Register      Login
Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Trigonella foenum-graecum morphophysiological and phytochemical processes controlling iron uptake and translocation

Wiem Mnafgui https://orcid.org/0000-0001-5855-4899 A B C , Valeria Rizzo D , Giuseppe Muratore https://orcid.org/0000-0003-3676-7580 D , Hichem Hajlaoui B C , Bianca de Oliveira Schinoff https://orcid.org/0000-0002-0270-0196 E , Kais Mnafgui F and Amine Elleuch A *
+ Author Affiliations
- Author Affiliations

A Laboratory of Plant Biotechnology, Faculty of Sciences, University of Sfax, BP 1171, 3000 Sfax, Tunisia.

B Regional Center for Agricultural Research in Sidi Bouzid. Sidi Bouzid 9100, Tunisia.

C Laboratory of Non–Conventional Water Valuation (INRGREF), University of Carthage, Carthage, Tunisia.

D Di3A, Dipartimento di Agricoltura, Alimentazione e Ambiente, University of Catania, via S. Sofia 100, 95123 Catania, Italy.

E Department of Pharmaco Sciences, Universidade Federal de Ciências da Saúde de Porto Alegre, Porto Alegre, Rio Grande do Sul, Brazil.

F Department of Biology, Faculty of Science of Gafsa, Gafsa 2112, Tunisia.

* Correspondence to: amine.elleuch@fss.usf.tn

Handling Editor: Shahid Hussain

Crop & Pasture Science - https://doi.org/10.1071/CP21419
Submitted: 21 June 2021  Accepted: 22 November 2021   Published online: 23 February 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context: Iron (Fe) is considered as a major cause of rural Tunisian soil contamination. Developing strategies for the cultivation of accumulator plants with permissible iron (Fe) concentrations is an urgent challenge.

Aims: In this study, the effects of FeSO4 concentration (0, 50, 500 and 1000 mg L−1) on fenugreek morpho-biochemical parameters were investigated.

Methods: The use of fenugreek as a phytoremediation strategy to control not only the uptake of Fe but also its safe consumption after treatments was evaluated.

Key results: Results showed that elevated Fe concentrations did not affect the germination rate, but, rather, decreased the radicle length and amylase activity. The elemental analysis showed that Fe uptake was higher in shoots than in roots, but lower in harvested seeds. The translocation factor was higher than 1, suggesting a safe use of fenugreek as an accumulator. Moreover, the increase in Fe concentrations reduced the chlorophyll content and enhanced the production of lipid peroxidation, hydrogen peroxide and superoxide dismutase more frequently on fenugreek shoots than on their roots. In turn, the maximum concentrations of flavonoids and phenols were recorded under the Fe concentration of 50 mg L−1. High-performance liquid chromatography analysis showed that the gallic and syringic acids were the major phenols produced under Fe stress in shoots and that 50 mg L−1 of added Fe concentration induced their elevation. However, the quercetin was detected only in roots and was reduced under the increasing Fe concentrations.

Conclusions: These results showed that fenugreek is an accumulator plant with admissible concentrations of Fe accumulation, which deploys multiple mechanisms to adapt to Fe stress.

Keywords: amylase activity, catalase, fenugreek, flavonoide, iron stress, oxidant activities, phenols, seed germination.


References

Adib SS, Dehaghi MA, Rezazadeh A, Naji AM (2020) Evaluation of sulfur and foliar application of Zn and Fe on yield and biochemical factors of cumin (Cuminum cyminum L.) under irrigation regimes. Journal of HerbMed Pharmacology 9, 161–170.
Evaluation of sulfur and foliar application of Zn and Fe on yield and biochemical factors of cumin (Cuminum cyminum L.) under irrigation regimes.Crossref | GoogleScholarGoogle Scholar |

Aebi H (1984) Oxygen radicals in biological systems. Methods in Enzymology 105, 121–126.
Oxygen radicals in biological systems.Crossref | GoogleScholarGoogle Scholar | 6727660PubMed |

Ahammed GJ, Wu M, Wang Y, Yan Y, Mao Q, Ren J, Ma R, Liu A, Chen S (2020) Melatonin alleviates iron stress by improving iron homeostasis, antioxidant defense and secondary metabolism in cucumber. Scientia Horticulturae 265, 109205
Melatonin alleviates iron stress by improving iron homeostasis, antioxidant defense and secondary metabolism in cucumber.Crossref | GoogleScholarGoogle Scholar |

Akinci IE, Akinci S, Yilmaz K (2010) Response of tomato (Solanum lycopersicum L.) to lead toxicity: growth, element uptake, chlorophyll and water content. African Journal of Agricultural Research 5, 416–423.
Response of tomato (Solanum lycopersicum L.) to lead toxicity: growth, element uptake, chlorophyll and water content.Crossref | GoogleScholarGoogle Scholar |

Akrimi R, Hajlaoui H, Rizzo V, Muratore G, Mhamdi M (2020) Agronomical traits, phenolic compounds and antioxidant activity in raw and cooked potato tubers growing under saline conditions. Journal of the Science of Food and Agriculture 100, 3719–3728.
Agronomical traits, phenolic compounds and antioxidant activity in raw and cooked potato tubers growing under saline conditions.Crossref | GoogleScholarGoogle Scholar | 32248537PubMed |

Araújo TO, Freitas-Silva L, Franklin FMO, Ribeiro C, Kuki KN, Pereira EG, Nunes-Nesi A, Silva LC (2020) Understanding photosynthetic and metabolic adjustments in iron hyperaccumulators grass. Theoretical and Experimental Plant Physiology 32, 147–162.
Understanding photosynthetic and metabolic adjustments in iron hyperaccumulators grass.Crossref | GoogleScholarGoogle Scholar |

Askari S, Azmat R (2016) Codium mediated anatomical improvement in Trigonella foenum-graecum shoot under mercury stress. Journal of Pharmacognosy and Phytochemistry 5, 170–174.

Assche Van F, Clijsters H (1990) Effects of metals on enzyme activity in plants. Plant, Cell and Environment 13, 195–206.
Effects of metals on enzyme activity in plants.Crossref | GoogleScholarGoogle Scholar |

Aung MS, Masuda H, Kobayashi T, Nishizawa NK (2018) Physiological and transcriptomic analysis of responses to different levels of iron excess stress in various rice tissues. Soil Science and Plant Nutrition 64, 370–385.
Physiological and transcriptomic analysis of responses to different levels of iron excess stress in various rice tissues.Crossref | GoogleScholarGoogle Scholar |

Bao T, Sun L, Sun T, Zhang P, Niu Z (2009) Iron-deficiency induces cadmium uptake and accumulation in Solanum nigrum L. Bulletin of Environmental Contamination and Toxicology 82, 338–342.
Iron-deficiency induces cadmium uptake and accumulation in Solanum nigrum L.Crossref | GoogleScholarGoogle Scholar | 19002364PubMed |

Blasco B, Navarro-León E, Ruiz JM (2018) Oxidative stress in relation with micronutrient deficiency or toxicity. In ‘Plant micronutrient use efficiency: molecular and genomic perspectives in crop plants’. (Eds MA Hossain, T Kamiya, DJ Burritt, L-S Phan Tran, T Fujiwara) pp. 181–194.
| Crossref |

Casierra-Posada F, Cortés-Bayona JD, Cutler J (2017) Effect of iron excess on growth of sisal plants (Furcraea hexapetala). Gesunde Pflanzen 69, 123–129.
Effect of iron excess on growth of sisal plants (Furcraea hexapetala).Crossref | GoogleScholarGoogle Scholar |

Das U, Rahman MM, Roy ZR, Rahman MM, Kabir AH (2020) Morpho-physiological retardations due to iron toxicity involve redox imbalance rather than photosynthetic damages in tomato. Plant Physiology and Biochemistry 156, 55–63.
Morpho-physiological retardations due to iron toxicity involve redox imbalance rather than photosynthetic damages in tomato.Crossref | GoogleScholarGoogle Scholar | 32906022PubMed |

Duan X, Liu T, Zhang D, Su X, Lin H, Jiang Y (2011) Effect of pure oxygen atmosphere on antioxidant enzyme and antioxidant activity of harvested litchi fruit during storage. Food Research International 44, 1905–1911.
Effect of pure oxygen atmosphere on antioxidant enzyme and antioxidant activity of harvested litchi fruit during storage.Crossref | GoogleScholarGoogle Scholar |

Ebrahimzadeh MA, Pourmorad F, Bekhradnia AR (2008) Iron chelating activity, phenol and flavonoid content of some medicinal plants from Iran. African Journal of Biotechnology 7, 3188–3192.
Iron chelating activity, phenol and flavonoid content of some medicinal plants from Iran.Crossref | GoogleScholarGoogle Scholar |

Elleuch A, Chaâbene Z, Grubb DC, Drira N, Mejdoub H, Khemakhem B (2013) Morphological and biochemical behavior of fenugreek (Trigonella foenum-graecum) under copper stress. Ecotoxicology and Environmental Safety 98, 46–53.
Morphological and biochemical behavior of fenugreek (Trigonella foenum-graecum) under copper stress.Crossref | GoogleScholarGoogle Scholar | 24135423PubMed |

Fatima A, Farid M, Alharby HF, Bamagoos AA, Rizwan M, Ali S (2020) Efficacy of fenugreek plant for ascorbic acid assisted phytoextraction of copper (Cu); a detailed study of Cu induced morpho-physiological and biochemical alterations. Chemosphere 251, 126424
Efficacy of fenugreek plant for ascorbic acid assisted phytoextraction of copper (Cu); a detailed study of Cu induced morpho-physiological and biochemical alterations.Crossref | GoogleScholarGoogle Scholar | 32443239PubMed |

Gargouri S, Berraies S, Gharbi MS, Paulitz T, Murray TD, Burgess LW (2017) Occurence of sclerotinia stem rot of fenugreek caused by Sclerotinia trifoliorum and S. sclerotiorum in Tunisia. European Journal of Plant Pathology 149, 587–597.
Occurence of sclerotinia stem rot of fenugreek caused by Sclerotinia trifoliorum and S. sclerotiorum in Tunisia.Crossref | GoogleScholarGoogle Scholar |

Ghosh M, Singh S (2005) Review on phytoremediation of heavy metals and utilization of it’s by products. Journal Applied Ecology and Environmental Research 3, 153–179.

Guo M, Perez C, Wei Y, Rapoza E, Su G, Bou-Abdallah F, Chasteen ND (2007) Iron-binding properties of plant phenolics and cranberry’s bio-effects. Dalton Transactions 4951–4961.
Iron-binding properties of plant phenolics and cranberry’s bio-effects.Crossref | GoogleScholarGoogle Scholar | 17992280PubMed |

Hanafy RS, Akladious SA (2018) Physiological and molecular studies on the effect of gamma radiation in fenugreek (Trigonella foenum-graecum L.) plants. Journal of Genetic Engineering and Biotechnology 16, 683–692.
Physiological and molecular studies on the effect of gamma radiation in fenugreek (Trigonella foenum-graecum L.) plants.Crossref | GoogleScholarGoogle Scholar | 30733789PubMed |

Kabir AH, Begum MC, Haque A, Amin R, Swaraz AM, Haider SA, Paul NK, Hossain MM (2016) Genetic variation in Fe toxicity tolerance is associated with the regulation of translocation and chelation of iron along with antioxidant defence in shoots of rice. Functional Plant Biology 43, 1070–1081.
Genetic variation in Fe toxicity tolerance is associated with the regulation of translocation and chelation of iron along with antioxidant defence in shoots of rice.Crossref | GoogleScholarGoogle Scholar | 32480527PubMed |

Kapoor N, Awasthi DK, Vimala Y (2011) Effect of iron toxicity on growth of fenugreek. Journal of Plant Development Sciences 3, 297–300.

Karmakar N, Chakravarty A, Bandopadhyay PK, Das PK (2014) Response of fenugreek (Trigonella foenum-graecum L.) seedlings under moisture and heavy metal stress with special reference to antioxidant system. African Journal of Biotechnology 13, 434–440.
Response of fenugreek (Trigonella foenum-graecum L.) seedlings under moisture and heavy metal stress with special reference to antioxidant system.Crossref | GoogleScholarGoogle Scholar |

Khazan Al MM (2020) Priming with moringa (Moringa oleifera lam.) leaf extract boosts the growth and physio-biochemical attributes of lead-stressed fenugreek (Trigonella foenum-graecum L.) seedlings. Applied Ecology and Environmental Research 18, 6949–6967.
Priming with moringa (Moringa oleifera lam.) leaf extract boosts the growth and physio-biochemical attributes of lead-stressed fenugreek (Trigonella foenum-graecum L.) seedlings.Crossref | GoogleScholarGoogle Scholar |

Kisa D, Kayır Ö, Sağlam N, Şahin S, Öztürk L, Elmastaş M (2019) Changes of phenolic compounds in tomato associated with the heavy metal stress. Journal of Natural and Applied Sciences 2, 35–43.

Licciardello F, Lombardo S, Rizzo V, Pitino I, Pandino G, Strano MG, Muratore G, Restuccia C, Mauromicale G (2018) Integrated agronomical and technological approach for the quality maintenance of ready-to-fry potato sticks during refrigerated storage. Postharvest Biology and Technology 136, 23–30.
Integrated agronomical and technological approach for the quality maintenance of ready-to-fry potato sticks during refrigerated storage.Crossref | GoogleScholarGoogle Scholar |

López A, Rico M, Santana-Casiano JM, González AG, González-Dávila M (2015) Phenolic profile of Dunaliella tertiolecta growing under high levels of copper and iron. Environmental Science and Pollution Research 22, 14820–14828.
Phenolic profile of Dunaliella tertiolecta growing under high levels of copper and iron.Crossref | GoogleScholarGoogle Scholar | 25989863PubMed |

Mahender A, Swamy BPM, Anandan A, Ali J (2019) Tolerance of iron-deficient and -toxic soil conditions in rice. Plants 8, 31
Tolerance of iron-deficient and -toxic soil conditions in rice.Crossref | GoogleScholarGoogle Scholar |

Mishra S, Srivastava S, Tripathi RD, Kumar R, Seth CS, Gupta DK (2006) Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation. Chemosphere 65, 1027–1039.
Lead detoxification by coontail (Ceratophyllum demersum L.) involves induction of phytochelatins and antioxidant system in response to its accumulation.Crossref | GoogleScholarGoogle Scholar | 16682069PubMed |

Nagajyoti PC, Lee KD, Sreekanth TVM (2010) Heavy metals, occurrence and toxicity for plants: a review. Environmental Chemistry Letters 8, 199–216.
Heavy metals, occurrence and toxicity for plants: a review.Crossref | GoogleScholarGoogle Scholar |

Onyango DA, Entila F, Dida MM, Ismail AM, Drame KN (2019) Mechanistic understanding of iron toxicity tolerance in contrasting rice varieties from Africa: 1. Morpho-physiological and biochemical responses. Functional Plant Biology 46, 93–105.
Mechanistic understanding of iron toxicity tolerance in contrasting rice varieties from Africa: 1. Morpho-physiological and biochemical responses.Crossref | GoogleScholarGoogle Scholar |

Pandey N, Verma L (2019) Nitric oxide alleviates iron toxicity by reducing oxidative damage and growth inhibition in wheat (Triticum aestivum L.) Seedlings. International Journal of Plant and Environment 5, 16–22.
Nitric oxide alleviates iron toxicity by reducing oxidative damage and growth inhibition in wheat (Triticum aestivum L.) Seedlings.Crossref | GoogleScholarGoogle Scholar |

Pinto SS, de Souza AE, Oliva MA, Pereira EG (2016) Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron. Scientia Agricola 73, 217–226.
Oxidative damage and photosynthetic impairment in tropical rice cultivars upon exposure to excess iron.Crossref | GoogleScholarGoogle Scholar |

Pugh RE, Dick DG, Fredeen AL (2002) Heavy metal (Pb, Zn, Cd, Fe and Cu) contents of plant foliage near the anvil range lead/zinc mine, Faro, Yukon territory. Ecotoxicology Environmental Safety 52, 273–279.
Heavy metal (Pb, Zn, Cd, Fe and Cu) contents of plant foliage near the anvil range lead/zinc mine, Faro, Yukon territory.Crossref | GoogleScholarGoogle Scholar | 12297090PubMed |

Rico M, López A, Santana-Casiano JM, González AG, González-Dávila M (2013) Variability of the phenolic profile in the diatom Phaeodactylum tricornutum growing under copper and iron stress. Limnology and Oceanography 58, 144–152.
Variability of the phenolic profile in the diatom Phaeodactylum tricornutum growing under copper and iron stress.Crossref | GoogleScholarGoogle Scholar |

Rizzo V, Clifford MN, Brown JE, Siracusa L, Muratore G (2016) Effects of processing on the polyphenol and phenolic acid content and antioxidant capacity of semi-dried cherry tomatoes (Lycopersicon esculentum M.). Journal of the Science of Food and Agriculture 96, 2040–2046.
Effects of processing on the polyphenol and phenolic acid content and antioxidant capacity of semi-dried cherry tomatoes (Lycopersicon esculentum M.).Crossref | GoogleScholarGoogle Scholar | 26089187PubMed |

Rout GR, Sahoo S (2015) Role of iron in plant growth and metabolism. Reviews in Agricultural Science 3, 1–24.
Role of iron in plant growth and metabolism.Crossref | GoogleScholarGoogle Scholar |

Sagisaka S (1976) The occurrence of peroxide in a perennial plant, Populus gelrica. Plant Physiology 57, 308–309.
The occurrence of peroxide in a perennial plant, Populus gelrica.Crossref | GoogleScholarGoogle Scholar | 16659472PubMed |

Salehi A, Fallah S, Kaul H-P, Zitterl-Eglseer K (2018) Antioxidant capacity and polyphenols in buckwheat seeds from fenugreek/buckwheat intercrops as influenced by fertilization. Journal of Cereal Science 84, 142–150.
Antioxidant capacity and polyphenols in buckwheat seeds from fenugreek/buckwheat intercrops as influenced by fertilization.Crossref | GoogleScholarGoogle Scholar |

Santana BVN, de Araújo TO, Andrade GC, de Freitas-Silva L, Kuki KN, Pereira EG, Azevedo AA, da Silva LC (2014) Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential. Environmental Science and Pollution Research 21, 2550–2562.
Leaf morphoanatomy of species tolerant to excess iron and evaluation of their phytoextraction potential.Crossref | GoogleScholarGoogle Scholar |

Sevindik M, Rasul A, Hussain G, Anwar H, Zahoor MK, Sarfraz I, Kamran KS, Akgul H, Akata I, Selamoglu Z (2018) Determination of anti-oxidative, anti-microbial activity and heavy metal contents of Leucoagaricus leucothites. Pakistan Journal of Pharmaceutical Sciences 31, 2163–2168.

Sun W, Shahrajabian MH, Cheng Q (2021) Fenugreek cultivation with emphasis on historical aspects and its uses in traditional medicine and modern pharmaceutical science. Mini-Reviews in Medicinal Chemistry 21, 724–730.
Fenugreek cultivation with emphasis on historical aspects and its uses in traditional medicine and modern pharmaceutical science.Crossref | GoogleScholarGoogle Scholar | 33245271PubMed |

Tadaiesky LBA, da Silva BRS, Batista BL, Lobato AKS (2021) Brassinosteroids trigger tolerance to iron toxicity in rice. Physiologia Plantarum 171, 371–387.
Brassinosteroids trigger tolerance to iron toxicity in rice.Crossref | GoogleScholarGoogle Scholar | 33090462PubMed |

Wang L, Liu B, Wang Y, Qin Y, Zhou Y, Qian H (2020) Influence and interaction of iron and lead on seed germination in upland rice. Plant and Soil 455, 187–202.
Influence and interaction of iron and lead on seed germination in upland rice.Crossref | GoogleScholarGoogle Scholar |

Zayneb C, Bassem K, Zeineb K, Grubb CD, Noureddine D, Hafedh M, Amine E (2015) Physiological responses of fenugreek seedlings and plants treated with cadmium. Environmental Science and Pollution Research 22, 10679–10689.
Physiological responses of fenugreek seedlings and plants treated with cadmium.Crossref | GoogleScholarGoogle Scholar | 25752634PubMed |

Zohra BS, Habib A (2016) Assessment of heavy metal contamination levels and toxicity in sediments and fishes from the Mediterranean Sea (southern coast of Sfax, Tunisia). Environmental Science and Pollution Research 23, 13954–13963.
Assessment of heavy metal contamination levels and toxicity in sediments and fishes from the Mediterranean Sea (southern coast of Sfax, Tunisia).Crossref | GoogleScholarGoogle Scholar | 27040542PubMed |