1 ) 6 2 0 Zn (µ M L -1 ) 0 4 Zn (µ M L -1 ) 0 40 20 40 60 80 500 3000 3500 4000 2500 2000 1500 1000 0 2 6 0 20 40 60 80 15 25 27 29 23 21 19 17 Zn (µ M L -1 ) FIgURE 2. Content of Fe in the roots (A), total Fe in the roots (B), content of Fe in the boll (C), total Fe in the boll (D) and efficiency of absorption (E) and transport (F) of Fe of cotton in response to different B and Zn concentrations in the nutrient solution. The total Mn in the shoots and Mn transport efficiency were negatively inf luenced by the increase in B concentra- tion at 0 µM L-1 of Zn and positively inf luenced at 8 µM L-1 of Zn (Figs. 3B, 3D). It is possible to observe an increment of 49% in the transport of Mn by the roots with the increase in Zn concentrations at 0 µM L-1 of B. This reduction in Mn content and total Mn in cotton roots and shoots in response to the increase in B concentrations may be due to the ef- fect of dilution or the antagonistic relationship between B and Mn. The source of B can inf luence, as a regulator or inhibitor, the accumulation and use of other nutrients (Aref, 2011). Mn absorption efficiency linearly increased with 56 Agron. Colomb. 36(1) 2018 the increment in B concentrations (Fig. 3C). B is involved in physiological processes that control the absorption and transport of Cu, Fe, Mn and Zn (Malavolta, 2006; Wim- mer and Eichert, 2013). Dursun et al. (2010) also observed increase in Cu, Fe and Mn contents in leaves of tomato and pepper as a function of B doses. Conclusions Cu content and total Cu in the fruit, total Cu in the roots, Cu use efficiency, Fe content in the roots, Fe absorption efficiency, Mn content in the fruit and Mn absorption ef- ficiency of cotton are inf luenced by the concentrations of B in the solution. The B-Zn interaction affected total Fe in the roots, Fe con- tent and total Fe in the fruit, Fe transport efficiency, total Mn in the shoots and Mn transport efficiency; in addition, Zn acts differently according to the B supply and vice versa. literature cited Ahmed, N., M. Abid, F. Ahmad, M.A. Ullah, Q. Javaid, and M.A. Ali. 2011. 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Content of Mn in the boll (A), total Mn in the shoots (B) and efficiency of absorption (C) and transport (D) of Mn of cotton in response to different B and Zn concentrations in the nutrient solution. y=0.0069x2 + 0.2395x + 33.58 R2 = 0.66 y=0.0062x2 - 0.4753x + 40.256 R2 = 0.98 Ŷ=3452.3927 + 66.0153B + 304.7927Zn - 4.5169B*Zn R2: 0.07 P<.0001 Ŷ=3802.2387 - 30.3201B + 2.7300Zn + 0.001135B*Zn R2: 0.73 P<.0001 B (µM L -1) DC B (µM L -1) To ta l M n in th e sh oo ts ( m g) 0 20 40 60 80 B (µM L-1) A bs or pt io n ef fic ie nc y of M n (m g g- 1 ) 370 450 430 410 390 350 330 310 290 270 250 0 20 40 60 80 B (µM L-1) M n co nt en t i n th e bo ll (m g g- 1 ) BA 0 20 40 60 80 1500 1000 500 0 2000 2500 Tr an sp or t e ff ic ie nc y of M n (% ) 30 50 45 40 35 25 Zn (µ M L -1 )4 0 Zn (µ M L -1 ) 0 40 20 40 60 80 10 35 45 40 50 30 25 20 15 http://dx.doi.org/10.1093/pcp/pcu156 http://dx.doi.org/10.1093/pcp/pcu156 57De Oliveira Araújo, Ferreira Dos Santos, and Camacho: Boron-zinc interaction in the absorption of micronutrients by cotton sense zinc deficiency. 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