Effect of Bacterial Inoculation on Morphological and Pomological Characteristics of Three Strawberry (Fragaria x ananassa Duch.) Cultivars Under Cadmium Toxicity

Abstract

Cadmium (Cd) is one of the main elements that cause heavy metal pollution, which is one of the important types of environmental pollution. There is a constant quest to reduce or eliminate the effects of Cd pollution. Plant growth-promoting rhizobacteria (PGPR) is one of these possible solutions. PGPRs not only increase plant growth but also protect plants against organic and inorganic stresses. In this study, the effects of three different Pseudomonas strains (MS-7, MS-12, and MS-13) on morphological and pomological characteristics of three different strawberry cultivars (Rubygem, Kabarla, and YFL) exposed to three different Cd doses (0, 100 and 300 mg kg-1) were investigated to determine the effectiveness of PGPR against Cd toxicity in strawberry. To this end, root collar diameter (RCD), root length (RL), root fresh weight (RFW), root dry weight (RDW), shot fresh weight (SFW), shot dry weight (SDW), leaf area (LA), mean fruit weight (MFW), mean fruit length (MFL), and mean fruit diameter (MFD) were examined. It was observed that the effects of different Pseudomonas strains were cultivar-specific and affected some parameters more. Rubygem MS-7 bacterial strain preserved SDW (3.21 g) and MS-12 bacterial strain preserved RFW (13.01 g) at 300 mg kg-1 Cd dose significantly better against Cd toxicity than other bacterial strains. In Kabarla MS-7 bacterial strain preserved RDW (3.72 g) at 300 mg kg-1 Cd dose and MS-12 bacterial strain preserved SFW (15.27 g) at 100 mg kg-1 Cd dose significantly better against Cd toxicity than other bacterial strains. Likewise, in YFL, MS-13 bacterial strains preserved MFW (7.509 g) and RL (30.00 cm) at 300 mg kg-1 Cd dose, and MS-7 bacterial strain preserved LA (57.87 cm2) at 100 mg kg-1 Cd dose significantly better against Cd toxicity than other bacterial strains. The results of the study showed that formulations containing Pseudomonas sp. can be used as an agricultural improver in areas with heavy metal pollution. As a result of the study, it was observed that PGPR applications were effective in preserving the morphological and pomological characteristics that decreased with the increase in Cd dose.

Keywords

• Strawberry
• cadmium toxicity
• morphological characteristics
• pomological characteristics
• Pseudomonas

References

1. Abdelatey, L.M., Khalil, W.K., Ali, T.H., Mahrous, K.F., 2011. Heavy metal resistance and gene expression analysis of metal resistance genes in gram-positive and gram-negative bacteria present in egyptıan soils. Journal of Applied Sciences in Environmental Sanitation, 6(2): 201-211.
2. Ahmad, P., Nabi, G., Ashraf, M., 2011. Cadmium-induced oxidative damage in mustard [Brassica juncea (L.) Czern. & Coss.] plants can be alleviated by salicylic acid. South African Journal of Botany, 77(1): 36-44.
3. Aloui, A., Recorbet, G., Robert, F., Schoefs, B., Bertrand, M., Henry, C., Gianinazzi-Pearson, V., Dumas-Gaudot, E., Aschi-Smiti, S., 2011. Arbuscular mycorrhizal symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biology, 11(1): 1-17.
4. Al-Yemeni, M.N., 2001. Effect of cadmium, mercury and lead on seed germination and early seedling growth of Vigna ambacensis L. Indian Journal of Plant Physiology, 6(2): 147-151.
5. Andresen, E., Küpper, H., 2013. Cadmium toxicity in plants. In: A. Sigel, H. Sigel, R. Sigel (Eds.), Cadmium: From Toxicity to Essentiality, Metal Ions in Life Sciences, Vol 11., 1st Edn., Springer, Dordrecht, pp. 395-413.
6. Angelone, M., Bini, C., 2017. Trace element concentrations in soils and plants of Western Europe. In: D.C. Adriano (Ed.), Biogeochemistry of Trace Metals, CRC Press, Boca Raton, pp. 31-72.
7. Anonymous, 2022. Crops and livestock Products. (https://www.fao.org/faostat/en/#data/QCL/visualize), (Accessed: 19.08.2022).
8. Arnon, D.I., Stout, P.R., 1939. Molybdenum as an essential element for higher plants. Plant Physiology, 14(3): 599-602.

9. Aslantaş, R., Çakmakçi, R., Şahin, F., 2007. Effect of plant growth promoting rhizobacteria on young apple tree growth and fruit yield under orchard conditions. Scientia Horticulturae, 111(4): 371-377.
10. Awan, S.A., Ilyas, N., Khan, I., Raza, M.A., Rehman, A.U., Rizwan, M., Rastogi, A., Tariq, R., Brestic, M., 2020. Bacillus siamensis reduces cadmium accumulation and improves growth and antioxidant defense system in two wheat (Triticum aestivum L.) varieties. Plants, 9(7): 878-891.
11. Bakkaus, E., Gouget, B., Gallien, J.P., Khodja, H., Carrot, F., Morel, J.L., Collins, R., 2005. Concentration and distribution of cobalt in higher plants: the use of micro-PIXE spectroscopy. Nuclear Instruments and Methods in Physics Research Section B: Beam Interactions with Materials and Atoms, 231(1-4): 350-356.
12. Balcı, G., 2018. Effect of 24–epibrassinosteroid on the vegetative growth criteria of strawberry seedling under cadmium stress conditions. Bahçe, 47(2): 33-38. (In Turkish).
13. Barcelo, J., Vazquez, M.D., Poschenrieder, C.H., 1988. Structural and ultrastructural disorders in cadmium‐treated bush bean plants (Phaseolus vulgaris L.). New Phytologist, 108(1): 37-49.
14. 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(5): 696-709.
15. Benavides, M.P., Gallego, S.M., Tomaro, M.L., 2005. Cadmium toxicity in plants. Brazilian Journal of Plant Physiology, 17(1): 21-34.
16. Bissonnette, L., St-Arnaud, M., Abrecque, M., 2010. Phytoextraction of heavy metals by two Salicaceae clones in symbiosis with arbuscular mycorrhizal fungi during the second year of a field trial. Plant and Soil, 332(1): 55-67.
17. Chanway, C.P., Radley, R.A., Holl, F.B., 1991. Inoculation of conifer seed with plant growth promoting Bacillus strains causes increased seedling emergence and biomass. Soil Biology and Biochemistry, 23(6): 575-580.
18. Chen, B., Zhang, Y., Rafiq, M.T., Khan, K.Y., Pan, F., Yang, X., Feng, Y., 2014. Improvement of cadmium uptake and accumulation in Sedum alfredii by endophytic bacteria Sphingomonas SaMR12: effects on plant growth and root exudates. Chemosphere, 117: 367-373.
19. Chipasa, K.B., 2003. Accumulation and fate of selected heavy metals in a biological wastewater treatment system. Waste Management, 23(2): 135-143.
20. Chugh, L.K., Sawhney, S.K., 1999. Photosynthetic activities of Pisum sativum seedlings grown in presence of cadmium. Plant Physiology and Biochemistry, 37(4): 297-303.
21. Cieśliński, G., Neilsen, G.H., Hogue, E.J., 1996. Effect of soil cadmium application and pH on growth and cadmium accumulation in roots, leaves and fruit of strawberry plants (Fragaria× ananassa Duch.). Plant and Soil, 180(2): 267-276.
22. Das, P., Samantaray, S., Rout, G.R., 1997. Studies on cadmium toxicity in plants: a review. Environmental Pollution, 98(1): 29-36.
23. de Andrade, S.A.L., da Silveira, A.P.D., Jorge, R.A., de Abreu, M.F., 2008. Cadmium accumulation in sunflower plants influenced by arbuscular mycorrhiza. International Journal of Phytoremediation, 10(1): 1-13.
24. Dey, R.K.K.P., Pal, K.K., Bhatt, D.M., Chauhan, S.M., 2004. Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiological Research, 159(4): 371-394.
25. Dobbelaere, S., Croonenborghs, A., Thys, A., Ptacek, D., Okon, Y., Vanderleyden, J., 2002. Effect of inoculation with wild type Azospirillum brasilense and A. irakense strains on development and nitrogen uptake of spring wheat and grain maize. Biology and Fertility of Soils, 36(4): 284-297.
26. Doble, M., Kumar, A., 2005. Biotreatment of Industrial Effluents. Elsevier, Oxford.
27. Egamberdiyeva, D., 2005. Plant‐growth‐promoting rhizobacteria isolated from a Calcisol in a semi‐arid region of Uzbekistan: biochemical characterization and effectiveness. Journal of Plant Nutrition and Soil Science, 168(1): 94-99.
28. Ekmekçi, Y., Tanyolac, D., Ayhan, B., 2008. Effects of cadmium on antioxidant enzyme and photosynthetic activities in leaves of two maize cultivars. Journal of Plant Physiology, 165(6): 600-611.
29. El-Beltagi, H.S., Mohamed, A.A., Rashed, M.M., 2010. Response of antioxidative enzymes to cadmium stress in leaves and roots of radish (Raphanus sativus L.). Notulae Scientia Biologicae, 2(4): 76-82.
30. Epstein, E. 1972. Mineral Nutrition of Plants: Principles and Perspectives. Wiley, New York.
31. Gao, Y., Miao, C., Mao, L., Zhou, P., Jin, Z., Shi, W., 2010. Improvement of phytoextraction and antioxidative defense in Solanum nigrum L. under cadmium stress by application of cadmium-resistant strain and citric acid. Journal of Hazardous Materials, 181(1-3): 771-777.
32. García-Fraile, P., Carro, L., Robledo, M., Ramírez-Bahena, M.H., Flores-Félix, J.D., Fernández, M. T., Mateos, P.F., Rivas, R., Igual, J.M., Martinez-Molina, E.,Peix, A., Velázquez, E., 2012. Rhizobium promotes non-legumes growth and quality in several production steps: towards a biofertilization of edible raw vegetables healthy for humans. PLoS One, 7(5): e38122.
33. Garrido, M.L., Munoz-Olivas, R., Cámara, C., 1998. Determination of cadmium in aqueous media by flow injection cold vapour atomic absorption spectrometry: Application to natural water samples. Journal of Analytical Atomic Spectrometry, 13(4): 295-300.
34. Ghorbanli, M., Kaveh, S.H., Sepehr, M.F., 1999. Effects of cadmium and gibberellin on growth and photosynthesis of Glycine max. Photosynthetica, 37(4): 627-631.
35. Griffiths, P.G., Sasse, J.M., Yokota, T., W. Cameron, D., 1995. 6-Deoxotyphasterol and 3-Dehydro-6-deoxoteasterone, Possible Precursors to Brassinosteroidsin the Pollen of Cupressus arizonica. Bioscience, Biotechnology, and Biochemistry, 59(5): 956-959.
36. Gunathilakae, N., Yapa, N., Hettiarachchi, R., 2018. Effect of arbuscular mycorrhizal fungi on the cadmium phytoremediation potential of Eichhornia crassipes (Mart.) Solms. Groundwater for Sustainable Development, 7: 477-482.
37. Guo, J.H., Qi, H.Y., Guo, Y.H., Ge, H.L., Gong, L.Y., Zhang, L.X., Sun, P.H., 2004. Biocontrol of tomato wilt by plant growth-promoting rhizobacteria. Biological Control, 29(1): 66-72.
38. Guo, J., Chi, J., 2014. Effect of Cd-tolerant plant growth-promoting rhizobium on plant growth and Cd uptake by Lolium multiflorum Lam. and Glycine max (L.) Merr. in Cd-contaminated soil. Plant and Soil, 375(1): 205-214.
39. Hasan, S.A., Fariduddin, Q., Ali, B., Hayat, S., Ahmad, A., 2009. Cadmium: toxicity and tolerance in plants. Journal of Environmental Biology, 30(2): 165-174.
40. Hashem, A., Abd-Allah, E.F., Alqarawi, A.A., Al Huqail, A.A., Egamberdieva, D., Wirth, S., 2016. Alleviation of cadmium stress in Solanum lycopersicum L. by arbuscular mycorrhizal fungi via induction of acquired systemic tolerance. Saudi Journal of Biological Sciences, 23(2): 272-281.
41. Hassan, M., Mansoor, S., 2014. Oxidative stress and antioxidant defense mechanism in mung bean seedlings after lead and cadmium treatments. Turkish Journal of Agriculture and Forestry, 38(1): 55-61.
42. Hayat, S., Alyemeni, M.N., Hasan, S.A., 2012. Foliar spray of brassinosteroid enhances yield and quality of Solanum lycopersicum under cadmium stress. Saudi Journal of Biological Sciences, 19(3): 325-335.
43. Ipek, M., Pirlak, L., Esitken, A., Dönmez, M.F, Turan, M., Sahin, F., 2014. Plant growth-promoting rhizobacteria (PGPR) increase yield, growth and nutrition of strawberry under high-calcareous soil conditions. Journal of Plant Nutrition, 37(7): 990-1001.
44. Jeon, J.S., Lee, S.S., Kim, H.Y., Ahn, T.S., Song, H.G., 2003. Plant growth promotion in soil by some inoculated microorganisms. Journal of Microbiology, 41(4): 271-276.
45. Jiang, W., Liu, D., Hou, W., 2001. Hyperaccumulation of cadmium by roots, bulbs and shoots of garlic (Allium sativum L.). Bioresource Technology, 76(1): 9-13.
46. Jiang, C.Y., Sheng, X.F., Qian, M., Wang, Q.Y., 2008. Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere, 72(2): 157-164.
47. Jiang, Q.Y., Zhuo, F., Long, S.H., Zhao, H.D., Yang, D.J., Ye, Z.H., Li, S.S., Jing, Y.X., 2016. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Scientific Reports, 6(1): 1-9.
48. Jinbiao, Z., Yusen, C., Weinan, H., Guohua, Z., Youli, H., 2001. Effect of Cd contamination on the growth of strawberry. Journal of Fujian Agricultural University, 30(4): 528-531.
49. Kamran, M.A., Syed, J.H., Eqani, S.A.M.A.S., Munis, M.F.H., Chaudhary, H.J., 2015. Effect of plant growth-promoting rhizobacteria inoculation on cadmium (Cd) uptake by Eruca sativa. Environmental Science and Pollution Research, 22(12): 9275-9283.
50. Kanchana, D., Jayanthi, M., Usharani, G., Saranraj, P., Sujitha, D., 2014. Interaction effect of combined inoculation of PGPR on growth and yield parameters of chilli var k1 (Capsicum annuum L.). International Journal of Microbiological Research, 5(3): 144-151.
51. Karakurt, H., Aslantaş, R., 2010. Effects of some plant growth promoting rhizobacteria (PGPR) strains on plant growth and leaf nutrient content of apple. Journal of Fruit and Ornamental Plant Research, 18(1): 101-110.
52. Karakurt, H., Kotan, R., Dadaşoğlu, F., Aslantaş, R., Şahin, F., 2011. Effects of plant growth promoting rhizobacteria on fruit set, pomological and chemical characteristics, color values, and vegetative growth of sour cherry (Prunus cerasus cv. Kütahya). Turkish Journal of Biology, 35(3): 283-291.
53. Kaya, C., Aslan, M., 2020. Hydrogen sulphide partly involves in thiamine-induced tolerance to cadmium toxicity in strawberry (Fragaria x ananassa Duch) plants. Environmental Science and Pollution Research, 27(1): 941-953.
54. Kaymak, H.C., Yarali, F., Güvenç, I., Donmez, M.F., 2008. The effect of inoculation with plant growth rhizobacteria (PGPR) on root formation of mint (Mentha piperita L.) cuttings. African Journal of Biotechnology, 7(24): 4479-4483.
55. Khan, M.I.R., Nazir, F., Asgher, M., Per, T.S., Khan, N.A., 2015. Selenium and sulfur influence ethylene formation and alleviate cadmium-induced oxidative stress by improving proline and glutathione production in wheat. Journal of Plant Physiology, 173: 9-18.
56. Khan, N., Bano, A., Zandi, P., 2018. Effects of exogenously applied plant growth regulators in combination with PGPR on the physiology and root growth of chickpea (Cicer arietinum) and their role in drought tolerance. Journal of Plant Interactions, 13(1): 239-247.
57. Kloepper, J.W., 1978. Plant growth-promoting rhizobacteria on radishes. In: Procedings of the 4th International. Conferance on Plant Pathogenic Bacter, Station de Pathologie Vegetale et Phytobacteriologie, Aug 27-Sep 2, INRA, Angers, France, pp. 879-882.
58. Kloepper, J.W., Schroth, M.N., Miller, T.D., 1980. Effects of rhizosphere colonization by plant growth-promoting rhizobacteria on potato plant development and yield. Phytopathology, 70(11): 1078-1082.
59. Kuffner, M., Puschenreiter, M., Wieshammer, G., Gorfer, M., Sessitsch, A., 2008. Rhizosphere bacteria affect growth and metal uptake of heavy metal accumulating willows. Plant and Soil, 304(1): 35-44.
60. Kurokura, T., Hiraide, S., Shimamura, Y., Yamane, K., 2017. PGPR improves yield of strawberry species under less-fertilized conditions. Environmental Control in Biology, 55(3): 121-128.
61. Küpper, H., Kochian, L.V., 2010. Transcriptional regulation of metal transport genes and mineral nutrition during acclimatization to cadmium and zinc in the Cd/Zn hyperaccumulator, Thlaspi caerulescens (Ganges population). New Phytologist, 185(1): 114-129.
62. Küpper, H., Küpper, F., Spiller, M., 1996. Environmental relevance of heavy metal-substituted chlorophylls using the example of water plants. Journal of Experimental Botany, 47(2): 259-266.
63. Larsen, P.B., Degenhardt, J., Tai, C.Y., Stenzler, L.M., Howell, S.H., Kochian, L.V., 1998. Aluminum-resistant Arabidopsis mutants that exhibit altered patterns of aluminum accumulation and organic acid release from roots. Plant Physiology, 117(1): 9-17.
64. Lin, L., Zhou, T., Tang, F., Hu, H., Fu, Q., 2013. Effects of phosphorus on growth and uptake of heavy metals in strawberry grown in the soil contaminated by Cd and Pb. Journal of Agro-Environment Science, 32(3): 503-507.
65. Liu, D., Jiang, W., Gao, X., 2003. Effects of cadmium on root growth, cell division and nucleoli in root tip cells of garlic. Biologia Plantarum, 47(1): 79-83.
66. Liu, W., Wang, Q., Wang, B., Hou, J., Luo, Y., Tang, C., Franks, A.E., 2015. Plant growth-promoting rhizobacteria enhance the growth and Cd uptake of Sedum plumbizincicola in a Cd-contaminated soil. Journal of Soils and Sediments, 15(5): 1191-1199.
67. Loi, N.N., Sanzharova, N.I., Shchagina, N.I., Mironova, M.P., 2018. The effect of cadmium toxicity on the development of lettuce plants on contaminated sod-podzolic soil. Russian Agricultural Sciences, 44(1): 49-52.
68. Lux, A., Vaculík, M., Martinka, M., Lišková, D., Kulkarni, M.G., Stirk, W.A., van Staden, J., 2011. Cadmium induces hypodermal periderm formation in the roots of the monocotyledonous medicinal plant Merwilla plumbea. Annals of Botany, 107(2): 285-292.
69. MacFarlane, G.R., Burchett, M.D., 2001. Photosynthetic pigments and peroxidase activity as indicators of heavy metal stress in the Grey mangrove, Avicennia marina (Forsk.) Vierh. Marine Pollution Bulletin, 42(3): 233-240.
70. Mahdavi, A., Khermandar, K., 2018. Potential of lead and cadmium accumulation in Washingtonia filifera. Iranian Journal of Science and Technology, Transactions A: Science, 42(1): 273-282.
71. Malan, H.L., Farrant, J.M., 1998. Effects of the metal pollutants cadmium and nickel on soybean seed development. Seed Science Research, 8(4): 445-453.
72. Mendoza‐Cózatl, D.G., Butko, E., Springer, F., Torpey, J.W., Komives, E.A., Kehr, J., Schroeder, J.I., 2008. Identification of high levels of phytochelatins, glutathione and cadmium in the phloem sap of Brassica napus. A role for thiol‐peptides in the long‐distance transport of cadmium and the effect of cadmium on iron translocation. The Plant Journal, 54(2): 249-259.
73. Moral, R., Gomez, I., Pedreno, J.N., Mataix, J., 1994. Effects of cadmium on nutrient distribution, yield, and growth of tomato grown in soilless culture. Journal of Plant Nutrition, 17(6): 953-962.
74. Moral, R., Pedreño, J.N., Gómez, I., Palacios, G., Mataix, J., 1996. Tomato fruit yield and quality are affected by organic and inorganic fertilization and cadmium pollution. Journal of Plant Nutrition, 19(12): 1493-1498.
75. Moreno, J.L., Hernández, T., Garcia, C., 1999. Effects of a cadmium-contaminated sewage sludge compost on dynamics of organic matter and microbial activity in an arid soil. Biology and Fertility of Soils, 28(3): 230-237.
76. Moustaine, M., Elkahkahi, R., Benbouazza, A., Benkirane, R., Achbani, E.H., 2017. Effect of plant growth promoting rhizobacterial (PGPR) inoculation on growth in tomato (Solanum lycopersicum L.) and characterization for direct PGP abilities in Morocco. International Journal of Environment, Agriculture and Biotechnology, 2(2): 238708.
77. Nawaz, S., Bano, A., 2020. Effects of PGPR (Pseudomonas sp.) and Ag-nanoparticles on enzymatic activity and physiology of cucumber. Recent Patents on Food, Nutrition & Agriculture, 11(2): 124-136.
78. Nies, D.H., 1999. Microbial heavy-metal resistance. Applied Microbiology and Biotechnology, 51(6): 730-750. O'connell, P.F., 1992. Sustainable agriculture-a valid alternative. Outlook on Agriculture, 21(1): 5-12.
79. Pal, A.K., Chakraborty, A., Sengupta, C., 2018. Differential effects of plant growth promoting rhizobacteria on chilli (Capsicum annuum L.) seedling under cadmium and lead stress. Plant Science Today, 5(4): 182-190.
80. Pan, F., Meng, Q., Luo, S., Shen, J., Chen, B., Khan, K.Y., Japenga, J., Ma, X., Yang, X., Feng, Y., 2017. Enhanced Cd extraction of oilseed rape (Brassica napus) by plant growth-promoting bacteria isolated from Cd hyperaccumulator Sedum alfredii Hance. International Journal of Phytoremediation, 19(3): 281-289.
81. Perfus‐Barbeoch, L., Leonhardt, N., Vavasseur, A., Forestier, C., 2002. Heavy metal toxicity: cadmium permeates through calcium channels and disturbs the plant water status. The Plant Journal, 32(4): 539-548.
82. Pırlak, L., Köse, M., 2009. Effects of plant growth promoting rhizobacteria on yield and some fruit properties of strawberry. Journal of Plant Nutrition, 32(7): 1173-1184.
83. Pishchik, V.N., Vorobyev, N.I., Chernyaeva, I.I., Timofeeva, S.V., Kozhemyakov, A.P., Alexeev, Y.V., Lukin, S.M., 2002. Experimental and mathematical simulation of plant growth promoting rhizobacteria and plant interaction under cadmium stress. Plant and Soil, 243(2): 173-186.
84. Prapagdee, B., Chanprasert, M., Mongkolsuk, S., 2013. Bioaugmentation with cadmium-resistant plant growth-promoting rhizobacteria to assist cadmium phytoextraction by Helianthus annuus. Chemosphere, 92(6): 659-666.
85. Prapagdee, B., Chumphonwong, N., Khonsue, N., Mongkolsuk, S., 2012. Influence of cadmium resistant bacteria on promoting plant root elongation and increasing cadmium mobilization in contaminated soil. Fresenius Environmental Bulletin, 21(5): 1186-1191.
86. Punz, W.F., Sieghardt, H., 1993. The response of roots of herbaceous plant species to heavy metals. Environmental and Experimental Botany, 33(1): 85-98.
87. Raj, S.N., Deepak, S.A., Basavaraju, P., Shetty, H.S., Reddy, M.S., Kloepper, J.W., 2003. Comparative performance of formulations of plant growth promoting rhizobacteria in growth promotion and suppression of downy mildew in pearl millet. Crop Protection, 22(4): 579-588.
88. Rajkumar, M., Ae, N., Freitas, H., 2009. Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere, 77(2): 153-160.
89. Rajkumar, M., Freitas, H., 2008. Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere, 71(5): 834-842.
90. Rehman, F., Khan, F.A., Varshney, D., Naushin, F., Rastogi, J., 2011. Effect of cadmium on the growth of tomato. Biology and Medicine, 3(2): 187-190.
91. Rojjanateeranaj, P., Sangthong, C., Prapagdee, B., 2017. Enhanced cadmium phytoremediation of Glycine max L. through bioaugmentation of cadmium-resistant bacteria assisted by biostimulation. Chemosphere, 185: 764-771.
92. Rostamikia, Y., Tabari Kouchaksaraei, M., Asgharzadeh, A., Rahmani, A., 2016. The effect of Plant Growth-Promoting Rhizobacteria on growth and physiological characteristics of Corylus avellana seedlings. Ecopersia, 4(3): 1471-1479.
93. Ryan, R.P., Monchy, S., Cardinale, M., Taghavi, S., Crossman, L., Avison, M.B., Berg, G., van der Lelie, D., Dow, J.M., 2009. The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nature Reviews Microbiology, 7(7): 514-525.
94. Seema, K., Mehta, K., Singh, N., 2018. Studies on the effect of plant growth promoting rhizobacteria (PGPR) on growth, physiological parameters, yield and fruit quality of strawberry cv. chandler. Journal Pharmacognosy Phytochemistry, 7(2): 383-387.
95. Sen, S., Chandrasekhar, C.N., 2014. Effect of PGPR on growth promotion of rice (Oryza sativa L.) under salt stress. Asian Journal of Plant Science & Research, 4(5): 62-67.
96. Shah, F.R., Ahmad, N., Masood, K.R., Zahid, D.M., Zubair, M., 2011. Response of Eucalyptus camaldulensis to exogenous application of cadmium and chromium. Pakistan Journal of Botany, 43(1): 181-189.
97. Sharafzadeh, S., 2012. Effects of PGPR on growth and nutrients uptake of tomato. International Journal of Advances in Engineering & Technology, 2(1): 27-31.
98. Shen, M., Kang, Y.J., Wang, H.L., Zhang, X.S., Zhao, Q.X., 2012. Effect of plant growth-promoting rhizobacteria (PGPRs) on plant growth, yield, and quality of tomato (Lycopersicon esculentum Mill.) under simulated seawater irrigation. The Journal of General and Applied Microbiology, 58(4): 253-262.
99. Sheng, X.F., Xia, J.J., 2006. Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere, 64(6): 1036-1042.
100. Sheoran, I.S., Aggarwal, N., Singh, R., 1990. Effects of cadmium and nickel on in vivo carbon dioxide exchange rate of pigeon pea (Cajanus cajan L.). Plant and Soil, 129(2): 243-249.
101. Souguir, D., Ferjani, E., Ledoigt, G., Goupil, P., 2011. Sequential effects of cadmium on genotoxicity and lipoperoxidation in Vicia faba roots. Ecotoxicology, 20(2): 329-336.
102. Şahin, M., Pırlak, L., Eşitken, A., Deveci, F.N., 2017. The effects of cadmium doses on plant characteristics of CAB-6P (Prunus cerasus L.). In: III. International Conference on Environmental Science and Technology, Ç. Özer (Ed.), Oct. 19-23, Yıldız Technical University and National University of Public Service, Budapest, Hungary, pp. 7-14.
103. Tahiri, A.I., Meddich, A., Raklami, A., Alahmad, A., Bechtaoui, N., Anli, M., Göttfert, M., Heulin, T., Achouak, W., Oufdou, K., 2022. Assessing the potential role of compost, PGPR, and AMF in improving tomato plant growth, yield, fruit quality, and water stress tolerance. Journal of Soil Science and Plant Nutrition, 22(1): 743-764.
104. Tanwir, K., Javed, M.T., Abbas, S., Shahid, M., Akram, M.S., Chaudhary, H.J., Iqbal, M., 2021. Serratia sp. CP-13 alleviates Cd toxicity by morpho-physio-biochemical improvements, antioxidative potential and diminished Cd uptake in Zea mays L. cultivars differing in Cd tolerance. Ecotoxicology and Environmental Safety, 208: 111584.
105. Treder, W., Cieśliński, G., 2005. Effect of silicon application on cadmium uptake and distribution in strawberry plants grown on contaminated soils. Journal of Plant Nutrition, 28(6): 917-929.
106. Tripathi, D.K., Singh, V.P., Kumar, D., Chauhan, D.K., 2012. Rice seedlings under cadmium stress: effect of silicon on growth, cadmium uptake, oxidative stress, antioxidant capacity and root and leaf structures. Chemistry and Ecology, 28(3): 281-291.
107. Vassilev, A., Perez-Sanz, A., Semane, B., Carleer, R., Vangronsveld, J., 2005. Cadmium accumulation and tolerance of two Salix genotypes hydroponically grown in presence of cadmium. Journal of Plant Nutrition, 28(12): 2159-2177.
108. Vijendra, P.D., Huchappa, K.M., Lingappa, R., Basappa, G., Jayanna, S.G., Kumar, V., 2016. Physiological and biochemical changes in moth bean (Vigna aconitifolia L.) under cadmium stress. Journal of Botany, 2016: 1-13.
109. Wang, G., Wang, L., Ma, F., You, Y., Wang, Y., Yang, D., 2020. Integration of earthworms and arbuscular mycorrhizal fungi into phytoremediation of cadmium-contaminated soil by Solanum nigrum L. Journal of Hazardous Materials, 389: 121873.
110. Wang, M., Zou, J., Duan, X., Jiang, W., Liu, D., 2007. Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). Bioresource Technology, 98(1): 82-88.
111. Wu, S., Wang, Y., Zhang, J., Gong, X., Zhang, Z., Sun, J., Chen, X., Wang, Y., 2021. Exogenous melatonin improves physiological characteristics and promotes growth of strawberry seedlings under cadmium stress. Horticultural Plant Journal, 7(1): 13-22.
112. Yaron, B., Calvet, R., Prost, R., Prost, R., 1996. Soil Pollution: Processes and Dynamics. Springer-Verlag, Berlin. Yoshihara, T., Hodoshima, H., Miyano, Y., Shoji, K., Shimada, H., Goto, F., 2006. Cadmium inducible Fe deficiency responses observed from macro and molecular views in tobacco plants. Plant Cell Reports, 25(4): 365-373.
113. Zahir, Z.A., Arshad, M., Frankenberger, W.T., 2004. Plant growth promoting rhizobacteria: applications and perspectives in agriculture. In: D.L. Sparks (Ed.), Advances in Agronomy, Volume 81, 1st Edn., Elsevier Science, New York, pp. 98-169.
114. Zhang, X., Chen, B., Ohtomo, R., 2015. Mycorrhizal effects on growth, P uptake and Cd tolerance of the host plant vary among different AM fungal species. Soil Science and Plant Nutrition, 61(2): 359-368.
115. Zhang, Z., Gao, S., Shan, C., 2020. Effects of sodium selenite on the antioxidant capacity and the fruit yield and quality of strawberry under cadmium stress. Scientia Horticulturae, 260: 108876.