Endophytic infection alleviates Pb2+ stress effects on photosystem II functioning of Oryza sativa leaves

Journal of Hazardous Materials 295 (2015) 79–85

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Endophytic infection alleviates Pb2+ stress effects on photosystem II functioning of Oryza sativa leaves Xuemei Li a,∗ , Lihong Zhang b,∗∗ a b

College of Chemistry and Life Science, Shenyang Normal University, Shenyang 110034, PR China Environmental Science Department of Liaoning University,Shenyang 110036, PR China

h i g h l i g h t s • • • • •

Chl fluorescence parameters of endophyte-infected rice under Pb2+ stress were tested. The efficiency and stability of PSII are markedly affected by Pb2+ stress. Endophyte infection improved photosynthetic system activity under Pb2+ stress. JIP-test is a suitable tool for monitoring of Pb2+ stress. Endophyte infection may increase tolerance to Pb2+ in rice.

a r t i c l e

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Article history: Received 24 December 2014 Received in revised form 1 April 2015 Accepted 6 April 2015 Available online 8 April 2015 Keywords: Chlorophyll fluorescence Endophytic infection Pb2+ stress Photosystem II

a b s t r a c t The aims of this study were to examine the effect of Pb2+ stress on the primary reaction of photosynthesis and to assess the potential benefits of endophytic infection on the Pb2+ tolerance of rice seedlings. Rice inoculated with an endophytic fungus (E+) and non-inoculated (E−) were subjected to 0, 50, 100, 150 and 200 ␮M Pb2+ . The responses to Pb2+ stress were characterized by the analysis of Chl a fluorescence. A comparison of E− with E+ rice seedlings, as evaluated by their performance index (PIABS and PItot ), revealed the inhibitory effects of Pb2+ on photosystem II (PSII) connectivity, the oxygen evolving complex (OEC), and on the J step of the induction curves, which is associated with an inhibition of electron transport from the quinone acceptor QA to QB . Furthermore, the changes of the donor and the acceptor parameters of PSII were greater in E− than in E+ under Pb2+ stress. These observations suggest that the efficiency and stability of PSII are markedly affected by Pb2+ stress, and the photosynthetic energy conservation in E+ was more effective than in E−. We showed that endophytic infection plays an important role in enhancing the photosynthetic mechanism of rice seedlings exposed to Pb2+ stress. © 2015 Published by Elsevier B.V.

1. Introduction Plants are normally exposed to environmental stresses that may directly restrict growth or cause metabolism dysfunction [1]. Rice is a staple food for over 3 billion people and provides more than 20% of their daily calorie intake. In China, large areas of paddy fields have been polluted by heavy metals with agricultural applications of phosphate fertilizer, industrial effluent, and sewage sludge [2,3]. Lead (Pb) is one of the most abundant, globally distributed toxic elements [4]. Pb increasing level in paddy soil exerts adverse effects on

∗ Corresponding author. Tel.: +86 24 86578977; fax: +86 24 8659254. ∗∗ Corresponding author. Tel.: +86 24 62204591; fax: +86 24 62204818. E-mail addresses: [email protected] (X. Li), [email protected] (L. Zhang). http://dx.doi.org/10.1016/j.jhazmat.2015.04.015 0304-3894/© 2015 Published by Elsevier B.V.

rice and the healthy of human beings by food chains [5,6]. Pb treatment influences growth and photosynthetic processes, inhibits enzyme activities, causes water imbalance, and alters membrane permeability and mineral nutrition [7]. All plants in natural ecosystems appear to be symbiotic with fungal endophytes [8]. There is an increasing amount of data suggests that endophytic fungi alter the physiology of host plants and affect the way that they respond to environmental stresses [9–11]. Recently, we identified an endophytic fungus (EF0801), which was isolated from Suaeda salsa. EF0801 is congeneric to Sordariomycetes sp. (99% similarity). We have earlier reported that infection with the endophyte EF0801 can enhance the photosynthetic capacity in rice exposed to Pb2+ stress [12]; however, the mechanisms underlying such an enhancement are poorly understood.

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Photosynthesis is a very heavy-metal-sensitive process and can be inhibited by heavy metal stress before other symptoms of the stress are detected [13,14]. In recent years, chlorophyll (Chl) fluorescence analysis has been applied as a rapid non-destructive, non-invasive tool to obtain information about the state of photosynthetic apparatus, especially photosystem II (PSII) [15]. The polyphasic fluorescence transient (OJIP) test is used in different areas of plant biology to evaluate the responses of the photosynthetic apparatus to different stresses. The calculated parameters include those related to energy fluxes for absorption (ABS), trapping (TR0 ) and dissipation (DI0 ) per reaction center (RC) [16]. The Performance Index (PIABS ) is a multicomponent fluorescence parameter derived from fast chlorophyll induction curves and used to describe the PSII-dependent first phase of the induction curve [17]. The shape of the OJIP curve of leaves is altered by stresses, such as heavy metal [18], salinity [19], temperature [20], drought [21], nutrient deficiency [22] as well as exogenous glycine betaine and proline [23], and salicylic acid [24]. A few studies have reported that Pb2+ stress induced marked changes in the shape of the Chl a fluorescence induction curve [25,26]. However, in our review of the literature, no study was found that investigated the alteration of Chl a fluorescence due to endophytic infection and Pb2+ stress. The present study examined Chl a fluorescence induction curve of endophytic-infected (E+) and uninfected (E−) detached rice leaves in order to evaluate the endophyte effect on primary photosynthesis under Pb2+ stress. The objective of the work presented here was to better understand the mechanisms of Pb2+ stress mitigation within rice seedlings due to endophytic infection.

2. Materials and methods 2.1. Microorganisms and plant material Rice seedlings were cultivated with Hoagland’s solution and were grown in a growth chamber (27 ◦ C/20 ◦ C day/night, 16 h/8 h light/dark period, 600 ␮mol m−2 s−1 PPFD, and 80% relative

humidity) according to Li et al. [12] for two days. The endophytic fungus (EF0801) was maintained on potato dextrose agar (PDA) plates under refrigerated conditions (4 ◦ C). The strain was inoculated at the 3 day instar stage at 5% into 75 ml of potato dextrose culture solution and cultured in a 150 ml shaker flask for 12 days at 180 rpm and 24 ±1 ◦ C. This fermentation broth was used for the treatments. 2.2. Endophytic infection and Pb2+ stress treatments The endophyte and Pb2+ treatments were initiated on the third day in the growth chamber [12]. Rice seedlings were divided into two groups: (1) E+, endophytic-infected seedlings, which were inoculated with the 5% fermentation broth by planting in full Hoagland’s solution, and (2) E−, endophytic-uninfected seedlings, which were not inoculated (the control group) were planted in full Hoagland’s solution separately. Each group (15 pots, 3 replicates × 5 treatments) was randomly assigned to one of five Pb2+ treatments (i.e., concentrations of 0, 50, 100, 150 and 200 ␮M Pb2+ in Hoagland’s solution). 2.3. Analysis of Chl fluorescence transient rise: OJIP test The polyphasic fluorescence transient was measured during 11:00–12:00 after exposure to Pb2+ stress for one week. Measurements were conducted using a portable Pocket-PEA chl fluorometer (Plant Efficiency Analyzer, Hansatech, Norfolk, UK). Before measurement, the leaves were dark-acclimated for 20 min with plastic clips (Hansatech, Norfolk, UK). The fluorescence OJIP transients were analyzed according to the OJIP test [17]. The following fluorescence intensity values from the original measurements were used: fluorescence intensity at 20 ␮s (the O step, considered as minimum fluorescence, F0 ); 300 ␮s (F300 ␮s ) used for calculation of the initial slope (Mo ) of the relative variable fluorescence kinetics; 2 ms (the J step, FJ ); 30 ms (the I step, FI ) and the P step (considered as maximum fluorescence, Fm ). The specific parameters are

Table 1 Summary of parameters, formulae and their description using data extracted from chlorophyll a fluorescence (OJIP) transient. Fluorescence parameters

Description

Ft F20 ␮s F300 ␮s FJ FI Fm = Fp Mo = 4(F300 ␮s − F0 )/(Fm − F0 ) VJ = (F2 ms − F0 )/(Fm − F0 ) VI = (F30 ms − F0 )/(Fm − F0 ) WK = (F300 ␮s − F0 )/(FJ – F0 )

Fluorescence intensity at time t after onset of actinic illumination Minimum reliable recorded fluorescence, at 20 ␮s with the Handy-PEA-fluorimeter Fluorescence intensity at 300 ␮s Fluorescence intensity at the J-step (2 ms) of OJIP Fluorescence intensity at the I-step (30 ms) of OJIP Maximum fluorescence, when all PSII RCs are closed Approximated initial slope of the fluorescence transient Relative variable fluorescence at 2 ms Relative variable fluorescence at 30 ms Represent the damage to OEC

Specific energy fluxes per active PSII reaction center-RC ABS/RC = Mo (1/VJ ) (1//␾Po ) TR0 /RC = Mo (1/VJ ) DI0 /RC = BS/RC–TR0 /RC

Absorption flux (of antenna Chls) per RC Trapped energy flux (leading to QA reduction) per RC Dissipation flux

Quantum efficiency/flux ratios ␾Po = TR0 /ABS = 1 − (F0 /Fm ) ␾Eo = ET0 /ABS = (Fv /Fm ) (1 − VJ ) ␺Eo = ET0 /TR0 = 1 − VJ ␾Do =1 − ␾Po

Maximum quantum yield of primary photochemistry at t = 0 Quantum yield for electron transport at t = 0 Probability that a trapped exciton moves an electron into the electron transport chain beyond QA − Maximum quantum yield of non-photochemical de-excitation

Area above the induction curve Area Sm = Area/(Fm − F0 ) Performance Index PIABS = (RC/ABS)[(␾Po )/(1 − ␾Po )] [(1 − VJ )/(1 − (1 − VJ ))] PItot =PIABS [␦Ro /(1 − ␦Ro )]

Integrated area between the induction curve and F = Fm Normalized total complementary area above the OJIP transient (reflecting multiple turnover QA reduction events) Performance index on an absorption basis Performance index total for energy conservation from photons absorbed by PSII to the reduction of PSI end acceptors

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calculated according to the OJIP test and their meanings are presented in Table 1 [17]. 2.4. Statistical analysis The differences of the OJIP test parameters between the infected and the uninfected seedlings under Pb2+ stress were determined using two-way analysis of variance (ANOVA) (with endophytic infection or not as one factor and Pb2+ concentration as the other factor) followed by LSD’s multiple-range test for multiple comparisons. All analyses were made using the SPSS statistical software package (Ver. 13.0, SPSS Inc., Chicago, IL, USA). 3. Results 3.1. OJIP curve The effects of the endophytic infection on Chl a fluorescence induction kinetics for the leaves of rice seedlings under Pb2+ stress for one-week are shown in Fig. 1. A typical polyphasic rise of fluorescence induction (O–J–I–P) was found, suggesting that all leaf samples were photosynthetically active. After one week of exposure, all the concentrations caused inhibition of original fluorescence and the leaf samples treated with 100, 150 and 200 ␮M Pb2+ stress induced significant decreases in the fluorescence yield at phases O, J, I, P between E− and E+. In the leaves of E+ plant with 50 ␮M Pb2+ stress, the O, J, I, and P steps were the highest, which in the leaves of E+ plant with 200 ␮M Pb2+ stress were significantly higher than that in the leaves of E− plant.

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K-band in Fig. 2B. The negative K-band suggested better performance of the E+ plants compared with the corresponding E− plants. However, at 150 and 200 ␮M Pb2+ concentrations, there was a reversion of the L-band and the K-band to narrower amplitude bands, indicating both E+ and E− were severely affected at high concentrations of Pb2+ . 3.3. Quantum efficiency and specific energy fluxes With increasing concentrations of Pb2+ stress, the yield for electron transport (␾Eo ), and the probability that a trapped exciton moves an electron into the electron transport chain beyond QA (␺Eo ) significantly decreased; whereas, the maximum quantum yield of non-photochemical de-excitation (␾Do ) significantly increased in E− plant (Fig. 3A–C). Compared with E− plants, ␺Eo and ␾Eo were higher, while ␾Do was lower in E+ samples under 150 and 200 ␮M Pb2+ stress. The specific energy fluxes (TR0 /RC, ABS/RC and DI0 /RC) increased with increasing concentration of Pb2+ stress (Fig. 3D–F). The specific energy fluxes of E− samples were significantly lower than those of the E+ samples.

3.2. L-band and K-band The fluorescence data were double normalized between the steps O (50 ␮s) and K (300 ␮s) and plotted with the difference kinetics VOK = (VOK )E+ − (VOK )E− in the 50–300 ␮s time range revealing an L-band in Fig. 2A. We showed that the E+ plants exhibited higher connectivity (negative L-bands) compared to the E− plants. The fluorescence data were double normalized between steps O and J (2 ms) and were plotted with the difference kinetics VOJ = (VOJ )E+ − (VOJ )E− in the 50 ␮s–2 ms time range revealing a

Fig. 1. Average Chl a fluorescence transient (OJIP) of dark-adapted leaves of the endophytic-uninfected (E−) and endophytic-infected (E+) rice after a week’s treatment with 0, 50, 100, 150, and 200 ␮M concentration of Pb2+ in Hoagland’s solution. The square, circle, triangle, diamond and star symbol curves represent the 0, 50, 100, 150, and 200 ␮M concentrations of Pb2+ , respectively. Closed symbol curves are used for E− and open symbol curves for the corresponding E+ samples.

Fig. 2. L-band (A); double normalization of endophytic-uninfected (E−) and endophytic-infected (E+) rice after a week’s treatment with 0, 50, 100, 150, and 200 ␮M concentrations of Pb2+ in Hoagland’s solution at F0 and FK , VOK = (Ft − F0 )/(FK − F0 ) and curves with symbols to difference kinetics, VOK of E+ versus E− on the logarithmic scale. K-band (B); double normalization of E+ and E− at F0 and FJ , VOJ = (Ft − F0 )/(FJ − F0 ) and curves with symbols to difference kinetics, VOJ of E+ versus E− on the logarithmic scale.

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Fig. 3. Quantum efficiency (␺Eo , ␾Eo and ␾Do ) and specific energy fluxes (TR0 /RC, ABS/RC and DI0 /RC) of endophytic-uninfected (E−) and endophytic-infected (E+) rice after a week’s treatment with 0, 50, 100, 150, and 200 ␮M concentrations of Pb2+ in Hoagland’s solution. The bars indicate standard deviations (n = 9). At the same concentration, an asterisk indicates significant difference in comparison with E− (*P < 0.05; **P < 0.01). The different letters indicate significant difference at P < 0.05 (LSD test).

3.4. Performance index and fluorescence parameters More information could be obtained from the OJIP test parameters shown in Fig 4. The ␾Po (Fv/Fm) is a parameter that expresses the maximum efficiency of PSII. The ␾Po decreased significantly with increasing concentrations of Pb2+ stress, while there was no difference between E+ and E− plant leaf samples (Fig. 4A). The reduction of intersystem electron acceptors (PIABS ) and the reduction of PSI end acceptors (PItot ) describe the energy conservation between photons absorbed by PSII [27]. PIABS and PItot first increased and then decreased with the increasing concentration of Pb2+ stress, whereas, the PIABS and PItot of E+ were significantly higher than those of the E− samples, except the 200 ␮M Pb2+ treatment (Fig. 4B,C). Sm reflected changes of the PSII acceptor site, which first increased and then decreased with the increasing concentration of Pb2+ stress. The Sm of E+ was significantly higher than that of E− samples under the 50, 100 and 150 ␮M Pb2+ stresses (Fig. 4D). The Mo and Wk increased with the increasing concentration of Pb2+ stress, except for the 200 ␮M Pb2+ treatment (Fig. 4E,F). Compared with the E− plants, Mo and Wk were lower in the E+ plants.

4. Discussion In the present study, the fluorescence induction trace shape was sensitive to Pb2+ stress in the leaf tissue of the rice plants,

which demonstrated the protective role of the endophytic infection against the toxicity of Pb2+ . Fluorescence intensities at the O, J, I and P steps were markedly reduced under Pb2+ stress. The quenching effect was decreased by the infection of the endophyte, and the O, J, I, and P steps were the highest in the leaves of E+ plant under 50 ␮M Pb2+ stress. Our previous study also reported that net photosynthetic rate of rice was significant increased by the endophytic infection under moderate (50 ␮M and 100 ␮M) Pb2+ stress [12]. The L-band revealed by such a subtraction is an indicator of the energetic connectivity (grouping) of the PSII units, which is higher when connectivity is lower [28]. Strasser et al. [17] reported that a higher energetic connectivity results in higher system stability and better utilization of the excitation energy. Therefore, Fig. 2A demonstrated that, the subtraction of the E+ samples from E− samples exhibited negative L-bands indicating the increase of the energetic connectivity. Yusuf et al. [18] observed a negative L-band when transgenic Brassica juncea plants were treated with CdCl2 (20 mM). Venkatesh et al. [19] also demonstrated that the subtraction of the WT samples from the TS samples exhibited negative L-bands in transgenic Solanum tuberosum treated with NaCl stress. It was proposed that Pb2+ inhibits the water oxidizing complex of PSII and the re-oxidation of the quinone acceptor, QA [26]. The K-band usually reflects the intactness of the oxygen-evolving complex (OEC) against stress treatments that cause changes in the functional PSII antenna size [17,29]. Significant change in the amplitude of the K-band (at 300 ␮s) was observed with the interaction

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Fig. 4. Performance index (PIABS and PITota ) and fluorescence parameters (␾Po , Sm, Mo and Wk ) of endophytic-uninfected (E−) and endophytic-infected (E+) rice after a week’s treatment with 0, 50, 100, 150, and 200 ␮M concentration of Pb2+ in Hoagland’s solution. The bars indicate standard deviations (n = 9). For a given concentration, an asterisk indicates a significant difference of E+ in comparison with E− (*P < 0.05; **P < 0.01). The different letters indicate significant difference at P < 0.05 (LSD test).

of Pb2+ stress and endophytic infection (Fig. 2B); the negative Kband indicates the intactness of the functional antenna of E+ under Pb2+ stress conditions. It has also been demonstrated previously that a negative K-band is an indication of better performance of plants under stress conditions [18,19]. The present data suggest that the endophytic infection may partially alleviate damage to the OEC of the rice seedlings exposed to Pb2+ stress. The decreases in ␾Eo and ␺Eo in the presence of Pb2+ indicates that the toxin inhibited the primary light reaction and the redox reactions after QA due to the interruption of the electron flow from QA toward PSI, and the endophytic infection protects the electron transport chain from the toxicity of Pb2+ . Similar results were reported in Cyanophyta exposed to Hg2+ stress; researchers have shown the inhibition of electron transport on both the donor side and acceptor sides [30]. Wang et al. [31] investigated the toxic effects of chromium on the photosystem in Microcystis aeruginoga and found that the quantum yield and the electron transport rate of PSII were greatly decreased under Cr (VI) stress. Pb2+ stress caused small increases in both the trapping rate of the RC (TR0 /RC) and the functional antenna size (ABS/RC), which caused a drastic increase in the dissipation flux (DI0 /RC) and the maximum quantum yield of non-photochemical de-excitation (␾Do ) (Fig. 3). The results implied that the cells are unable to regulate the light-harvesting capacity to adapt to stress [32]. More energy was dissipated to protect or maintain the cellular homeostasis, which may explain the decrease of cell growth under

environment stresses [33]. Zhang et al. [30] also reported that some reaction centers were transformed to dissipation sinks under Hg2+ stress. In the present study, ABS/RC, TR0 /RC, and DI0 /RC were lower in the E+ seedlings than in the E− under Pb2+ stress, which indicated that the inhibitory effect was alleviated by the infection of the endophyte. In the present study, the decreases in Sm and the increases in Mo showed that the activity of the electron transport beyond QA was inhibited in Pb2+ stressed leaves. The results indicated that Pb2+ stress also damaged the acceptor site of PSII. In addition, the changes of Sm and Mo were inhibited by the endophytic infection, indicating that endophytic infection can protect the acceptor site of PSII. Previous reports showed that Mo increased under heat stress [34]. WK was the donor site parameter of PSII, which expresses the changes in amplitude in the K step. Appearance of a K-step in the OJIP polyphasic fluorescence transient can be used as a specific indicator of injury to OEC [35]. In this study, we took advantage of the appearance of a K-step in the OJIP transient to examine if the endophytic infection-induced protection of, or improvement to, PSII during Pb2+ stress was related to OEC. WK in both E− and E+ plants significantly increased when these plants were exposed to Pb2+ stress, but WK in the E+ plants was lower than that of E−. Therefore, the above hypothesis is supported by the data. The performance indices PIABS and PItot are products of the terms expressing partial potentials for energy conservation at the sequential bifurcations from the photons absorbed by PSII to the reduction

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of intersystem electron acceptors and to the reduction of PSI end acceptors, respectively [36]. A dramatic decrease of PItot resulted not only from the loss of PSII activity but also from the damage to the PSI structure and function. The most direct factor related to the decrease of PIABS is a rapid lowering of the efficiency of the redox reaction of the electron transport chain [36]. The performance index PIABS was highly sensitive to environmental stress, such as heavy metals [37], which is in accordance with the results of our investigation of rice seedlings under Pb2+ stress. Decreases in PIABS and PItot indicate that the leaves were in a stressed condition and that their vitality had been damaged due to the rise in Pb2+ concentration. The endophytic infection restored the performance indices of the Pb2+ stressed rice seedlings, and it protected PIABS and PItot up to 200 ␮M Pb2+ . The above results showed that the structural modifications induced in E+ seedlings enable the photosynthetic machinery of those seedlings to perform better when they are exposed to Pb2+ stress. Our previous study also confirmed that the endophytic infection improved rice photosynthesis under moderate Pb2+ stress by enhancing photosynthetic pigment content and antioxidant enzymes activity relative to non-infected rice [12]. 5. Conclusions The present study investigated the effect of an endophyte on the Pb2+ tolerance of rice using the technique of Chl a fluorescence. The key findings were as follows: (1) the efficiency and stability of PSII are markedly affected by Pb2+ stress; (2) the endophyte could enhance the Pb2+ tolerance of rice by maintaining the PSII function; and (3) the donor and acceptor parameters of PSII in E+ rice showed little change compared with the E− rice. These results have both theoretical and applied importance. However, there is considerable variation in the Chl a fluorescence of plants under different environmental conditions such as other heavy metal stress, drought stress, temperature stress etc. In addition, to be able to fully understand the endophyte’s influence on Chl a fluorescence in plants, further detailed studies on the plant-endophyte interactions and the mechanisms of photosynthesis in field condition will be needed. Acknowledgments This research was financially supported by National Natural Science Foundation of China (Grant nos. 31270369, 31470398), and the Director Foundation of Eco-Environmental Research Center at Shenyang Normal University (EERC-K-201302). References [1] P.E. Gundel, L.A. Garibaldi, M.A. Martínez-Ghersa, C.M. Ghersa, Neotyphodium endophyte transmission to Lolium multiflorum seeds depends on the host plant fitness, Environ. Exp. Bot. 71 (2011) 359–366. [2] X.S. Hang, H.Y. Wang, J.M. Zhou, C.L. Ma, C.W. Du, X.Q. Chen, Risk assessment of potentially toxic element pollution in soils and rice (Oryza sativa) in a typical area of the Yangtze River Delta, Environ. Pollut. 157 (2009) 2542–2549. [3] P.N. Williams, M. Lei, G.X. Sun, Q. Huang, Y. Lu, C. Deacon, A.A. Meharg, Y.G. Zhu, Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: Hunan, China, Sci. Total Environ. 43 (2009) 637–642. [4] D.K. Gupta, F.T. Nicoloso, M.R.C. Schetinger, L.V. Rossato, L.B. Pereira, G.Y. Castro, S. Srivastava, R.D. Tripathi, Antioxidant defense mechanism in hydroponically grown Zea mays seedlings under moderate lead stress, J. Hazard Mater. 172 (2009) 479–484. [5] B. Li, X. Wang, X.L. Qi, L. Huang, Z.H. Ye, Identification of rice cultivars with low brown rice mixed cadmium and lead contents and their interactions with the micronutrients iron, zinc, nickel and manganese, J. Environ. Sci. 24 (2012) 1–9. [6] H. Cheng, M. Wang, M.H. Wong, Z. Ye, Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant Soil 375 (2014) 137–148. [7] P. Sharma, R.S. Dubey, Lead toxicity in plants, Braz. J. Plant Physiol. 17 (2005) 35–52.

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