44. Puppo A, Pauly N, Boscari A, Mandon K, Brouquisse R (2013) Hydrogen peroxide and nitric
oxide: key regulators of the Legume-Rhizobium and mycorrhizal symbioses. Antioxid Redox
Signal 18:2202–2219. https://doi.org/10.1089/ars.2012.5136
45. Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R (2015) Nitric oxide:
a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66:2877–2887. https://doi.
org/10.1093/jxb/erv051
46. Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A (2016) Reactive oxygen species and
nitric oxide control early steps of the Legume – Rhizobium symbiotic interaction. Front Plant
Sci 7:1–8. https://doi.org/10.3389/fpls.2016.00454
47. Montiel J, Arthikala MK, Cardenas L, Quinto C (2016) Legume NADPH oxidases have
crucial roles at different stages of nodulation. Int J Mol Sci 17:1–12. https://doi.org/10.3390/
ijms17050680
48. Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants:
modulation effects of rhizobial symbiosis. Biomed Res Int 2018:8031213. https://doi.org/
10.1155/2018/8031213
49. Zahran HH (1999) Rhizobium -legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
50. Johnston AW, Yeoman KH, Wexler M (2001) Metals and the rhizobial-legume symbiosis –
uptake, utilization and signalling. Adv Microb Physiol 45:113–156
51. Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H,
Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms
and plants. FEMS Microbiol Rev 25:335–347. https://doi.org/10.1016/S0168-6445(01)
00057-2
52. Broos K, Mertens J, Smolders E (2005) Toxicity of heavy metals in soil assessed with various
soil microbial and plant growth assays: a comparative study. Environ Toxicol Chem
24:634–640
53. Arora NK, Khare E, Singh S, Maheshwari DK (2010) Effect of Al and heavy metals on
enzymes of nitrogen metabolism of fast and slow growing rhizobia under explanta conditions.
World J Microbiol Biotechnol 26:811–816
54. Ahmad E, Oves M (2012) Heavy metal toxicity to symbiotic nitrogen-fixing microorganism
and host legumes. In: Zaidi A, Wani PA, Khan NS (eds) Toxicity of heavy metals to Legumes
and bioremediation. Springer, Wien, pp 29–44. https://doi.org/10.1007/978-3-7091-0730-0
55. DalCorso G (2012) Heavy metal toxicity in plants. In: Furini A (ed) Plants and heavy metals.
Springer, Netherlands, Dordrecht, pp 1–25
56. Sangwan P, Kumar V, Joshi UN (2014) Effect of Chromium(VI) toxicity on enzymes of
nitrogen metabolism in clusterbean (Cyamopsis tetragonoloba L.). Enzyme Res 2014:1–9.
https://doi.org/10.1155/2014/784036
57. Chaudhary P, Dudeja SS, Kapoor KK (2004) Effectivity of host- Rhizobium leguminosarum
symbiosis in soils receiving sewage water containing heavy metals. Microbiol Res
159:121–127. https://doi.org/10.1016/j.micres.2004.01.009
58. Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium
contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with
the MTL4 and the PCS genes. Chemosphere 66:1670–1676. https://doi.org/10.1016/j.
chemosphere.2006.07.058
59. Kong Z, Mohamad OA, Deng Z, Liu X, Glick BR, Wei G (2015) Rhizobial symbiosis effect on
the growth, metal uptake, and antioxidant responses of Medicago lupulina under copper stress.
Environ Sci Pollut Res 22:12479–12489. https://doi.org/10.1007/s11356-015-4530-7
60. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting
rhizobacteria: current perspective. J King Saud Univ – Sci 26:1–20. https://doi.org/10.1016/
j.jksus.2013.05.001
61. Hao X, Taghavi S, Xie P, Orbach MJ, Alwathnani HA, Rensing C, Wei G (2014)
Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. Int J
Phytoremediation 16:179–202. https://doi.org/10.1080/15226514.2013.773273
316
U. Y. Stambulska and M. M. Bayliak
oxide: key regulators of the Legume-Rhizobium and mycorrhizal symbioses. Antioxid Redox
Signal 18:2202–2219. https://doi.org/10.1089/ars.2012.5136
45. Hichri I, Boscari A, Castella C, Rovere M, Puppo A, Brouquisse R (2015) Nitric oxide:
a multifaceted regulator of the nitrogen-fixing symbiosis. J Exp Bot 66:2877–2887. https://doi.
org/10.1093/jxb/erv051
46. Damiani I, Pauly N, Puppo A, Brouquisse R, Boscari A (2016) Reactive oxygen species and
nitric oxide control early steps of the Legume – Rhizobium symbiotic interaction. Front Plant
Sci 7:1–8. https://doi.org/10.3389/fpls.2016.00454
47. Montiel J, Arthikala MK, Cardenas L, Quinto C (2016) Legume NADPH oxidases have
crucial roles at different stages of nodulation. Int J Mol Sci 17:1–12. https://doi.org/10.3390/
ijms17050680
48. Stambulska UY, Bayliak MM, Lushchak VI (2018) Chromium (VI) toxicity in legume plants:
modulation effects of rhizobial symbiosis. Biomed Res Int 2018:8031213. https://doi.org/
10.1155/2018/8031213
49. Zahran HH (1999) Rhizobium -legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989
50. Johnston AW, Yeoman KH, Wexler M (2001) Metals and the rhizobial-legume symbiosis –
uptake, utilization and signalling. Adv Microb Physiol 45:113–156
51. Cervantes C, Campos-García J, Devars S, Gutiérrez-Corona F, Loza-Tavera H,
Torres-Guzmán JC, Moreno-Sánchez R (2001) Interactions of chromium with microorganisms
and plants. FEMS Microbiol Rev 25:335–347. https://doi.org/10.1016/S0168-6445(01)
00057-2
52. Broos K, Mertens J, Smolders E (2005) Toxicity of heavy metals in soil assessed with various
soil microbial and plant growth assays: a comparative study. Environ Toxicol Chem
24:634–640
53. Arora NK, Khare E, Singh S, Maheshwari DK (2010) Effect of Al and heavy metals on
enzymes of nitrogen metabolism of fast and slow growing rhizobia under explanta conditions.
World J Microbiol Biotechnol 26:811–816
54. Ahmad E, Oves M (2012) Heavy metal toxicity to symbiotic nitrogen-fixing microorganism
and host legumes. In: Zaidi A, Wani PA, Khan NS (eds) Toxicity of heavy metals to Legumes
and bioremediation. Springer, Wien, pp 29–44. https://doi.org/10.1007/978-3-7091-0730-0
55. DalCorso G (2012) Heavy metal toxicity in plants. In: Furini A (ed) Plants and heavy metals.
Springer, Netherlands, Dordrecht, pp 1–25
56. Sangwan P, Kumar V, Joshi UN (2014) Effect of Chromium(VI) toxicity on enzymes of
nitrogen metabolism in clusterbean (Cyamopsis tetragonoloba L.). Enzyme Res 2014:1–9.
https://doi.org/10.1155/2014/784036
57. Chaudhary P, Dudeja SS, Kapoor KK (2004) Effectivity of host- Rhizobium leguminosarum
symbiosis in soils receiving sewage water containing heavy metals. Microbiol Res
159:121–127. https://doi.org/10.1016/j.micres.2004.01.009
58. Ike A, Sriprang R, Ono H, Murooka Y, Yamashita M (2007) Bioremediation of cadmium
contaminated soil using symbiosis between leguminous plant and recombinant rhizobia with
the MTL4 and the PCS genes. Chemosphere 66:1670–1676. https://doi.org/10.1016/j.
chemosphere.2006.07.058
59. Kong Z, Mohamad OA, Deng Z, Liu X, Glick BR, Wei G (2015) Rhizobial symbiosis effect on
the growth, metal uptake, and antioxidant responses of Medicago lupulina under copper stress.
Environ Sci Pollut Res 22:12479–12489. https://doi.org/10.1007/s11356-015-4530-7
60. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting
rhizobacteria: current perspective. J King Saud Univ – Sci 26:1–20. https://doi.org/10.1016/
j.jksus.2013.05.001
61. Hao X, Taghavi S, Xie P, Orbach MJ, Alwathnani HA, Rensing C, Wei G (2014)
Phytoremediation of heavy and transition metals aided by legume-rhizobia symbiosis. Int J
Phytoremediation 16:179–202. https://doi.org/10.1080/15226514.2013.773273
316
U. Y. Stambulska and M. M. Bayliak