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Published online: 27 Jan 2012.
To cite this article: Henrique Coutinho Junqueira Franco , Jos Lavres Junior , Adilson de
Oliveira Junior , Gean Carlos Silva Matias , Cleusa Pereira Cabral & Eurpedes Malavolta (2012)
OPTIMUM RATIO OF CALCIUM AND BORON IN THE NUTRIENT SOLUTION OR IN CASTOR BEAN
SHOOT FOR FRUIT YIELD AND SEED OIL CONTENT, Journal of Plant Nutrition, 35:3, 413-427, DOI:
10.1080/01904167.2012.639921
To link to this article: http://dx.doi.org/10.1080/01904167.2012.639921
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Calcium (Ca) and boron (B) have been reported as the major macro- and micronutrient required
for castor bean plant yield. The objective of this study was to determine the Ca:B ratios (in the
growth media and plant tissue) for fruit yield and shoot dry weight of the castor bean (Ricinus
communis L.), grown in a nutrient solution, and to evaluate Ca and B supply on concentration
and total uptake of Ca, potassium (K), magnesium (Mg), and B, as well on the seed oil content.
The treatments were arranged in a 3 3 factorial fashion, consisting of three rates of Ca (40, 80,
and 160 mg L 1) and three of B (0.32, 0.96, and 1.60 mg L 1). Calcium and B rates increased
the shoot and root dry weight and fruit yield at a Ca:B ratio in the nutrient solution of 166 and
100, respectively. Symptoms of B deficiency were observed in plants supplied with 0.32 mg B L 1,
regardless of the Ca concentration in the nutrient solution. Plants which showed visual symptoms
of Ca deficiency cultivated with 40 mg Ca L 1 presented concentration of Ca in plant tissue up
to 10 g kg 1. The concentration and total Ca and B uptake increased with the rates of them.
Notwithstanding, the shoot Ca accumulation was improved by B rates. In addition, there were
no decreases in K and Mg uptake due to Ca rates. Furthermore, addition of 80 mg L 1 of Ca and
1.60 mg L 1 of B in the growth media increased the seed oil content. The Ca:B ratio in the diagnostic
leaf associated with the highest plant dry weight (shoot and root) and fruit yield, was 500 (16 to
20 g kg 1 of Ca, and for 30 to 40 mg kg 1 of B).
Keywords:
Deceased.
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H. C. J. Franco et al.
INTRODUCTION
Castor bean plant (Ricinus communis L.) is one of the 7,000 species of the
Euforbiacea family, possibly originating from ancient Abyssinia, currently
Ethiopia. The castor bean seed contains 90% ricinoleic acid, which represents a practically pure source of fatty acid, being the only oil soluble in
alcohol (Beltrao et al., 2001). Such a characteristic confers broad industrial
application to castor bean oil, including that of an alternative fuel source,
providing important economic and strategic potential to the castor bean
crop (Savy Filho, 2005) mainly due to the growing interest of the Brazilian government in biodiesel production. On the other hand, although the
castor bean plant is a crop with high economic potential for Brazil, there
are few studies and little information regarding the nutrient requirements
of this plant, making the development of new research warranted. In turn,
previous studies from Lavres Jr. et al. (2005) and Lange et al. (2005) have reported calcium (Ca) and boron (B) as the major macro- and micronutrient
required for castor bean plant yield.
In the area of mineral plant nutrition, similarities between the nutrients
Ca and B on the forms and functions they exercise on plants stand out (Mills
and Jones, 1997). Nevertheless, Ca is absorbed in the ionic form and B as
undissociated boric acid. Ca uptake is active, as related to the MichaelisMentens kinetics, whereas that of B is a result of active and passive processes
(Kochian, 1991). Nevertheless, nowadays, a number of B transporters have
been cloned and functionally identified, some of them being necessary for
efficient B uptake and allocation under B-limiting conditions. Indeed, the
mRNA levels of some of these B-transporter genes are regulated by B avail
ability (Camacho-Cristobal
et al., 2011). Long distance transport of these two
nutrients in the transpiratory stream of the plants occurs in the same vessel
system, being principally one-directional. Once inside the plant, Ca and B
dont move from older to younger tissue, with the exception of B in species
which produce cis-diols, such as B-polyol complexes, and present redistribution (Konsaeng et al., 2010), or even in certain conditions of transpiratory
flow governed by relative air humidity conditions, as observed recently in
the castor bean plant Impala (Eichert and Goldbach, 2010). These two
nutrients have the youngest organs as a common denominator in which
symptoms of deficiency show.
The Ca and B nutrients contribute to the maintenance of structure and to
membrane function and both are involved in the adenosine triphosphatases
(ATP-ase) activity (Schaller and Sussman, 1988; Cakmak and Romheld,
1997). While Ca, in the form of pectate, contributes to cell wall rigidity, controlled by indole acetic acid (Marschner, 1995), B is involved in
the biosynthesis of pectic acid (Kobayashi et al., 1996; Power and Woods,
1997). When there is B deficiency, the activity of polyphenol oxidase increases, which oxidizes the indole acetic acid, which in turn impeded from
collaborating with Ca in diminishing the rigidity of the cell wall (Ali and
415
Jarvis, 1988; Blevins and Lukaszewski, 1998). In addition, Ca and B influence the germination of the pollen grain and the pollen tube growth
(Gupta, 2001), with these nutrients also performing similar functions in carbohydrate transport from leaves to roots, which is reflected in nodulation of
leguminosae (Clark, 1984).
Considering Ca and B participation in the same functions or processes,
Mills and Jones (1997) and Kanwal et al. (2008) pointed out that both nutrients must be balanced for adequate plant growth. Practical results illustrate
the relationship between these two elements, e.g., leaf application of B reduces the incidence of bitter pit in apples, which is a disorder related to Ca
deficiency. Boron helps in metabolism or incorporation of Ca in the cell wall
(Yamauchi et al., 1986); in other words, B is active in the biosynthesis of the
cell wall, assisting Ca in the deposition and formation of pectates involved
in the construction of these structures. Another factor to be considered is
that visual symptoms of B deficiency are accentuated by Ca deficiency and
less evident when Ca is found in excess (Chatterjee et al., 1987).
In this context, the present study takes as a hypothesis the existence of
Ca:B ratio or a range of this ratio in the growth medium and in the plant
tissue which would be most reasonable for the plant yield. The objective was
to determine the Ca:B ratio in the growth media and in the plant tissue for
fruit yield and shoot dry weight of the castor bean (Ricinus communis L.)
grown in a nutrient solution; as well evaluate the relationship between the
Ca and B supply on concentration and total uptake of Ca, potassium (K),
magnesium (Mg), and B, as well on the seed oil content.
416
H. C. J. Franco et al.
4H2 O] and ammonium nitrate (NH4 NO3 ) was used to maintain the nitrogen rate. Boron was supplied as boric acid (H3 BO3 ). One month after the
beginning of the experiment, at the second renewal of the nutrient solution,
the lowest rate of B (0.32 mg L1) was no longer supplied, conditions of B
deficiency and withdrawal of external B supply.
During the development of the experiment, the nutrient solutions added
to all the containers contained: 9 mL potassium nitrate (KNO3 ) 1 mol L1;
3 mL ammonium phosphate (NH4 H2 PO4 ) 1 mol L1; 1.5 mL magnesium
sulfate (MgSO4 7H2 O) 1 mol L1; 1.5 mL of the iron (Fe) ethylenediaminetetraacetic acid (EDTA) solution with 6.922 g L1; 5 mL micronutrient stock
solution containing 3.728 g L1 of potassium chloride (KCl), 0.338 g L1
of manganese sulfate (MnSO4 H2 O); 0.575 g L1 of zinc sulfate (ZnSO4
7H2 O); 0.125 g L1 of copper sulfate (CuSO4 5H2 O); 0.081 g L1 of molybdic acid (H2 MoO4 ). This nutrient solution was maintained under constant
aeration in the containers and was renewed every 15 days, completing the
volume with deionized water when necessary. The pH of the solution was
maintained near 5.5.
During plant growth, samples of plant matter were collected for leaf
diagnosis, with the organ used being the fourth leaf below the inflorescence,
collected when the female reproductive organ became visible. In these leaves,
the concentrations of Ca, B, Mg and K were determined in accordance with
the methodology described by Malavolta et al. (1997).
Castor bean plants were harvested as the fruit matured (around 90 days
after the beginning of the application of Ca and B), gathering the above
ground part and the roots. Then the samples were dried in forced air circulation oven at 65 C for 72 hours. Afterwards, this material was weighed
to obtain the total dry matter yield (roots and above ground part) and the
fruit yield. After processing of the samples, the concentrations of Ca, B, K,
and Mg were determined (Malavolta et al., 1997). The ether extract (total
lipids) was obtained by means of extraction of approximately 1g of the sample for approximately four hours, with ethyl ether, in accordance with the
methodology proposed by the AOAC (1995).
The results were submitted to statistical analyses using the SAS System for
Windows 6.11 (SAS Institute, Cary, NC, USA) statistical program. Analysis of
variance was undertaken and, in terms of the level of significance on the F
test, the study of polynomial regression (response surface) was carried out,
by intermediation of the RSREG procedure.
417
FIGURE 1 Total dry matter weight (shoot plus roots) of the castor bean Iris, related to Ca and B rates
in the nutrient solution.
FIGURE 2 Fruit yield of the castor bean Iris, related to Ca and B rates in the nutrient solution.
418
H. C. J. Franco et al.
hamper the castor bean fruit yield, which were observed in the present study
as well. This impaired yield was notably observed under high nutritional
imbalance caused by the imbalance between the Ca and B supply in the
nutrient solution (e.g., higher rates of Ca related with a smaller B rate, and
vice versa) (Figure 2). On the other hand, greatest fruit yield was reached
when plants received the highest Ca and B rates (of 160 mg L1 and 1.6 mg
L1, respectively, at a relationship of 100:1).
Furthermore, in regard to fruit yield, it is fitting to highlight that the
castor bean plants grown under limiting conditions in B (0.32 mg L1), even
though the Ca rates in the nutrient solution did not produce fruit, only
an inflorescence that was not very developed. These results mirror those
of stated by Asad et al. (2002) who observed in an experiment carried out
with canola (Brassica napus L.) and sunflower plants (Helianthus annus L.)
grown in a nutrient solution, the importance of B in the reproductive stage
and, consequently, in fruit yield. Moreover, these authors verified that the
greater demand for B occurred at the end of the vegetative stage and at
the beginning of the reproductive one, since under the conditions of a
lower B supply in the nutrient solution (less than 0.121 mg L1). In other
words, symptoms of B deficiency in the shoot first became evident at 45 days
after transplanting, with young leaf blades ceasing to expand and becoming
curled upwards at the edges. Lange et al. (2005) observed visual B deficiency
in castor bean Iris at 63 days after seedling transplant in those treatments
with omission of B in the nutrient solution. According to Gupta (2001),
even in moderate B deficiency conditions, plants may grow normally, which
in part is explained by the contribution of B seed reserves, though the fruit
yield may be drastically affected, due to the high nutritional requirement
in this period, such as the effect of the strong sink. The development of
the pollen tube is more affected by the nutritional shortage of B than the
germination of the pollen grain. Furthermore, B deficiency impairs the fruit
setting and seed formation (Marschner, 1995).
Considering the rates of Ca and B in the nutrient solution that promoted
the maximum total dry matter yields (160 mg L1 of Ca and 0.96 mg L1 of
B) and of fruit (160 mg L1 of Ca and 1.60 mg L1 of B), the Ca:B ratio or
quotient of the nutrient solution of 166 for total dry matter production and
100 for fruit yield was calculated. In this way, for the normal development
and high yield of the castor bean plant to occur, it may be expected that
the relationship between the adequate supply of the rates of Ca and B on
the growth medium should be between 100 and 170, being maintained
throughout the growth cycle and mainly in the fruit set. It is also interesting
to compare these values with those of the soil solution. Asher and Edwards
(1978) reported that the Ca concentration (mg L1) of the soil solution
may be classified as: very low, from 0.012 to 0.24; critical, from 0.24 to 40
and average, at 76. It may thus be noted that the rate of 160 mg L1 of Ca
is much higher than those concentrations suggested by these authors. In
419
FIGURE 3 Visual symptoms of calcium (A and B) and boron deficiency (C and D) in the castor bean
Iris grown in nutrient solutions with the rates of Ca and B of 40 and 0.32 mg L1, respectively (Color
figure available online).
420
H. C. J. Franco et al.
TABLE 1 Calcium concentration and total Ca uptake by castor bean Iris, related to Ca and B rates in
the nutrient solution
Rate
Ca1
Ca2
Ca4
Average
Ca1
Ca2
Ca4
Average
B1
7.7Ab
11.8Aa
13.4Aa
11.0
B3
B5
Ca concentration (g kg1)
6.8Ab
5.4Ac
8.9Ab
11.4Ab
16.4Aa
16.4Aa
10.7
11.1
FCa = 60.8
FB = 0.10NS
FCa B = 3.5
244Ab
476Ab
783Ba
501b
FCa = 121,8
Average
6.6c
10.7b
15.4a
SMD = 2.0 CV = 18%
268c
541b
1131a
SMD = 140 CV = 21%
Rates: Ca1 = 40 mg L1; Ca2 = 80 mg L1; Ca3 = 160 mg L1; B1 = 0.32 mg L1; B2 = 0.96 mg L1
and B3 = 1.96 mg L1; means followed by different letters, lowercase letters in the column and capital
letters in the row, differ among themselves by the Tukey test at 5% probability; and significant at
1 and 5% probability respectively; NS: not significant; DMS = minimum significant difference; C.V. =
coefficient of variation.
Ca1
Ca2
Ca4
Average
Ca1
Ca2
Ca4
Average
B1
B3
B5
15.3Ba
16.3Ba
14.2Ba
15.3b
FCa = 20.1
0.490
0.660
0.853
0.667b
FCa = 5.7
L1;
L1;
L1;
Average
22.6a
20.8a
17.2b
SMD = 2.1 CV = 11%
0.964b
1.100ab
1.270a
SMD = 0.225 CV = 20%
Rates: Ca1 = 40 mg
Ca2 = 80 mg
Ca3 = 160 mg
B1 = 0.32 mg L1; B2 = 0.96 mg L1
and B3 = 1.96 mg L1; means followed by different letters, lowercase letters in the column and capital
letters in the row, differ among themselves by the Tukey test at 5% probability; and significant at
1 and 5% probability respectively; NS: not significant; DMS = minimum significant difference; C.V. =
coefficient of variation.
421
B in some parts of the plant, which are near to those obtained in this study.
On the other hand, Lavres Jr. et al. (2005) determined the critical level of Ca
in the order of 13 g kg1 of upper leaf blade dry mass for a 10% reduction
of maximum dry matter yield of the castor bean plants.
The total Ca uptake (Ca content) by castor bean Iris were significantly
attained with the increase of the Ca and B rates in the nutrient solution
(Table 1). However, Ca concentrations in the castor bean plant were changed
a bit by the rates of B. Nevertheless, a synergetic effect was observed between
the rates of B and the total Ca uptake (Table 1). An enhanced Ca accumulation in plants by increased B supply has been reported in the literature (Kanwal et al., 2008). According to Malavolta et al. (1997), B deficiency reduces
the activity of adenosine triphosphatases (ATP-ases) and, consequently, the
availability of energy necessary for active ionic absorption (Matas et al., 2009),
which in turn may reduce Ca absorption. Salvador et al. (1999), evaluating
the mineral composition of guava tree leaves (Psidium guajava) in an experiment carried out with a nutrient solution, concluded that the lack of B in
the growth medium resulted in reduction of Ca concentrations in the plant.
However, it should be pointed out that the plant dry weigh and the value of
the nutrient concentrations must be associated to predict its uptake.
Boron rates in the nutrient solution promoted increases in the concentration and total B uptake in castor bean Iris (Table 2). In general, the Ca
supplying resulted in reduction of B concentrations in the plants. Nevertheless, such a fact is associated with the dilution effect as a result of plant growth
and biomass yield (Jarrell and Beverly, 1981). Results show that application
of B significantly increased uptake of B at various levels of Ca addition in
nutrient solution. In other words, there was a synergetic effect between these
nutrients. Similar results may be observed both for K and for Mg as related
to Ca supply (Tables 3 and 4). In addition, both of these elements were
determined due to the known relationship between them and Ca, called
the Viets effect (Viets, 1944) on the one hand, and competitive inhibition
uptake on the other (Ozaki et al., 2005). Some studies in the literature have
frequently been reported the decreasing of K and Mg concentration in plant
tissues due to Ca supplying (such as a dilution effect), notably at high Ca
rates. However, as observed for the supplying of B, total K and Mg uptake
also increased with the addition of Ca (Tables 3 and 4), probably due to
the improving of the plant dry matter yield. These ranges for K and Mg
concentrations in castor bean Iris tissues are considered adequate (Lavres
Jr. et al., 2005). In addition, there were not observed either K or Mg visual
symptoms of deficiency.
The assessment of leaf diagnosis showed that the Ca and B concentrations in the diagnostic leaf maintained a close relationship with the castor
bean Iris dry matter yield (Figure 4). The greatest yields were obtained
with concentrations between 16 and 20 g kg1 of Ca and 30 to 40 mg
kg1 of B. In regards to fruit dry matter weight (Figure 5), the Ca and B
422
H. C. J. Franco et al.
FIGURE 4 Relationship among total dry matter weight and the Ca and B concentrations in the diagnostic
leaves of the castor bean Iris.
FIGURE 5 Relationship among fruit dry matter weight and the Ca and B concentrations in the diagnostic
leaves of the castor bean Iris.
423
TABLE 3 Potassium concentration and total K uptake by castor bean Iris, related to Ca and B rates in
the nutrient solution
Rate
Ca1
Ca2
Ca4
Average
Ca1
Ca2
Ca4
Average
B1
B3
B5
32.1
28.3
28.0
29.5
FCa = 8.8
K concentration (g kg1)
30.9
29.4
27.8
30.9
25.4
24.3
28.1
28.2
FB = 0.80NS
FCa B = 1.4NS
1028
1164
1683
1291
FCa = 11.5
L1;
L1;
Average
30.8a
29.0a
25.9b
SMD = 2.9 CV = 10%
1265b
1499b
1882a
SMD = 323 CV = 21%
L1;
Rates: Ca1 = 40 mg
Ca2 = 80 mg
Ca3 = 160 mg
B1 = 0.32 mg L1; B2 = 0.96 mg L1
1
and B3 = 1.96 mg L ; means followed by different letters, lowercase letters in the column and capital
letters in the row, differ among themselves by the Tukey test at 5% probability; and significant at
1 and 5% probability respectively; NS: not significant; DMS = minimum significant difference; C.V. =
coefficient of variation.
concentrations that are related to greatest fruit yield were in the same average values mentioned to total dry matter. According to Marschner (1995)
the Ca B interaction must be based on the fact that both of them play a role
on the membrane structural functions, as well on the middle lamella and the
cell wall. So in this sense, it is to be expected that castor bean plants grown
with adequate availability of these nutrients present a determined Ca:B
TABLE 4 Magnesium concentration and total Mg uptake by castor bean Iris, related to Ca and B rates
in the nutrient solution
Rate
B1
Ca1
Ca2
Ca4
Average
6.9
5.7
5.4
6.0
= 6.7
Mg concentration (g kg1)
6.8
5.6
5.2
5.5
5.4
5.8
5.8
5.6
FB = 0.60NS
FCa B = 2.1NS
221
232
323
259b
FCa = 11.2
FCa
Ca1
Ca2
Ca4
Average
L1;
B3
L1;
B5
L1;
Average
6.4a
5.5b
5.5b
SMD = 0.7 CV = 12%
264b
287b
406a
SMD = 80 CV = 25%
Rates: Ca1 = 40 mg
Ca2 = 80 mg
Ca3 = 160 mg
B1 = 0.32 mg L1; B2 = 0.96 mg L1
and B3 = 1.96 mg L1; means followed by different letters, lowercase letters in the column and capital
letters in the row, differ among themselves by the Tukey test at 5% probability; and significant at
1 and 5% probability respectively; NS: not significant; DMS = minimum significant difference; C.V. =
coefficient of variation.
424
H. C. J. Franco et al.
ratio in their mineral composition. In this study, the leaf Ca:B ratio used
for diagnosis, associated with maximum total dry matter and fruit yield, was
approximately 500 (16 to 20 g Ca kg1 per 30 to 40 mg B kg1). This could
be stated as a suitable Ca:B ratio to predict normal growth and yield of castor bean Iris, and also may be considered an indicative parameter of the
adequate nutrition. Nevertheless, Kanwal et al. (2008) obtained a Ca:B ratio
of 30 in the shoot of corn seedlings, grown in a nutrient solution, for obtain
95% of the maximum relative shoot dry matter yield.
After the harvest of the castor bean fruit, the technological quality of the
beans was determined, quantifying the ether extract and seed oil contents
(Figure 6). The treatment with the combination of Ca and B rates of 80 and
1.60 mg L1, respectively, promoted the greatest gross fat content per unit
of dry matter produced. Considering the greatest rate of B (1.6 mg L1) and
raising the rate of Ca in the solution from 40 to 80 mg L1, a 56% increase was
observed in the ether extract content (in g kg1 of dry matter) in the beans
produced. Nevertheless, the gross fat content reduced by 17% from the
Ca2B5 treatment to the treatment with a combination of the greatest rates
of Ca and of B, in a similar effect to that of nutrient dilution. On the other
hand, in the treatment corresponding to the lowest combination of Ca and
B, due to the nutritional deficiencies, there was not adequate development
of the racemes (inflorescence) and then, inadequate fruit development. In
the literature there are few studies evaluating the technological quality of
the castor bean seeds related to mineral nutrition. However, an explanation
for this effect is not available, and requires further investigation.
FIGURE 6 Technological quality of the beans (ether extract and seed oil content) of the castor bean
plant, related to Ca and B rates in the nutrient solution.
425
426
H. C. J. Franco et al.
Asad, A., F. P. C. Blamey, and D. C. Edwards. 2002. Dry matter production and boron concentrations of
vegetative and reproductive tissues of canola and sunflower plants grown in nutrient solution. Plant
and Soil 243: 243252.
Asher, C. J., and D. G. Edwards. 1978. Relevance of dilute solution culture studies to problems of low
fertility tropical soils. In: Mineral Nutrition of Legumes in Tropical and Subtropical Soils, eds. C. S. Andrew,
and E. J. Kamprath, pp. 131152. Melbourne: CSIRO.
Beltrao, N. E. M., L. C. Silva, O. L. Vasconcelos, D. M. P. Azevedo, and D. J. Vieira. 2001. Fitology. In: The
Agribusiness of the Castor Bean in Brazil, eds. D. M. P. Azevedo, and E. L. Lima, pp. 3761. Braslia,
Brazil: Embrapa (in Portuguese).
Blevins, D. G., and K. M. Lukaszewski. 1998. Boron in plant structure and function. Annual Review of Plant
Physiology and Plant Molecular Biology 49: 481500.
Cakmak, I., and V. Romheld. 1997. Boron deficiency induced impairment of cellular functions in plants.
Plant and Soil 193: 9195.
Camacho-Cristobal, J. J., J. Rexach, M. B. Herrera-Rodrguez, M. T. Navarro-Gochicoa, and A. GonzalezFontes. 2011. Boron deficiency and transcript level changes. Plant Science 181: 5889.
Chatterjee, C., P. Sinha, N. Nautiyal, S. C. Agarwala, and C. P. Sharma. 1987. Metabolic changes associated
with boron-calcium interaction in maize. Soil Science and Plant Nutrition 33: 607617.
Clark, R. B. 1984. Physiological aspects of calcium, magnesium and molybdenum deficiencies in plants.
In: Soil Acidity and Liming, ed. F. Adams, pp. 99170. Madison, WI: American Society of Agronomy,
Crop Science Society of America, and Soil Science Society of America.
Eichert, T., and H. E. Goldbach. 2010. Transpiration rate affects the mobility of foliar-applied boron in
Ricinus communis L. cv. Impala. Plant and Soil 328: 165174.
Gupta, U. C. 2001. Yield response to boron and factors affecting its uptake by crops. In: Perspectives on the
Micronutrient Nutrition of Crops, eds. K. Singh, S. Mori, and R. M. Welch, pp. 91118. Jodhpur, India:
Scientific Publishers.
Jarrell, W. M., and R. B. Beverly. 1981. The dilution effect in plant nutrition studies. Advances in Agronomy
34: 197224.
Johnson, C. M., P. R. Stout, T. C. Broyer, and A. B. Carlton. 1957. Comparative chlorine requirements of
different plant species. Plant and Soil 8: 337353.
Kabata-Pendias, A., and H. Pendias. 2001. Trace Elements in Soils and Plants. Boca Raton, FL: CRC Press.
Kanwal, S., K. Rahmatullah, T. Aziz, M. A. Maqsood, and N. Abbas. 2008. Critical ratio of calcium and
boron in maize shoot for optimum growth. Journal of Plant Nutrition 31: 15351542.
Kobayashi, M., T. Matoh, and T. Azuma. 1996. Two chains of rhamnogalacturonan II are cross linked by
borate-diol ester bonds in higher plant cell walls. Plant Physiology 110: 10171020.
Kochian, L. V. 1991. Mechanisms of micronutrient uptake and translocation in plants. In: Micronutrients
in Agriculture, ed. J. J. Mortvedt, pp. 251270. Madison, WI: Soil Science Society of America.
Konsaeng, S., B. Dell, and B. Rerkasem. 2010. Boron mobility in peanut (Arachis hypogaea L.). Plant and
Soil 330: 281289.
Lange, A., A. M. Martines, M. A. C. Silva, M. C. M. Sorreano, C. P. Cabral, and E. Malavolta. 2005.
Micronutrient deficiency effect on the nutritional status of the castor bean cultivar Iris. Pesquisa
Agropecuaria Brasileira 40: 6167 (in Portuguese).
Lavres Jr, J., R. M. Boaretto, M. L. S. Silva, D. Correia, C. P. Cabral, and E. Malavolta. 2005. Deficiencies
of macronutrients on nutritional status of castor bean cultivar Iris. Pesquisa Agropecuaria Brasileira
40: 145151. (in Portuguese).
Malavolta, E., G. C. Vitti, and S. A. Oliveira. 1997. Evaluation of Plant Nutritional Status: Principles and
Applications. Piracicaba, Brazil: Potafos. (in Portuguese).
Marschner, H. 1995. Mineral Nutrition of Higher Plants. London: Academic Press.
Matas, M. A., A. Gonzalez-Fontes, and J. J. Camacho-Cristobal. 2009. Effect of boron supply on nitrate
concentration and its reduction in roots and leaves of tobacco plants. Biologia Plantarum 53: 120
124.
Mills, H. A., and J. B. Jones Jr.. 1997. Plant Analysis Handbook II: A Practical Sampling, Preparation, Analysis,
and Interpretation Guide. Athens, GA: MicroMacro Publishing.
Ozaki, T., S. Ambe, T. Abe, and A. J. Francis. 2005. Competitive inhibition and selectivity enhancement
by Ca in the uptake of inorganic elements (Be, Na, Mg, K, Ca, Sc, Mn, Co, Zn, Se, Rb, Sr, Y, Zr, Ce,
Pm, Gd, Hf) by carrot (Daucus carota cv. U.S. harumakigosun). Biological Trace Element Research 103:
6982.
427
Power, P. P., and W. G. Woods. 1997. The chemistry of boron and its speciation in plants. Plant and Soil
193: 113.
Salvador, J. O., A. Moreira, and T. Muraoka. 1999. Visual symptoms of micronutrient deficiency and
of mineral content in guava young plant leaves. Pesquisa Agropecuaria Brasileira 34: 16551662 (in
Portuguese).
Savy Filho, A. 2005. Castor bean: Agricultural technology. Campinas, Brazil: Emopi (in Portuguese).
Schaller, G. E., and M. R. Sussman. 1988. Phosphorylation of the plasma membrane H+-ATPase of oat
roots by calcium stimulated protein kinase. Planta 173: 509518.
Severino, L. S., G. B. Ferreira, C. R. A. Moraes, T. M. S. Gondim, W. S. A. Freire, D. A. Castro, G. D.
Cardoso, and D. E. M. Beltrao. 2006. Growth and yield of castor bean fertilized with macronutrients
and micronutrients. Pesquisa Agropecuaria Brasileira 41: 563568 (in Portuguese).
Viets, F. G. 1944. Calcium and other polyvalent cations as accelerators of ion accumulation by excised
barley roots. Plant Physiology 19: 6979.
Xu, G., and R. Wang. 2011. Sulfur and boron-magnesium-zinc compound fertilizer contribute to the
reproductive growth of Jatropha curcas L. Journal of Plant Nutrition 34: 18431852.
Yamauchi, T., T. Hara, and Y. Sonoda. 1986. Effects of boron deficiency and calcium supply on the
calcium metabolism in tomato plant. Plant and Soil 93: 223230.