Chromium (Cr) is one of the top seven toxic heavy metals, being ranked 21st among the abundantly found metals in the earth’s crust. A huge amount of Cr releases from various industries and Cr mines, which is accumulating in the agricultural land, is significantly reducing crop development, growth, and yield. Chromium mediates phytotoxicity either by direct interaction with different plant parts and metabolic pathways or it generates internal stress by inducing the accumulation of reactive oxygen species (ROS). Thus, the role of Cr-induced ROS in phytotoxicity is very important. In the current study, we reviewed the most recent publications regarding Cr-induced ROS, Cr-induced alteration in the enzymatic antioxidant system, Cr-induced lipid peroxidation and cell membrane damage, Cr-induced DNA damage and genotoxicity, Cr-induced ultrastructural changes in cell and subcellular level, and Cr-induced alterations in photosynthesis and photosynthetic apparatus. Taken together, we conclude that Cr-induced ROS and the suppression of the enzymatic antioxidant system actually mediate Cr-induced cytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants
- reactive oxygen species
- antioxidants
- cytotoxicity
- genotoxicity
- photosynthesis
1. Introduction
Plants that are exposed to unfavorable conditions produce reactive oxygen species (ROS) as a defense mechanism [1][2]. The hyperaccumulation of ROS generates endogenous stress that can damage plant growth and development [3]. Hydrogen peroxide (H
Plants that are exposed to unfavorable conditions produce reactive oxygen species (ROS) as a defense mechanism [15,16]. The hyperaccumulation of ROS generates endogenous stress that can damage plant growth and development [8]. Hydrogen peroxide (H
2
O
2
), superoxide anion (O
2−
), singlet oxygen (
1
O
2
), hydroxyl ion (HO
−
), peroxyl (RO
−
), alkoxyl (RO
−), and organic hydroperoxide (ROOH) are the various ROS that are found in plants [4][5][6]. Reactive oxygen species are produced in the mitochondria, peroxisome, and chloroplast as a byproduct of various biochemical reactions [6][7][8][9]. Plants mechanisms that are in the regulation of ROS level include ROS biosynthesis, enzymatic, and/or non-enzymatic ROS scavenging [3]. Heavy metals, such as lead (Pb), cadmium (Cd), aluminum (Al), nickel (Ni), and Cr, are reported for the enhancement in ROS productions and accumulation [3][7][10]. Various plant species that are exposed to toxic Cr level or industrial wastes containing the toxic level of Cr, showed induced ROS accumulation, as summarized in Table 1.
), and organic hydroperoxide (ROOH) are the various ROS that are found in plants [2,17,18]. Reactive oxygen species are produced in the mitochondria, peroxisome, and chloroplast as a byproduct of various biochemical reactions [18–21]. Plants mechanisms that are in the regulation of ROS level include ROS biosynthesis, enzymatic, and/or non-enzymatic ROS scavenging [8]. Heavy metals, such as lead (Pb), cadmium (Cd), aluminum (Al), nickel (Ni), and Cr, are reported for the enhancement in ROS productions and accumulation [8,19,22]. Various plant species that are exposed to toxic Cr level or industrial wastes containing the toxic level of Cr, showed induced ROS accumulation, as summarized in Table 1.
Table 1. Accumulations and investigations of various ROS species in numerous plant species exposed to Cr(VI) and/or Cr(III). Superoxide (O
2−
), hydrogen peroxide (H
2
O
2),
hydroxyl ion (HO
−
), and singlet oxygen (
1
O
2
).
|
Plant Species |
Common Name |
ROS Types |
Cr(VI) Concentration |
References |
|
Arabidopsis thaliana |
Arabidopsis |
O2−, H2O2 |
100–400 µM |
[8,23] |
|
Helianthus annuus |
Sunflower |
O2−, OH−, H2O2 |
20 mg/L & 20 mg/Kg |
[24–26] |
|
Zea mays |
Maize |
O2−, H2O2, OH− |
100–300 µM & 100–300 mg/Kg |
[27–32] |
|
Brassica juncea |
Indian mustard |
1O2, O2−, H2O2, OH− |
300 µM |
[17,33] |
|
Glycine max |
Soybean |
H2O2 |
400 mg/kg & 500 mg/kg Cr(III) |
[22] |
|
Oryza sativa |
Rice |
O2−, H2O2 |
80–200 µM |
[34–37] |
|
Amaranthus viridis & Amaranthus cruentus |
Green & Blood amaranth |
O2−, H2O2 |
50 µM |
[38] |
|
Chenopodium quinoa |
Quinoa |
H2O2 |
5 mM Cr(III) |
[39] |
|
Cucumis sativus |
Cucumber |
O2−, H2O2 |
200 µM |
[40] |
|
Brassica napus |
oilseed rape |
O2−, H2O2, OH− |
400 μM |
[41,42] |
|
Brassica campestris |
Cabbage |
O2− |
1 mg/L |
[43] |
|
Pisum sativum |
Pea |
O2−, H2O2 |
100 μM |
[44] |
|
Allium cepa |
Onion |
O2−, H2O2, OH− |
200 µM |
[45] |
|
Matricaria chamomilla |
Chamomile |
H2O2 |
120 µM Cr(III) |
[46] |
|
Lens culinaris |
Lentil |
H2O |
250 µM |
[47] |
|
Raphanus sativus |
Radish |
O2−, H2O2 |
1.2 mM |
[48] |
|
Pistia Stratiotes |
Lettuce |
H2O2 |
10 mM |
[49] |
|
Plant Species |
Common Name |
ROS Types |
Cr(VI) Concentration |
References |
|
Arabidopsis thaliana |
Arabidopsis |
O2−, H2O2 |
100–400 µM |
|
|
Helianthus annuus |
Sunflower |
O2−, OH−, H2O2 |
20 mg/L & 20 mg/Kg |
|
|
Zea mays |
Maize |
O2−, H2O2, OH− |
100–300 µM & 100–300 mg/Kg |
|
|
Brassica juncea |
Indian mustard |
1O2, O2−, H2O2, OH− |
300 µM |
|
|
Glycine max |
Soybean |
H2O2 |
400 mg/kg & 500 mg/kg Cr(III) |
[10] |
|
Oryza sativa |
Rice |
O2−, H2O2 |
80–200 µM |
|
|
Amaranthus viridis & Amaranthus cruentus |
Green & Blood amaranth |
O2−, H2O2 |
50 µM |
[26] |
|
Chenopodium quinoa |
Quinoa |
H2O2 |
5 mM Cr(III) |
[27] |
|
Cucumis sativus |
Cucumber |
O2−, H2O2 |
200 µM |
[28] |
|
Brassica napus |
oilseed rape |
O2−, H2O2, OH− |
400 μM |
|
|
Brassica campestris |
Cabbage |
O2− |
1 mg/L |
[31] |
|
Pisum sativum |
Pea |
O2−, H2O2 |
100 μM |
[32] |
|
Allium cepa |
Onion |
O2−, H2O2, OH− |
200 µM |
[33] |
|
Matricaria chamomilla |
Chamomile |
H2O2 |
120 µM Cr(III) |
[34] |
|
Lens culinaris |
Lentil |
H2O |
250 µM |
[35] |
|
Raphanus sativus |
Radish |
O2−, H2O2 |
1.2 mM |
[36] |
|
Pistia Stratiotes |
Lettuce |
H2O2 |
10 mM |
[37] |
2. Influence and response
Chromium-induced ROS accumulation mediates various physiological, biochemical, molecular, and developmental changes in plants [41]. These alterations in the physiological and biochemical process may be provoked by directly interacting with enzymes, lipids, proteins, and genetic material (DNA and/or RNA), or by Cr-induced ROS accumulation [8,50,51]. Cr direct interaction or Cr-induced ROS both mediated membrane damage, degradation and deactivation of genetic material, proteins, and enzymes, which resulted in the growth inhibition by the suppression cell division or activation programmed cell death [8,52,53].
Chromium-induced ROS accumulation mediates various physiological, biochemical, molecular, and developmental changes in plants [29]. These alterations in the physiological and biochemical process may be provoked by directly interacting with enzymes, lipids, proteins, and genetic material (DNA and/or RNA), or by Cr-induced ROS accumulation [3][38][39]. Cr direct interaction or Cr-induced ROS both mediated membrane damage, degradation and deactivation of genetic material, proteins, and enzymes, which resulted in the growth inhibition by the suppression cell division or activation programmed cell death [3][40][41].
Chromium-induced ROS mediates ultra-structural alteration in various plant tissues and irreversibly degrades biomolecules, except for DNA, cysteine, and methionine, which can be restored, in a dose-dependent and tissue-specific manner [23,45,49,54]. Reactive oxygen species are produced during the reduction reaction of Cr(VI) to Cr(III) and Fenton reaction. The catalytic power of Cr(III) is greater than iron (Fe), copper (Cu), cobalt (Co), manganese (Mn), and zinc (Zn) in the Fenton reaction [2,45,54,55]. The Cr involvement in such reactions is not well studied and some other intermediates and factors may also be involved in the Cr-induced ROS generation [8]. ROS mediated various physiological, biochemical, molecular, and ultrastructural changes, as shown in Figure 1.
Chromium-induced ROS mediates ultra-structural alteration in various plant tissues and irreversibly degrades biomolecules, except for DNA, cysteine, and methionine, which can be restored, in a dose-dependent and tissue-specific manner [11][33][37][42]. Reactive oxygen species are produced during the reduction reaction of Cr(VI) to Cr(III) and Fenton reaction. The catalytic power of Cr(III) is greater than iron (Fe), copper (Cu), cobalt (Co), manganese (Mn), and zinc (Zn) in the Fenton reaction [4][33][42][43]. The Cr involvement in such reactions is not well studied and some other intermediates and factors may also be involved in the Cr-induced ROS generation [11]. ROS mediated various physiological, biochemical, molecular, and ultrastructural changes, as shown in Figure 1.
Figure 1. Cr(VI)-induced ROS mediated alteration in plants: Cr(VI)-induces ROS accumulation by suppressing enzymatic antioxidant system, which damages cellular and subcellular membranes; induces ultrastructural changes in cell organelles such as mitochondria, plastids, and thylakoids; inhibits protein and enzymes at transcriptional or post-transcriptional level as well as degrades various enzymes and proteins; and DNA damages. All of these alterations inhibit photosynthesis and trigger and enhance necrosis, apoptosis, and programmed cell death, and significantly inhibit plant growth and development. Superoxide (O
Figure 1. Cr(VI)-induced ROS mediated alteration in plants: Cr(VI)-induces ROS accumulation by suppressing enzymatic antioxidant system, which damages cellular and subcellular membranes; induces ultrastructural changes in cell organelles such as mitochondria, plastids, and thylakoids; inhibits protein and enzymes at transcriptional or post-transcriptional level as well as degrades various enzymes and proteins; and DNA damages. All of these alterations inhibit photosynthesis and trigger and enhance necrosis, apoptosis, and programmed cell death, and significantly inhibit plant growth and development. Superoxide (O
2−
), hydrogen peroxide (H
2
O
2
), hydroxyl ion (HO
−
), and singlet oxygen (
1
O
2
). Ascorbate peroxidase (APX), catalase (CAT, dehydroascorbate reductase (DHAR), glutathione peroxidase (GPX), glutathione reductase (GR), glutathione S-transferase (GST), monodehydroascorbate reductase (MDHAR), peroxidase (POD), and superoxide dismutase (SOD). T-bars represent inhibition or suppression of the target, arrows represent promotion or upregulation of the target, and bold arrows represent the ultimate downstream result or impact of the process.