Abstract
Arable lands getting contaminated with heavy metals have a very high negative impact on crop plants. The establishment of the mycorrhizal association with crop plants is a sustainable strategy to overcome metal toxicity. The major aim of this study was to analyze mycorrhizae-mediated alterations on the physiology and metabolism of Oryza sativa, as well as the impact of these alterations in the metal tolerance potential of the host on exposure to cadmium (Cd) and zinc (Zn) stresses. For this, 45 d old O. sativa (var. Varsha) plants inoculated with Claroideoglomus claroideum were exposed to 1.95 g Zn kg−1 soil and 0.45 g Cd kg−1 soil. Mycorrhization significantly increased shoot weight, root weight, moisture content, and chlorophyll biosynthesis under Cd and Zn stresses. Mycorrhization mitigated the oxidative stress elicited in O. sativa by the elevated Cd and Zn content, and it aided in maintaining the metabolite’s level and rate of photosynthesis as compared to non-mycorrhizal plants. The circular-shaped unique structures seen as opening on the leaf surface of non-mycorrhizal plants under Zn stress, possibly for the emission of volatile compounds synthesized as a result of Zn stress, have a great chance of leaf tissue destruction. This structural modification was characterized in the case of Zn stress and not in Cd stress and can lead to the reduction of photosynthesis in O. sativa exposed to Zn stress. The reduction in oxidative stress could be correlated to the reduced uptake and transport of Cd and Zn ions in mycorrhizal plants. The exudation of tributyl acetyl citrate, 3-beta-acetoxystigmasta-4,6,22-triene, and linoleic acid from the mycorrhizal roots of rice plants has a crucial role in the stabilization of metal ions. This study proposes mycorrhization as a strategy to strengthen the Cd and Zn stress tolerance level of rice plants by regulating the physiology and metabolomics of the host plant.
Similar content being viewed by others
References
Abdelhameed RE, Metwally RA (2019) Alleviation of cadmium stress by arbuscular mycorrhizal symbiosis. Int J Phytoremediation 21:663–671. https://doi.org/10.1080/15226514.2018.1556584
Aboobucker SI, Suza WP (2019) Why do plants convert sitosterol to stigmasterol? Front Plant Sci 10:354. https://doi.org/10.3389/fpls.2019.00354
Andrade SA, Gratão PL, Schiavinato MA, Silveira AP, Azevedo RA, Mazzafera P (2009) Zn uptake, physiological response and stress attenuation in mycorrhizal jack bean growing in soil with increasing Zn concentrations. Chemosphere 75:1363–1370. https://doi.org/10.1016/j.chemosphere.2009.02.008
Andrejić G, Gajić G, Prica M, Dželetović Ž, Rakić T (2018) Zinc accumulation, photosynthetic gas exchange, and chlorophyll a fluorescence in Zn-stressed Miscanthus× giganteus plants. Photosynthetica 56:1249–1258. https://doi.org/10.1007/s11099-018-0827-
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1. https://doi.org/10.1104/pp.24.1.1
Arun K, Janeeshma E, Job J, Puthur JT (2021) Physiochemical responses in coconut leaves infected by spiraling whitefly and the associated sooty mold formation. Acta Physiol Plant 43:1–13. https://doi.org/10.1007/s11738-021-03213-5
Barceló JUAN, Poschenrieder C (1990) Plant water relations as affected by heavy metal stress: a review. J Plant Nutr 13:1–37. https://doi.org/10.1080/01904169009364057
Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67:1661–1672. https://doi.org/10.1016/j.phytochem.2006.02.004
Baryla A, Carrier P, Franck F, Coulomb C, Sahut C, Havaux M (2001) Leaf chlorosis in oilseed rape plants (Brassica napus) grown on cadmium-polluted soil: causes and consequences for photosynthesis and growth. Planta 212:696–709. https://doi.org/10.1007/s004250000439
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207. https://doi.org/10.1007/BF00018060
Bibbiani S, Colzi I, Taiti C, Nissim WG, Papini A, Mancuso S, Gonnelli C (2018) Smelling the metal: volatile organic compound emission under Zn excess in the mint Tetradenia riparia. Plant Sci 271:1–8. https://doi.org/10.1016/j.plantsci.2018.03.006
Buckley TN (2005) The control of stomata by water balance. New phytol 168:275–292. https://doi.org/10.1111/j.1469-8137.2005.01543.x
Burleigh SH, Kristensen BK, Bechmann IE (2003) A plasma membrane zinc transporter from Medicago truncatula is up-regulated in roots by Zn fertilization, yet down-regulated by arbuscular mycorrhizal colonization. Plant Mol Biol 52:1077–1088. https://doi.org/10.1023/A:1025479701246
Charest C, Ton Phan C (1990) Cold acclimation of wheat (Triticum aestivum): Properties of enzymes involved in proline metabolism. Physiol Plant 80:159–168. https://doi.org/10.1111/j.1399-3054.1990.tb04391.x
Chen CT, Chen TH, Lo KF, Chiu CY (2004a) Effects of proline on copper transport in rice seedlings under excess copper stress. Plant Sci 166:103–111. https://doi.org/10.1016/j.plantsci.2003.08.015
Chen B, Shen H, Li X, Feng G, Christie P (2004b) Effects of EDTA application and arbuscular mycorrhizal colonization on growth and zinc uptake by maize (Zea mays L.) in soil experimentally contaminated with zinc. Plant Soil 261:219–229. https://doi.org/10.1023/B:PLSO.0000035538.09222.ff
Chen S, Wang Q, Lu H, Li J, Yang D, Liu J, Yan C (2019a) Phenolic metabolism and related heavy metal tolerance mechanism in Kandelia Obovata under Cd and Zn stress. Ecotoxicol Environ Saf 169:134–143. https://doi.org/10.1016/j.ecoenv.2018.11.004
Chen XW, Wu L, Luo N, Mo CH, Wong MH, Li H (2019b) Arbuscular mycorrhizal fungi and the associated bacterial community influence the uptake of cadmium in rice. Geoderma 337:749–757. https://doi.org/10.1016/j.geoderma.2018.10.029
Christie P, Li X, Chen B (2004) Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil 261:209–217. https://doi.org/10.1023/B:PLSO.0000035542.79345.1b
Cui Y, Zhao N (2011) Oxidative stress and change in plant metabolism of maize (Zea mays L.) growing in contaminated soil with elemental sulfur and toxic effect of zinc. Plant Soil Environ 57:34–39. https://doi.org/10.17221/193/2010-PSE
Dell’Amico E, Cavalca L, Andreoni V (2008) Improvement of Brassica napus growth under cadmium stress by cadmium-resistant rhizobacteria. Soil Biol Biochem 40:74–84
Dhalaria R, Kumar D, Kumar H, Nepovimova E, Kuča K, Torequl Islam M, Verma R (2020) Arbuscular mycorrhizal fungi as potential agents in ameliorating heavy metal stress in plants. Agronomy 10:815. https://doi.org/10.3390/agronomy10060815
Doke N (1983) Involvement of superoxide anion generation in the hypersensitive response of potato tuber tissues to infection with an incompatible race of Phytophthora infestans and to the hyphal wall components. Physiol Plant Pathol 23:345–357. https://doi.org/10.1016/0048-4059(83)90019-X
Dong S, Beckles DM (2019) Dynamic changes in the starch-sugar interconversion within plant source and sink tissues promote a better abiotic stress response. J Plant Physiol 234:80–93. https://doi.org/10.1016/j.jplph.2019.01.007
Dubois M, Gilles KA, Hamilton JK, Rebers PT, Smith F (1956) Colorimetric method for determination of sugars and related substances. Anal Chem 28:350-356. 10. 1021/ac60111a017
Ef A, Abeer H, Aa A, Hend A (2015) Alleviation of adverse impact of cadmium stress in sunflower (Helianthus annuus L.) by arbuscular mycorrhizal fungi. Pak J Bot 47:785–795
Filipović A (2020) Water plant and soil relation under stress situations. In: Meena RS (ed) Soil Moisture Importance. IntechOpen, London. https://doi.org/10.5772/intechopen.93528
Folin O, Denis W (1915) A colorimetric method for the determination of phenol (and derivatives) in urine. J Biol Chem 22:305–308. https://doi.org/10.1016/S0021-9258(18)87648-7
Garg N, Baher N (2013) Role of arbuscular mycorrhizal symbiosis in proline biosynthesis and metabolism of Cicer arietinum L. (chickpea) genotypes under salt stress. J Plant Growth Regul 32:767–778. https://doi.org/10.1007/s00344-013-9346-4
Garg N, Bhandari P (2012) Influence of cadmium stress and arbuscular mycorrhizal fungi on nodule senescence in Cajanus cajan (L.) Millsp. Int J phytoremediation 14:62–74. https://doi.org/10.1080/15226514.2011.573822
Garg N, Chandel S (2012) Role of arbuscular mycorrhizal (AM) fungi on growth, cadmium uptake, osmolyte, and phytochelatin synthesis in Cajanus cajan (L.) Millsp. under NaCl and Cd stresses. J Plant Growth Regul 31:292–308. https://doi.org/10.1007/s00344-011-9239-3
Garg N, Singh S (2018) Arbuscular mycorrhiza Rhizophagus irregularis and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan L. Millsp.(pigeonpea) genotypes under cadmium and zinc stress. J Plant Growth Regul 37:46–63. https://doi.org/10.1007/s00344-017-9708-4
Girija C, Smith BN, Swamy PM (2002) Interactive effects of sodium chloride and calcium chloride on the accumulation of proline and glycinebetaine in peanut (Arachis hypogaea L.). Environ Exp Bot 47:1–10. https://doi.org/10.1016/S0098-8472(01)00096-X
Gonzalez-Chavez MC, Carrillo-Gonzalez R, Wright SF, Nichols KA (2004) The role of glomalin, a protein produced by arbuscular mycorrhizal fungi, in sequestering potentially toxic elements. Environ Pollut 130:317–323
Grajek H, Rydzyński D, Piotrowicz-Cieślak A, Herman A, Maciejczyk M, Wieczorek Z (2020) Cadmium ion-chlorophyll interaction–Examination of spectral properties and structure of the cadmium-chlorophyll complex and their relevance to photosynthesis inhibition. Chemosphere 261:127434. https://doi.org/10.1016/j.chemosphere.2020.127434
Grover N, Patni V (2013) Phytochemical characterization using various solvent extracts and GC-MS analysis of methanolic extract of Woodfordia fruticosa (L) Kurz. Leaves. Int J Pharm Pharm Sci 5:291–295 https://www.scopus.com/inward/record.uri?eid=2-s2.0-84885359437&partnerID=40&md5=7efcd58abcabac879963af99ee05e9df
Gu HH, Zhan SS, Wang SZ, Tang YT, Chaney RL, Fang XH et al (2012) Silicon-mediated amelioration of zinc toxicity in rice (Oryza sativa L.) seedlings. Plant Soil 350:193–204. https://doi.org/10.1007/s11104-011-0894-8
Hashem A, EF Abd_Allah, Alqarawi AA, Al Huqail AA, Egamberdieva D, Wirth S (2016a) Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi J Biol Sci 23:272–281. https://doi.org/10.1016/j.sjbs.2015.11.002
Hashem A, Abd-Allah EF, Alqarawi AA et al (2016b) Bioremediation of adverse impact of cadmium toxicity on Cassia italica Mill by arbuscular mycorrhizal fungi. Saudi J Biol Sci 23:39–47. https://doi.org/10.1016/j.sjbs.2015.11.007
Heidarabadi MD, Ghanati F, Fujiwara T (2011) Interaction between boron and aluminum and their effects on phenolic metabolism of Linum usitatissimum L. roots. Plant Physiol Biochem 49:1377–1383. https://doi.org/10.1016/j.plaphy.2011.09.008
Hiba H, Janeeshma E, Puthur JT (2021) Dynamic alterations of metabolites in Plectranthus amboinicus (Lour.) Spreng. to encounter drought and Zn toxicity. Rev Bras Bot 44:587–599. https://doi.org/10.1007/s40415-021-00738-4
Huang S, Ma JF (2020) Silicon suppresses zinc uptake through down-regulating zinc transporter gene in rice. Physiol Plant 170:580–591. https://doi.org/10.1111/ppl.13196
Janeeshma E, Johnson R, Amritha MS, Noble L, Aswathi KPR, Telesinski A, Kalaji HM, Auriga A, Puthur JT (2022) Modulations in Chlorophyll a Fluorescence Based on Intensity and Spectral Variations of Light. Int J Mol Sci 23:5599. https://doi.org/10.3390/ijms23105599
Janeeshma E, Kalaji HM, Puthur JT (2021b) Differential responses in the photosynthetic efficiency of Oryza sativa and Zea mays on exposure to Cd and Zn toxicity. Acta Physiol Plant 43:1–16. https://doi.org/10.1007/s11738-020-03178-x
Janeeshma E, Puthur JT (2020) Direct and indirect influence of arbuscular mycorrhizae on enhancing metal tolerance of plants. Arch Microbiol 202:1–16. https://doi.org/10.1007/s00203-019-01730-z
Janeeshma E, Ahmad PJT (2020) Silicon distribution in leaves and roots of rice and maize in response to cadmium and zinc toxicity and the associated histological variations. Physiol Plant 173:460–471. https://doi.org/10.1111/ppl.13310
Janeeshma E, Rajan VK, Puthur JT (2021c) Spectral variations associated with anthocyanin accumulation; an apt tool to evaluate zinc stress in Zea mays L. Chem Ecol 37:32–49. https://doi.org/10.1080/02757540.2020.1799993
Janeeshma E, Wróbel J, Kalaji HM, Puthur JT (2021a) Metabolic alterations elicited by Cd and Zn toxicity in Zea mays with the association of Claroideoglomus claroideum. Ecotoxicology 1-12. https://doi.org/10.1007/s10646-021-02492-5
Javed MT, Akram MS, Tanwir K, Chaudhary HJ, Ali Q, Stoltz E, Lindberg S (2017) Cadmium spiked soil modulates root organic acids exudation and ionic contents of two differentially Cd tolerant maize (Zea mays L.) cultivars. Ecotoxicol Environ Saf 141:216–225. https://doi.org/10.1016/j.ecoenv.2017.03.027
Jesus DDSD, Azevedo BOD, Pinelli MS, Korn MDGA, Azevedo Neto ADD, Lucchese AM, Oliveira LMD (2016) Growth and volatile compounds of Martianthus leucocephalus exposed to heavy metal stress. Ciência Rural 46:2110–2117. https://doi.org/10.1590/0103-8478cr20150576
Joner EJ, Briones R, Leyval C (2000) Metal-binding capacity of arbuscular mycorrhizal mycelium. Plant Soil 226:227–234. https://doi.org/10.1023/A:1026565701391
Junglee S, Urban L, Sallanon H, Lopez-Lauri F (2014) Optimized assay for hydrogen peroxide determination in plant tissue using potassium iodide. Am J Anal Chem 5:730–736. https://doi.org/10.4236/ajac.2014.511081
Kanwal S, Bano A, Malik RN (2015) Effects of arbuscular mycorrhizal fungi on wheat growth, physiology, nutrition and cadmium uptake under increasing cadmium stress. IJAAR 7:30-42. http://citeseerx.ist.psu.edu/viewdoc/download?doi=10.1.1.735.5649&rep=rep1&type=pdf
Keunen ELS, Peshev D, Vangronsveld J, Van Den Ende WIM, Cuypers ANN (2013) Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant Cell Environ 36:1242–1255. https://doi.org/10.1111/pce.12061
Kısa D, Elmastaş M, Öztürk L, Kayır Ö (2016) Responses of the phenolic compounds of Zea mays under heavy metal stress. Appl Biol Chem 59:813–820. https://doi.org/10.3390/molecules24132452
Kontos F, Spyropoulos CG (1996) Effect of linoleic, linolenic and jasmonic acid on the production of α-galactosidase and endo-β-mannanase in the endosperms of carob and fenugreek seeds. J plant Physiol 149:629–632. https://doi.org/10.1016/S0176-1617(96)80346-4
Kramer CM, Prata RT, Willits MG, De Luca V, Steffens JC, Graser G (2003) Cloning and regiospecificity studies of two flavonoid glucosyltransferases from Allium cepa. Phytochemistry 64:1069–1076. https://doi.org/10.1016/S0031-9422(03)00507-7
Kumar MS, Ali K, Dahuja A, Tyagi A (2015a) Role of phytosterols in drought stress tolerance in rice. Plant Physiol Biochem 96:83–89. https://doi.org/10.1016/j.plaphy.2015.07.014
Kumar P, Lucini L, Rouphael Y, Cardarelli M, Kalunke RM, Colla G (2015b) Insight into the role of grafting and arbuscular mycorrhiza on cadmium stress tolerance in tomato. Front Plant Sci 6:477. https://doi.org/10.3389/fpls.2015.00477
Latef A (2013) Growth and some physiological activities of pepper (Capsicum annuum L.) in response to cadmium stress and mycorrhizal symbiosis. J Agric Sci Technol 15:1437–1448
Leyval C, Turnau K, Haselwandter K (1997) Effect of heavy metal pollution on mycorrhizal colonization and function: physiological, ecological and applied aspects. Mycorrhiza 7:139–153 http://hdl.handle.net/123456789/4355
Li H, Luo N, Zhang LJ, Zhao HM, Li YW, Cai QY et al (2016) Do arbuscular mycorrhizal fungi affect cadmium uptake kinetics, subcellular distribution and chemical forms in rice? Sci Total Enviro 571:1183–1190. https://doi.org/10.1016/j.scitotenv.2016.07.124
Lippold F, vom Dorp K, Abraham M, Hölzl G, Wewer V, Yilmaz JL et al (2012) Fatty acid phytyl ester synthesis in chloroplasts of Arabidopsis. Plant Cell 24:2001–2014. https://doi.org/10.1105/tpc.112.095588
Lokhande RS, Singare PU, Pimple DS (2011) Toxicity study of heavy metals pollutants in waste water effluent samples collected from Taloja industrial estate of Mumbai, India. Resources and Environment 1:13–19. https://doi.org/10.5923/j.re.20110101.02
Lombardi L, Sebastiani L (2005) Copper toxicity in Prunus cerasifera: growth and antioxidant enzymes responses of in vitro grown plants. Plant Sci 168:797–802. https://doi.org/10.1016/j.plantsci.2004.10.012
Ma JF, Zheng SJ, Matsumoto H (1997) Specific secretion of citric acid induced by Al stress in Cassia tora L. Plant, Cell Physiol 38:1019–1025. https://doi.org/10.1093/oxfordjournals.pcp.a029266
Zhao AQ, Tian XH, Lu WH, Gale WJ, Lu XC, Cao YX (2011) Effect of zinc on cadmium toxicity in winter wheat. J Plant Nutr 34:1372–1385. https://doi.org/10.1080/01904167.2011.580879
Mitra S, Pramanik K, Sarkar A, Ghosh PK, Soren T, Maiti TK (2018) Bioaccumulation of cadmium by Enterobacter sp. and enhancement of rice seedling growth under cadmium stress. Ecotoxicol Environ Safety 156:183–196
Mitra D, Saritha B, Janeeshma E, Gusain P, Khoshru B, Nouh FAA et al (2021) Arbuscular mycorrhizal fungal association boosted the arsenic resistance in crops with special responsiveness to rice plant. Environ Exp Bot 193:104681. https://doi.org/10.1016/j.envexpbot.2021.104681
Moore S, Stein WH (1948) Photometric ninhydrin method for use in the chromatography of amino acids. J Biol Chem 176:367-388. https://www.cabdirect.org/cabd irect/abstract/19481405468
Pauno M, Koleva L, Vassilev A, Vangronsveld J, Goltsev V (2018) Effects of different metals on photosynthesis: Cadmium and zinc affect chlorophyll fluorescence in durum wheat. Int J Mol Sci 19:787. https://doi.org/10.3390/ijms19030787
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Transactions of the British Mycological Society 55:158–161. https://doi.org/10.1016/S0007-1536(70)80110-3
Prakash V, Khan MY, Rai P, Prasad R, Tripathi DK, Sharma S (2020) Exploring plant rhizobacteria synergy to mitigate abiotic stress: a new dimension toward sustainable agriculture. In: Durgesh K. Tripathi, Vijay P. Singh, Chauhan D, Sharma S, Prasad S, Nawal K. Dubey, Ramawat N (ed) Plant life under changing environment. Academic Press, India pp. 861-882. https://doi.org/10.1016/B978-0-12-818204-8.00040-0
Rahul VD, Panda RK, Lenka D, Rout GR (2019) A Study on the Root Characters of Maize Hybrid Germplasm Lines under Moisture Deficit Stress. Int J Curr Microbiol App Sci 82:836–845. https://doi.org/10.20546/ijcmas.2019.808.326
Rai V, Mehrotra S (2008) Chromium-induced changes in ultramorphology and secondary metabolites of Phyllanthus amarus Schum & Thonn.–an hepatoprotective plant. Environ Monit Assess 147:307–315. https://doi.org/10.1007/s10661-007-0122-4
Rizwan MS, Imtiaz M, Huang G, Chhajro MA, Liu Y, Fu Q et al (2016) Immobilization of Pb and Cu in polluted soil by superphosphate, multi-walled carbon nanotube, rice straw and its derived biochar. Environ Sci Pollut Res 23:15532–15543. https://doi.org/10.1007/s11356-016-6695-0
Rohani N, Daneshmand F, Vaziri A, Mahmoudi M, Saber-Mahani F (2019) Growth and some physiological characteristics of Pistacia vera L. cv Ahmad Aghaei in response to cadmium stress and Glomus mosseae symbiosis. S Afr J Bot 124:499–507. https://doi.org/10.1016/j.sajb.2019.06.001
Rout JR, Kerry R, Panigrahi D, Sahoo et al (2019) Biochemical, molecular, and elemental profiling of Withania somnifera L. with response to zinc stress. Environ Sci Pollut Res 26:4116–4129. https://doi.org/10.1007/s11356-018-3926-6
Roychoudhury A, Tripathi DK (2020) Protective Chemical Agents in the Amelioration of Plant Abiotic Stress, John Wiley & Sons Ltd, India. https://onlinelibrary.wiley.com/doi/book/10.1002/9781119552154
Ruscitti M, Arango M, Beltrano J (2017) Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theor Exp Plant Physiol 29:37–49. https://doi.org/10.1007/s40626-016-0081-7
Ruytinx J, Kafle A, Usman M, Coninx L, Zimmermann SD, Garcia K (2020) Micronutrient transport in mycorrhizal symbiosis; zinc steals the show. Fungal Biol Rev 34:1–9. https://doi.org/10.1016/j.fbr.2019.09.001
Sagardoy R, Vázquez S, Florez‐Sarasa ID, Albacete A, Ribas‐Carbó M, Flexas J et al (2010) Stomatal and mesophyll conductances to CO2 are the main limitations to photosynthesis in sugar beet (Beta vulgaris) plants grown with excess zinc. New Phytol 187:145–158
Salisbury FB, Ross CW (1994) Fisiología Vegetal [Plant Physiology]. Mexico: Grupo editorial Iberoamericana. https://www.worldcat.org/title/fisiologia-vegetal/oclc/35762214
Sarraf M, Vishwakarma K, Kumar V, Arif N, Das S, Johnson R, Janeeshma E, Puthur JT, Chauhan DK (2022) Metal/Metalloid-Based Nanomaterials for Plant Abiotic Stress Tolerance: An Overview of the Mechanisms. Plants 11:316. https://doi.org/10.3390/plants11030316
Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012a) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58. https://doi.org/10.1016/j.plaphy.2012.07.018
Shahabivand S, Maivan HZ, Goltapeh EM, Sharifi M, Aliloo AA (2012b) The effects of root endophyte and arbuscular mycorrhizal fungi on growth and cadmium accumulation in wheat under cadmium toxicity. Plant Physiol Biochem 60:53–58. https://doi.org/10.1016/j.plaphy.2012.07.018
Sharma SS, Dietz KJ (2006) The significance of amino acids and amino acid-derived molecules in plant responses and adaptation to heavy metal stress. J Exp Bot 57:711–726. https://doi.org/10.1093/jxb/erj073
Sharma V, Parmar P, Kumari N (2016) Differential cadmium stress tolerance in wheat genotypes under mycorrhizal association. J Plant Nutr 39:2025-2036. 10.1080/01904167.20 16.1170851
Shewfelt RL, Purvis AC (1995) Toward a comprehensive model for lipid peroxidation in plant tissue disorders. Hort Sci 30:213-218. https://journals.ashs.org/hortsci/view/journals/hortsci/30/4/article-p213.xml
Šimonovičová M, Huttová J, Mistrík I, Široká B, Tamás L (2004) Peroxidase mediated hydrogen peroxide production in barley roots grown under stress conditions. Plant Growth Regul 44:267–275. https://doi.org/10.1007/s10725-004-4662-0
Singh HP, Mittal S, Kaur S, Batish DR, Kohli RK (2009) Chemical composition and antioxidant activity of essential oil from residues of Artemisia scoparia. Food Chem 114:642–645. https://doi.org/10.1016/j.foodchem.2008.09.101
Singh P, Shah K (2014) Evidences for reduced metal-uptake and membrane injury upon application of nitric oxide donor in cadmium stressed rice seedlings. Plant Physiol Biochem 83:180–184. https://doi.org/10.1016/j.plaphy.2014.07.018
Singh S, Singh VP, Prasad SM, Sharma S, Ramawat N, Dubey NK et al (2019) Interactive effect of silicon (Si) and salicylic acid (SA) in maize seedlings and their mechanisms of cadmium (Cd) toxicity alleviation. J Plant Growth Regul 38:1587–1597. https://doi.org/10.1007/s00344-019-09958-1
Sruthi P, Puthur JT (2019) Characterization of physiochemical and anatomical features associated with enhanced phytostabilization of copper in Bruguiera cylindrica (L.) Blume. Int J Phytoremediation 21:1423–1441. https://doi.org/10.1080/15226514.2019.1633263
Stålfelt MG (1955) The stomata as a hydrophotic regulator of the water deficit of the plant. Physiol Plant 8:572–593. https://doi.org/10.1111/j.1399-3054.1955.tb07753.x
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence. Springer, Dordrecht, pp 321–362. https://doi.org/10.1007/978-1-4020-3218-9_12
Subramanian S, Cho UH, Keyes C, Yu O (2009) Distinct changes in soybean xylem sap proteome in response to pathogenic and symbiotic microbe interactions. BMC Plant Biol 9:119. https://doi.org/10.1186/1471-2229-9-119
Tripathi DK, Vishwakarma K, Singh VP, Prakash V, Sharma S, Muneer S et al (2020) Silicon crosstalk with reactive oxygen species, phytohormones and other signaling molecules. J Hazard Mater 408:124820. https://doi.org/10.1016/j.jhazmat.2020.124820
Uraguchi S, Mori S, Kuramata M, Kawasaki A, Arao T, Ishikawa S (2009) Root-to-shoot Cd translocation via the xylem is the major process determining shoot and grain cadmium accumulation in rice. J Exp Bot 60:2677–2688. https://doi.org/10.1093/jxb/erp119
Wang P, Chen H, Kopittke PM, Zhao FJ (2019) Cadmium contamination in agricultural soils of China and the impact on food safety. Environ Pollut 249:1038-1048. 10.1016/j.envpol.2019.03.063
Weryszko-Chmielewska E, Chwil M (2005) Lead-induced histological and ultrastructural changes in the leaves of soybean (Glycine max (L.) Merr.). Soil Sci Plant Nutr 51:203–212. https://doi.org/10.1111/j.1747-0765.2005.tb00024.x
Wojcik M, Tukiendorf A (2004) Phytochelatin synthesis and cadmium localization in wild type of Arabidopsis thaliana. Plant Growth Regul 44:71–80. https://doi.org/10.1007/s10725-004-1592-9
Zengin FK, Munzuroglu O (2005) Effects of some heavy metals on content of chlorophyll, proline and some antioxidant chemicals in bean (Phaseolus vulgaris L.) seedlings. Acta Biol Cracov Bot 47:157–164 https://abcbot.pl/pdf/47_2/157-164.pdf
Zhang XH, Zhu YG, Chen BD, Lin AJ, Smith SE, Smith FA (2005) Arbuscular mycorrhizal fungi contribute to resistance of upland rice to combined metal contamination of soil. J Plant Nutr 28:2065–2077. https://doi.org/10.1080/01904160500320871
Acknowledgements
The authors greatly acknowledge the Regional Agricultural Research Station (RARS) of Kerala Agricultural University, Pattambi, Kerala, India, for providing seeds essential to conduct experiments and Centre for Mycorrhizal Culture Collection (CMCC), The Energy and Resources Institute (TERI), New Delhi, for providing the inoculum of mycorrhiza.
Availability of data and materials
Data sharing is not applicable to this article as all new created data is already contained within this article
Funding
This work was supported by the University Grant Commission (UGC), India, in the form of JRF under grant 319492.
Author information
Authors and Affiliations
Contributions
E Janeeshma performed the analysis, processed the experimental data, interpreted the results, drafted the manuscript and designed the figures. Jos T. Puthur provided critical feedback and helped shape the research and analysis aided in interpreting the results and worked on the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethics approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Additional information
Responsible Editor: Gangrong Shi
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 25477 kb)
Rights and permissions
Springer Nature or its licensor holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Janeeshma, E., Puthur, J.T. Physiological and metabolic dynamism in mycorrhizal and non-mycorrhizal Oryza sativa (var. Varsha) subjected to Zn and Cd toxicity: a comparative study. Environ Sci Pollut Res 30, 3668–3687 (2023). https://doi.org/10.1007/s11356-022-22478-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-022-22478-y