Efficiency of antioxidant system in barrel medic (Medicago truncatula) genotypes and the orchestration of their key components under iron deficiency
Nadia Kallala A B , Wissal M’sehli
A , Khaoula Mkadmini Hammi C , Ghassen Abid A and Haythem Mhadhbi A D
+ Author Affiliations
- Author Affiliations
A Laboratory of Legumes and Sustainable Agrosystems, Centre of Biotechnology of Borj-Cedria, (L2AD, CBBC) P. B. 901, 2050 Hammam-Lif, Tunisia.
B University Tunis El Manar (UTM), Faculty of Sciences of Tunis (FST), 2092 Tunis, Tunisia.
C Laboratory of Medicinal and Aromatic Plants Biotechnology Centre of Borj-Cedria, Hammam-Lif 2050, Tunisia.
D Corresponding author. Email: mhadhbihay@yahoo.fr
Crop and Pasture Science - https://doi.org/10.1071/CP21041
Submitted: 22 January 2021 Accepted: 21 April 2021 Published online: 14 July 2021
Abstract
Iron (Fe) deficiency leads to an overproduction of reactive oxygen species (ROS) in plants that activate their antioxidant systems to control oxidative burst. In this study, contrasting Medicago truncatula genotypes, A17 and TN8.20 (tolerant) and TN1.11 (sensitive), were grown under Fe deficiency. The superoxide dismutase (SOD: EC1.15.1.1) activity, their isoforms’ coding genes, the copper chaperone expression patterns, and leaf phenolic contents were analysed. Our results showed that Fe deficiency decreases the photosynthetic capacity and plant biomass production with a prominent effect on TN1.11 genotype. The tolerance of A17 and TN8.20 was correlated with a maintenance of Fe content and the photosynthetic apparatus and an increase of Cu concentration compared with the sensitive genotype. We revealed a significant increase of H2O2 in Fe-deficient plants, mainly in TN1.11 sensitive genotype. TN8.20 and A17 tolerance were concomitant with a significant increase of SOD activities (SOD, Cu/Zn-SOD, and Mn-SOD) under Fe deficiency. This increment was correlated to an induction of the copper chaperone gene expression level, as well as an accumulation of isoquercitin phenolic compound. Our study provides new insights into the orchestration of SOD’s isoforms activities, the expression of the copper chaperone, FeSOD, Cu/ZnSOD genes, and the leaf phenolic compounds accumulation that allows Medicago truncatula to overcome Fe deficiency.
Keywords: antioxidant capacity, gene expression, genotype variation, Fe starvation, legumes, Medicago truncatula.
References
Abid G, Ouertani RN, Jebara SH, Boubakri H, Muhovski Y, Ghouili E, Abdelkarim S, Chaieb O, Hidri Y, Kadri S, El Ayed M, Elkahoui S, Barhoumi F, Jebara M (2020) Alleviation of drought stress in faba bean (Vicia faba L.) by exogenous application of β-aminobutyric acid (BABA). Physiology and Molecular Biology of Plants 26, 1173–1186.| Alleviation of drought stress in faba bean (Vicia faba L.) by exogenous application of β-aminobutyric acid (BABA).Crossref | GoogleScholarGoogle Scholar | 32549681PubMed |
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341.
| Role of superoxide dismutases (SODs) in controlling oxidative stress in plants.Crossref | GoogleScholarGoogle Scholar | 11997379PubMed |
Arora D, Bhatla SC (2017) Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radical Biology & Medicine 106, 315–328.
| Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD.Crossref | GoogleScholarGoogle Scholar |
Banerjee A, Roychoudhury A (2019) Abiotic stress tolerance in plants by priming and pretreatment with hydrogen peroxide. In ‘Priming and pretreatment of seeds and seedlings’. (Eds M Hasanuzzaman, V Fotopoulos) pp. 417–426. (Springer: Singapore)
Barman A, Marak CM, Barman RM, Sangma CS (2018) Nutraceutical properties of legume seeds and their impact on human health. In ‘Legume seed nutraceutical research’. pp. 4–24. (IntechOpen)
Bracher A (2019) Les légumineuses comme alternative aux protéines importées. Recherche Agronomique Suisse 10, 180–189.
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilising the principal of protein-dye binding. Analytical Biochemistry 72, 248–254.
| A rapid and sensitive method for the quantification of microgram quantities of proteins utilising the principal of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 942051PubMed |
Carrasco-Gil S, Rodríguez-menéndez S, Fernández B, Pereiro R, De la Fuente V, Hernandez-apaolaza L (2018) Silicon induced Fe deficiency affects Fe, Mn, Cu and Zn distribution in rice (Oryza sativa L.) growth in calcareous conditions. Plant Physiology and Biochemistry 125, 153–163.
| Silicon induced Fe deficiency affects Fe, Mn, Cu and Zn distribution in rice (Oryza sativa L.) growth in calcareous conditions.Crossref | GoogleScholarGoogle Scholar | 29453092PubMed |
Castro PH, Lilay GH, Assunção AGL (2018) Regulation of micronutrient homeostasis and deficiency response in plants. In ‘Plant micronutrient use efficiency: molecular and genomic perspectives in crop plants’. (Eds MA Hossain, T Kamiya, DJ Burritt, LSP Tran, T Fujiwara) pp. 1–15. (Academic Press) https://doi.org/10.1016/B978-0-12-812104-7.00002-2
Chang S, Puryear J, Cairney J (1993) A simple and efficient method for isolating RNA from pine trees. Plant Molecular Biology Reporter 11, 113–116.
| A simple and efficient method for isolating RNA from pine trees.Crossref | GoogleScholarGoogle Scholar |
da Silveira VC, de Oliveira AP, Sperotto RA, Espindola LS, Amaral L, Dias JF, Da Cunha JB, Fett JP (2007) Influence of iron on mineral status of two rice (Oryza sativa L.) cultivars. Brazilian Journal of Plant Physiology 19, 127–139.
| Influence of iron on mineral status of two rice (Oryza sativa L.) cultivars.Crossref | GoogleScholarGoogle Scholar |
David AVA, Arulmoli R, Parasuraman S (2016) Overviews of biological importance of quercetin: a bioactive flavonoid. Pharmacognosy Reviews 10, 84–89.
| Overviews of biological importance of quercetin: a bioactive flavonoid.Crossref | GoogleScholarGoogle Scholar |
Dey S, Chowardhara B, Regon P, Kar S, Saha B, Panda SK (2020) Iron deficiency in blackgram (Vigna mungo L.): redox status and antioxidant activity. Plant Biosystems.
| Iron deficiency in blackgram (Vigna mungo L.): redox status and antioxidant activity.Crossref | GoogleScholarGoogle Scholar |
dos Santos LR, Paula LdS, Pereira YC, da Silva BRS, Batista BL, Alsahli AA, Lobato AK da S (2020) Brassinosteroids-mediated amelioration of iron deficiency in soybean plants: beneficial effects on the nutritional status, photosynthetic pigments and chlorophyll fluorescence. Journal of Plant Growth Regulation.
| Brassinosteroids-mediated amelioration of iron deficiency in soybean plants: beneficial effects on the nutritional status, photosynthetic pigments and chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |
Gao S, Wang Y, Yu S, Huang Y, Liu H (2020) Effects of drought stress on growth, physiology and secondary metabolites of two Adonis species in Northeast China. Scientia Horticulturae 259, 108795
| Effects of drought stress on growth, physiology and secondary metabolites of two Adonis species in Northeast China.Crossref | GoogleScholarGoogle Scholar |
Gepts P, Beavis WD, Brummer EC, Shoemaker RC, Stalker HT, Weeden NF, Young ND (2005) Legumes as a Model Plant Family. Genomics for Food and Feed Report of the Cross-Legume Advances through Genomics Conference. Plant Physiology 137, 1228–1235.
| Legumes as a Model Plant Family. Genomics for Food and Feed Report of the Cross-Legume Advances through Genomics Conference.Crossref | GoogleScholarGoogle Scholar | 15824285PubMed |
Grusak MA (1995) Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L. (Fabaceae): relevance to the iron nutrition of developing seeds. Planta 197, 111–117.
| Whole-root iron(III)-reductase activity throughout the life cycle of iron-grown Pisum sativum L. (Fabaceae): relevance to the iron nutrition of developing seeds.Crossref | GoogleScholarGoogle Scholar |
Hammi KM, Ennigrou DJ, Majdoub H, Ksouri R (2017) Recovery of phenolic compounds and carbohydrates from hydro-ethanolic extract of Zizyphus lotus fruit using ultrafiltration process. International Journal of Food Engineering 13, 20170343
| Recovery of phenolic compounds and carbohydrates from hydro-ethanolic extract of Zizyphus lotus fruit using ultrafiltration process.Crossref | GoogleScholarGoogle Scholar |
Imran M, Rauf A, Shah ZA, Saeed F, Imran A, Arshad MU, Ahmad B, Bawazeer S, Atif M, Peters DG, Mubarak MS (2019) Chemo-preventive and therapeutic effect of the dietary flavonoid kaempferol: a comprehensive review. Phytotherapy Research 33, 263–275.
| Chemo-preventive and therapeutic effect of the dietary flavonoid kaempferol: a comprehensive review.Crossref | GoogleScholarGoogle Scholar | 30402931PubMed |
Kallala N, M’sehli W, Jelali K, Batnini M, Badri M, Nouairi I, Mhadhbi H (2019) Biodiversity within Medicago truncatula genotypes toward response to iron deficiency: investigation of main tolerance mechanisms. Plant Species Biology 34, 95–109.
| Biodiversity within Medicago truncatula genotypes toward response to iron deficiency: investigation of main tolerance mechanisms.Crossref | GoogleScholarGoogle Scholar |
Kavita , Kumar V (2020) Effect of iron and phytohormones application on antioxidant enzymes activity, chlorophyll and grain yield of maize in iron-deficient soil. Current Journal of Applied Science and Technology 39, 100–109.
Kaya C, Akram N, Ashref M (2019) Influence of exogenously applied nitric oxide on strawberry (Fragaria × ananassa) plants grown under m deficiency and/or saline stress. Physiologia Plantarum 165, 247–263.
| Influence of exogenously applied nitric oxide on strawberry (Fragaria × ananassa) plants grown under m deficiency and/or saline stress.Crossref | GoogleScholarGoogle Scholar | 30091474PubMed |
Kaya C, Ashraf M, Alyemeni MN, Ahmad P (2020) Nitrate reductase rather than nitric oxide synthase activity is involved in 24-epibrassinolide-induced nitric oxide synthesis to improve tolerance to iron deficiency in strawberry (Fragaria × annassa) by up-regulating the ascorbate-glutathione cycle. Plant Physiology and Biochemistry 151, 486–499.
| Nitrate reductase rather than nitric oxide synthase activity is involved in 24-epibrassinolide-induced nitric oxide synthesis to improve tolerance to iron deficiency in strawberry (Fragaria × annassa) by up-regulating the ascorbate-glutathione cycle.Crossref | GoogleScholarGoogle Scholar | 32302942PubMed |
Kurutas EB (2015) The importance of antioxidants which play the role in cellular response against oxidative / nitrosative stress: current state. Nutrition Journal 15, 71
| The importance of antioxidants which play the role in cellular response against oxidative / nitrosative stress: current state.Crossref | GoogleScholarGoogle Scholar |
Le CTT, Brumbarova T, Bauer P (2019) The interplay of ROS and iron signaling in plants. In ‘Redox homeostasis in plants’. pp. 43–66. (Springer: Cham)
Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods in Enzymology 148, 350–382.
| Chlorophylls and carotenoids: pigments of photosynthetic biomembranes.Crossref | GoogleScholarGoogle Scholar |
M’sehli W, Houmani H, Donnini S, Zocchi G, Abdelly C, Gharsalli M (2014) Iron deficiency tolerance at leaf level in Medicago ciliaris plants. American Journal of Plant Sciences 5, 2541–2553.
| Iron deficiency tolerance at leaf level in Medicago ciliaris plants.Crossref | GoogleScholarGoogle Scholar |
Mabrouk Y, Hemissi I, Salem B, Mejri S, Saidi M, Belhadj O (2018) Potential of rhizobia in improving nitrogen fixation and yields of legumes. In ‘Symbiosis’. (Ed. E Cid Rigobelo) pp. 1–15.
Mahanty S, Kaul T, Pandey P, Reddy RA, Mallikarjuna G, Reddy CS, Sopory SK, Reddy MK (2012) Biochemical and molecular analyses of copper–zinc superoxide dismutase from a C4 plant Pennisetum glaucum reveals an adaptive role in response to oxidative stress. Gene 505, 309–317.
| Biochemical and molecular analyses of copper–zinc superoxide dismutase from a C4 plant Pennisetum glaucum reveals an adaptive role in response to oxidative stress.Crossref | GoogleScholarGoogle Scholar | 22688121PubMed |
Martínez JJM, Naso LG, Pérez AL, Rizzi A, Ferrer EG, Williams PAM (2017) Antioxidant and anticancer effects and bioavailability studies of the flavonoid baicalin and its oxidovanadium (IV) complex. Journal of Inorganic Biochemistry 166, 150–161.
| Antioxidant and anticancer effects and bioavailability studies of the flavonoid baicalin and its oxidovanadium (IV) complex.Crossref | GoogleScholarGoogle Scholar |
Masuda H, Aung MS, Maeda K, Kobayashi T, Taniguchi T, Nishizawa NK (2018) Iron-deficiency response and expression of genes related to iron homeostasis in poplars. Soil Science and Plant Nutrition 64, 576–588.
| Iron-deficiency response and expression of genes related to iron homeostasis in poplars.Crossref | GoogleScholarGoogle Scholar |
Pandey N (2017) Impact of iron stress on oxidative metabolism in green gram plants (Vigna radiata (L.) Wilczek). Journal of Biosciences 6, 5120–5130.
Rahoui S, Martinez Y, Sakouhi L, Ben C, Rickauer M, El Ferjani E, Gentzbittel L, Chaoui A (2017) Cadmium-induced changes in antioxidative systems and differentiation in roots of contrasted Medicago truncatula lines. Protoplasma 254, 473–489.
| Cadmium-induced changes in antioxidative systems and differentiation in roots of contrasted Medicago truncatula lines.Crossref | GoogleScholarGoogle Scholar | 27055657PubMed |
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 |
Samsonowicz M, Regulska E (2017) Spectroscopic study of molecular structure, antioxidant activity and biological effects of metal hydroxyflavonol complexes. Spectrochimica Acta. Part A: Molecular and Biomolecular Spectroscopy 173, 757–771.
| Spectroscopic study of molecular structure, antioxidant activity and biological effects of metal hydroxyflavonol complexes.Crossref | GoogleScholarGoogle Scholar |
Sharma P, Kumar A, Bhardwaj R (2016) Plant steroidal hormone epibrassinolide regulate heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression. Environmental and Experimental Botany 122, 1–9.
| Plant steroidal hormone epibrassinolide regulate heavy metal stress tolerance in Oryza sativa L. by modulating antioxidant defense expression.Crossref | GoogleScholarGoogle Scholar |
Song J, Zeng L, Chen R, Wang Y, Zhou Y (2018) In silico identification and expression analysis of superoxide dismutase (SOD) gene family in Medicago truncatula. 3 Biotech 8, 348
| In silico identification and expression analysis of superoxide dismutase (SOD) gene family in Medicago truncatula.Crossref | GoogleScholarGoogle Scholar | 30073133PubMed |
Soulé M, Bassirou ID, Saley K, Matalabi AA, Oumani AA, Mahamane A, Mahamane S (2017) Floristic composition, structural analysis and socio-economic importance of legume flora of the commune of Mayahi, Niger, West Africa. IJEAB 2, 1322–1329.
| Floristic composition, structural analysis and socio-economic importance of legume flora of the commune of Mayahi, Niger, West Africa.Crossref | GoogleScholarGoogle Scholar |
Sun C, Wu T, Zhai L, Li D, Zhang X, Xu X, Ma H, Wang Y, Han Z (2016) Reactive oxygen species Function to mediate the Fe deficiency response in an Fe-efficient apple genotype: an early response mechanism for enhancing reactive oxygen production. Frontiers in Plant Science 7, 1726
| Reactive oxygen species Function to mediate the Fe deficiency response in an Fe-efficient apple genotype: an early response mechanism for enhancing reactive oxygen production.Crossref | GoogleScholarGoogle Scholar | 27899933PubMed |
Teixeira GCM, Prado RDM, Oliveira KS, D’Amico-Damico V, da Silveira Sousa G (2020) Silicon increases leaf chlorophyll content and iron nutritional efficiency and reduces iron deficiency in sorghum plants. Journal of Soil Science and Plant Nutrition 20, 1311–1320.
| Silicon increases leaf chlorophyll content and iron nutritional efficiency and reduces iron deficiency in sorghum plants.Crossref | GoogleScholarGoogle Scholar |
Torabian S, Morteza SF (2018) Efficacy of FeSO4 nano formulations on osmolytes and antioxidative enzymes of sunflower under salt stress. Indian Journal of Plant Physiology 23, 305–315.
| Efficacy of FeSO4 nano formulations on osmolytes and antioxidative enzymes of sunflower under salt stress.Crossref | GoogleScholarGoogle Scholar |
Vadez V, Rodier F, Payre H, Drevon JJ (1996) Nodule permeability to O2 and nitrogenase-linked respiration in bean genotypes varying in the tolerance of N2 fixation to P deficiency. Plant Physiology and Biochemistry 34, 871–878.
Valipour M, Baninasab B, Khoshgoftarmanesh AH, Gholami M (2020) Oxidative stress and antioxidant responses to direct and bicarbonate-induced iron deficiency in two quince rootstocks. Scientia Horticulturae 261, 108933
| Oxidative stress and antioxidant responses to direct and bicarbonate-induced iron deficiency in two quince rootstocks.Crossref | GoogleScholarGoogle Scholar |
Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain-treated bean plants Protective role of exogenous polyamines. Plant Science 151, 59–66.
| Oxidative stress and some antioxidant systems in acid rain-treated bean plants Protective role of exogenous polyamines.Crossref | GoogleScholarGoogle Scholar |
Vogel C, Marcotte EM (2012) Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nature Reviews. Genetics 13, 227–232.
| Insights into the regulation of protein abundance from proteomic and transcriptomic analyses.Crossref | GoogleScholarGoogle Scholar | 22411467PubMed |
Wang F, Liu J, Zhou L, Pan G, Li Z (2016) Plant physiology and biochemistry senescence-specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves. Plant Physiology and Biochemistry 109, 248–261.
| Plant physiology and biochemistry senescence-specific change in ROS scavenging enzyme activities and regulation of various SOD isozymes to ROS levels in psf mutant rice leaves.Crossref | GoogleScholarGoogle Scholar | 27756006PubMed |
Wasli H, Jelali N, Silva AMS, Ksouri R, Cardoso SM (2018) Variation of polyphenolic composition, antioxidants and physiological characteristics of dill (Anethum graveolens L.) as affected by bicarbonate-induced iron deficiency conditions. Industrial Crops and Products 126, 466–476.
| Variation of polyphenolic composition, antioxidants and physiological characteristics of dill (Anethum graveolens L.) as affected by bicarbonate-induced iron deficiency conditions.Crossref | GoogleScholarGoogle Scholar |
Waters BM, McInturf SA, Stein RJ (2012) Rosette iron deficiency transcript and micro RNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. Journal of Experimental Botany 63, 5903
| Rosette iron deficiency transcript and micro RNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 22962679PubMed |
Zhai L, Sun C, Feng Y, Li D, Chai X, Wang L (2018) AtROP6 is involved in reactive oxygen species signaling in response to iron-deficiency stress in Arabidopsis thaliana. FEBS Letters 592, 3446–3459.
| AtROP6 is involved in reactive oxygen species signaling in response to iron-deficiency stress in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 30238451PubMed |
Zhou Y, Hu L, Wu H, Jiang L, Liu S (2017) Genome-wide identification and transcriptional expression analysis of cucumber superoxide dismutase (SOD) Family in response to various abiotic stresses. International Journal of Plant Genomics 2017, 7243973
