Skip to main content
Log in

Differential Role of Silicon and Rhizoglomus intraradices in Modulating Amide and Ureide Metabolism of Seasonally Different Legume Species Subjected to Nickel Toxicity

  • Research
  • Published:
Silicon Aims and scope Submit manuscript

Abstract

Nickel (Ni) toxicity disrupts the cellular processes and is detrimental for plant growth and development. Silicon (Si) and AMF (arbuscular mycorrhizal fungi) alleviate heavy metal stress induced toxic responses in plants. Although Fabaceae members are considered low Si accumulators, however, variations in their ability for Si uptake have been reported. Present study compared the individual and cumulative roles of Si and AM (R. irregularis) in alleviating Ni (150 mg/kg) toxicity in three seasonally different legume species namely chickpea (HC3), mungbean (Pusa-9531) and pigeonpea (Pusa-2002). Presence of Ni in the root rhizosphere declined growth, nitrogen fixing ability, N-assimilation and yield attributes, with chickpea displaying highest sensitivity, mungbean showcasing moderate tolerance, while pigeonpea having maximum resistance against metal stress. AM and Si were highly beneficial in mitigating the toxic effects of Ni especially in pigeonpea followed by mungbean and chickpea. The higher beneficial effects of AM could be related to its ability in improving soil enzymatic activities, nutrient availability and reduced metal uptake. Moreover, AM symbiosis complemented rhizobial symbiosis by improving nodulation potential, trehalose turnover, thus leading to higher ammonia assimilation, ureide and amide synthesis as well as their transport. Interestingly, mycorrhization significantly induced Si uptake and therefore, their co-applications (+ Si + AM) proved to be most effective in alleviating Ni toxicity in all three legume species with maximum positive impacts displayed by pigeonpea. Hence, study suggested the need of exploring more legume species having an ability to uptake Si and establish efficient AM symbiosis in order to reduce Ni toxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

Data Availability

The datasets used and/or analyzed during the currentstudy are available from the corresponding author on request.

References

  1. Nagajyoti PC, Lee KD, Sreekanth T (2010) Heavy metals, occurrence and toxicity for plants: a review. Environ Chem Lett 8:199–216. https://doi.org/10.1007/s10311-010-0297-8

    Article  CAS  Google Scholar 

  2. Hussain MB, Ali S, Azam A, Hina S, Farooq MA, Ali B, Bharwana SA, Gill MB (2013) Morphological, physiological and biochemical responses of plants to nickel stress: a review. Afr J Agric Res 8:1596–1602. https://doi.org/10.5897/AJAR12.407

    Article  CAS  Google Scholar 

  3. National Academy of Sciences (NAS) (1975) Nickel, medical and biological effects of environmental pollutants. National Research Council, National Academy of Sciences, Washington

  4. Duke JM (1980) Production and uses of nickel. In: Nriagu JO (ed) Nickel in the environment. Wiley, New York 

  5. Kasprzak KS (1987) Nickel. Adv Mod Environ Toxicol 11:145–183

    CAS  Google Scholar 

  6. Eisler R (1998) Nickel hazards to fish, wildlife, and invertebrates: a synoptic review. Biological science report GS/BRD/BSR- 1998–0001, Patuxent Wildlife Research Center, U.S. Geological Survey, Laurel

  7. Mustafiz A, Ghosh A, Tripathi AK, Kaur C, Ganguly AK, Bhavesh NS, Tripathi JK, Pareek A, Sopory SK, Singla-Pareek SL (2014) A unique Ni2+-dependent and methylglyoxal- inducible rice glyoxalase I possesses a single active site and functions in abiotic stress response. Plant J 78:951–963. https://doi.org/10.1111/tpj.12521

    Article  PubMed  CAS  Google Scholar 

  8. Gajewska E, Słaba M, Andrzejewska R, Skłodowska M (2006) Nickel-induced inhibition of wheat root growth is related to H2O2 production, but not to lipid peroxidation. Plant Growth Regul 49:95–103. https://doi.org/10.1007/s10725-006-0018-2

    Article  CAS  Google Scholar 

  9. Taylor GJ, Stadt KJ (1990) Interactive effects of cadmium, copper, manganese, nickel and zinc on root growth of wheat (Triticum aestivum) in solution culture. Plant Soil Sci 4:317–322. https://doi.org/10.1007/978-94-009-0585-6_54

    Article  Google Scholar 

  10. Yang X, Baligar VC, Martens DC, Clark RB (1996) Plant tolerance to Ni toxicity. I. Influx, transport and accumulation of Ni in four species. J Plant Nutr 19:73–85. https://doi.org/10.1080/01904169609365108

    Article  CAS  Google Scholar 

  11. Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. Int J Environ Sci Technol 10:1129–1140. https://doi.org/10.1007/s13762-013-0245-9

    Article  CAS  Google Scholar 

  12. Athar R, Ahmad M (2002) Heavy metal toxicity in legume-microsymbiont system. J Plant Nutr 25:369–386. https://doi.org/10.1081/PLN-100108842

    Article  CAS  Google Scholar 

  13. Garg N, Saroy K (2020) Interactive effects of polyamines and arbuscular mycorrhiza in modulating plant biomass, N2 fixation, ureide, and trehalose metabolism in Cajanus cajan (L.) Millsp. genotypes under nickel stress. Environ Sci Pollut Res 27:3043–3064. https://doi.org/10.1007/s11356-019-07300-6

    Article  CAS  Google Scholar 

  14. Bhalerao SA, Sharma AS, Poojari AC (2015) Toxicity of nickel in plants. Int J Pure ApplBiosci 3:345–355

    Google Scholar 

  15. Seregin IV, Kozhevnikova AD (2006) Physiological role of nickel and its toxic effects on higher plants. Russ J Plant Physiol 53:257–277. https://doi.org/10.1134/S1021443706020178

    Article  CAS  Google Scholar 

  16. Chen C, Huang D, Liu J (2009) Functions and toxicity of nickel in plants: recent advances and future prospects. Clean 37:304–313. https://doi.org/10.1002/clen.200800199

    Article  CAS  Google Scholar 

  17. Temp GA (1991) Nickel in plants and its toxicity: Ustoichivost’ktyazhelymmetallamdikorastushchikhvidov (Resistance of wild species to heavy metals). In: Alekseeva-Popova NV (ed). Lenuprizdat, Leningrad

  18. Seregin IV, Kozhevnikova AD, Kazyumina EM, Ivanov VB (2003) Nickel toxicity and distribution in maize roots. Russ J Plant Physiol 50:1–7

    Article  Google Scholar 

  19. El-Bashiti T, Hamamcı H, Öktem HA, Yücel M (2005) Biochemical analysis of trehalose and its metabolizing enzymes in wheat under abiotic stress conditions. Plant Sci 169:47–54. https://doi.org/10.1016/j.plantsci.2005.02.024

    Article  CAS  Google Scholar 

  20. Jules M, Beltran G, Francois J, Parrou JL (2008) New insights into trehalose metabolism by Saccharomyces cerevisiae: NTH2 encodes a functional cytosolic trehalase, and deletion of TPS1 reveals ATH1p-dependent trehalose mobilization. Appl Environ Microbiol 74:605–614. https://doi.org/10.1128/AEM.00557-07

    Article  PubMed  CAS  Google Scholar 

  21. Sharma MP, Grover M, Chourasiya D, Bharti A, Agnihotri R, Maheshwari HS, Pareek A, Buyer JS, Sharma SK, Schütz L, Bagyaraj DJ (2020) Deciphering the role of trehalose in tripartite symbiosis among rhizobia, arbuscular mycorrhizal fungi, and legumes for enhancing abiotic stress tolerance in crop plants. Front Microbiol 11:509919. https://doi.org/10.3389/fmicb.2020.509919

    Article  PubMed  PubMed Central  Google Scholar 

  22. Vriezen JAC, De Bruijn FJ, Nüsslein K (2007) Responses of rhizobia to desiccation in relation to osmotic stress, oxygen, and temperature. Appl Environ Microbiol 73:3451–3459. https://doi.org/10.1128/AEM.02991-06

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. Lopez M, Tejera NA, Iribarne C, Lluch C, Herrera-Cervera JA (2008) Trehalose and trehalase in root nodules of Medicago truncatula and Phaseolus vulgaris in response to salt stress. Physiol Plant 134:575–582. https://doi.org/10.1111/j.1399-3054.2008.01162.x

    Article  PubMed  CAS  Google Scholar 

  24. Garg N, Singla P (2016) Stimulation of nitrogen fixation and trehalose biosynthesis by naringenin (Nar) and arbuscular mycorrhiza (AM) in chickpea under salinity stress. Plant Growth Regul 80:5–22. https://doi.org/10.1007/s10725-016-0146-2

    Article  CAS  Google Scholar 

  25. Suárez R, Wong A, Ramírez M, Barraza A, Orozco MDC, Cevallos MA, Lara M, Hernández G, Iturriaga G (2008) Improvement of drought tolerance and grain yield in common bean by overexpressing trehalose-6-phosphate synthase in rhizobia. Mol Plant Microbe Interact 21:958–966. https://doi.org/10.1094/MPMI-21-7-0958

    Article  PubMed  CAS  Google Scholar 

  26. Domínguez-Ferreras A, Soto MJ, Pérez-Arnedo R, Olivares J, Sanjuán J (2009) Importance of trehalose biosynthesis for Sinorhizobiummelilotiosmotolerance and nodulation of alfalfa roots. J Bacteriol 191:7490–7499. https://doi.org/10.1128/JB.00725-09

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  27. Sugawara M, Cytryn EJ, Sadowsky MJ (2010) Functional role of Bradyrhizobium japonicum trehalose biosynthesis and metabolism genes during physiological stress and nodulation. Appl Environ Microbiol 76:1071–1081. https://doi.org/10.1128/AEM.02483-09

    Article  PubMed  CAS  Google Scholar 

  28. Fernandez-Aunián C, Hamouda TB, Iglesias-Guerra F, Argandõa M, Reina- Bueno M, Nieto JJ, Aouani ME, Vargas C (2010) Biosynthesis of compatible solutes in rhizobial strains isolated from Phaseolus vulgaris nodules in Tunisian fields. BMC Microbiol 10:192. https://doi.org/10.1186/1471-2180-10-192

    Article  CAS  Google Scholar 

  29. Kouris-Blazos A, Belski R (2016) Health benefits of legumes and pulses with a focus on Australian sweet lupins. Asia Pac J Clin Nutr 25:1–17

    PubMed  CAS  Google Scholar 

  30. Quiles FA, Galvez-Valdivieso G, Guerrero-Casado J, Pineda M, Piedras P (2019) Relationship between ureidic/amidic metabolism and antioxidant enzymatic activities in legume seedlings. Plant PhysiolBiochem 138:1–8. https://doi.org/10.1016/j.plaphy.2019.02.016

    Article  CAS  Google Scholar 

  31. Sulieman S, Tran LSP (2013) Asparagine: an amide of particular distinction in the regulation of symbiotic nitrogen fixation of legumes. Crit Rev Biotechnol 33:309–327. https://doi.org/10.3109/07388551.2012.695770

    Article  PubMed  CAS  Google Scholar 

  32. Kaur H, Chowrasia S, Gaur VS, Mondal TK (2021) Allantoin: emerging role in plant abiotic stress tolerance. Plant Mol Biol Report 39:648–661. https://doi.org/10.1007/s11105-021-01280-z

    Article  CAS  Google Scholar 

  33. Ashfaque F, Inam A, Inam A, Iqbal S, Sahay S (2017) Response of silicon on metal accumulation, photosynthetic inhibition and oxidative stress in chromium-induced mustard (Brassica juncea L.). South Afr J Bot 111:153–160. https://doi.org/10.1016/j.sajb.2017.03.002

    Article  CAS  Google Scholar 

  34. Deshmukh RK, Ma JF, B´elanger RR, (2017) Role of silicon in plants. Front Plant Sci 8:1858. https://doi.org/10.3389/fpls.2017.01858

    Article  PubMed  PubMed Central  Google Scholar 

  35. Epstein E (1999) Silicon. Annu Rev Plant Physiol 50:641–644. https://doi.org/10.1146/annurev.arplant.50.1.641

    Article  CAS  Google Scholar 

  36. Sommer M, Kaczorek D, Kuzyakov Y, Breuer J (2006) Silicon pools and fluxes in soils and Landscapes: A review. J Plant Nutr Soil Sci 169:310–329. https://doi.org/10.1002/jpln.200521981

    Article  CAS  Google Scholar 

  37. Mitani N, Ma JF, Iwashita T (2005) Identification of the silicon form in xylem sap of rice (Oryza sativa L.). Plant Cell Physiol 46:279–283. https://doi.org/10.1093/pcp/pci018

    Article  PubMed  CAS  Google Scholar 

  38. Ma JF, Tamai K, Yamaji N, Mitani N, Konishi S, Katsuhara M, Yano MA (2006) Silicon transporter in rice. Nature 440:688–691. https://doi.org/10.1038/nature04590

    Article  PubMed  CAS  Google Scholar 

  39. Ma JF, Yamaji N (2006) Silicon uptake and accumulation in higher plants. Trends Plant Sci 11:392–397. https://doi.org/10.1016/j.tplants.2006.06.007

    Article  PubMed  CAS  Google Scholar 

  40. Ma JF, Yamaji N (2008) Functions and transport of silicon in plants. Cell Mol Life Sci 65:3049–3057. https://doi.org/10.1007/s00018-008-7580-x

    Article  PubMed  CAS  Google Scholar 

  41. Epstein E (1994) The anomaly of Si in plant biology. Proc Natl Acad Sci 91:11–17. https://doi.org/10.1073/pnas.91.1.1

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  42. Henriet C, Draye X, Oppitz I, Swennen R, Delvaux B (2006) Effects, distribution and uptake of silicon in banana (Musa spp.) under controlled conditions. Plant Soil 287:359–374. https://doi.org/10.1007/s11104-006-9085-4

    Article  CAS  Google Scholar 

  43. Liang YC, Zhang WH, Chen Q, Liu YL, Ding RX (2006) Effect of exogenous silicon (Si) on HÞ-ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 57:212–219. https://doi.org/10.1016/j.envexpbot.2005.05.012

    Article  CAS  Google Scholar 

  44. Ma JF, Miyake Y, Takahashi E (2001) Si as a beneficial element for crop plants. Stud Plant Sci 8:17–39. https://doi.org/10.1016/S0928-3420(01)80006-9

    Article  CAS  Google Scholar 

  45. Liang YC, Si J, Ro€mheld V (2005) Si uptake and transport is an active process in Cucumis sativus L. New Phytol 67:797–804. https://doi.org/10.1111/j.1469-8137.2005.01463.x

  46. Ouellette S, Goyette MH, Labb´e C, Laur, J, Gaudreau L, Gosselin A, Dorais M, Deshmukh RK, B´elanger RR (2017) Silicon transporters and effects of silicon amendments in strawberry under high tunnel and field conditions. Front Plant Sci 8:949. https://doi.org/10.3389/fpls.2017.00949

  47. Zargar SM, Nagar P, Deshmukh R, Nazir M, Wani AA, Masoodi KZ, Agrawal GK, Rakwal R (2017) Aquaporins as potential drought tolerance inducing proteins: towards instigating stress tolerance. J Proteom 169:233–238. https://doi.org/10.1016/j.jprot.2017.04.010

    Article  CAS  Google Scholar 

  48. Shivaraj SM, Mandlik R, Bhat JA, Raturi G, Elbaum R, Alexander L, Tripathi DK, Deshmukh R, Sonah H (2021) Outstanding questions on the beneficial role of silicon in crop plants. Plant Cell Physiol 63:4–18. https://doi.org/10.1093/pcp/pcab145

    Article  CAS  Google Scholar 

  49. Mandlik R, Thakral V, Raturi G, Shinde S, Nikoli´c M, Tripathi DK, Sonah H, Deshmukh R, (2020) Significance of silicon uptake, transport, and deposition in plants. J Exp Bot 71:6703–6718. https://doi.org/10.1093/jxb/eraa301

    Article  PubMed  CAS  Google Scholar 

  50. Lee JK, Kozono D, Remis J, Kitagawa Y, Agre P, Stroud RM (2005) Structural Basis for Conductance by the Archaeal Aquaporin AqpM at 1.68 Å. Proc Natl Acad Sci 102:18932–18937. https://doi.org/10.1073/pnas.0509469102

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  51. Liang Y, Sun W, Zhu YG, Christie P (2007) Mechanisms of silicon-mediated alleviation of abiotic stresses in higher plants: a review. Environ Pollu 147:422–428. https://doi.org/10.1016/j.envpol.2006.06.008

    Article  CAS  Google Scholar 

  52. Amin M, Ahmad R, Ali A, Aslam M, Lee DJ (2016) Silicon fertilization improves the maize (Zea mays L.) performance under limited moisture supply. Cereal Res Comm 44:172–185. https://doi.org/10.1556/0806.43.2015.035

    Article  CAS  Google Scholar 

  53. Antunes PM, Goss MJ (2005) Communication in the tripartite symbiosis formed by arbuscular mycorrhizal fungi, rhizobia and legume plants: a review. Roots and Soil Management: Interactions between Roots and the Soil 48:199–222. https://doi.org/10.2134/agronmonogr48.c11

    Article  CAS  Google Scholar 

  54. Antunes PM, De Varennes A, Zhang T, Goss MJ (2006) The tripartite symbiosis formed by indigenous arbuscular mycorrhizal fungi, Bradyrhizobium japonicum and soybean under field conditions. J Agron Crop Sci 192:373–378. https://doi.org/10.1111/j.1439-037X.2006.00223.x

    Article  Google Scholar 

  55. Smith SE, Smith FA, Jakobsen I (2003) Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol 133:16–20. https://doi.org/10.1104/pp.103.024380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  56. Nell M, Wawrosch C, Steinkellner S, Vierheilig H, Kopp B, Lössl A (2010) Root colonization by symbiotic arbuscular mycorrhizal fungi increases sesquiterpenic acid concentrations in Valeriana officinalis L. Planta Med 76:393–398. https://doi.org/10.1055/s-0029-1186180

    Article  PubMed  CAS  Google Scholar 

  57. Garg N, Cheema A (2021) Relative roles of Arbuscular Mycorrhizae in establishing a correlation between soil properties, carbohydrate utilization and yield in Cicer arietinum L under As stress. Ecotox Environ Safe 207:111196. https://doi.org/10.1016/j.ecoenv.2020.111196

    Article  CAS  Google Scholar 

  58. Garg N, Singla P (2012) The role of Glomus mosseae on key physiological and biochemical parameters of pea plants grown in arsenic contaminated soil. Sci Hortic 143:92–101. https://doi.org/10.1016/j.scienta.2012.06.010

    Article  CAS  Google Scholar 

  59. Latef AAHA, Hashem A, Rasool S, Abd-Allah EF, Alqarawi AA, Egamberdieva D, Jan S, Anjum NA, Ahmad P (2016) Plants mycorrhizal symbiosis and abiotic stress in plants: A Review. J Plant Biol 59:407–426. https://doi.org/10.1007/s12374-016-0237-7

    Article  CAS  Google Scholar 

  60. Yost RS, Fox RL (1982) Influence of mycorrhizae on the mineral contents of cowpea and soybean grown in an oxisol. Agron J 74:475–481. https://doi.org/10.2134/agronj1982.00021962007400030018x

    Article  Google Scholar 

  61. Clark RB, Zeto SK (2000) Mineral acquisition by arbuscular mycorrhizal plants. J Plant Nutr 23:867–902. https://doi.org/10.1080/01904160009382068

    Article  CAS  Google Scholar 

  62. Garg N, Singh S (2017) Arbuscular mycorrhiza Rhizophagusirregularis, and silicon modulate growth, proline biosynthesis and yield in Cajanus cajan, L. Millsp. (pigeon pea) genotypes under cadmium and zinc stress. J Plant Growth Regul 37:1–18. https://doi.org/10.1007/s00344-017-9708-4

    Article  CAS  Google Scholar 

  63. Garg N, Kashyap L (2019) Joint effects of Si and mycorrhiza on the antioxidant metabolism of two pigeonpea genotypes under As (III) and (V) stress. Environ Sci Pollut Res 26:7821–7839. https://doi.org/10.1007/s11356-019-04256-5

    Article  CAS  Google Scholar 

  64. Hammer EC, Nasr H, Pallon J, Olsson PA, Wallander H (2011) Elemental composition of arbuscular mycorrhizal fungi at high salinity. Mycorrhiza 21:117–129. https://doi.org/10.1007/s00572-010-0316-4

    Article  PubMed  CAS  Google Scholar 

  65. Hajiboland R, Moradtalab N, Aliasgharzad N, Eshaghi Z, Feizy J (2018) Silicon influences growth and mycorrhizal responsiveness in strawberry plants. Physiol Mol Biol Plants 24:1103–1115. https://doi.org/10.1007/s12298-018-0533-4

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  66. Fillinger S, Chaveroche M, Van Dijck P, De Vries R, Ruijter G, Thevelein J, d’Enfert C (2001) Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiol 147:1851–1862. https://doi.org/10.1099/00221287-147-7-1851

    Article  CAS  Google Scholar 

  67. Gancedo C, Flores C (2004) The importance of a functional trehalose biosynthetic pathway for the life of yeasts and fungi. FEMS Yeast Res 4:351–359. https://doi.org/10.1016/S1567-1356(03)00222-8

    Article  PubMed  CAS  Google Scholar 

  68. Van Dijck P, De Rop L, Szlufcik K, Van Ael E, Thevelein JM (2002) Disruption of the Candida albicans TPS2 gene encoding trehalose-6-phosphate phosphatase decreases infectivity without affecting hypha formation. Infect Immun 147:1772–1782. https://doi.org/10.1128/IAI.70.4.1772-1782.2002

    Article  CAS  Google Scholar 

  69. Merga B, Haji J (2019) Economic importance of chickpea: Production, value, and world trade. Cogent Food Agric 5:1615718. https://doi.org/10.1080/23311932.2019.1615718

    Article  Google Scholar 

  70. Pandey AK, Burlakoti RR, Kenyon L, Nair RM (2018) Perspectives and challenges for sustainable management of fungal diseases of mungbean [Vigna radiata (L.) R. Wilczek var. radiata]: a review. Front Environ Sci 6:53. https://doi.org/10.3389/fenvs.2018.00053

  71. Leport L, Turner NC, Davies SL, Siddique KHM (2006) Variation in pod production and abortion among chickpea cultivars under terminal drought. Eur J Agron 24:236–246. https://doi.org/10.1016/j.eja.2005.08.005

    Article  Google Scholar 

  72. Giovannetti M, Mosse B (1980) An evaluation of techniques formeasuring vesicular arbuscular mycorrhizal infection in roots. New Phytol 84:489–500

    Article  Google Scholar 

  73. Hetrick BAD, Wilson GWT, Todd TC (1992) Relationships of mycorrhizal symbiosis, rooting strategy, and phenology among tallgrass prairie forbs. Can J Bot 70:1521–1528. https://doi.org/10.1139/b92-191

    Article  Google Scholar 

  74. Velikova V, Yordanov I, Edreva A (2000) Oxidative stress and some antioxidant systems in acid rain treated bean plants. Plant Sci 151:59–66. https://doi.org/10.1016/S0168-9452(99)00197-1

    Article  CAS  Google Scholar 

  75. 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

    Article  CAS  Google Scholar 

  76. Heath RL, Packer I (1968) Photoperoxidation in isolated chloroplast I, kinetics and stochiometry of fatty acid peroxidation. Arch BiochemBiophys 125:189–198. https://doi.org/10.1016/0003-9861(68)90654-1

    Article  CAS  Google Scholar 

  77. Zwiazek JJ, Blake TJ (1991) Early detection of membrane injury in black spruce (Piceamariana). Can J For Res 21:401–404. https://doi.org/10.1139/x91-050

    Article  Google Scholar 

  78. Hartree EF (1957) Haematin compounds. In: Paech K, Tracey MV (eds) Modern methods of plant analysis. Springer-Verlag, Germany, Berlin

  79. Herdina JA, Silsbury JH (1990) Estimating nitrogenase activity of faba bean (Vicia faba) by acetylene reduction (AR) assay. Aust J Plant Physiol 17:489–502

    CAS  Google Scholar 

  80. Streeter JG, Strimbu CE (1998) Simultaneous extraction and derivatization of carbohydrates from green plant tissues for analysis by gas–liquid chromatography. Anal Biochem 259:253–257. https://doi.org/10.1006/abio.1998.2675

    Article  PubMed  CAS  Google Scholar 

  81. Salminen SO, Streeter JG (1986) Enzymes of alpha, alpha-trehalose metabolism in soybean nodules. Plant Physiol 81:538–541

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  82. Padilla L, Krämer R, Stephanopoulos G, Agosin E (2004) Overproduction of trehalose: heterologous expression of Escherichia coli trehalose-6-phosphate synthase and trehalose-6- phosphate phosphatase in Corynebacterium glutamicum. Appl Environ Microbiol 70:370–376. https://doi.org/10.1128/AEM.70.1.370-376.2004

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  83. Müller J, Xie ZP, Staehelin C, Mellor RB, Boller T, Wiemken A (1994) Trehalose and trehalase in root nodules from various legumes. Physiol Plant 90:86–92. https://doi.org/10.1111/j.1399-3054.1994.tb02196.x

    Article  Google Scholar 

  84. Miller GL (1959) Use of dinitrosulphosalicylic acid (DNSA) reagent for determination of reducing sugar. Anal Chem 31:426–428. https://doi.org/10.1021/ac60147a030

    Article  CAS  Google Scholar 

  85. May PB, Douglas LA (1976) Assay for soil urease activity. Plant Soil 45:301–305. https://doi.org/10.1007/BF00011156

    Article  CAS  Google Scholar 

  86. Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil BiolBiochem 9:167–172. https://doi.org/10.1016/0038-0717(77)90070-0

  87. Casida LE Jr, Klein DA, Santoro T (1964) Soil dehydrogenase activity. Soil Sci 98:371–376

    Article  CAS  Google Scholar 

  88. Thimmaiah SR (1999) Standard methods of biochemical analysis. Kalyani Publisher, New Delhi

    Google Scholar 

  89. Schubert KR (1981) Enzymes of purine biosynthesis and catabolism in Glycine max: Comparison of activities with N2 fixation and composition of xylem exudates during nodule development. Plant Physiol 68:1115–1122. https://doi.org/10.1104/pp.68.5.1115

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  90. Vogels GD, Van der Drift C (1970) Differential analyses of glyoxylate derivatives. Anal Biochem 33:143–157. https://doi.org/10.1016/0003-2697(70)90448-3

    Article  PubMed  CAS  Google Scholar 

  91. Kyllingsbæk A (1975) Extraction and colorimetric determination of urea in plants. Acta Agric Scand 25:109–112. https://doi.org/10.1080/00015127509436239

    Article  Google Scholar 

  92. Hogan ME, Swift IE, Done J (1983) Urease assay and ammonia release from leaf tissues. Phytochemistry 22:663–667. https://doi.org/10.1016/S0031-9422(00)86958-7

    Article  CAS  Google Scholar 

  93. Gonza´ lez EM, Gordon AJ, James CL, Arrese-Igor C, (1995) The role of sucrose synthase in the response of soybean nodules to drought. J Exp Bot 46:1515–1523. https://doi.org/10.1093/jxb/46.10.1515

    Article  Google Scholar 

  94. Rognes SE (1975) Glutamine-dependent asparagine synthetase from Lupinus luteus. Phytochemistry 14:1–8. https://doi.org/10.1016/0031-9422(75)83108-6

    Article  Google Scholar 

  95. Vadez V, Sinclair TR, Sarraj R (2000) Asparagine and ureide accumulation in nodules and shoots as feedback inhibitors of N2 fixation in soybean. Physiol Plant 110:215–233. https://doi.org/10.1034/j.1399-3054.2000.110211.x

    Article  CAS  Google Scholar 

  96. Yang Y, Song Y, Scheller HV, Ghosh A, Ban Y, Chen H, Tang M (2015) Community structure of arbuscular mycorrhizal fungi associated with Robiniapseudoacacia in uncontaminated and heavy metal contaminated soils. Soil BiolBiochem 86:146–158. https://doi.org/10.1016/j.soilbio.2015.03.018

    Article  CAS  Google Scholar 

  97. Philippot L, Raaijmakers JM, Lemanceau P, van der Putten WH (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799. https://doi.org/10.1038/nrmicro3109

    Article  PubMed  CAS  Google Scholar 

  98. Abd-Alla MH, Bashandy SR, Bagy MK, El-enany AWE (2014) Rhizobium tibeticum activated with a mixture of flavonoids alleviates nickel toxicity in symbiosis with fenugreek (Trigonella foenum graecum L.). Ecotoxicology 23:946–959. https://doi.org/10.1007/s10646-014-1239-1

    Article  PubMed  CAS  Google Scholar 

  99. Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants: modulation effects of rhizobial symbiosis. BioMed Res Int. https://doi.org/10.1155/2018/8031213

    Article  PubMed  PubMed Central  Google Scholar 

  100. Ali B, Hayat S, Hayat Q, Ahmad A (2010) Cobalt stress affects nitrogen metabolism, photosynthesis and antioxidant system in chickpea (Cicer arietinum L.). J Plant Interact 5:223–231. https://doi.org/10.1080/17429140903370584

    Article  CAS  Google Scholar 

  101. Gonzalez EM, Galvez RL, Aparicio-Tejo PM, Arrese-lgor C (2001) Insights into the regulation of nitrogen fixation in pea nodules: lessons from drought, abscissic acid and increased photo-assimilate availability. Agronomie 21:607–613. https://doi.org/10.1051/agro:2001151

    Article  Google Scholar 

  102. Sethi S, Gupta S (2015) Responses of soil enzymes to different heavy metals. Biolife 3:147–153

    Google Scholar 

  103. Hussain RM (2017) The effect of phosphorus in nitrogen fixation in legumes. J Plant Nutr Soil Sci 167:125–137. https://doi.org/10.19080/ARTOAJ.2017.04.555654

  104. Hassan MU, Chattha MU, Khan I, Chattha MB, Aamer M, Nawaz M, Ali A, Khan MA, Khan TA (2019) Nickel toxicity in plants: reasons, toxic effects, tolerance mechanisms, and remediation possibilities—a review. Environ Sci Pollut Res 26:12673–12688. https://doi.org/10.1007/s11356-019-04892-x

    Article  CAS  Google Scholar 

  105. Haider FU, Wang X, Farooq M, Hussain S, Cheema SA, Ul Ain N, Virk AL, Ejaz M, Janyshova U, Liqun C (2022) Biochar application for the remediation of trace metals in contaminated soils: Implications for stress tolerance and crop production. Ecotox Environ Safe 230:113165. https://doi.org/10.1016/j.ecoenv.2022.113165

    Article  CAS  Google Scholar 

  106. Rizwan M, Usman K, Alsafran M, Jabri HA, Samreen T, Saleem MH, Tu S (2022) Nickel Toxicity Interferes with NO3−/NH4+ Uptake and Nitrogen Metabolic Enzyme Activity in Rice (Oryza sativa L.). Plants 11:1401. https://doi.org/10.1016/j.ecoenv.2022.113165

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  107. Balestrasse KB, Benavides MP, Gallego SM, Tomaro ML (2003) Effect of cadmium stress on nitrogen metabolism in nodules and roots of soybean plants. Funct Plant Biol 30:57–64. https://doi.org/10.1071/FP02074

    Article  PubMed  CAS  Google Scholar 

  108. Khadri M, Pliego L, Soussi M, Lluch C, Ocaña A (2001) Ammonium assimilation and ureide metabolism in common bean (Phaseolus vulgaris) nodules under salt stress. Agronomie 21:635–643

    Article  Google Scholar 

  109. Todd CD, Tipton PA, Blevins DG, Piedras P, Pineda M, Polacco JC (2006) Update on ureide degradation in legumes. J Expl Bot 57:5–12. https://doi.org/10.1093/jxb/erj013

    Article  Google Scholar 

  110. Dresler S, Hawrylak-Nowak B, Kováčik J, Pochwatka M, Hanaka A, Strzemski M, Sowa I, Wójciak-Kosior M (2019) Allantoin attenuates cadmium-induced toxicity in cucumber plants. Ecotox Environ Safe 170:120–126. https://doi.org/10.1016/j.ecoenv.2018.11.119

    Article  CAS  Google Scholar 

  111. Barcelos JPQ, Reis HPG, Godoy CV, Gratão PL, Furlani Junior E, Putti FF, Campos M, Reis AR (2018) Impact of foliar nickel application on urease activity, antioxidant metabolism and control of powdery mildew (Microsphaeradiffusa) in soybean plants. Plant Pathol 67:1502–1513. https://doi.org/10.1111/ppa.12871

    Article  CAS  Google Scholar 

  112. Ali S, Abbas Z, Seleiman MF, Rizwan M, YavaŞ İ, Alhammad BA, Shami A, Hasanuzzaman M, Kalderis D (2020) Glycine betaine accumulation, significance and interests for heavy metal tolerance in plants. Plants 9:896. https://doi.org/10.3390/plants9070896

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  113. Irfan M, Hasan SA, Hayat S, Ahmad A (2015) Photosynthetic variation and yield attributes of two mustard varieties against cadmium phytotoxicity. Cogent Food Agric 1:1106186. https://doi.org/10.1080/23311932.2015.1106186

    Article  CAS  Google Scholar 

  114. Wyszkowski M, Radziemska M (2010) Effects of chromium (III and VI) on spring barley and maize biomass yield and content of nitrogenous compounds. J Toxicol Environ Health 73:1274–1282. https://doi.org/10.1080/15287394.2010.492016

    Article  CAS  Google Scholar 

  115. Kumar S, Shah SH, Vimala Y, Jatav HS, Ahmad P, Chen Y, Siddique KH (2022) Abscisic acid: Metabolism, transport, crosstalk with other plant growth regulators, and its role in heavy metal stress mitigation. Front Plant Sci 13:972856. https://doi.org/10.3389/fpls.2022.972856

    Article  PubMed  PubMed Central  Google Scholar 

  116. Bhat JA, Shivaraj SM, Singh P, Navadagi DB, Tripathi DK, Dash PK, Solanke AU, Sonah H, Deshmukh R (2019) Role of silicon in mitigation of heavy metal stresses in crop plants. Plants 8:71. https://doi.org/10.3390/plants8030071

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  117. Riaz M, Kamran M, Fang Y, Wang Q, Cao H, Yang G, Deng L, Wang Y, Zhou Y, Anastopoulos I, Wang X (2021) Arbuscular mycorrhizal fungi-induced mitigation of heavy metal phytotoxicity in metal contaminated soils: A critical review. J Hazard Mater 402:123919. https://doi.org/10.1016/j.jhazmat.2020.123919

    Article  PubMed  CAS  Google Scholar 

  118. Chandrasekaran M (2022) Arbuscular mycorrhizal fungi mediated enhanced biomass, root morphological traits and nutrient uptake under drought stress: A meta-analysis. J Fungi 8:660. https://doi.org/10.3390/jof8070660

    Article  CAS  Google Scholar 

  119. Mandlik R, Singla P, Kumawat S, Khatri P, Ansari W, Singh A, Sharma Y, Singh A, Solanke A, Nadaf A, Sonah H, Deshmukh R (2022) Understanding aquaporin regulation defining silicon uptake and role in arsenic, antimony and germanium stress in pigeonpea (Cajanus cajan). Environ Pollut 294:118606. https://doi.org/10.1016/j.envpol.2021.118606

    Article  PubMed  CAS  Google Scholar 

  120. Meena VD, Dotaniya ML, Coumar V, Rajendiran S, Kundu S, RaoAS, (2014) A case for silicon fertilization to improve crop yieldsin tropical soils. Proc Natl Acad Sci, India Sect b: Biol Sci 84:505–518. https://doi.org/10.1007/s40011-013-0270-y

    Article  CAS  Google Scholar 

  121. Etesami H, Jeong BR, Glick BR (2021) Contribution of arbuscular mycorrhizal fungi, phosphate–solubilizing bacteria, and silicon to P uptake by plant. Front Plant Sci 12:699618. https://doi.org/10.3389/fpls.2021.699618

    Article  PubMed  PubMed Central  Google Scholar 

  122. Putra R, Waterman JM, Mathesius U, Wojtalewicz D, Powell JR, Hartley SE, Johnson SN (2022) Benefits of silicon-enhanced root nodulation in a model legume are contingent upon rhizobial efficacy. Plant Soil 77:201–217. https://doi.org/10.1007/s11104-022-05358-9

    Article  CAS  Google Scholar 

  123. Gough EC, Owen KJ, Zwart RS, Thompson JP (2021) Arbuscular mycorrhizal fungi acted synergistically with Bradyrhizobium sp. to improve nodulation, nitrogen fixation, plant growth and seed yield of mung bean (Vigna radiata) but increased the population density of the root-lesion nematode Pratylenchusthornei. Plant Soil 465:431–452. https://doi.org/10.1007/s11104-021-05007-7

    Article  CAS  Google Scholar 

  124. Putra R, Powell JR, Hartley SE, Johnson SN (2020) Is it time to include legumes in plant silicon research? FunctEcol 34:1142–1157. https://doi.org/10.1111/1365-2435.13565

    Article  Google Scholar 

  125. Dakora F, Atkins C (1989) Diffusion of oxygen in relation to structure and function in legume root nodules. Aust J Plant Physiol 16:131–140. https://doi.org/10.1071/PP9890131

    Article  CAS  Google Scholar 

  126. Sheehy JE, Minchin FR, Witty JF (1985) Control of nitrogen fixation in a legume nodule: An analysis of the role of oxygen diffusion in relation to nodule structure. Annal Bot 55:549–562. https://doi.org/10.1093/oxfordjournals.aob.a086930

    Article  Google Scholar 

  127. Wang K, Li F, Gao M, Huang Y, Song Z (2020) Mechanisms of trehalose-mediated mitigation of Cd toxicity in rice seedlings. J Clean Prod 267:121982. https://doi.org/10.1016/j.jclepro.2020.121982

    Article  CAS  Google Scholar 

  128. Calonne M, Fontaine J, Debiane D, Laruelle F, Grandmougin-Ferjani A, Sahraoui ALH (2014) The arbuscular mycorrhizal Rhizophagusirregularis activates storage lipid biosynthesis to cope with the benzo [a] pyrene oxidative stress. Phytochemistry 97:30–37. https://doi.org/10.1016/j.phytochem.2013.10.014

    Article  PubMed  CAS  Google Scholar 

  129. González-Párraga P, Hernández JA, Argüelles JC (2003) Role of antioxidant enzymatic defences against oxidative stress (H2O2) and the acquisition of oxidative tolerance in Candida albicans. Yeast 20:1161–1169. https://doi.org/10.1002/yea.1029

    Article  PubMed  CAS  Google Scholar 

  130. Luo Y, Li WM, Wang W (2008) Trehalose: protector of antioxidant enzymes or reactive oxygen species scavenger under heat stress? Environ Exp Bot 63:378–384. https://doi.org/10.1016/j.envexpbot.2007.11.016

    Article  CAS  Google Scholar 

  131. Kaiser C, Kilburn MR, Clode PL, Fuchslueger L, Koranda M, Cliff JB, Solaiman ZM, Murphy DV (2015) Exploring the transfer of recent plant photosynthates to soil microbes: mycorrhizal pathway vs direct root exudation. New Phytolo 205:1537–1551. https://doi.org/10.1111/nph.13138

    Article  CAS  Google Scholar 

  132. Qian K, Wang L, Yin N (2012) Effects of AMF on soil enzyme activity and carbon sequestration capacity in reclaimed mine soil. Int J Min Sci Technol 22(4):553–557. https://doi.org/10.1016/j.ijmst.2012.01.019

    Article  CAS  Google Scholar 

  133. Bhalla S, Garg N (2021) Arbuscular mycorrhizae and silicon alleviate arsenic toxicity by enhancing soil nutrient availability, starch degradation and productivity in Cajanus cajan (L.) Millsp. Mycorrhiza 31:735–754. https://doi.org/10.1007/s00572-021-01056-z

    Article  PubMed  CAS  Google Scholar 

  134. Khan E, Gupta M (2018) Arsenic–silicon priming of rice (Oryza sativa L.) seeds influence mineral nutrient uptake and biochemical responses through modulation of Lsi-1, Lsi-2, Lsi-6 and nutrient transporter genes. Sci Rep 8:1–16. https://doi.org/10.1038/s41598-018-28712-3

    Article  CAS  Google Scholar 

  135. Paradisone V, Navarro-León E, Ruiz JM, Esposito S, Blasco B (2021) Calcium silicate ameliorates zinc deficiency and toxicity symptoms in barley plants through improvements in nitrogen metabolism and photosynthesis. Acta Physiol Plant 43:1–11. https://doi.org/10.1007/s11738-021-

    Article  Google Scholar 

  136. Sheteiwy MS, Ahmed M, Korany SM, Alsherif EA, Mowafy AM, Chen J, ośko I, Selim S AbdElgawad H, (2022) Arbuscular Mycorrhizal Fungus “Rhizophagusirregularis” impacts on physiological and biochemical responses of ryegrass and chickpea plants under beryllium stress. Environ Pollut 315:120356. https://doi.org/10.1016/j.micres.2022.127254

    Article  PubMed  CAS  Google Scholar 

  137. Irani S, Todd CD (2016) Ureide metabolism under abiotic stress in Arabidopsis thaliana. Plant Physiol 199:87–95. https://doi.org/10.1016/j.jplph.2016.05.011

    Article  CAS  Google Scholar 

  138. Lescano CI, Martini C, González CA, Desimone M (2016) Allantoin accumulation mediated by allantoinase down regulation and transport by Ureide Permease 5 confers salt stress tolerance to Arabidopsis plants. Plant Mol Biol 91:581–595. https://doi.org/10.1007/s11103-016-0490-7

    Article  PubMed  CAS  Google Scholar 

  139. Nourimand M, Todd CD (2016) Allantoin increases cadmium tolerance in Arabidopsis via activation of antioxidant mechanisms. Plant Cell Physiol 57:2485–2496. https://doi.org/10.1093/pcp/pcw162

    Article  PubMed  CAS  Google Scholar 

  140. Irani S, Lobo JM, Gray GR, Todd CD (2018) Allantoin accumulation in response to increased growth irradiance in Arabidopsis thaliana. Biol Plant 62:181–187. https://doi.org/10.1007/s10535-017-0747-2

    Article  CAS  Google Scholar 

  141. Brychkova G, Alikulov Z, Fluhr R, Sagi M (2008) A critical role for ureides in dark and senescence-induced purine remobilization is unmasked in the Atxdh1 Arabidopsis mutant. Plant J 54:496–509. https://doi.org/10.1111/j.1365-313X.2008.03440.x

    Article  PubMed  CAS  Google Scholar 

  142. Andrade SA, Gratao PL, Azevedo RA, Silveira AP, Schiavinato MA, Mazzafera P (2010) Biochemical and physiological changes in jack bean under mycorrhizal symbiosis growing in soil with increasing Cu concentrations. Environ Exp Bot 68:198–207. https://doi.org/10.1016/j.envexpbot.2009.11.009

    Article  CAS  Google Scholar 

  143. He Z, He C, Zhang Z, Zou Z, Wang H (2007) Changes of antioxidative enzymes and cell membrane osmosis in tomato colonized by arbuscular mycorrhizae under NaCl stress. Colloids Surf B: Biointerfaces 59:128–133. https://doi.org/10.1016/j.colsurfb.2007.04.023

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

We gratefully acknowledge Pulse Laboratory and TERI, New Delhi, India for providing biological material for research and LA-ICP-MS (Laser Ablation Inductively Coupled Plasma Mass Spectrometry) located in at SAIF (Sophisticated Analytical Instrumentation Facility), Panjab University, Chandigarh.

Funding

The authors would like to thank Department of Biotechnology (DBT),Government of India[BT/PR13409/BPA/118/122/2015] for financial assistance for undertaking the research.

Author information

Authors and Affiliations

Authors

Contributions

The corresponding author (NG) designed and monitored the research experiments. The first author (KT) performed the experiments under direct supervision and involvement of the corresponding author (NG). Both authors have contributed equally in preparation of manuscript.

Corresponding author

Correspondence to Neera Garg.

Ethics declarations

Ethics Approval

Not applicable.

Consent to Participate

Not applicable.

Consent for Publication

Not applicable.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 2719 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thakur, K., Garg, N. Differential Role of Silicon and Rhizoglomus intraradices in Modulating Amide and Ureide Metabolism of Seasonally Different Legume Species Subjected to Nickel Toxicity. Silicon 15, 7499–7522 (2023). https://doi.org/10.1007/s12633-023-02599-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12633-023-02599-w

Keywords

Navigation