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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Early interconnectivity between metabolic and defense events against oxidative stress induced by cadmium in roots of four citrus rootstocks

Griselda Podazza A , Marta Arias B and Fernando E. Prado C D
+ Author Affiliations
- Author Affiliations

A Instituto de Ecología, Fundación Miguel Lillo, Miguel Lillo 251, CP 4000, Tucumán, Argentina.

B Cátedra de Anatomía Vegetal, Facultad de Ciencias Naturales e IML, Miguel Lillo 205, CP 4000, Tucumán, Argentina.

C Cátedra de Fisiología Vegetal, Facultad de Ciencias Naturales e IML, Miguel Lillo 205, CP 4000, Tucumán, Argentina.

D Corresponding author. Email: fepra@csnat.unt.edu.ar

Functional Plant Biology 43(10) 973-985 https://doi.org/10.1071/FP16153
Submitted: 10 August 2015  Accepted: 1 June 2016   Published: 30 June 2016

Abstract

The effect of cadmium on roots of four citrus rootstocks was studied to assess the relationships between oxidative stress, carbohydrates, phenolics and antioxidant responses. Swingle citrumelo (SC), Rangpur lime (RL), Troyer citrange (TC) and Volkamer lemon (VL) genotypes were exposed to 0, 5 and 10 µM Cd over 7 days, after which Cd accumulation was markedly higher in roots compared with stems and leaves. Malondialdehyde (MDA) and lipoxygenase (LOX) activity increased in Cd-treated SC and RL roots, suggesting that a lipid peroxidation is the main driver of plasma membrane damage. In contrast, in TC and VL genotypes, LOX-mediated lipid peroxidation does not appear to play a key role in Cd-induced lipid peroxidation, but H2O2 accumulation seems to be responsible of less plasma membrane damage. Catalase (CAT), superoxide dismutase (SOD) and guaiacol and syringaldazine peroxidases (G-POD and S-POD respectively) were differentially affected by Cd. Lipid profile and ATPase-dependant proton extrusion indicated higher disfunctionalities of root plasma membrane in SC and RL genotypes than in TC and VL genotypes. Differences in carbohydrates and phenolic compounds were also observed. Histochemical analysis of G-POD activity and lignin and suberin deposition revealed differences among genotypes. A model to explain the relationships among carbohydrates, soluble phenolics, lipid peroxidation and H2O2 accumulation in Cd-exposed roots was proposed.

Additional keywords: cadmium, defence, genotype, metabolism, oxidative stress, root.


References

Alloway BJ, Steinnes E (1999) Anthropogenic addition of cadmium to soils. In ‘Cadmium in soils and plants’. (Eds MJ McLaughlin, BR Singh) pp. 97–123. (Kluwer Academic Publishers: Dordrecht, The Netherlands)

Arbona V, Hosain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiologia Plantarum 132, 452–466.
Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXksFWktb8%3D&md5=9e424867c873a4582f161a03ba89f537CAS | 18333999PubMed |

Balal RM, Khan MM, Shahid MA, Mattson NS, Abbas T, Ashfaq M, Garcia-Sanchez F, Ghazanfer U, Gimeno V, Iqbal Z (2012) Comparative studies on the physiobiochemical, enzymatic, and ionic modifications in salt-tolerant and salt-sensitive citrus rootstocks under NaCl stress. Journal of the American Society for Horticultural Science 137, 86–95.

Benavides MP, Gallego SM, Tomaro ML (2005) Cadmium toxicity in plants. Brazilian Journal of Plant Physiology 17, 21–34.
Cadmium toxicity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXltVWrs7c%3D&md5=f099312521e0ca840fc7781c1717353aCAS |

Bolouri-Moghaddam MR, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. The FEBS Journal 277, 2022–2037.
Sugar signalling and antioxidant network connections in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvFejt7c%3D&md5=dc6af3c0343063f4bb2332d5dba30a82CAS | 20412056PubMed |

Cheeseman JM (2007) Hydrogen peroxide and plant stress: challenging relationship. Plant Stress 1, 4–15.

Chen LS, Han S, Qi YP, Yang LT (2012) Boron stresses and tolerance in citrus. African Journal of Biotechnology 11, 5961–5969.
Boron stresses and tolerance in citrus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltlOjtbw%3D&md5=a03d2c362cf844f0e0006a7f316ab658CAS |

Elloumi N, Zouari M, Chaari L, Jomni C, Marzouk B, Ben Abdallah F (2014) Effects of cadmium on lipids of almond seedlings (Prunus dulcis). Botanical Studies 55, 61
Effects of cadmium on lipids of almond seedlings (Prunus dulcis).Crossref | GoogleScholarGoogle Scholar |

Elobeid M, Göbel C, Feussner I, Polle A (2012) Cadmium interferes with auxin physiology and lignification in poplar. Journal of Experimental Botany 63, 1413–1421.
Cadmium interferes with auxin physiology and lignification in poplar.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1Ols7w%3D&md5=47e4fd7e7271dff8621e0a40d8a465afCAS | 22140243PubMed |

Ernst WHO (2006) Evolution of metal tolerance in higher plants. Forest Snow and Landscape Research 80, 251–274.

Fodor E, Szabó-Nagy A, Erdei L (1995) The effects of cadmium on the fluidity and H+-ATPase activity of plasma membrane from sunflower and wheat roots. Journal of Plant Physiology 147, 87–92.
The effects of cadmium on the fluidity and H+-ATPase activity of plasma membrane from sunflower and wheat roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXpsVKjurg%3D&md5=b77ac727c5b933e9edacdfb2a4efbfcaCAS |

Gallego SM, Benavides MP, Tomaro ML (1996) Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress. Plant Science 121, 151–159.
Effect of heavy metal ion excess on sunflower leaves: evidence for involvement of oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28Xnt1Whtrc%3D&md5=7235c6d049d9ac09710d2a363262574dCAS |

Gaudet M, Pietrini F, Beritognolo I, Iori V, Zacchini M, Massacci A, Mugnozza GS, Sabatti M (2011) Intraspecific variation of physiological and molecular response to cadmium stress in Populus nigra L. Tree Physiology 31, 1309–1318.
Intraspecific variation of physiological and molecular response to cadmium stress in Populus nigra L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1yktrc%3D&md5=c8939f6f402095921aaa0f13cb5c8ab9CAS | 21949013PubMed |

Gill SS, Khan NA, Tuteja N (2011) Differential cadmium stress tolerance in five Indian mustard (Brassica juncea L.) cultivars. An evaluation of the role of antioxidant machinery. Plant Signaling & Behavior 6, 293–300.
Differential cadmium stress tolerance in five Indian mustard (Brassica juncea L.) cultivars. An evaluation of the role of antioxidant machinery.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yjs70%3D&md5=d6030445f2a4487d31b5938a37addcaeCAS |

Gogorcena Y, Larbi A, Andaluz S, Carpena RO, Abadía A, Abadía J (2011) Effects of cadmium on cork oak (Quercus suber L.) plants grown in hydroponics. Tree Physiology 31, 1401–1412.
Effects of cadmium on cork oak (Quercus suber L.) plants grown in hydroponics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xit1ykt7s%3D&md5=716567b11894c19ae56f7ddba2c94616CAS | 22121153PubMed |

Hartmann MA (1998) Plant sterols and the membrane environment. Trends in Plant Science 3, 170–175.
Plant sterols and the membrane environment.Crossref | GoogleScholarGoogle Scholar |

Irfan M, Hayat S, Ahmad A, Alyemeni MN (2013) Soil cadmium enrichment: allocation and plant physiological manifestations. Saudi Journal of Biological Sciences 20, 1–10.
Soil cadmium enrichment: allocation and plant physiological manifestations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Chsr8%3D&md5=11864c17bb8177036708abc80235c02cCAS | 23961213PubMed |

Kabata-Pendias A (2011) ‘Trace elements in soils and plants.’ (4th edn) (CRC Press: Bocca Raton, FL, USA).

Kováčik J, Klejdus B (2008) Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots. Plant Cell Reports 27, 605–615.
Dynamics of phenolic acids and lignin accumulation in metal-treated Matricaria chamomilla roots.Crossref | GoogleScholarGoogle Scholar | 18066553PubMed |

Liao XY, Yang LT, Lu YB, Ye X, Chen LS (2015) Roles of rootstocks and scions in aluminum tolerance of Citrus. Acta Physiologiae Plantarum 37, 1743
Roles of rootstocks and scions in aluminum tolerance of Citrus.Crossref | GoogleScholarGoogle Scholar |

Liavonchanka A, Feussner I (2006) Lipoxygenases: occurrence, functions and catalysis. Journal of Plant Physiology 163, 348–357.
Lipoxygenases: occurrence, functions and catalysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislSmtbw%3D&md5=aad8868873287c9f6911d8381f75b5b5CAS | 16386332PubMed |

Liptáková Ľ, Huttová J, Mistrík I, Tamás L (2013) Enhanced lipoxygenase activity is involved in the stress response but not in the harmful lipid peroxidation and cell death of short-term cadmium-treated barley root tip. Journal of Plant Physiology 170, 646–652.
Enhanced lipoxygenase activity is involved in the stress response but not in the harmful lipid peroxidation and cell death of short-term cadmium-treated barley root tip.Crossref | GoogleScholarGoogle Scholar | 23395539PubMed |

López-Climent MF, Arbona V, Pérez-Clemente RM, Zandalinas SI, Gómez-Cadenas A (2014) Effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants. Plant Biology 16, 79–87.
Effect of cadmium and calcium treatments on phytochelatin and glutathione levels in citrus plants.Crossref | GoogleScholarGoogle Scholar | 23574491PubMed |

Merlin T, Lima GP, Leonel S, Vianello F (2012) Peroxidase activity and total phenol content in citrus cuttings treated with different copper sources. South African Journal of Botany 83, 159–164.
Peroxidase activity and total phenol content in citrus cuttings treated with different copper sources.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhslCgtrjK&md5=c0638ca7d98688ed5455fa29653fa4abCAS |

Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies 15, 523–530.

Mohamed AA, Castagna A, Ranieri A, Sanità di Toppi L (2012) Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis. Plant Physiology and Biochemistry 57, 15–22.
Cadmium tolerance in Brassica juncea roots and shoots is affected by antioxidant status and phytochelatin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFaitLvK&md5=7fcc8f4d2f23fb8201460a53245628faCAS | 22652410PubMed |

Mustafa NR, Verpoorte R (2007) Phenolic compounds in Catharanthus roseus. Phytochemistry Reviews 6, 243–258.
Phenolic compounds in Catharanthus roseus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXnvFWks7g%3D&md5=0f3f94d45827a844644687f4d4ed75cbCAS |

Nocito FF, Lancilli C, Dendena B, Lucchini G, Sacchi GA (2011) Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation. Plant, Cell & Environment 34, 994–1008.
Cadmium retention in rice roots is influenced by cadmium availability, chelation and translocation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1Sgtbc%3D&md5=c4516ef94223a17c8088d8c2dac2d310CAS |

Obata H, Omebayashi M (1997) Effects of cadmium on mineral nutrient concentrations in plant differing in tolerance for cadmium. Journal of Plant Nutrition 20, 97–105.
Effects of cadmium on mineral nutrient concentrations in plant differing in tolerance for cadmium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXht1GitL4%3D&md5=bb5f1335372eefeb58c9c62b87df3c86CAS |

Parrotta L, Guerriero G, Sergeant K, Cai G, Hausman JF (2015) Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: differences in the response mechanisms. Frontiers in Plant Science 6, 133
Target or barrier? The cell wall of early- and later-diverging plants vs cadmium toxicity: differences in the response mechanisms.Crossref | GoogleScholarGoogle Scholar | 25814996PubMed |

Petrov VD, Van Breusegem F (2012) Hydrogen peroxide – a central hub for information flow in plant cells. AoB Plants 2012, pls014
Hydrogen peroxide – a central hub for information flow in plant cells.Crossref | GoogleScholarGoogle Scholar | 22708052PubMed |

Peyrano G, Taleisnik E, Quiroga M, Forchetti SM, Tigier H (1997) Salinity effects on hydraulic conductance, lignin content and peroxidase activity in tomato roots. Plant Physiology and Biochemistry 35, 387–393.

Podazza G, Arias M, Prado FE (2012) Cadmium accumulation and strategies to avoid its toxicity in roots of the citrus rootstock Citrumelo. Journal of Hazardous Materials 215–216, 83–89.
Cadmium accumulation and strategies to avoid its toxicity in roots of the citrus rootstock Citrumelo.Crossref | GoogleScholarGoogle Scholar | 22410717PubMed |

Prado FE, Boero C, Gallardo M, Gonzalez JA (2000) Effect of NaCl on growth germination and soluble sugars content in Chenopodium quinoa Willd. seeds. Botanical Bulletin of Academia Sinica 41, 27–34.

Prado C, Rosa M, Pagano E, Hilal M, Prado FE (2010) Seasonal variability of physiological and biochemical aspects of chromium accumulation in outdoor-grown Salvinia minima. Chemosphere 81, 584–593.
Seasonal variability of physiological and biochemical aspects of chromium accumulation in outdoor-grown Salvinia minima.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Wmu73P&md5=b5f09cd945391acc4377cf29d6cbb4bfCAS | 20832840PubMed |

Prado C, Podazza G, Pagano E, Prado FE, Rosa M (2011) Heavy metals – functional and metabolic interactions between carbohydrates and secondary metabolites in plants. A review. In ‘Hazardous materials: types, risks and control’. (Ed. SK Brar) pp. 1–52. (Nova Publisher: New York)

Rascio N, Dalla Vecchia F, La Rocca N, Barbato R, Pagliano C, Raviolo M, Gonnelli C, Gabbrielli R (2008) Metal accumulation and damage in rice (cv. Vialonenano) seedlings exposed to cadmium. Environmental and Experimental Botany 62, 267–278.
Metal accumulation and damage in rice (cv. Vialonenano) seedlings exposed to cadmium.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXivVyjsrs%3D&md5=a24324ab97d4b9df99ca6af85c50b17dCAS |

Ribeiro RV, Espinoza-Núñez E, Pompeu Junior J, Mourão Filho FAA, Machado EC (2014) Citrus rootstocks for improving the horticultural performance and physiological responses under constraining environments. In ‘Improvement of crops in the era of climatic changes’. (Eds P Ahmad, MR Wani, MM Azooz) pp. 1–37. (Springer Science + Business Media: New York)

Roche Y, Gerbeau-Pissot P, Buhot B, Thomas D, Bonneau L, Gresti J, Mongrand S, Perrier-Cornet JM, Simon-Plas F (2008) Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts. FASEB Journal 22, 3980–3991.
Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCgt77N&md5=d56931a081a1cb3e0ff0eb45708e70d6CAS | 18676403PubMed |

Rui H, Chen C, Zhang X, Shen Z, Zhang F (2016) Cd-induced oxidative stress and lignification in the roots of two Vicia sativa L. varieties with different Cd tolerances. Journal of Hazardous Materials 301, 304–313.
Cd-induced oxidative stress and lignification in the roots of two Vicia sativa L. varieties with different Cd tolerances.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVyqtLjP&md5=62564a47fc42671f5821811c033b57caCAS | 26372696PubMed |

Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. Journal of Botany 2012, Article ID 217037
Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions.Crossref | GoogleScholarGoogle Scholar |

Skórzyńska-Polit E (2007) Lipid peroxidation in plant cells, its physiological role and changes under heavy metal stress. Acta Societatis Botanicorum Poloniae 76, 49–54.
Lipid peroxidation in plant cells, its physiological role and changes under heavy metal stress.Crossref | GoogleScholarGoogle Scholar |

Skórzyńska-Polit E, Krupa Z (2006) Lipid peroxidation in cadmium-treated Phaseolus coccineus plants. Archives of Environmental Contamination and Toxicology 50, 482–487.
Lipid peroxidation in cadmium-treated Phaseolus coccineus plants.Crossref | GoogleScholarGoogle Scholar | 16418896PubMed |

Sterckeman T, Redjala T, Morel JL (2011) Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake. Environmental and Experimental Botany 74, 131–139.
Influence of exposure solution composition and of plant cadmium content on root cadmium short-term uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlChsrjI&md5=3af545f8ee7c87568ad7b17912d4f44fCAS |

Tamás L, Mistrík I, Huttová J, Halušková Ľ, Valentovičová K, Zelinová V (2010) Role of reactive oxygen species-generating enzymes and hydrogen peroxide during cadmium, mercury and osmotic stresses in barley root tip. Planta 231, 221–231.
Role of reactive oxygen species-generating enzymes and hydrogen peroxide during cadmium, mercury and osmotic stresses in barley root tip.Crossref | GoogleScholarGoogle Scholar | 19898864PubMed |

Tran TA, Popova LP (2013) Functions and toxicity of cadmium in plants: recent advances and future prospects. Turkish Journal of Botany 37, 1–13.

USEPA (United States Environmental Protection Agency) (1994) Microwave assisted acid digestion of sediments, sludges, soils, and oils. Method 3051. Office of Solid Waste and Emergency Response, US Government Printing Office, Washington, DC.

Wu J, Seliskar DM, Gallagher JL (1998) Stress tolerance in the marsh plant Spartina patens: impact of NaCl on growth and root plasma membrane lipid composition. Physiologia Plantarum 102, 307–317.
Stress tolerance in the marsh plant Spartina patens: impact of NaCl on growth and root plasma membrane lipid composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXit1eku7c%3D&md5=6523e3020496b515b046ef0d726a2b9bCAS |

Yamasaki H, Sakihama Y, Ikehara N (1997) Flavonoid-peroxidase reaction as a detoxification mechanism of plant cells against H2O2. Plant Physiology 115, 1405–1412.

Zenoff AM, Hilal M, Galo M, Moreno H (1994) Changes in roots lipid composition and inhibition of the extrusion of protons during salt stress in two genotypes of soybean resistant or susceptible to stress. Varietal differences. Plant & Cell Physiology 35, 729–735.

Zhang X, Zhang S, Xu X, Li T, Gong G, Jia Y, Li Y, Deng L (2010) Tolerance and accumulation characteristics of cadmium in Amaranthus hybridus L. Journal of Hazardous Materials 180, 303–308.
Tolerance and accumulation characteristics of cadmium in Amaranthus hybridus L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXms1Cisbg%3D&md5=0f9d8150ec74293d9ef55d1bc3578aedCAS | 20439133PubMed |

Zhou ZS, Wang SJ, Yang ZM (2008) Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants. Chemosphere 70, 1500–1509.
Biological detection and analysis of mercury toxicity to alfalfa (Medicago sativa) plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlvV2qsw%3D%3D&md5=430dcf028ec7af4c5f5b7ffeeeabcca2CAS | 17905409PubMed |