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Plant function and evolutionary biology
RESEARCH ARTICLE

The impact of Cu-polluted and organic soil on the fibrous plant; insights into plant growth promotion, antioxidant defences system, and oxidative stress

Farukh Ameen A , Sahar Mumtaz B , Baber Ali https://orcid.org/0000-0003-1553-2248 C , Iqbal Hussain https://orcid.org/0000-0002-8449-0494 A * , Aqsa Hafeez C , Ambreen Gul D , Mohsen Mohamed Elsharkawy E , Taghred A. Hashim F , Ghulam Yasin G , Muhammad Nauman Khan https://orcid.org/0000-0003-3790-0902 H I , Iftikhar Ali https://orcid.org/0000-0003-2319-2175 J K , Sayed M. Eldin L , Mohamed A. Rashwan M , Hosam O. Elansary N and Shafaqat Ali O P *
+ Author Affiliations
- Author Affiliations

A Department of Botany, Government College University, Faisalabad 38000, Pakistan.

B Department of Botany, Division of Science and Technology, University of Education, Lahore 54770, Pakistan.

C Department of Plant Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan.

D College of Life Sciences, Huazhong Agricultural University, Wuhan 430070, China.

E Department of Agricultural Botany, Faculty of Agriculture, Kafrelsheikh University, Kafr El-Sheikh 33516, Egypt.

F Soils and Water Department, Faculty of Agriculture, Benha University, Moshtohor 13736, Egypt.

G Department of Botany, Bahauddin Zakariya University, Multan 60800, Pakistan.

H Department of Botany, Islamia College Peshawar, 25120 Peshawar, Pakistan.

I University Public School, University of Peshawar, 25120 Peshawar, Pakistan.

J Center for Plant Science and Biodiversity, University of Swat, Charbagh 19120, Pakistan.

K Department of Genetics and Development, Columbia University Irving Medical Center, New York, NY 10032, USA.

L Center of Research, Faculty of Engineering, Future University in Egypt, New Cairo 11835, Egypt.

M Department of Agricultural Engineering, College of Food and Agriculture Sciences, King Saud University, Riyadh 11451, Saudi Arabia.

N Department of Plant Production, College of Food & Agriculture Sciences, King Saud University, Riyadh 11451, Saudi Arabia.

O Department of Environmental Sciences and Engineering, Government College University, Allama Iqbal Road, Faisalabad 38000, Pakistan.

P Department of Biological Sciences and Technology, China Medical University, Taichung City 40402, Taiwan.


Handling Editor: Suleyman Allakhverdiev

Functional Plant Biology 50(8) 623-632 https://doi.org/10.1071/FP23027
Submitted: 13 February 2023  Accepted: 8 May 2023   Published: 26 May 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Copper (Cu) is an abundant essential micronutrient element in various rocks and minerals and is required for a variety of metabolic processes in both prokaryotes and eukaryotes. However, excess Cu can disturb normal development by adversely affecting biochemical reactions and physiological processes in plants. However, organic soil is rich in micronutrients and can assist plants to tolerate toxicity by promoting growth and biomass. This study explored the potential of organic and Cu-contaminated soil on fibrous jute (Corchorus capsularis). Plants were grown in the organic soil, natural soil (normal soil) and Cu-contaminated soil for 60 days, and we studied different growth, physiological and ultra-structure alterations in the plant. Results showed that the addition of organic acid in the soil showed a remarkable increase in seed germination, plant height, fresh biomass, photosynthetic pigment and gas exchange parameters, and decreased the malondialdehyde (MDA) concentration in the tissues when compared to the plants grown in the natural soil. In contrast, plants grown in the Cu-contaminated soil significantly (P < 0.05) decreased the seed germination, plant height, fresh biomass, photosynthetic pigment and gas exchange parameters, and increased MDA content, proline concentration and the activities of various antioxidant compounds; i.e. peroxidase (POD) and superoxidase dismutase (SOD). In addition, Cu toxicity also destroyed many membrane bounded organelles especially the chloroplast, which was revealed from transmission electron microscopy (TEM). We concluded that Cu toxicity affected growth and physiological attributes in C. capsularis, while addition of organic soil increased plant growth and biomass.

Keywords: anthropogenic activities, antioxidative enzymes, Corchorus capsularis, environmental pollution, gas exchange parameters, heavy metal, jute, organic soil, reactive oxygen species.


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Heavy metal induced stress on wheat: phytotoxicity and microbiological management.Crossref | GoogleScholarGoogle Scholar |

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Phytoremediation of heavy metals: an indispensable contrivance in green remediation technology.Crossref | GoogleScholarGoogle Scholar |

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Variations of peroxidase activity in cocoa (Theobroma cacao L.) beans during their ripening, fermentation and drying.Crossref | GoogleScholarGoogle Scholar |

Salam A, Afridi MS, Javed MA, Saleem A, Hafeez A, Khan AR, Zeeshan M, Ali B, Azhar W, Sumaira , Ulhassan Z, Gan Y (2022) Nano-priming against abiotic stress: a way forward towards sustainable agriculture. Sustainability 14, 14880
Nano-priming against abiotic stress: a way forward towards sustainable agriculture.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Ali S, Seleiman MF, Rizwan M, Rehman M, Akram NA, Liu L, Alotaibi M, Al-Ashkar I, Mubushar M (2019) Assessing the correlations between different traits in copper-sensitive and copper-resistant varieties of jute (Corchorus capsularis L.). Plants 8, 545
Assessing the correlations between different traits in copper-sensitive and copper-resistant varieties of jute (Corchorus capsularis L.).Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Kamran M, Zhou Y, Parveen A, Rehman M, Ahmar S, Malik Z, Mustafa A, Anjum RMA, Wang B, Liu L (2020a) Appraising growth, oxidative stress and copper phytoextraction potential of flax (Linum usitatissimum L.) grown in soil differentially spiked with copper. Journal of Environmental Management 257, 109994
Appraising growth, oxidative stress and copper phytoextraction potential of flax (Linum usitatissimum L.) grown in soil differentially spiked with copper.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Ali S, Rehman M, Rana MS, Rizwan M, Kamran M, Imran M, Riaz M, Soliman MH, Elkelish A, Liu L (2020b) Influence of phosphorus on copper phytoextraction via modulating cellular organelles in two jute (Corchorus capsularis L.) varieties grown in a copper mining soil of Hubei Province, China. Chemosphere 248, 126032
Influence of phosphorus on copper phytoextraction via modulating cellular organelles in two jute (Corchorus capsularis L.) varieties grown in a copper mining soil of Hubei Province, China.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Fahad S, Khan SU, Ahmar S, Khan MHU, Rehman M, Maqbool Z, Liu L (2020c) Morpho-physiological traits, gaseous exchange attributes, and phytoremediation potential of jute (Corchorus capsularis L.) grown in different concentrations of copper-contaminated soil. Ecotoxicology and Environmental Safety 189, 109915
Morpho-physiological traits, gaseous exchange attributes, and phytoremediation potential of jute (Corchorus capsularis L.) grown in different concentrations of copper-contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Ali S, Rehman M, Rizwan M, Kamran M, Mohamed IAA, khan Z, Bamagoos AA, Alharby HF, Hakeem KR, Liu L (2020d) Individual and combined application of EDTA and citric acid assisted phytoextraction of copper using jute (Corchorus capsularis L.) seedlings. Environmental Technology & Innovation 19, 100895
Individual and combined application of EDTA and citric acid assisted phytoextraction of copper using jute (Corchorus capsularis L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Rehman M, Kamran M, Afzal J, Noushahi HA, Liu L (2020e) Investigating the potential of different jute varieties for phytoremediation of copper-contaminated soil. Environmental Science and Pollution Research 27, 30367–30377.
Investigating the potential of different jute varieties for phytoremediation of copper-contaminated soil.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Ali S, Kamran M, Iqbal N, Azeem M, Tariq Javed M, Ali Q, Zulqurnain Haider M, Irshad S, Rizwan M, Alkahtani S, Abdel-Daim MM (2020f) Ethylenediaminetetraacetic Acid (EDTA) mitigates the toxic effect of excessive copper concentrations on growth, gaseous exchange and chloroplast ultrastructure of Corchorus capsularis L. and improves copper accumulation capabilities. Plants 9, 756
Ethylenediaminetetraacetic Acid (EDTA) mitigates the toxic effect of excessive copper concentrations on growth, gaseous exchange and chloroplast ultrastructure of Corchorus capsularis L. and improves copper accumulation capabilities.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Ali S, Rehman M, Hasanuzzaman M, Rizwan M, Irshad S, Shafiq F, Iqbal M, Alharbi BM, Alnusaire TS, Qari SH (2020g) Jute: a potential candidate for phytoremediation of metals—a review. Plants 9, 258
Jute: a potential candidate for phytoremediation of metals—a review.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Fahad S, Adnan M, Ali M, Rana MS, Kamran M, Ali Q, Hashem IA, Bhantana P, Ali M, Hussain RM (2020h) Foliar application of gibberellic acid endorsed phytoextraction of copper and alleviates oxidative stress in jute (Corchorus capsularis L.) plant grown in highly copper-contaminated soil of China. Environmental Science and Pollution Research 27, 37121–37133.
Foliar application of gibberellic acid endorsed phytoextraction of copper and alleviates oxidative stress in jute (Corchorus capsularis L.) plant grown in highly copper-contaminated soil of China.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Ali S, Irshad S, Hussaan M, Rizwan M, Rana MS, Hashem A, Abd Allah EF, Ahmad P (2020i) Copper uptake and accumulation, ultra-structural alteration, and bast fibre yield and quality of fibrous jute (Corchorus capsularis L.) plants grown under two different soils of China. Plants 9, 404
Copper uptake and accumulation, ultra-structural alteration, and bast fibre yield and quality of fibrous jute (Corchorus capsularis L.) plants grown under two different soils of China.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Fahad S, Rehman M, Saud S, Jamal Y, Khan S, Liu L (2020j) Morpho-physiological traits, biochemical response and phytoextraction potential of short-term copper stress on kenaf (Hibiscus cannabinus L.) seedlings. PeerJ 8, e8321
Morpho-physiological traits, biochemical response and phytoextraction potential of short-term copper stress on kenaf (Hibiscus cannabinus L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Rehman M, Fahad S, Tung SA, Iqbal N, Hassan A, Ayub A, Wahid MA, Shaukat S, Liu L, Deng G (2020k) Leaf gas exchange, oxidative stress, and physiological attributes of rapeseed (Brassica napus L.) grown under different light-emitting diodes. Photosynthetica 58, 836–845.
Leaf gas exchange, oxidative stress, and physiological attributes of rapeseed (Brassica napus L.) grown under different light-emitting diodes.Crossref | GoogleScholarGoogle Scholar |

Saleem MH, Wang X, Ali S, Zafar S, Nawaz M, Adnan M, Fahad S, Shah A, Alyemeni MN, Hefft DI, Ali S (2021) Interactive effects of gibberellic acid and NPK on morpho-physio-biochemical traits and organic acid exudation pattern in coriander (Coriandrum sativum L.) grown in soil artificially spiked with boron. Plant Physiology and Biochemistry 167, 884–900.
Interactive effects of gibberellic acid and NPK on morpho-physio-biochemical traits and organic acid exudation pattern in coriander (Coriandrum sativum L.) grown in soil artificially spiked with boron.Crossref | GoogleScholarGoogle Scholar |

Saleem A, Zulfiqar A, Ali B, Naseeb MA, Almasaudi AS, Harakeh S (2022) Iron sulfate (FeSO4) improved physiological attributes and antioxidant capacity by reducing oxidative stress of Oryza sativa L. cultivars in alkaline soil. Sustainability 14, 16845
Iron sulfate (FeSO4) improved physiological attributes and antioxidant capacity by reducing oxidative stress of Oryza sativa L. cultivars in alkaline soil.Crossref | GoogleScholarGoogle Scholar |

Sarwar S, Akram NA, Saleem MH, Zafar S, Alghanem SM, Abualreesh MH, Alatawi A, Ali S (2022) Spatial variations in the biochemical potential of okra [Abelmoschus esculentus L. (Moench)] leaf and fruit under field conditions. PLoS ONE 17, e0259520
Spatial variations in the biochemical potential of okra [Abelmoschus esculentus L. (Moench)] leaf and fruit under field conditions.Crossref | GoogleScholarGoogle Scholar |

Shabbir Z, Sardar A, Shabbir A, Abbas G, Shamshad S, Khalid S, Natasha , Murtaza G, Dumat C, Shahid M (2020) Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment. Chemosphere 259, 127436
Copper uptake, essentiality, toxicity, detoxification and risk assessment in soil-plant environment.Crossref | GoogleScholarGoogle Scholar |

Sharma S, Rana VS, Rana N, Sharma U, Gudeta K, Alharbi K, Ameen F, Bhat SA (2022) Effect of organic manures on growth, yield, leaf nutrient uptake and soil properties of Kiwifruit (Actinidia deliciosa Chev.) cv. Allison. Plants 11, 3354
Effect of organic manures on growth, yield, leaf nutrient uptake and soil properties of Kiwifruit (Actinidia deliciosa Chev.) cv. Allison.Crossref | GoogleScholarGoogle Scholar |

Ulhassan Z, Khan I, Hussain M, Khan AR, Hamid Y, Hussain S, Allakhverdiev SI, Zhou W (2022) Efficacy of metallic nanoparticles in attenuating the accumulation and toxicity of chromium in plants: Current knowledge and future perspectives. Environmental Pollution 315, 120390
Efficacy of metallic nanoparticles in attenuating the accumulation and toxicity of chromium in plants: Current knowledge and future perspectives.Crossref | GoogleScholarGoogle Scholar |

Ullah N, Ditta A, Imtiaz M, Li X, Jan AU, Mehmood S, Rizwan MS, Rizwan M (2021) Appraisal for organic amendments and plant growth-promoting rhizobacteria to enhance crop productivity under drought stress: a review. Journal of Agronomy and Crop Science 207, 783–802.
Appraisal for organic amendments and plant growth-promoting rhizobacteria to enhance crop productivity under drought stress: a review.Crossref | GoogleScholarGoogle Scholar |

Wahab A, Munir A, Saleem MH, AbdulRaheem MI, Aziz H, Mfarrej MFB, Abdi G (2023) Interactions of metal-based engineered nanoparticles with plants: an overview of the state of current knowledge, research progress, and prospects. Journal of Plant Growth Regulation 11, 1620
Interactions of metal-based engineered nanoparticles with plants: an overview of the state of current knowledge, research progress, and prospects.Crossref | GoogleScholarGoogle Scholar |

Yasin M, Anwar F, Noorani H, Muhammad S, Mahmood A, Javed T, Ali B, Alharbi K, Saleh IA, Abu-Harirah HA (2023) Evaluating non-composted Red Cotton Tree (Bombax ceiba) sawdust mixtures for raising okra (Abelmoschus esculentus (L.) Moench) in pots. Agronomy 13, 97
Evaluating non-composted Red Cotton Tree (Bombax ceiba) sawdust mixtures for raising okra (Abelmoschus esculentus (L.) Moench) in pots.Crossref | GoogleScholarGoogle Scholar |

Zaheer IE, Ali S, Saleem MH, Ali M, Riaz M, Javed S, Sehar A, Abbas Z, Rizwan M, El-Sheikh MA, Alyemeni MN (2020a) Interactive role of zinc and iron lysine on Spinacia oleracea L. growth, photosynthesis and antioxidant capacity irrigated with tannery wastewater. Physiology and Molecular Biology of Plants 26, 2435–2452.
Interactive role of zinc and iron lysine on Spinacia oleracea L. growth, photosynthesis and antioxidant capacity irrigated with tannery wastewater.Crossref | GoogleScholarGoogle Scholar |

Zaheer IE, Ali S, Saleem MH, Imran M, Alnusairi GSH, Alharbi BM, Riaz M, Abbas Z, Rizwan M, Soliman MH (2020b) Role of iron–lysine on morpho-physiological traits and combating chromium toxicity in rapeseed (Brassica napus L.) plants irrigated with different levels of tannery wastewater. Plant Physiology and Biochemistry 155, 70–84.
Role of iron–lysine on morpho-physiological traits and combating chromium toxicity in rapeseed (Brassica napus L.) plants irrigated with different levels of tannery wastewater.Crossref | GoogleScholarGoogle Scholar |

Zaheer IE, Ali S, Saleem MH, Yousaf HS, Malik A, Abbas Z, Rizwan M, Abualreesh MH, Alatawi A, Wang X (2022) Combined application of zinc and iron-lysine and its effects on morpho-physiological traits, antioxidant capacity and chromium uptake in rapeseed (Brassica napus L.). PLoS ONE 17, e0262140
Combined application of zinc and iron-lysine and its effects on morpho-physiological traits, antioxidant capacity and chromium uptake in rapeseed (Brassica napus L.).Crossref | GoogleScholarGoogle Scholar |

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Exogenous nitric oxide on antioxidative system and ATPase activities from tomato seedlings under copper stress.Crossref | GoogleScholarGoogle Scholar |