Your browser does not fully support modern features. Please upgrade for a smoother experience.
Chromium-Induced Oxidative Stress in Plants: Comparison
Please note this is a comparison between Version 2 by Catherine Yang and Version 1 by Abdul Wakeel Umar.

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

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

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

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 [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.

), 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.

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

[3][11]

Helianthus annuus

Sunflower

O2, OH, H2O2

20 mg/L & 20 mg/Kg

[12][13][14]

Zea mays

Maize

O2, H2O2, OH

100–300 µM & 100–300 mg/Kg

[15][16][17][18][19][20]

Brassica juncea

Indian mustard

1O2, O2, H2O2, OH

300 µM

[5][21]

Glycine max

Soybean

H2O2

400 mg/kg & 500 mg/kg Cr(III)

[10]

Oryza sativa

Rice

O2, H2O2

80–200 µM

[22][23][24][25]

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

[29][30]

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

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.

References

  1. Cui, W.; Wang, H.; Song, J.; Cao, X.; Rogers, H.J.; Francis, D.; Jia, C.; Sun, L.; Hou, M.; Yang, Y.; et al. Cell cycle arrest mediated by Cd-induced DNA damage in Arabidopsis root tips. Ecotoxicol. Environ. Saf. 2017, 145, 569–574.
  2. Gielen, H.; Vangronsveld, J.; Cuypers, A. Cd-induced Cu deficiency responses in Arabidopsis thaliana: Are phytochelatins involved? Plant Cell Environ. 2017, 40, 390–400.
  3. Wakeel, A.; Ali, I.; Wu, M.; Kkan, A.R.; Jan, M.; Ali, A.; Liu, Y.; Ge, S.; Wu, J.; Gan, Y. Ethylene mediates dichromate-induced oxidative stress and regulation of the enzymatic antioxidant system-related transcriptome in Arabidopsis thaliana. Environ. Exp. Bot. 2019, 161, 166–179.
  4. Shahid, M.; Shamshad, S.; Rafiq, M.; Khalid, S.; Bibi, I.; Niazi, N.K.; Dumat, C.; Rashid, M.I. Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: A review. Chemosphere 2017, 178, 513–533.
  5. Al Mahmud, J.; Hasanuzzaman, M.; Nahar, K.; Rahman, A.; Hossain, M.S.; Fujita, M. Maleic acid assisted improvement of metal chelation and antioxidant metabolism confers chromium tolerance in Brassica juncea L. Ecotoxicol. Environ. Saf. 2017, 144, 216–226.
  6. Shahid, M.; Dumat, C.; Khalid, S.; Niazi, N.K.; Antunes, P.M.C. Cadmium Bioavailability, Uptake, Toxicity and Detoxification in Soil-Plant System. In Reviews of Environmental Contamination and Toxicology; DeVoogt, P., Ed.; Springer: Cham, Germany, 2017; Volume 241, pp. 73–137.
  7. Abbas, G.; Murtaza, B.; Bibi, I.; Shahid, M.; Niazi, N.K.; Khan, M.I.; Amjad, M.; Hussain, M.; Natasha. Arsenic Uptake, Toxicity, Detoxification, and Speciation in Plants: Physiological, Biochemical, and Molecular Aspects. Int. J. Environ. Res. Public Health 2018, 15, 59.
  8. Chen, Q.; Wu, K.; Tang, Z.; Guo, Q.; Guo, X.; Wang, H. Exogenous ethylene enhanced the cadmium resistance and changed the alkaloid biosynthesis in Catharanthus roseus seedlings. Acta Physiol. Plant. 2017, 39, 267.
  9. Hasanuzzaman, M.; Nahar, K.; Gill, S.S.; Alharby, H.F.; Razafindrabe, B.H.N.; Fujita, M. Hydrogen Peroxide Pretreatment Mitigates Cadmium-Induced Oxidative Stress in Brassica napus L.: An Intrinsic Study on Antioxidant Defense and Glyoxalase Systems. Front. Plant Sci. 2017, 8, 115.
  10. Balasaraswathi, K.; Jayaveni, S.; Sridevi, J.; Sujatha, D.; Aaron, K.P.; Rose, C. Cr-induced cellular injury and necrosis in Glycine max L.: Biochemical mechanism of oxidative damage in chloroplast. Plant Physiol. Biochem. 2017, 118, 653–666.
  11. Eleftheriou, E.P.; Adamakis, I.-D.S.; Panteris, E.; Fatsiou, M. Chromium-Induced Ultrastructural Changes and Oxidative Stress in Roots of Arabidopsis thaliana. Int. J. Mol. Sci. 2015, 16, 15852–15871.
  12. Farid, M.; Ali, S.; Rizwan, M.; Ali, Q.; Saeed, R.; Nasir, T.; Abbasi, G.H.; Rehmani, M.I.A.; Ata-Ul-Karim, S.T.; Bukhari, S.A.H.; et al. Phyto-management of chromium contaminated soils through sunflower under exogenously applied 5-aminolevulinic acid. Ecotoxicol. Environ. Saf. 2018, 151, 255–265.
  13. Farid, M.; Ali, S.; Akram, N.A.; Rizwan, M.; Abbas, F.; Bukhari, S.A.H.; Saeed, R. Phyto-management of Cr-contaminated soils by sunflower hybrids: Physiological and biochemical response and metal extractability under Cr stress. Environ. Sci. Pollut. Res. 2017, 24, 16845–16859.
  14. Farid, M.; Ali, S.; Rizwan, M.; Ali, Q.; Abbas, F.; Bukhari, S.A.H.; Saeed, R.; Wu, L. Citric acid assisted phytoextraction of chromium by sunflower; morpho-physiological and biochemical alterations in plants. Ecotoxicol. Environ. Saf. 2017, 145, 90–102.
  15. Kharbech, O.; Houmani, H.; Chaoui, A.; Corpas, F.J. Alleviation of Cr(VI)-induced oxidative stress in maize (Zea mays L.) seedlings by NO and H2S donors through differential organ-dependent regulation of ROS and NADPH-recycling metabolisms. J. Plant Physiol. 2017, 219, 71–80.
  16. Anjum, S.A.; Ashraf, U.; Khan, I.; Tanveer, M.; Shahid, M.; Shakoor, A.; Wang, L. Phyto-Toxicity of Chromium in Maize: Oxidative Damage, Osmolyte Accumulation, Anti-Oxidative Defense and Chromium Uptake. Pedosphere 2017, 27, 262–273.
  17. Singh, V.P.; Kumar, J.; Singh, M.; Singh, S.; Prasad, S.M.; Dwivedi, R.; Singh, M.P.V.V.B. Role of salicylic acid-seed priming in the regulation of chromium(VI) and UV-B toxicity in maize seedlings. Plant Growth Regul. 2016, 78, 79–91.
  18. Islam, F.; Yasmeen, T.; Arif, M.S.; Riaz, M.; Shahzad, S.M.; Imran, Q.; Ali, I. Combined ability of chromium(Cr) tolerant plant growth promoting bacteria (PGPB), and salicylic acid (SA) in attenuation of chromium stress in maize plants. Plant Physiol. Biochem. 2016, 108, 456–467.
  19. Singh, S.; Srivastava, P.K.; Kumar, D.; Tripathi, D.K.; Chauhan, D.K.; Prasad, S.M. Morpho-anatomical and biochemical adapting strategies of maize (Zea mays L.) seedlings against lead and chromium stresses. Biocatal. Agric. Biotechnol. 2015, 4, 286–295.
  20. Maiti, S.; Ghosh, N.; Mandal, C.; Das, K.; Dey, N.; Adak, M.K. Responses of the maize plant to chromium stress with reference to antioxidation activity. Braz. J. Plant Physiol. 2012, 24, 203–212.
  21. Handa, N.; Kohli, S.K.; Thukral, A.K.; Arora, S.; Bhardwaj, R. Role of Se(VI) in counteracting oxidative damage in Brassica juncea L. under Cr(VI) stress. Acta Physiol. Plant. 2017, 39, 51.
  22. Chen, Q.; Zhang, X.; Liu, Y.; Wei, J.; Shen, W.; Shen, Z.; Cui, J. Hemin-mediated alleviation of zinc, lead and chromium toxicity is associated with elevated photosynthesis, antioxidative capacity; suppressed metal uptake and oxidative stress in rice seedlings. Plant Growth Regul. 2017, 81, 253–264.
  23. Ma, J.; Lv, C.; Xu, M.; Chen, G.; Lv, C.; Gao, Z. Photosynthesis performance, antioxidant enzymes, and ultrastructural analyses of rice seedlings under chromium stress. Environ. Sci. Pollut. Res. 2016, 23, 1768–1778.
  24. Zeng, F.; Wu, X.; Qiu, B.; Wu, F.; Jiang, L.; Zhang, G. Physiological and proteomic alterations in rice (Oryza sativa L.) seedlings under hexavalent chromium stress. Planta 2014, 240, 291–308.
  25. Ngoc-Nam, T.; Huang, T.-L.; Chi, W.-C.; Fu, S.-F.; Chen, C.-C.; Huang, H.-J. Chromium stress response effect on signal transduction and expression of signaling genes in rice. Physiol. Plant. 2014, 150, 205–224.
  26. Bashri, G.; Parihar, P.; Singh, R.; Singh, S.; Singh, V.P.; Prasad, S.M. Physiological and biochemical characterization of two Amaranthus species under Cr(VI) stress differing in Cr(VI) tolerance. Plant Physiol. Biochem. 2016, 108, 12–23.
  27. Scoccianti, V.; Bucchini, A.E.; Iacobucci, M.; Ruiz, K.B.; Biondi, S. Oxidative stress and antioxidant responses to increasing concentrations of trivalent chromium in the Andean crop species Chenopodium quinoa Willd. Ecotoxicol. Environ. Saf. 2016, 133, 25–35.
  28. Tripathi, A.; Tripathi, D.K.; Chauhan, D.K.; Kumar, N. Chromium(VI)-induced phytotoxicity in river catchment agriculture: Evidence from physiological, biochemical and anatomical alterations in Cucumis sativus (L.) used as model species. Chem. Ecol. 2016, 32, 12–33.
  29. Gill, R.A.; Zang, L.; Ali, B.; Farooq, M.A.; Cui, P.; Yang, S.; Ali, S.; Zhou, W. Chromium-induced physio-chemical and ultrastructural changes in four cultivars of Brassica napus L. Chemosphere 2015, 120, 154–164.
  30. Gill, R.A.; Zhang, N.; Ali, B.; Farooq, M.A.; Xu, J.; Gill, M.B.; Mao, B.; Zhou, W. Role of exogenous salicylic acid in regulating physio-morphic and molecular changes under chromium toxicity in black- and yellow-seeded Brassica napus L. Environ. Sci. Pollut. Res. 2016, 23, 20483–20496.
  31. Qing, X.; Zhao, X.; Hu, C.; Wang, P.; Zhang, Y.; Zhang, X.; Wang, P.; Shi, H.; Jia, F.; Qu, C. Selenium alleviates chromium toxicity by preventing oxidative stress in cabbage (Brassica campestris L. ssp. Pekinensis) leaves. Ecotoxicol. Environ. Saf. 2015, 114, 179–189.
  32. Tripathi, D.K.; Singh, V.P.; Prasad, S.M.; Chauhan, D.K.; Dubey, N.K. Silicon nanoparticles (SiNp) alleviate chromium(VI) phytotoxicity in Pisum sativum (L.) seedlings. Plant Physiol. Biochem. 2015, 96, 189–198.
  33. Patnaik, A.R.; Achary, V.M.M.; Panda, B.B. Chromium(VI)-induced hormesis and genotoxicity are mediated through oxidative stress in root cells of Allium cepa L. Plant Growth Regul. 2013, 71, 157–170.
  34. Kovacik, J.; Babula, P.; Klejdus, B.; Hedbavny, J. Chromium Uptake and Consequences for Metabolism and Oxidative Stress in Chamomile Plants. J. Agric. Food Chem. 2013, 61, 7864–7873.
  35. Eleftheriou, E.P.; Adamakis, I.-D.S.; Fatsiou, M.; Panteris, E. Hexavalent chromium disrupts mitosis by stabilizing microtubules in Lens culinaris root tip cells. Physiol. Plant. 2013, 147, 169–180.
  36. Choudhary, S.P.; Kanwar, M.; Bhardwaj, R.; Yu, J.-Q.; Lam-Son Phan, T. Chromium Stress Mitigation by Polyamine-Brassinosteroid Application Involves Phytohormonal and Physiological Strategies in Raphanus sativus L. PLoS ONE 2012, 7, e33210.
  37. Upadhyay, R.; Panda, S.K. Influence of Chromium Salts on Increased Lipid Peroxidation and Differential Pattern in Antioxidant Metabolism in Pistia stratiotes L. Braz. Arch. Biol. Technol. 2010, 53, 1137–1144.
  38. Gill, S.S.; Tuteja, N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol. Biochem. 2010, 48, 909–930.
  39. Zhang, M.; Smith, J.A.C.; Harberd, N.P.; Jiang, C. The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol. Biol. 2016, 91, 651–659.
  40. Pourrut, B.; Shahid, M.; Douay, F.; Dumat, C.; Pinelli, E. Molecular mechanisms involved in lead uptake, toxicity and detoxification in higher plants. In Heavy Metal Stress in Plants; Springer: Berlin/Heidelberg, Germany, 2013; pp. 121–147.
  41. Shahid, M.; Austruy, A.; Echevarria, G.; Arshad, M.; Sanaullah, M.; Aslam, M.; Nadeem, M.; Nasim, W.; Dumat, C. EDTA-enhanced phytoremediation of heavy metals: A review. Soil Sediment Contam. Int. J. 2014, 23, 389–416.
  42. Panda, S.K. Chromium-mediated oxidative stress and ultrastructural changes in root cells of developing rice seedlings. J. Plant Physiol. 2007, 164, 1419–1428.
  43. Singh, H.P.; Mahajan, P.; Kaur, S.; Batish, D.R.; Kohli, R.K. Chromium toxicity and tolerance in plants. Environ. Chem. Lett. 2013, 11, 229–254.
More
Academic Video Service