Abstract
The effect of calcareous soil on growth, photosynthetic gas exchanges, symbiotic nitrogen fixation (SNF), iron nutrition, and antioxidative enzymes activities was investigated in two lines of Medicago truncatula: TN8.20 and Jemalong. The results showed that growth (especially in shoots) was significantly lower on calcareous soil in both lines, but Jemalong was more impacted than TN8.20. Plants cultivated on calcareous soil showed significantly lower values for photosynthesis activity (as net CO2 assimilation and stomatal conductance) and nodule performance (nodulation, nodule growth and SNF), but this trend was more pronounced in the sensitive line (Jemalong). The better performance of TN8.20 as compared to Jemalong could be ascribed due to its aptitude to preferentially allocate iron to nodules, thereby ensuring nodule growth and a higher SNF activity, besides showing higher iron use efficiency for SNF. In both lines, superoxide dismutase (SOD, EC.15.1.1), catalase (EC.1.11.1.6), and peroxidase (POX, EC 1.11.1.7) activities were increased significantly when they were grown on a calcareous soil. Yet, this tendency was more pronounced in the tolerant line, TN8.20. Overall, our results strongly suggest that on calcareous soils, the successful adaptation of TN8.20 would be related to its ability to induce an antioxidant response in order to preserve important metabolic paths such as photosynthetic activity and symbiotic nitrogen fixation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abadía J, Morales F, Abadía A (2000) Photosystem efficiency in low chlorophyll, iron deficient leaves. Plant Soil 215:183–192
Abadía J, Vázquez S, Rellán-Álvarez R (2011) Towards a knowledge-based correction of iron chlorosis. Plant Physiol Biochem 49:471–482. https://doi.org/10.1016/j.plaphy.2011.01.026
Anderson MD, Prasad TK, Stewart CR (1995) Changes in isozyme profiles of catalase, peroxidase and glutathione reductase during acclimation to chilling in mesocotyls of maize seedlings. Plant Physiol 109:1247–1257. https://doi.org/10.1104/pp.109.4.1247
Aydi S, Drevon JJ, Abdelly C (2004) Effect of salinity on rootnodule conductance to the oxygen diffusion in the Medicago truncatula–Sinorhizobium meliloti symbiosis. Plant Physiol Biochem 42:833–840. https://doi.org/10.1016/j.plaphy.2004.10.003
Beauchamp C, Fridovich I (1971) Superoxide dismutase, improved assays and an assay applicable to acrylamide gels. Anal Biochem 44:276–287. https://doi.org/10.1016/0003-2697(71)90370-8
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of proteins utilizing the principal of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3
Briat JF, Vert G (2004) Acquisition et gestion du fer par les plantes. Cah Agric 13:183–201
Brumbarova T, Bauer P, Ivanov R (2015) Molecular mechanisms governing Arabidopsis iron uptake. Trends Plant Sci 20:124–133. https://doi.org/10.1016/j.tplants.2014.11.004
Busch AWU, Montgomery BL (2015) Interdependence of tetrapyrrole metabolism, the generation of oxidative stress and the mitigative oxidative stress response. Redox Biol 4:260–271. https://doi.org/10.1016/j.redox.2015.01.010
Carvalho SMP, Vasconcelos MW (2013) Producing more with less: Strategies and novel technologies for plant-based food biofortification. Food Res Int 54:961–971. https://doi.org/10.1016/j.foodres.2012.12.021
Chatterjee A, Lovas S, Rasmussena H, Goos RJ (2017) Foliar application of iron fertilizers to control iron deficiency chlorosis of soybean. Crop. Forage Turfgrass Manag. 3:1–7. https://doi.org/10.2134/cftm2017.05.0037
Clarke VC, Loughlin PC, Day DA, Smith PMC (2014) Transport processes of the legume symbiosome membrane. Front Plant Sci 5:699. https://doi.org/10.3389/fpls.2014.00699
Cook D (1999) Medicago truncatula: A model in the making! Curr Opin Plant Biol 2:301–304. https://doi.org/10.1016/s1369-5266(99)80053-3
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Env Sci 2:53. https://doi.org/10.3389/fenvs.2014.00053
Day DA, Smith PMC (2021) Iron Transport across Symbiotic Membranes of Nitrogen-Fixing Legumes. Int J Mol Sci 22:432. https://doi.org/10.3390/ijms22010432
Donnini S, Dell’Orto M, Zocchi G (2011) Oxidative stress responses and root lignification induced by Fe deficiency conditions in pear and quince genotypes. Tree Physiol 31:102–113. https://doi.org/10.1093/treephys/tpq105
Downie JA (2005) Legume haemoglobins: symbiotic nitrogen fixation needs bloody nodules. Current Biol 15:196–197. https://doi.org/10.1016/j.cub.2005.03.007
Elkhouni A, Rabhi M, Ivanov AG, Krol M, Zorrig W, Smaoui A (2017) Structural and functional integrity of Sulla carnosa photosynthetic apparatus under iron deficiency conditions. Plant Biol 20:415–425. https://doi.org/10.1111/plb.12684
Ellwood SR, D’Souza NK, Kamphuis LG, Burgess TI, Nair RM, Oliver RP (2006) SSR analysis of the Medicago truncatula SARDI core collection reveals substantial diversity and unusual genotype dispersal throughout the Mediterranean basin. Theor Appl Genet 112:977–983. https://doi.org/10.1007/s00122-005-0202-1
Ferreira CMH, López-Rayo S, Lucena JJ, Soares EV, Soares HMVM (2019) Evaluation of the efficacy of two new biotechnological-based freeze- dried fertilizers for sustainable Fe deficiency correction of soybean plants grown in calcareous soils. Front Plant Sci 10:1335. https://doi.org/10.3389/fpls.2019.01335
Gonzalez-Guerrero M, Escudero V, Saez A, Tejada-Jimenez M (2016) Transition metal transport in plants and associated endosymbionts: Arbuscular mycorrhizal fungi and rhizobia. Front Plant Sci. 7:1088. https://doi.org/10.3389/fpls.2016.01088
Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322. https://doi.org/10.1104/pp.106.077073
Hansen NC, Hopkins BG, Ellsworth JW, Jolley VD (2006) Iron nutrition in field crops. In: Barton LL, Abadía J (eds) Iron Nutrition in Plants and Rhizospheric Microorganisms. Springer, Dordrecht, pp 23–59. https://doi.org/10.1007/1-4020-4743-6_2
Iturbe-Ormaetxe I, Moran JF, Arrese-Igor C, Gogorcena Y, Klucas RV, Becana M (1995) Activated oxygen and antioxidant defences in iron-deficient pea plants. Plant Cell Environ 18:421–429. https://doi.org/10.1111/j.1365-3040.1995.tb00376.x
Jelali N, Donnini S, Dell’orto M, Abdelly C, Gharsalli M, Zocchi G (2014) Root antioxidant responses of two Pisum sativum cultivars to direct and induced Fe deficiency. Plant Biol 16:607–614. https://doi.org/10.1111/plb.12093
Jelali N, Donnini S, Dellorto M, Abdelly C, Gharsalli M, Zocchi G (2017) Implication of antioxidant defence in tolerance to Fe deficiency of pisum sativum leaves. J Appl Biotechnol Bioeng 5:164–173. https://doi.org/10.15406/jabb.2017.02.00041
Jin LF, Liu YZ, Du W, Fu LN, Hussain SB, Peng SA (2017) Physiological and transcriptional analysis reveals pathways involved in iron deficiency chlorosis in fragrant citrus. Tree Genet Genomes 13:51–59. https://doi.org/10.1007/s11295-017-1136-x
Khan MA, Nguyen NT (2020) Chapter eight – Genome editing of staple crop plants to combat iron deficiency. In: Kiran U, Abdin MZ, Kamaluddin (eds) Transgenic Technology Based Value Addition in Plant Biotechnology. Academic Press, London, pp 187–206. https://doi.org/10.1016/B978-0-12-818632-9.00008-3
Kobayashi T, Nozoye T, Nishizawa NK (2019) Iron transport and its regulation in plants. Free Radic. Biol. Med. 133:11–20. https://doi.org/10.1016/j.freeradbiomed.2018.10.439
Köscoglu AT, Açikgöz V (1995) Determination of iron chlorosis with extractable iron analysis in peach leaves. J Plant Nutr 18:153–161. https://doi.org/10.1080/01904169509364892
Krouma A, Drevon JJ, Abdelly C (2006) Genotypic variation of N2 fixing common bean (Phaseolus vulgaris L.) in response to iron deficiency. J Plant Physiol 163:1094–1100. https://doi.org/10.1016/j.jplph.2005.08.013
Larbi A, Abadía A, Abadía J, Morales F (2006) Down co-regulation of light absorption, photochemistry, and carboxylation in Fe-deficient plants growing in different environments. Photosynth Res 89:113–126. https://doi.org/10.1007/s11120-006-9089-1
Li G, Wang B, Tian Q, Wang T, Wen-Hao Zhang W (2014) Medicago truncatula ecotypes A17 and R108 differed in their response to iron deficiency. J Plant Physiol 171:639–647. https://doi.org/10.1016/j.jplph.2013.12.018
Li G, Kronzucker HJ, Shi W (2016) The Response of the Root Apex in Plant Adaptation to Iron Heterogeneity in Soil. Front Plant Sci. 7:344. https://doi.org/10.3389/fpls.2016.00344
Li H, Wang L, Yang ZM (2015) Co-expression analysis reveals a group of genes potentially involved in regulation of plant response to iron-deficiency. Gene 554:16–24. https://doi.org/10.1016/j.gene.2014.10.004
Lund RE (1989) A User’s Guide to MSUSTAT Statistical Analysis Package Microcomputer version 4(12), p 202
M’Sehli W, Youssfi S, Donnini S, Dell’Orto M, De Nisi P, Zocchi G, Abdelly C, Gharsalli M (2008) Root exudation and rhizosphere acidification by two lines of Medicago ciliaris in response to lime-induced iron deficiency. Plant soil 312:151–162. https://doi.org/10.1007/s11104-008-9638-9
Mahmoudi H, Labidi N, Ksouri R, Gharsalli M, Abdelly C (2007) Differential tolerance to iron deficiency of chickpea varieties and Fe resupply effects. C R Biol 330:237–246. https://doi.org/10.1016/j.crvi.2007.02.007
Marino D, Damiani I, Gucciardo S, Mijangos I, Pauly N, Puppo A (2013) Inhibition of nitrogen fixation in symbiotic Medicago truncatula up on Cd exposure is a local process involving leghemoglobin. J Exp Bo 64:5651–5660. https://doi.org/10.1093/jxb/ert334
Marschner H (1995) Mineral Nutrition of Higher Plants. Academic Press, London
Mbonankira JE, Coq S, Vromman D, Lutts S, Nizigiyimana A, Bertin P (2015) Catalase and ascorbate peroxidase activities are not directly involved in the silicon-mediated alleviation of ferrous iron toxicity in rice. J Plant Nutr Soil Sci 178:477–485. https://doi.org/10.1002/jpln.201400068
Mengel K (1995) Iron availability in plant tissues-iron chlorosis on calcareous soils. Plant Soil 165:275–283
Mikami Y, Saito A, Miwa E, Higuchi K (2011) Allocation of Fe and ferric chelate reducatse activities in mesophyll cells of barley and sorghum under Fe-deficient conditions. Plant Physiol Biochem 49:513–519. https://doi.org/10.1016/j.plaphy.2011.01.009
Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498. https://doi.org/10.1016/j.tplants.2004.08.009
Moreau S, Meyer JM, Puppo A (1995) Uptake of iron by symbiosomes and bacteroids from soybean nodules. FEBS Letters 361:225–228. https://doi.org/10.1016/0014-5793(95)00155-3
Moseley JL, Allinger T, Herzog S, Hoerth P, Wehinger E, Merchant S, Hippler M (2002) Adaptation to Fe-deficiency requires remodeling of the photosynthetic apparatus. The EMBO Journal 21:6709–6720. https://doi.org/10.1093/emboj/cdf666
Nozoye T, Nagasaka S, Kobayashi T, Takahashi M, Sato Y, Sato Y, Nobuyuki Uozumi N, Nakanishi H, Nishizawa NK (2011) Phytosiderophore efflux transporters are crucial for iron acquisition in graminaceous plants. J Biol Chem 286:5446–5454. https://doi.org/10.1074/jbc.M110.180026
Orikasa Y, Nodasaka Y, Ohyama T, Okuyama H, Ichise N, Yumoto I, Morita N, Wei M, Ohwada T (2010) Enhancement of the nitrogen fixation efficiency of genetically-engineered Rhizobium with high catalase activity. J. Biosci. Bioeng 110:397–402. https://doi.org/10.1016/j.jbiosc.2010.04.007
Osório J, Osório ML, Correia PJ, VarennesA Pestana M (2014) Chlorophyll fluorescence imaging as a tool to understand the impact of iron deficiency and resupply on photosynthetic performance of strawberry plants. Sci Hortic 165:148–155. https://doi.org/10.1016/j.scienta.2013.10.042
Pestana M, Correia PJ, Saavedra T, Gama F, Abadía A, de Varennes A (2012) Development and recovery of iron deficiency by iron resupply to roots or leaves of strawberry plants. Plant Physiol Biochem 53:1–5. https://doi.org/10.1016/j.plaphy.2012.01.001
Prasad PVV (2003) Nutrition | iron chlorosis. Encyclopedia of Applied Plant Sciences pp. 649–656. https://doi.org/10.1016/B0-12-227050-9/00240-4
Porcel R, Barea JM, Ruiz-Lozano JM (2003) Antioxidant activities in mycorrhizal soybean plants under drought stress and their possible relationship to the process of nodule senescence. New Phytol 157:135–143. https://doi.org/10.1046/j.1469-8137.2003.00658.x
Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R (2014) Hydrogen peroxideand nitric oxide: key regulators of the legume-rhizobium and mycorrhizalsymbioses. Antioxid Redox Signal 18:2202–2219. https://doi.org/10.1089/ars.2012.5136
Ramirez L, Bartoli CG, Lamattina L (2013) Glutathione and ascorbic acid protect Arabidopsis plants against detrimental effects of iron deficiency. J Exp Bot 64:3169–3178. https://doi.org/10.1093/jxb/ert153
Rodriguez-Haas B, Finney L, Vogt S, Gonzalez-Melendi P, Imperial J, Gonzalez-Guerrero M (2013) Iron distribution through the developmental stages of Medicago truncatula nodules. Metallomics 5:1247–1253. https://doi.org/10.1039/c3mt00060e
Santos SC, Ozgur R, Uzilday B, Turkan I, Roriz M, Rangel AOSS, Susana MP, Carvalho SMP, Vasconcelos MW (2019) Understanding the role of the antioxidant system and the tetrapyrrole cycle in iron deficiency chlorosis. Plants 8:348. https://doi.org/10.3390/plants8090348
Saito A, Iino T, Sonoike K, Miwa E, Higuchi K (2010) Remodeling of the major light-harvesting antenna protein of PSII protects the young leaves of barley (Hordeum vulgare L.) from photoinhibition under prolonged iron deficiency. Plant Cell Physiol 51:2013–2030. https://doi.org/10.1093/pcp/pcq160
Satbhai SB, Setzer C, Freynschlag F, Slovak R, Kerdaffrec E, Busch W (2017) Natural allelic variation of FRO2 modulates Arabidopsis root growth under iron deficiency. Nature Communications. 8:15603. https://doi.org/10.1038/ncomms15603
Schmidt W (1999) Mechanisms and regulation of reduction-based iron uptake in plants. New Phytol 141:1–26. https://doi.org/10.1046/j.1469-8137.1999.00331.x
Shenker M, Chen Y (2005) Increasing iron availability to crops: Fertilizers, organo-fertilizers, and biological approaches. Soil Sci Plant Nutr 51:1–17. https://doi.org/10.1111/j.17470765.2005.tb00001.x
Slatni T, Ben Salah I, Kouas S, Abdelly C (2014) The roles of nodules in the tolerance of common bean to iron deficiency. J Plant Res. 127:455–465. https://doi.org/10.1007/s10265-014-0632-4/
Slatni T, Krouma A, Aydi S, Chaiffi C, Gouia H, Abdelly C (2008) Growth, nitrogen fixation and ammonium assimilation in common bean (Phaseolus vulgaris L) subjected to iron deficiency. Plant Soil 312:49–57. https://doi.org/10.1007/s11104-007-9481-4
Slatni T, Krouma A, Gouia H, Abdelly C (2009) Importance of ferric-chelate reductase activity and acidification capacity in root nodules of N2-fixing Common bean (Phaseolus vulgaris L) Subjected to iron deficiency. Symbiosis 47:35–42
Sun B, Jing Y, Chen K, Song L, Chen F, Zhang L (2007) Protective effect of nitric oxide on iron deficiency-induced oxidative stress in maize (Zea mays). J Plant Physiol 164:536–543. https://doi.org/10.1016/j.jplph.2006.02.011
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. Front Plant Sci 7:1726. https://doi.org/10.3389/fpls.2016.01726
Taalab AS, Ageeb GW, Siam HS, Mahmoud SA (2019) Some Characteristics of Calcareous soils. A review. Middle East J Agric Res 8:96–105
Taha AIBHM, Okuyama H, Ohwada T et al (2012) Exogenous catalase gene expression as a tool for enhancing metabolic activity and production of biomaterials in host microorganisms. In: Agbo EC (ed) Innovations in biotechnology. In-Tech, Rijeka, pp 251–276
Tang C, Hinsinger P, Drevon JJ, Jaillard B (2000) Phosphorus deficiency impairs early nodule functioning and enhances proton release in roots of Medicago truncatula L. Ann Bot 88:131–138. https://doi.org/10.1006/anbo.2001.1440
Tewari RK, Kumar RP, Neetu SPN (2005) Signs of oxidative stress in the chlorotic leaves of iron starved plants. Plant Sci 169:1037–1045. https://doi.org/10.1016/j.plantsci.2005.06.006
Torrecillas A, Léon A, Del Amor F, Martinez-Mompean MC (1984) Determinacion rapida de clorofila en discos foliares de limonero. Fruits 39:617–622
Tsai HH, Schmidt W (2017) Mobilization of Iron by Plant-Borne Coumarins. Trends Plant Sci. 22:538–548. https://doi.org/10.1016/j.tplants.2017.03.008
Tran D, Camps C (2021) Early diagnosis of iron deficiency in commercial tomato crop using electrical signals. Front Sustain Food Syst 5. https://doi.org/10.3389/fsufs.2021.631529
Wang TZ, Chen L, Zhao MG, Tian QY, Zhang WH (2011) Identification of drought-responsive microRNAs and their targets in Medicago truncatula by genome-wide high-throughput sequencing. BMC Genomics 12:367
Wang Y, Xu C, Li K, Cai X, Wu M, Chen G (2017) Fe deficiency induced changes in rice (Oryza sativa L.) thylakoids. Environml Sci Pollut Res 24:1380–1388. https://doi.org/10.1007/s11356-016-7900-x
Watanabe Y, Nakajima H (2016) Chapter Twenty – Creation of a thermally tolerant peroxidase. Methods Enzym 580:455–470. https://doi.org/10.1016/bs.mie.2016.05.038
Waters BM, Mcinturf SA, Stein RJ (2012) Rosette iron deficiency transcript and microRNA profiling reveals links between copper and iron homeostasis in Arabidopsis thaliana. J Exp Bot 63:5903–5918. https://doi.org/10.1093/jxb/ers239
Zhang Y, Ding S, Lu Q, Yang Z, Wen X, Zhang L, Lu C (2011) Characterization of photosystem II in transgenic tobacco plants with decreased iron superoxide dismutase. Biochim Biophys Acta Bioenerg 1807:391–403. https://doi.org/10.1016/j.bbabio.2011.01.006
Zhang X, Zhang D, Sun W, Wang T (2019) The adaptive mechanism of plants to iron deficiency via iron uptake, transport, and homeostasis. Int. J Mol Sci 20:2424. https://doi.org/10.3390/ijms20102424
Zhao J, Zhang W, Qiu Q, Meng F, Zhang M, Rao D, Wang Z, Yan X (2018) Physiological regulation associated with di_erential tolerance to iron deficiency in soybean. Crop Sci 57:1349–1359. https://doi.org/10.2135/cropsci2017.03.0154
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: Haroun Chenchouni
Rights and permissions
About this article
Cite this article
Kouas, S., Slatni, T., Chihaoui, SA. et al. Differential behavior of Medicago truncatula to calcareous soil is explained by modulation of stomatal responses, antioxidant activity, and iron use efficiency. Arab J Geosci 14, 1669 (2021). https://doi.org/10.1007/s12517-021-07978-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s12517-021-07978-4