Mineral composition, chlorophyll fluorescence, and enzyme activity of maize cultivars with different tolerance to cadmium

ABSTRACT

Cadmium (Cd) toxicity harms photosynthesis, crop nutrition, and crop yield. Here, we submitted five maize cultivars with different tolerance to Cd to a toxic Cd concentration in the nutrient solution to assess their physiological responses. The study aimed at assessing the Cd effect on biomass and Cd and nutrient concentration in maize cultivars, evaluating how the photosynthetic is affected by Cd in maize cultivars exposed to Cd for different lengths of time, and understanding how the antioxidant defense system of different cultivars acts under Cd stress. To evaluate the effects of Cd stress, biomass, tolerance index, and plant mineral composition (N, P, K, Ca, Mg, Fe, Mn, Cu, and Zn), chlorophyll a fluorescence, and enzyme activity were determined. Cd toxicity reduced the biomass by 24% in the most tolerant cultivar and 41% in the most sensitive. The concentration of Fe, Mn, Cu, and Zn in the plants was reduced owing to the Cd application. In contrast, N, P, K, Ca, and Mg concentrations were unaffected. The chlorophyll a fluorescence variables were not affected by Cd. Superoxide dismutase, peroxidase, and polyphenol oxidase reduced their activities by 69, 20, and 14% in the sensitive CMS36 cultivar. For the tolerant cultivar (Gorutuba), Cd stress altered the peroxidase activity only. The data revealed distinct profiles in the accumulation of Cd, biomass yield, enzyme activity, and photosynthetic efficiency of cultivars. The physiological variables were sensible to physiological alterations and may help monitor Cd toxicity.

Key words
heavy metals; trace elements; soil pollution; food safety; micronutrients

INTRODUCTION

Environmental contamination by cadmium (Cd) is a global concern due to its high toxicity to living beings as Cd occupies the seventh position in the list of priority contaminants of the Agency for Toxic Substances and Disease Registry (ATSDR 2022). Cd in the soil can originate from natural sources (e.g., soil parent material) and anthropic sources, such as mining, solid waste disposal, and fertilizers and pesticide applications (Smolder and Mertens 2013). As one of the most mobile metals in soils and plants (Santos et al. 2014, Silva et al. 2021), Cd is easily absorbed by the roots and translocated to the shoots and edible parts of crops, entering the food chain and threatening animal and human health (Shi et al. 2015, Zhou et al. 2018). The agronomic countermeasures to decrease crop Cd include mainly soil management, selection of cultivars, or post-harvest approaches (Smolders et al. 2020).

Cd is toxic to plants even at low concentrations, causing a decrease in germination rates, reduced growth, chlorosis, root browning, and death (Franić et al. 2018). Part of the harmful effects of Cd is related to its influence on plant nutrition. In a study evaluating the growth of maize hybrids, the plant concentrations of Mn, Cu, and Zn, respectively, were reduced by 28, 40, and 42% in plants exposed to 15 µmol·L^-1 Cd in the nutrient solution (Akhtar et al. 2017). The application of Cd at the concentration of 50 µmol·L^-1 for maize plants decreases the concentrations of Ca (50%), Fe (42%), and Zn (36%) in the plants (Tanwir et al. 2015). Cd affects membrane permeability and competes with other metals, including some micronutrients, for specific transporters in plant roots, impairing nutrient absorption. Furthermore, some authors (Marques and Nascimento 2013, Sarwar et al. 2010) found these effects vary among plant varieties.

Photosynthesis is especially sensitive to Cd toxicity. Previous studies have reported that photosynthesis inhibition by Cd is related to damages in stomatal conductance, changes in the chloroplasts structure, electron transport chain, and activity of enzymes such as rubisco and phosphoenolpyruvate carboxylase in the Calvin cycle (Asgher et al. 2014, Krantev et al. 2008, Wang et al. 2019, Huihui et al. 2020). In this context, measurements such as chlorophyll a fluorescence are helpful to assess the deleterious effects of Cd, providing information on damage to photosynthetic activity before the appearance of visible symptoms (De Souza et al. 2021). Through a continuous flow of photons, the method consists of inducing and measuring the chlorophyll fluorescence of a dark-acclimatized leaf, generating data on initial fluorescence, maximum fluorescence, and variables related to the efficiency of the photosynthetic system. These data provide information about the functioning and structure of photosystem II and the flow of electrons in thylakoid membranes (Kalaji et al. 2011, Rastogi et al. 2020).

Although not directly involved in redox reactions, Cd causes increased activity of NADPH oxidases, culminating in the production of reactive oxygen species (ROS), such as superoxide (O₂^·-), hydrogen peroxide (H₂O₂), and hydroxyl radicals (·OH) (Jakubowska et al. 2015, Shah et al. 2020). ROS are products originating from aerobic metabolism with cell signaling function, but in high concentrations they cause protein degradation, lipid peroxidation, and DNA damage, with the destruction of nucleotides (Berni et al. 2019). Therefore, to mitigate oxidative stress, plants adopt gene modulation strategies to produce proteins and molecules capable of maintaining homeostasis. For example, plants activate the enzymatic and non-enzymatic antioxidant defense system, increasing the activity of superoxide dismutase (SOD), catalase (CAT), peroxidases (POD), polyphenol oxidase (PPO), glutathione transferase (GST), as well as ascorbate, glutathione, flavonoids, and tocopherols (AbdElgawad et al. 2020, Javed et al. 2017). However, some studies have shown a decrease in antioxidant enzyme activity depending on the level of Cd stress faced by the plant (Cunha and Nascimento 2009, Javed et al. 2017, Shah et al. 2020, Tanwir et al. 2021). In addition, the antioxidant enzyme activity seems to depend on the plant’s tolerance to Cd, which requires further studies with cultivars differently affected by the metal.

Maize is consumed by more than 4.6 billion people, and it is the third most important crop in cultivated areas worldwide, behind only wheat and rice (Ahmad et al. 2018, Blandino et al. 2017, Nyirenda et al. 2021). Therefore, the contamination of maize grains grown with metals potentially diminishes food safety and hence has become a concern in several countries (Liu et al. 2022, Sagbara et al. 2020, Tanwir et al. 2015). However, studies evaluating Cd tolerance and accumulation in different maize cultivars are still scarce (Tanwir et al. 2021). We hypothesize that cultivars with different Cd tolerances have different profiles of growth and physiological and metabolic parameters that could influence their Cd accumulation. Thus, the study had the following objectives: to assess the effect of Cd on biomass and Cd and nutrient concentration in five maize cultivars; to evaluate how the photosynthetic activity is affected by Cd in maize cultivars exposed to the metal for different lengths of time; and to understand how the antioxidant defense system acts in the cultivars most and least tolerant to Cd stress.

MATERIAL AND METHODS

Pot experiment

Five maize (Zea mays L.) cultivars were initially selected for the study: AG1051, Gorutuba, São José, Milho doce, and CMS36. Surface sterilization of the seeds was performed with 1% sodium hypochlorite and subsequent washing with distilled water. The seeds germinated in layers of paper towels saturated with a solution of 0.67 mmol·L^-1 Ca(NO₃)₂·4H₂O (Vilela and Anghinoni 1984). Four days after germination, healthy seedlings of uniform size (10–12 cm) were transferred to pots with 6 L of Hoagland’s nutrient solution (Hoagland and Arnon 1950), leaving one plant per pot. Deionized water was added to the pots daily to compensate for evapotranspiration losses; pH was kept at 5.50 ± 0.2, and the nutrient solution was changed weekly.

After 10 days of adaptation in hydroponic cultivation, plants of the five cultivars were submitted to concentrations of 0 µmol·L^-1 (control) and 17 µmol·L^-1 of Cd (toxic concentration of the metal established in a previous experiment), supplied in the form of CdCl2 in the nutrient solution. The Cd dose was determined to obtain a concentration capable of reducing by 40% the biomass production of maize cultivars (Nascimento and Fontes 2002). The experiment was carried out in a randomized block design, with three replications and a 2 × 5 factorial scheme, with two Cd concentrations and five maize cultivars totaling 30 experimental units. The biomass, Cd, and nutrient concentrations in roots and shoots were determined. For the evaluation of chlorophyll fluorescence, the factorial scheme was 2 × 5 × 4, with two concentrations of Cd, five maize cultivars, and four times exposure (one, two, five, and nine days) to the metal. A factorial scheme 2 × 2 (two levels of Cd and the maize cultivars most and least tolerant to Cd) was set up to evaluate the antioxidant enzymatic activity. The plants were collected after nine days of exposure to the metal (26th day of hydroponic cultivation), with three leaves fully expanded.

Biomass and tolerance index

The plants were collected and separated into roots and shoots. The fresh mass (FW) of each part of the plant was determined after washing and drying on paper towels. Then, the samples were dried in a forced circulation oven at 65°C for 72 hours to obtain the dry weight (DW).

The tolerance index (TI) (Wilkins 1957) was calculated to evaluate the tolerance of the cultivars to Cd. Such index is based on the sum of the dry mass of the shoot and root, ranging from 0 (maximum sensitivity) to 1 (maximum tolerance). The Eq. 1 calculated TI:

$$\mathrm{T}\mathrm{I}=\frac{\mathrm{D}\mathrm{W}\text{ in metal solution }}{\mathrm{D}\mathrm{W}\text{ in control solution }}$$ (1)

Where DW in metal solution is the dry mass of plants grown with Cd, while DW in control solution is the dry mass of plants grown in the control (without Cd).

Cadmium and nutrient concentrations

The contents of Cd, Ca, Mg, Cu, Mn, Zn, P, and K were determined from the digestion of 0.5 g of the plant sample with a solution of HNO₀ + H₂O₂ (3:1) in a microwave oven (Milestone – Ethos Easy) at 180°C for 10 min. Cd, Ca, Mg, Cu, Mn, and Zn were determined by inductively coupled plasma optical emission spectroscopy (ICP – OES Perkin Elmer Optima 7000 DV). Phosphorus was obtained by photocolorimetry and K by flame photometry. Nitrogen was determined by digesting 0.2 g of the samples in sulfuric acid at 350ºC, using the Kjeldahl method (Malavolta et al. 1989). The quality control used blanks and the reference sample SRM 1570a (Spinach Leaves) from the National Institute of Standards and Technology. The recovery of the elements in the reference material varied between 80 and 95%.

Chlorophyll a fluorescence

Four determinations of chlorophyll fluorescence were performed during the experiment: one, two, five, and nine days after exposure (DAE) to Cd. The determination took place in the middle third of the first fully expanded leaf. Clips were used to adapt the leaves to the dark for 30 min to reach the maximum oxidation state of the photosynthetic electron transport system. Then, the leaves were exposed to pulses of high-intensity saturated light (2,250 mmil·m^-2·s^-1), and fluorescence was obtained using a Fluorpen fluorometer, FP 100 model (Photon Systems Instruments).

By determining the fast kinetic fluorescence, the initial fluorescence (Fo) and the maximum fluorescence (Fm) were obtained, from their variable fluorescence ratios (Fv = Fm – Fo), the photochemical efficiency of photosystem II (Fv/Fm), the specific absorption flux per reaction center (ABS/RC), the electron transport flux per reaction center (ETo/RC) and the energy dissipated per reaction center (Dio/RC) (Jafarinia and Shariati 2012).

Antioxidative enzyme activity assay

The antioxidant enzyme activity was evaluated in the cultivars Gorutuba and CMS36, the most and the least tolerant to Cd, respectively, according to their respective TI. The first fully expanded leaf was collected on the ninth day of exposure to Cd, packed in aluminum foil, and refrigerated to determine the antioxidant enzymatic activity.

To obtain the enzymatic extracts of CAT, GST, POD and SOD, a sample of 0.3 g of the leaf in a 0.1 mol·L^-1 potassium phosphate buffer solution (pH 6.8) was centrifuged at 4°C for 12,000 g for 30 min. The enzymatic extract of polyphenol oxidase (PPO) was obtained by homogenizing 0.3 g of the sample with 0.2 mol·L^-1 phosphate buffer (pH = 6.0) and centrifuging at 4°C in 10,000 g for 21 min. Enzymatic determinations in the supernatants were performed by spectrometry.

CAT activity was assessed by monitoring H₂O₂ consumption at 240 nm (Aebi 1984). GST activity was analyzed by the absorbance of the reduced glutathione conjugate and 1-chloro-2,4-dinitrobenzene (CDNB) at 340 nm (Wu et al. 1996). The POD activity was obtained by the oxidation of pyrogallol at 430 nm (Teisseire and Guy 2000). SOD was assessed by monitoring the photoreduction of nitroblue tetrazolium (NBT) at 540 nm (Giannopolitis and Ries 1977). Polyphenoloxidase was determined at 420 nm, evaluating the oxidation of the catechol substrate (Duangmal and Apenten 1999). The protein content in the extracts was calculated according to the method described by Bradford (1976).

Statistical analysis

Results are presented as mean ± standard deviation. Data were submitted to analysis of variance (ANOVA), and, in cases with significant treatment effects, a Tukey’s means comparison test was performed (p < 0.05).

RESULTS AND DISCUSSION

Biomass production and cadmium tolerance

The biomass of the cultivars was significantly reduced by Cd (p ≤ 0.01). The dry shoot biomass decreased by 41% in CMS36, 40% in AG1051, 27% in São José, and 24% in Milho Doce (Fig. 1a). The reductions in root biomass were 27 (AG1051) and 40% (CMS36), with no significant difference from the control for the other cultivars (Fig. 1b). For the fresh biomass of the aerial part, there were decreases of 41% in São José, 42% in Milho Doce, 37% in AG1051, 36% in CMS36, and 24% in Gorutuba due to Cd toxicity (Fig. 1c), while for the roots the reductions were 55% (CMS36), 38% (São José), 37% (Milho Doce) and 31% (AG1051) (Fig. 1d).

Figure 1
(a) Shoot dry, (b) root dry, (c) shoot fresh, (d) root fresh, (e) weights and tolerance index of maize plants of cv. AG1051 (V1), Gorutuba (V2), São José (V3), Milho doce (V4), and CMS36 (V5) grown in nutritive solution with 0 (control) and 17 µmol·L^-1 cadmium (Cd). Values are averages ± standard error. Significant differences in Cd exposure in each cultivar are represented by different letters (p < 0.05).

Our data are consistent with results found by Tanwir et al. (2021), who evaluated the toxic effect of the dose of 30 µmol·L^-1 of Cd on 10 maize cultivars and observed an average reduction of 35% in biomass. Similarly, Silva et al. (2012) found reductions of up to 69% in the biomass of maize plants exposed to the dose of 53 µmol·L^-1 of Cd. Growth inhibition is the main symptom of Cd disturbances in the plant’s metabolic and physiological processes (Cunha et al. 2008, Silva et al. 2021). The reduction of biomass is related to conformational changes in biomolecules caused by Cd, reduction of enzymatic activity, alterations in the absorption, transport, and distribution of nutrients and water, destruction of chloroplast structure, and accumulation of ROS (Liu, X. et al. 2020, Marques and Nascimento 2013, Yang et al. 2020.

Cd did not affect the biomass of cultivar Gorutuba, which had the highest TI (0.84) and was considered more tolerant to the heavy metal (Fig. 1e). In contrast, cultivar CMS36 had the lowest TI (0.64), indicating lower Cd tolerance. These differences are expected since tolerance to the deleterious effects of Cd is dependent on the species, cultivar, or even the specific tissue in which the metal is located in the plant (He et al. 2015).

Symptoms of Cd toxicity showed different intensities among cultivars, being seen primarily in cultivars with higher biomass (AG105, Milho Doce, and CMS36). In the aerial part, the symptoms manifested mainly in the older leaves, with chlorotic spots that evolved to necrotic. In addition, there was reduction in the volume and production of secondary roots. Other studies have reported similar symptoms in maize plants (Nascimento and Fontes 2002, Yang et al. 1996). Symptoms such as chlorosis and necrosis caused by Cd may be related to reduced absorption of nutrients structurally or functionally associated with chlorophyll, such as K, Mn, Cu, and Fe (Wahid and Ghani 2008).

Cadmium concentration in plants

The Cd content in different parts of the plants increased significantly with the application of Cd in the nutrient solution, with higher values in the roots (Fig. 2). The concentration of Cd in the roots significantly differed between the evaluated cultivars (p < 0.01), with CMS36 showing the highest metal content (976 mg·kg^-1). This concentration was 40, 37, 28, and 8% higher than in cultivars AG1051, Gorutuba, São José, and Milho Doce, respectively. Interestingly, no differences were observed between cultivars in the concentration of Cd in the shoots, probably due to the differences in roots and shoot biomass among cultivars (Fig. 1) and the ability of each cultivar to exclude Cd from uptake. For example, the most tolerant cultivar (Gorutuba) avoided Cd uptake and hence restricted its translocation to shoots (Fig. 2); on the other hand, the most sensitive cultivar (CMS36) absorbed high amounts of Cd, but it managed to keep it in roots, avoiding translocation.

Figure 2
Cadmium concentration in maize shoots and roots of cv. AG1051 (V1), Gorutuba (V2), São José (V3), Milho doce (V4), and CMS36 (V5) grown in nutritive solution with 0 (control) and 17 µmol·L^-1 Cd. Values are averages ± standard error. Significant differences in Cd concentration between cultivars are represented by different letters (p < 0.01).

Such results corroborate the findings of other authors that roots are the first barrier to restraining the Cd translocation to shoots. Higher concentrations of Cd in maize roots than in shoots have been reported in other studies (Javed et al. 2017, Silva et al. 2021, Veloso et al. 2021). In general, the preferential allocation of heavy metals to roots is a tolerance mechanism, as it limits translocation to the shoots (Gallego et al. 2012). Cadmium retention in roots occurs due to the metal-binding to polysaccharides, proteins, phytochelatins, and thiol groups of glutathione, which sequester the metal in the vacuole (Hasanuzzaman et al. 2017, Kabir et al. 2021).

The lower concentration of Cd in the roots of the cultivar Gorutuba (higher tolerance) suggests the action of a mechanism of exclusion of Cd from uptake, which justifies the smaller reduction of biomass in this cultivar and its greater tolerance. Similarly, Tanwir et al. (2015) found that, at the highest dose of exposure of plants to Cd (50 µmol·L^-1), the tolerant cultivar had a Cd concentration 1.8-fold lower than the sensitive cultivar. Evaluating wheat cultivars in hydroponic cultivation, Zhang et al. (2022) observed that, when exposed to 60 µmol·L^-1 of Cd, the tolerant cultivar had a metal concentration 1.5-fold lower than the sensitive cultivar. Once again, this fact seems to corroborate that excluding Cd from root uptake rather than internal mechanisms plays a crucial role in the Cd tolerance posed by different maize cultivars.

The lower concentration of Cd in the tolerant cultivar (Gorutuba) suggests higher food safety for the produced grains. Liu, X. et al. (2020) observed that, with a 60% reduction in the Cd concentration in the roots and shoots of maize plants, there was a decline in the same proportion of Cd concentration in the grains. In analyzing the accumulation of Zn and Cd in maize grains, Guo et al. (2011) reported that the cultivar with the lowest concentration of Cd in the shoots produced grains with a Cd content 45% lower than found in the other cultivars evaluated.

Nutrient concentration in plants

The macronutrients N, P, K, Ca, and Mg were the least affected by Cd and did not show differences in concentration between cultivars (Fig. 3). The levels of N and Ca showed reduction in the shoots of only two out of the five cultivars tested. Phosphorus and K showed significant differences only in the root, and Cd promoted a decrease of 28% in P and K contents in the Milho Doce cultivar. The concentration of Mg in the cultivars was affected by cadmium.

Figure 3
Nutrient concentration in shoot and root of maize plants of cv. AG1051 (V1), Gorutuba (V2), São José (V3), Milho doce (V4), and CMS36 (V5) grown in nutritive solution with 0 (control) and 17 µmol·L^-1 cadmium (Cd). Values are averages ± standard error. Significant differences for Cd exposure in nutrient concentration in each cultivar are represented by different letters (p < 0.05).

The addition of Cd to the solution caused a 30% decrease in the Fe concentrations in the shoots of the cultivars tested (Fig. 3). In contrast to the other cultivars, the Fe content in the Gorutuba cultivar was increased by 65%. The Mn content in the shoots was affected by Cd only in the cultivar CMS36. However, Cd reduced by 70% the Mn content of the roots for all cultivars. In the shoots, Cd reduced the Cu content of AG1051, Gorutuba, Milho Doce, and CMS36. On the other hand, root Cu concentrations in all cultivars were doubled by applying Cd. The Zn content was reduced in the cultivars AG1051, Gorutuba, Milho Doce, and CMS36 only in the roots.

The antagonistic effect of Cd on plant nutrients has been pointed out for rice (Liang et al. 2022), soybean (Cui et al. 2019), alfalfa (Zhang et al. 2019), and sorghum (Jawad Hassan et al. 2020). Cd affects the use, storage, and distribution of essential and non-essential elements by inhibiting and competing for nutrient channels and transporters, promoting a deleterious effect on plant growth (Nedjimi and Daoud 2009, Tran and Popova 2013). Similar to our results, Javed et al. (2017) reported decreased Fe uptake in maize cultivars treated with cadmium. The absorption of Fe can be affected by Cd because Cd reduces the activity of the IRTI transporter (iron-regulated transporter 1) (Greger et al. 2016). On the other hand, in a study evaluating Fe doses in the attenuation of Cd toxic effects on maize, Zhang et al. (2021) observed that micronutrient supplementation to the plant can mitigate the Cd harmful effects. In this context, the higher concentration of Fe observed in the roots of the cultivar Gorutuba under treatment with Cd may contribute to tolerance.

The reduction in the concentration of Mn (67%) and Zn (50%) in maize plants treated with Cd after 10 days of cultivation was reported by Wang et al. (2007). In contrast to our data, these authors observed reduction of up to 57% in copper contents. Cd competes for the transporters of Mn and Zn, called ZIP (ZRT- and IRT-like proteins) and natural resistance-associated macrophage protein, reducing the absorption of these nutrients (Gonçalves et al. 2009). In contrast, Cd can increase the uptake of Cu by stimulating the activity of the specific transporter copper transporter protein (Andrés-Colás et al. 2010), justifying the increase in the contents of Cu in all cultivars.

Chlorophyll a fluorescence

The variable Fv/Fm showed no difference between cultivars, exposure times, and Cd treatment (Fig. 4). However, except for the Gorutuba cultivar, which showed reduction in Fv/Fm only after the fifth day of exposure, the cultivars AG105, São José, Milho Doce, and CMS36 tended to decline in Fv/Fm throughout cultivation under Cd stress. The decrease in the Fv/Fm ratio points to photosynthetic inhibition. This variable estimates the maximum quantum efficiency of PSII photochemical activity when all reaction centers are open, detecting damage from biotic and abiotic stresses (Baker and Rosenqvist 2004).

Figure 4
Maximum quantum yield of photochemical efficiency of photosystem II (Fv/Fm) of maize cultivars grown in nutritive solution under cadmium treatment, measured on different days after exposure (DAE).

In contrast to our data, Zhao et al. (2018), evaluating the effect of growth regulator and Cd on enzymatic activity and chlorophyll, observed that Cd significantly affected the Fv/Fm ratio (0.75), which was 5% lower than the control. A similar result was reported by Qu et al. (2019), who, evaluating characteristics of the photosynthetic apparatus and the antioxidant defense system in maize plants, found an Fv/Fm ratio of 0.70 in the Cd treatment and 0.80 in the control. Silva et al. (2012), evaluating Cd phytotoxicity, observed a drop of 13% in the quantum yield of PSII in plants under Cd stress. All cultivars exposed or not to Cd showed an Fv/Fm ratio lower than 0.75, which indicates that they are under some stress (Bolhar-Nordenkampf et al. 1989). This fact may have masked the effects of Cd on variables related to the fast kinetics of chlorophyll fluorescence. According to Gonçalves et al. (2010), the factors that can stress the plant and influence the effects of treatments on the Fv/Fm ratio are the evaluation time, air humidity, and, mainly, temperature.

The specific absorption flux (ABS/RC) and electron transport per reaction center (ET₀/CR) did not vary between Cd treatments, cultivars, or time of exposure to the metal (Fig. 5). However, in contrast to our results, Cd toxicity caused an increase in ABS/RC and a reduction in ET0/CR in tomato (Singh et al. 2018), lettuce (Wang et al. 2019), sorghum (Xue et al. 2018), and maize (Franić et al. 2018). The increase in ABS/RC can be attributed to the increase in antenna size of an active, reactive center or the inactivity of a fraction of the RCs (Mehtas et al. 2010). On the other hand, the reduction in ET0/CR may represent damage to thylakoid membranes, partially blocking electron transport in the lipid-protein bilayer and impairing the activity of the complex (Ambede et al. 2012).

Figure 5
Absorption flux per reaction center (ABS/RC), electron flux per reaction center (ET_o/RC), and dissipation energy flux per reaction center (DI_o/RC) of maize cultivars under cadmium (Cd) stress, measured in different days after exposure (DAE). Values are averages ± standard error.

DI₀/RC did not show a significant difference between treatments. However, cultivar Gorutuba had high DI₀/RC in the first days of exposure to Cd, unlike the cultivars AG1051, São José, and Milho Doce, which showed increases in DI₀/RC throughout the cultivation. DI₀/RC characterizes a mechanism of protection of leaves from photo-oxidation, as its increase indicates that the energy absorbed in excess was dissipated instead of used to reduce quinone, decreasing the formation of ROS (Franić et al. 2018, Wang et al. 2019). Despite the non-significance, the behavior observed in Gorutuba for DI0/RC may suggest earlier activation of defense mechanisms of the photosynthetic apparatus against Cd toxicity compared to the other cultivars.

Antioxidative enzyme activity

The most sensitive and the most tolerant cultivars to Cd had their enzymatic activity evaluated. Except for the GSH enzyme, the antioxidant activity of the SOD, CAT, POD, and PPO enzymes varied significantly with the application of Cd and cultivars (p < 0.05) (Table 1). The SOD activity in the two cultivars was increased by Cd compared to control, the increase being more prominent in CMS36 (227%) than in Gorutuba (16%). The highest SOD activity under Cd stress was measured in the cultivar CMS36 (332.81 U·mg^-1 protein), 69% higher than in Gorutuba. Our results agree with data from Tanwir et al. (2021), who reported an increase in SOD activity (58–73%) in maize plants with increasing doses of Cd in the solution, in addition to finding the more significant activity of antioxidant enzymes in the cultivar with lower tolerance to Cd. SOD acts in the dismutation of superoxide (O₂·^-), appearing in plants under the groups iron SOD (Fe-SOD) in chloroplasts, manganese SOD (Mn-SOD) in mitochondria and peroxisomes, and copper-zinc SOD (Cu-Zn-SOD) in the cytosol, chloroplasts, and extracellular spaces. SOD activity depends on the heavy metal location and where O₂·^- production occurs in the plant cell, which may differ between cultivars (Alscher et al. 2002). Due to the lower tolerance to Cd, the higher SOD activity in CMS36 may indicate a defense strategy for damage caused in more tissues due to a higher O₂·^- formation compared to what occurs in Gorutuba.

Table 1
Superoxide dismutase (SOD), Catalase (CAT), peroxidases (POD), Polyphenol oxidase (PPO), Glutathione transferase (GST) of two maize cultivars after nine days of growing under 0 (control) and 17 µmol·L^-1 cadmium (Cd)^*.

Cd treatment	SOD			CAT			POD			PPO			GST
	cv. Gorutuba	cv. CMS36		cv. Gorutuba	cv. CMS36		cv. Gorutuba	cv. CMS36		cv. Gorutuba	cv. CMS36		cv. Gorutuba	cv. CMS36
µmol·L-1	- - - - - - - - - - - - - - - - - - - -U·mg-1 protein- - - - - - - - - - - - - - - - - - - -									µmol catecol· min-1·mg-1 F.W.			µmol·min-1·mg-1 protein
0	169.02 ± 13.17 Ba	101.55 ± 1.91 Bb		360.53 ± 38.54 Aa	291.36 ± 35.59 Ab		15.93 ± 0.18 Ab	20.09 ± 0.59 Aa		14.85 ± 0.18 Aa	15.42 ± 0.33 Aa		83,496.08 ± 4,074.94 Aa	84,196.78 ± 1,836.00 Aa
17	196.57 ± 7.59 Ab	332.81 ± 19.54 Aa		237.66 ± 46.37 Ba	199.03 ± 50.41 Bb		16.92 ± 1.01 Ab	19.43 ± 1.08 Aa		13.05 ± 1.01 Bb	15.00 ± 0.25 Aa		77,880.74 ± 11,864.72 Aa	84,690.24 ± 2,172.72 Aa

• ^*
  Averages followed by the same lower case letter in the row and the same upper case letter in the column, for each respective parameter, are not significantly different by the Tukey’s test (p < 0.05).

CD reduced CAT activity by 34 and 31% in Gorutuba and CMS36. The CAT activity in Gorutuba was 21% higher than in CMS36, regardless of the Cd presence. Our data agree with Javed et al. (2017), who evaluated the effect of Cd on the exudation of organic acids from maize cultivars and observed reductions in CAT activity between 73 and 83% with increasing Cd contents in the soil. Similarly, Shah et al. (2020) reported that Cd stress reduced CAT activity in Brassica oleracea plants by 25%. CAT is responsible for the deterioration of the toxic species hydrogen peroxide (H₂O₂), whose formation is favored by Cd (Franić et al. 2018). The significantly higher CAT values in Gorutuba indicate a more remarkable ability of the cultivar to deal with the oxidative stress caused by H₂O₂.

POD was not affected by exposure to Cd, but, concerning cultivars, the activity of peroxidases in CMS36 was on average 20% higher than that found in Gorutuba. These results contrast with Tanwir et al. (2021), who observed higher POD activities in more tolerant maize cultivars. However, Lian et al. (2019) reported 12% higher POD activity in the lesser Cd-tolerant rice cultivars. Barbosa et al. (2014) state that POD exists in many isoforms; some are constitutively expressed while environmental stresses induce others. Thus, low POD activities indicate mild stress and high activities indicate more severe symptoms. Therefore, the higher POD activity observed in CMS36 may indicate a higher level of physiological disorders.

Cd significantly affected PPO activity only in the cultivar Gorutuba, which showed a 12% decrease compared to the control. Under Cd stress, the PPO activity in Gorutuba was 14% lower than in CMS36. In contrast, increases in PPO activity by exposure to Cd were observed in Solanum nigrum (Khan et al. 2015), sunflower (Aghababaei and Raiesi 2015), and blackberry (Dai et al. 2020) plants. Our data suggest that the PPO enzyme was less effective in defending against oxidative damage in Gorutuba. This condition may be related to the genetic trait since Gorutuba showed higher tolerance to Cd even with lower enzyme activity.

CONCLUSION

We evaluated the physiological and metabolic parameters of five maize cultivars under Cd stress to select the most tolerant and least tolerant to the metal. Regardless of the degree of tolerance, all cultivars tested had their biomass reduced by adding Cd to the solution, which demonstrates the high phytotoxicity of the element. Interestingly, the Cd concentrations in the shoots of the plants were similar, while the Cd concentrations in the roots were significantly different between the cultivars. This result indicates that, in general, avoiding the uptake of Cd by the roots is the primary mechanism these cultivars use to deal with high levels of Cd in the medium. According to the TI, the cultivars Gorutuba and CMS36 were selected as the most and least tolerant of Cd stress. In addition to the exclusion mechanism, the cultivar Gorutuba showed a more efficient antioxidant enzymatic defense system and less reduction in the concentration of micronutrients associated with photosynthetic efficiency. Further studies on the mechanisms that govern such differences can aid in the understanding and breeding of maize cultivars that are more tolerant to Cd and safer for human and animal consumption.

ACKNOWLEDGMENTS

Not applicable.

• How to cite: Silva, J. R. and Nascimento, C. W. A. (2024). Mineral composition, chlorophyll fluorescence, and enzyme activity of maize cultivars with different tolerance to cadmium. Bragantia, 83, e20230182. https://doi.org/10.1590/1678-4499.20230182

DATA AVAILABILITY STATEMENT

The datasets generated during and/or analyzed are available from the corresponding author upon reasonable request.

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Section Editor: Gabriel Constantino Blain https://orcid.org/0000-0001-8832-7734

Publication Dates

• Publication in this collection
  27 Sept 2024
• Date of issue
  2024

History

• Received
  11 Apr 2024
• Accepted
  15 July 2024