Journal of Experimental Biology and Agricultural Sciences, May - 2014; Volume – 2(2S)

Journal of Experimental Biology and Agricultural Sciences

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ISSN No. 2320 – 8694

THE PROMOTIVE ROLE OF ALGAL ON THE GROWTH OF MAIZE (Zea mays L.) SEEDLINGS UNDER CADMIUM-STRESS

Hanan M Abou- Zeid

Botany & Microbiology department, Faculty of Science, Alexandria University, Egypt

Received – April 26, 2014; Revision – May 09, 2014, Accepted – May 20, 2014 Available Online – May 31, 2014.

KEYWORDS ABSTRACT

Cadmium 2+ The influence of various cadmium (Cd ) levels in absence and presence of algal biofertilizer on the growth, photosynthesis, and mineral contents of maize was examined. Cd2+ caused an inhibitory Biofertilizer effect on growth parameters of shoots and roots leading to lower tolerance index. Application of Cd 2+ in the nutrient medium in absence of biofertilizer suppressed the photosynthetic parameters (Fv/Fm, qP, Photosynthetic parameters Pn, NPQ, and Gs) resulting in a marked decline of photosynthetic rate. Cadmium interferes with the Macronutrients uptake, transport and utilization of several macro- and , which accounts, at least in part, for Cd2+ toxicity in plants. There was a marked reduction in the accumulation of macronutrient such as 2+ Maize (Zea mays) K, Ca, Mg, and P in the roots and shoots. Supplementation of algal biofertilizer with Cd - contaminated medium resulted in shift off the Cd2+ toxicity and improved to some extent the growth and photosynthetic machinery, as well as increased the intracellular macro-nutrients such as K, Ca, Mg, and P in maize plants.

* Corresponding author E-mail: [email protected] (Hanan M. Abou- Zeid)

Peer review under responsibility of Journal of Experimental Biology and Agricultural Sciences.

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257 Abou - Zeid

1 Introduction The healthy, homogenous grains of corn (Zea mays) were Heavy metal contamination is responsible for limiting crop purchased from the International Research Center, El-Dokki, productivity in agricultural lands (Smith, 2009). These heavy Giza, Egypt. Collected seeds were surface sterilized by 0.1% metals can enter the roots and translocated to the shoot via sodium hypochlorite solution for 5 min and then rinsed several xylem elements (Lux et al., 2011).Cadmium consider as a toxic times with distilled . The sterilized grains were allowed metal because of its relatively high mobility in the soil– to germinate in Petri dishes for 24h. The germinated grains system (Benavides et al., 2005; Groppa et al., 2012). It is were transferred to plastic pots filled with clay sandy soil (1:3). responsible for, causing an oxidative stress and disruption of The seed inoculated pots were divided into four sets. The first membrane composition and functioning (Gratao et al., 2009; set was irrigated with half strength Hoagland solution Gallego et al., 2012).Furthermore it is responsible for the (Hoagland & Arnon, 1950) and consider as control. The disturbances of several physiological processes, such as second set was irrigated with half strength Hoagland solution -1 photosynthesis, water relations, uptake, transport and supplied with 1, 2, 3, 4, and 5 mg L CdCl2. The third set was utilization of several macro- and micronutrients (Lopez- irrigated with half strength Hoagland supplied with 1mlL-1 Chuken & Young 2010; Gill et al., 2012; Li et al., 2012). super blue green biofertilizer (Nostoc and Anabaena sp) which According to Rivetta et al. (1997) and Sanità di Toppi & is produced by unit, General Organization of Gabbrielli (1999) uptake of Cd ions takes place in competition Agriculture Equalization Fund, Agriculture Research Centre, with the various essential elements such as K, Ca, Mg, Fe, Mn, Ministry of Agriculture, Giza, Egypt. The fourth set was Cu, Zn, and Ni, across the same transmembrane carrier. In irrigated with half strength Hoagland solution supplied with 1, -1 -1 addition Liu et al. (2003) concluded that, there was a 2, 3, 4, and 5 mg L CdCl2 and supplemented with 1mlL complicated relationship between the absorption and super blue green biofertilizer. The pots (in triplicates) were accumulation of Cd2+ and other mineral nutrients (Fe, Zn, Mn, incubated in natural environmental conditions. After 15-days, Cu, and Mg) in rice plants. Moreover, cadmium inhibits from the starting of experiment, homologous samples were photosynthesis and interferes in the biosynthesis of taken, washed by distilled water, and then divided into roots chlorophyll. Furthermore, it is responsible for the degradation and shoots for estimation of fresh and dry biomass and shoot of chlorophyll and responsible for affecting many other height. photosynthetic processes (Joshi & Mohanty 2004; Parmar et al., 2013). 2.2 Photosynthetic pigments contents

Biofertilizers are the products which containing living cells of Chlorophyll a (Chl. a), chlorophyll b (Chl. b), and carotenoids different origins including microorganisms that have the ability (Carot.) content were estimated according to the method to mobilize nutritionally important elements from non-usable described by Lichtenthaler (1987). forms (Chen, 2006). Mishra & Dash (2014) reported that biofertilizers have a great potential as supplementary, 2.3 Chlorophyll fluorescence renewable and environmental friendly sources of plant nutrients and are an important component of integrated nutrient Measurements of chlorophyll fluorescence were performed by management. Cyanobacteria or blue green are OS-30P pulse modulated chlorophyll fluorimeter (Opti- microalgae suggested to have some added advantages over sciences, Hudson, USA). Before every measurement, leaves other microorganisms because of their larger surface area, were dark- adapted for 30 min with leaf-clips. Photosynthetic great mucilage volume with high binding affinity and simple rate was measured with ADC portable LCi Ultra Compact. nutrient requirements (Anjana et al., 2007). Gardea-Torresdey (Moradi & Ismail, 2007). et al. (1990) reported that cyanobacterial cells may respond to metals such as copper, lead and cadmium through passive 2.4 Energy-dispersive X-ray fluorescence (EDXRF) technique, accumulation in cells, and played an important role in the Instrumentation and sample analysis removal of harmful metals from the environment. Moreover, Sikander et al. (1995) and Aziz & Hashem (2004) stated that Dried plant material (shoots and roots) were grinded into fine cynobacteria are used as biofertilizers which enhanced the powder. About 300 mg of each sample were pelletized using a growth of higher plants like wheat, rice, maize, vegetables and SPECAC press with a 2 tons/cm2 pressure for produce an certain medicinal plants. The main objective of this study was intermediate thick pellet sample. The pellets produced were to investigate the role of cynobacterial (Nostoc sp and kept in desiccators for at least 24 h to get rid of the moisture Anabaena sp) biological in alleviating the inhibitory contents. The irradiation was done using an EDXRF effect of Cd2+ on the growth, photosynthetic characteristics, spectrometer at the XRF special unit of Electron Microscope, and nutrient composition in maize plant. Faculty of Science, Alexandria University. Link ISIS analyzer programmed attached with Scanning Electron Microscope 2 Materials and Methods (SEM) was employed for the data collection. Three irradiations were made for each sample, for a spectrum collection life time 2.1 Plant materials and various treatments of 1500 s. Linear least squares fitting of the AXIL software

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The promotive role of algal biofertilizer on the growth of maize (Zea mays L.) seedlings under cadmium-stress. 258

2+ -1 programmed was used for the spectrum deconvolution (IAEA, However, at lower Cd concentration (1mgL ), the measured 2005). growth parameters were insignificantly changed compared to control. There was a marked decrease of tolerance index (TI) 2.5 Statistical analysis for fresh and dry mass and shoot height indicating that Cd2+ exerted an inhibitory impact on the growth of maize plants Based on the data obtained from the experiment, the results (Table 1). At 5mgL-1 Cd2+ TI values were 33% and 63% for presented are the mean ± standard deviation (SD) gained from fresh and dry mass respectively, and 35% for shoot height. at least three replicate samples using Microsoft Office Excel 2007. Statistical analysis by the least significant difference Application of biofertilizer to the Cd2+ - contaminated soil (LSD) for multiple comparisons, taking P ≤ 0.05 as significant, resulted in a positive increase of measured growth parameters was calculated by SPSS 13.0. compared to only Cd2+- contaminated treatments. Addition of the biofertilizer with 2mgL-1 Cd2+ - contaminated soil increased 3 Results the fresh and dry masses of shoots to approximately the level of the control. At the highest Cd2+ level (5mgL-1) the reduction Exposing of maize plants to various concentrations of Cd2+ percentages of the fresh biomass of shoots and roots were 67% resulted in a significant reduction of fresh and dry biomass as and 83% respectively comparing to the control well as shoot height (P≤0.05).

Table 1 Effect o Cd2+ impact in absence and presence of biofertilizer on shoots growth parameters and cadmium tolerance index of Zea plants.

Cd2+ Cd2+ + Biofertilizer

f.m. TI d.m. TI Height TI Suc. f.m. TI% d.m. TI Height TI Suc. (g) % (g) % (cm) % (g) (g) (g) % (cm) % (g)

0 1.082a 100 0.098 a 100 20.5 a 100 11.05 a 1.157 a 100 0.102 a 100 22.3 a 100 11.34 a

1 0.997 a 92 0.095 a 97 19.8 ab 97 10.49 ab 1.138 a 98 0.098 ab 96 21.0 a 94 11.25 a

2 0.875b 81 0.087 ab 89 19.1 b 93 10.05 b 1.105 a 96 0.097 b 95 19.2 b 86 10.68 b

3 0.758 b 70 0.081 b 83 15.8 c 77 9.36 c 0.891 b 77 0.086 c 84 18.0 c 81 10.36 b

4 0.504c 47 0.069 c 70 11.2 d 55 7.30 d 0.712 c 62 0.083cd 81 14.9 d 67 8.58 c

5 0.362 c 33 0.062 c 63 7.10 e 35 5.84 d 0.641d 55 0.079 d 77 10.5e 47 8.11 d

TI= cadmium tolerance index, f.m. = fresh mass, d.m.=dry mass, and suc.= succulent weight. -Different letters within each column indicate a significant difference at probability level ≤ 0.05 according to LSD.

Table 2 Effect of Cd2+ impact in absence and presence of biofertilizer on roots growth parameters and cadmium tolerance index of Zea plants.

Cd2+ Cd2+ + Biofertilizer f.m. TI d.m. TI Suc. f.m. TI d.m. TI Suc. (g) % (g) % (g) (g) % (g) % (g) 0 0.935 a 100 0.092 a 100 10.20 a 1.054 a 100 0.102 a 100 11.34 a 1 0.853 b 91 0.086 b 93 9.92 b 0.986 b 94 0.098 a 96 11.25 a 2 0.610c 65 0.073 c 79 8.36 c 0.759 c 72 0.097 a 95 10.68 b

3 0.348 d 37 0.050 d 54 6.96 d 0.626 d 59 0.086 b 84 10.36 b

4 0.235 de 25 0.042 d 46 5.60 d 0.421 e 40 0.083 b c 81 8.58 c

5 0.163 e 17 0.038 d 41 4.29 e 0.293 f 28 0.079 c 77 8.11 d

TI= cadmium tolerance index, f.m. = fresh mass, d.m. =dry mass, and Suc. = succulent weight. -Different letters within each column indicate a significant difference at probability level ≤ 0.05 according to LSD.

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259 Abou - Zeid

Figure 1 Effect of Cd2+ impact in absence and presence Figure 2 Effect of Cd2+ impact in absence and presence of

biofertilizer on the photosynthetic pigments content of biofertilizer on (Fv/Fm), the net rate of photosynthesis Zea mays. (Pn), Coefficient of photochemical quenching (qP), Non-

photochemical quenching (NPQ), and stomatal -Values are means ±SD and -Different letters within each column indicate a significant difference at probability conductance (Gs) of Zea mays. level ≤ 0.05 according to LSD. -Values are means ±SD. And -Different letters for each line indicate a significant difference at probability level ≤ 0.05 according to LSD. the corresponding values in presence of biofertilizer were 45% increasing Cd2+ concentrations in the nutrient medium. and 72% respectively. Results of Table 1 and Table 2 indicate Application of the biofertilizer with Cd2+- contaminated that the TI values of the plants grown in soil containing medium resulted in improvement in succulent values biofertilizer were higher than those grown in absence of comparing to those in absence of biofertilizer (Table 1 & Table biofertilizer. This means that the biofertilizer shift off, to some 2). These observations indicated the high tendency of Zea extent, the determinate effect of Cd2+ on the growth of shoots plants to maintain considerable water in presence of and roots. In general the succulent values (fresh mass/ dry biofertilizer. mass) of shoots and roots were markedly decreased with

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The promotive role of algal biofertilizer on the growth of maize (Zea mays L.) seedlings under cadmium-stress. 260

Figure 3 EDXRF spectrum of elements in Zea plants under Cd2+ stress in absence and presence biofertilizer. 1S = Shoot (control) 1R= Root (control) 2S = Shoot (2mgL-1 Cd2+ ) 2R= Root (2mgL-1 Cd2+ ) 3S = Shoot (5mgL-1 Cd2+ ) 3R= Root (5mgL-1 Cd2+ ) 4S = Shoot (2mgL-1 Cd2+) + biofertilizer 4R= Root (2mgL-1 Cd2+) + biofertilizer 5S = Shoot (5mgL-1 Cd2+) + biofertilizer 5R= Root (5mgL-1 Cd2+) + biofertilize

Table 3 Effect of Cd2+ impact in absence and presence of biofertilizer on the percentage of elements nutrients content in shoots and roots of Zea plants.

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Treatment Cd2+ Cd2+ + Biofertilizer 2+ -1 (Cd mgL ) 0 2 5 2 5 % Shoots K 21.1 6.8 4.3 19.0 16.0 Ca 12.1 4.3 2.3 9.0 7.1 Mg 1.2 1.1 0.4 3.6 1.3 P 6.9 4.8 1.1 5.5 4.8 Fe 3.3 1.8 1.1 2.5 1.9 Cu 3.3 2.5 2.4 1.5 0.7 Zn 1.6 1.6 1.3 0.5 0.3 Cd - 38.0 41.0 26.4 23.8 Cl 40.3 40.2 33.7 34.4 14.4 % Roots K 30.8 5.2 2.8 10.0 13.3 Ca 18.7 4.8 0.2 10.4 1.7 Mg 1.2 0.5 0.4 1.6 1.2 P 3.8 2.3 1.0 2.6 4.0 Fe 1.2 1.0 0.4 2.9 3.0 Cu 3.2 2.4 0.6 1.9 3.7 Zn 2.1 2.0 0.8 2.2 1.4 Cd - 43.1 45.9 29.9 26.7 Cl 23.8 39.4 48.5 27.2 31.3

The level of photosynthetic pigment contents showed a EDXRF microanalysis showed that in absence of biofertilizer a significant decrease in response to increase of Cd2+ marked increase in the percentage of Cd2+ and Cl- in the roots concentrations. At highest level (5mgL-1) of Cd2+, a significant and shoots of Zea plants. This increase was mainly reduction in the content of Chl. a & Chl. b (69% and 79% accompanied with a great decrease of K, Cu, Mg and P. respectively) was reported as compared to control (Figure 1). Conversely, application of biofertilizer resulted in a marked Application of biofertilizer resulted in an increase in the accumulation of K, Ca, Mg and P, whereas the percentage of content of Chl. a & Chl. b compared to those of Cd2+- stressed Cd2+ was markedly decreased (Table 3 & Figure 3). plants. The decrease in Chl. a and Chl. b contents in highly (5mgL-1) Cd2+- stressed leaves in presence of biofertilizer was 4 Discussion 56% and 64% respectively, compared to control. Cadmium also induced a greater reduction in carotenoids content of the The biomasses of shoot and root as well as shoot height were leaves in absence of biofertilizer. significantly decreased with increasing Cd2+ concentrations , and the reduction was greatly observed in roots than in shoots Significant changes in the photosynthetic parameters were (Table1 & Table 2) leading to lower tolerance index for roots. reported due to cadmium stress (Figure 2). Under cadmium The inhibitory effects of Cd2+ on plant growth were explored stress, the photosynthetic rate (Pn) and stomatal conductivity by many authors (Sanitá di Toppi & Gabbrielli, 1999; Perfus- (Gs) were significantly declined with increasing the Cd2+ levels Barbeoch et al., 2002; Rodríguez-Serrano et al., 2009). The in the nutrient medium. In addition, Cd2+ exerted a significant phenomenon of the inhibitory effects of Cd2+ on growth deleterious effect on chlorophyll florescence parameters. At parameters can be related to decrease in cell division of root -1 2+, 5mgL Cd the decrease of Fv/Fm and qP values was 33% apex (Eun et al., 2000). Furthermore, it might be due to the and 60% respectively compared to control. Contrary to other disturbance of plasma membrane integrity (Kennedy & chlorophyll fluorescence parameters, the NPQ value was Gonsalves, 1987; Burzynski & Kolano, 2003) which resulting significantly increased in Cd2+- stressed plants. Addition of in the alteration of the absorption of water and nutrients such biofertilizer ameliorated Cd2+ stress by improving the as K, Ca, Mg, and P (Pál et al., 2006) as well as damage to chlorophyll flouresence parameters. Under highly Cd2+- stress photosynthetic machinery (Najeeb et al.,2011). In present 2+ conditions, the percent inhibition Pn and Gs levels in the Zea study exposure of Zea plants to various Cd concentrations leaves were 41% and 18% respectively compared to control; resulted in a marked decrease of macronutrient K ,Ca, Mg, and the corresponding values in the presence of biofertilizer were P in the roots and shoots and that accompanied with a higher 64% and 44% respectively (Figure 2). accumulation of Cd2+ . Li et al. (2012) reported that K+ and Ca2+ contents in both roots and shoots of rice plant were significantly reduced when treated with exogenous Cd2+ by

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The promotive role of algal biofertilizer on the growth of maize (Zea mays L.) seedlings under cadmium-stress. 262 inhibiting the inward Ca2+- permeable and K+ channel the light use efficiency of PS II, whereas the damage of activities and by inducing the outward K+ currents. In addition, plasma membrane due to diminishment of macronutrients K, Cd2+ - induced depolarization of the membrane potential Ca, Mg resulted in a marked decrease of water content and attenuated the driving force for Ca2+, and K+, uptake and hence hence reduction of Gs. These observations could result in reduced plant growth. Therefore, the decrease of macronutrient suppression of growth of Zea plants under Cd2+ stress. in the present study might reveal the suppression of physiological and metabolic processes as well as the integrity In present study, application of biofertilizer showed a wide and functions of plasma membranes in Cd2+ - exposed plants. scope for alleviating Cd2+ stress and therefore restoring the On tested connections, the decrease of succulent values could growth and photosynthetic machinery in Zea plants. The indicate the disturbance of plasma membrane integrity of roots ameliorating feature of biofertilizer may be attributed to and shoots of Cd2+- exposed plants and hence reduce the increasing the macro and micro-nutrients in the rooting growth parameters. medium of Zea plants, and that might protect the plasma membrane integrity and water content. Also, the increasing of Several studies (Shariatmadari et al., 2011; Koliai et al., 2012; intracellular macronutrients such as K, Ca, Mg, and P might Sokhangoy et al., 2012) have been reported that biological enhance chlorophyll biosynthesis and protect the are able to change the basic nutrients lead to better photosynthetic systems. In addition, the competition between seed germination, plant growth and yield. Application of Cd2+ and available macro and micro-nutrients might result to biofertilizer to Cd2+ - contaminated nutrient medium resulted decrease the intercellular Cd2+ and hence decrease the toxic in an improvement of plasma membrane integrity in which and the damage effects of Cd2+ on photosynthetic rate and increased the maintenance of Zea plants to absorb considerable growth in Zea plants. water (increase of succulent) and macronutrients K, Ca, Mg and P, and hence increased the tolerance index. References

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