Role of PGPR for Alleviating Aluminum Toxicity in Acidic Soil

  • Jintu Dutta
  • Utpal Bora
Part of the Microorganisms for Sustainability book series (MICRO, volume 12)


The soil pH is a very crucial determining factor for the solubility of different metal ions, nutrient availability, and various physical properties. Among different factors, aluminum (Al) toxicity in acidic soil is considered as a limiting factor for plant growth. When soil pH falls to lower than 5, Al is solubilized into different ionic forms and causes toxicity to the plants. In acidic soils, Al limits the growth of roots either by restraining cell division, cell elongation, or both, causing stunted root growth. Moreover, Al ions also form complexes with phosphoric acid which makes phosphorus (P) unavailable to plants. In recent years, considerable efforts have been made to addressing how bacteria respond to the changing environment since the terrestrial ecosystems are increasingly under the pressure of human activities. The agricultural soil is a great example where most human interference occurred. Due to the extensive use of chemicals and pollutants, the agricultural soils gradually become acidic and less fertile. In this chapter, we are trying to include the Al chemistry in acidic soils and its toxic effects on plants at higher concentration. The chapter also includes the role of plant growth-promoting rhizobacteria (PGPR) to mitigate the Al toxicity in acidic soil.


Al toxicity Acidic soil PGPR 


  1. Adesemoye AO, Torbert HA, Kloepper JW (2009) Plant growth-promoting rhizobacteria allow reduced application rates of chemical fertilizers. Microb Ecol 58:921–929CrossRefGoogle Scholar
  2. Ahn SJ, Matsumoto H (2006) The role of the plasma membrane in the response of plant roots to aluminum toxicity. Plant Signal Behav 1:37–45PubMedPubMedCentralCrossRefGoogle Scholar
  3. Ahn SJ, Sivaguru M, Osawa H, Chung GC, Matsumoto H (2001) Aluminum inhibits the H+-ATPase activity by permanently altering the plasma membrane surface potentials in squash roots. Plant Physiol 126:1381–1390PubMedPubMedCentralCrossRefGoogle Scholar
  4. Ahn SJ, Sivaguru M, Chung GC, Rengel Z, Matsumoto H (2002) Aluminum-induced growth inhibition is associated with impaired efflux and influx of H+ across the plasma membrane in root apices of squash (Cucurbita pepo). J Exp Bot 53:1959–1966PubMedCrossRefGoogle Scholar
  5. Akeson MA, Munns DN (1989) Lipid bilayer permeation by neutral aluminum citrate and by three a-hydroxy carboxylic acids. Biochim Biophys Acta 984:200–206PubMedCrossRefGoogle Scholar
  6. Anwar S, Ali B, Sajid I (2016) Screening of rhizospheric actinomycetes for various in-vitro and in-vivo plant growth promoting (PGP) traits and for proactive compounds. Front Microbiol 7:1334PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bal HB, Das S, Dangar TK, Adhya TK (2013) ACC deaminase and IAA roducing growth promoting bacteria from the rhizosphere soil of tropical rice plants. J Basic Microbiol 53:972–984CrossRefPubMedGoogle Scholar
  8. Barber SA, Walker JM, Vasey EH (1962) Principles of ion movement through the soil to the plant root. Trans joint meeting Commission IV & V Internat. Soil Sci:121–124Google Scholar
  9. Bates TR, Lynch JP (1996) Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ 19:529–538CrossRefGoogle Scholar
  10. Bharathi R, Vivekananthan R, Harish S, Ramanathan A, Samiyappan R (2004) Rhizobacteria-based bio-formulations for the management of fruit rot infection in chilies. Crop Prot 23:835–843CrossRefGoogle Scholar
  11. Bhattacharyya PN, Jha DK (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350PubMedCrossRefGoogle Scholar
  12. Biari A, Gholami A, Rahmani HA (2008) Growth promotion and enhanced nutrient uptake of maize (Zea mays L.) by application of plant growth promoting rhizobacteria in the arid region of Iran. J Biol Sci 8:1015–1020CrossRefGoogle Scholar
  13. Blancaflor EB, Jones DL, Gilroy S (1998) Alterations in the cytoskeleton accompany aluminum-induced growth inhibition and morphological changes in primary roots of maize. Plant Physiol 118:159–172PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bojórquez-Quintal E, Escalante-Magaña C, Echevarría-Machado I, Martínez-Estévez M (2017) Aluminum, a friend or foe of higher plants in acid soils. Front Plant Sci 8:1767. Scholar
  15. Budikova S, Durcekova K (2004) Aluminum accumulation in roots of Al-sensitive barley cultivar changes root cell structure and induces callose synthesis. Biologia 59:215–220Google Scholar
  16. Burr TJ, Caesar A (1984) Beneficial plant bacteria. CRC Crit Rev Plant Sci 2:1–20CrossRefGoogle Scholar
  17. Çakmakçi R, Dönmez F, Aydın A, Sahin F (2006) Growth promotion of plants by plant growth-promoting rhizobacteria under greenhouse and two different field soil conditions. Soil Biol Biochem 38:1482–1487CrossRefGoogle Scholar
  18. Chen RF, Zhang FL, Zhang QM, Sun QB, Dong XY, Shen RF (2012) Aluminium-phosphorus interactions in plants growing on acid soils: does phosphorus always alleviate aluminium toxicity? J Sci Food Agric 92:995–1000PubMedCrossRefGoogle Scholar
  19. Cruz FJR, de Almeida HJ, dos Santos DMM (2014) Growth, nutritional status and nitrogen metabolism in Vigna unguiculata (L.) Walp is affected by aluminum. Aust J Crop Sci 8:1132Google Scholar
  20. Dai H, Zhao J, Ahmed IM, Cao F, Chen ZH, Zhang G, Wu F (2014) Differences in physiological features associated with aluminum tolerance in Tibetan wild and cultivated barleys. Plant Physiol Biochem 75:36–44PubMedCrossRefGoogle Scholar
  21. de Freitas JR (2000) Yield and N assimilation of winter wheat (Triticum aestivum L., var. Norstar) inoculated with rhizobacteria. Pedobiologia 44:97–104CrossRefGoogle Scholar
  22. de Vasconcellos RLF, Silva MCP, Ribeiro CMR, Cardoso EJBN (2010) Isolation and screening for plant growth-promoting (PGP) actinobacteria from Araucaria angustifolia rhizosphere soil. Sci Agric 67:743–746CrossRefGoogle Scholar
  23. Delfim J, Schoebitz M, Paulino L, Hirzel J, Zaga E (2018) Phosphorus availability in wheat, in volcanic soils inoculated with phosphate-solubilizing Bacillus thuringiensis. Sustainability 10:144. Scholar
  24. Delhaize E, Gruber BD, Ryan PR (2007) The roles of organic anion permeases in aluminum resistance and mineral nutrition. FEBS Lett 581:2255–2262CrossRefGoogle Scholar
  25. Dimkpa C, Weinand T, Asch F (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694CrossRefGoogle Scholar
  26. Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149CrossRefGoogle Scholar
  27. Doncheva S, Amenós M, Poschenrieder C, Barceló J (2005) Root cell patterning: a primary target for aluminum toxicity in maize. J Exp Bot 56:1213–1220PubMedCrossRefGoogle Scholar
  28. Dutta J, Thakur D (2017) Evaluation of multifarious plant growth promoting traits, antagonistic potential and phylogenetic affiliation of rhizobacteria associated with commercial tea plants grown in Darjeeling, India. PlosOne. Scholar
  29. Dutta J, Handique PJ, Thakur D (2015) Assessment of culturable tea rhizobacteria isolated from tea estates of Assam, India for growth promotion in commercial tea cultivars. Front Microbiol 6:1252PubMedPubMedCentralGoogle Scholar
  30. Eekhout T, Larsen P, De Veylder L (2017) Modification of DNA checkpoints to confer aluminum tolerance. Trends Plant Sci 22:102–105PubMedCrossRefGoogle Scholar
  31. Elliott LF, Lynch JM (1995) The international workshop on the establishment of microbial inocula in soils: cooperative research project on biological resource management of the organization for economic cooperation and development (OECD). Am J Altern Agric 10:50–73CrossRefGoogle Scholar
  32. Eticha D, Staβ A, Horst WJ (2005a) Cell-wall pectin and its degree of methylation in the maize root-apex: significance for genotypic differences in aluminum resistance. Plant Cell Environ 28:1410–1420CrossRefGoogle Scholar
  33. Eticha D, Thĕ C, Welcker C, Narro L, Staß A, Horst WJ (2005b) Aluminium-induced callose formation in root apices: inheritance and selection trait for adaptation of tropical maize to acid soils. Field Crops Res 93:252–263CrossRefGoogle Scholar
  34. Farh ME, Kim YJ, Sukweenadhi J, Singh P, Yang DC (2017) Aluminium resistant, plant growth promoting bacteria induce overexpression of Aluminium stress-related genes in Arabidopsis thaliana and increase the ginseng tolerance against Aluminium stress. Microbiol Res 200:45–52PubMedCrossRefGoogle Scholar
  35. Fierer N, Jackson RB (2006) The diversity and biogeography of soil bacterial communities. PNAS 103:626–631PubMedCrossRefGoogle Scholar
  36. Fierer N, Leffb JW, Adamsc BJ, Nielsend UN, Batesb ST, Lauberb CL et al (2012) Cross-biome metagenomic analyses of soil microbial communities and their functional attributes. PNAS 109:21390–21395PubMedCrossRefGoogle Scholar
  37. FitzPatrick EA (1986) An introduction to soil science. Longman Scientific & Technical, pp 2–55Google Scholar
  38. Foehse D, Jungk A (1983) Influence of phosphate and nitrate supply on root hair formation of rape, spinach, and tomato plants. Plant Soil 74:359–368CrossRefGoogle Scholar
  39. Fox RL, Kamprath EJ (1970) Phosphate sorption isotherms for evaluating the phosphate requirements of soils. Soil Sci Sot Am Proc 34:902–907CrossRefGoogle Scholar
  40. Foy CD (1984) Physiological effects of hydrogen, Al and manganese toxicities in acid soil. In: acidity S, liming Adams F (eds) American society of agronomy. American Society of Agronomy, Madison, pp 57–97Google Scholar
  41. Franco-Correa M, Quintana A, Duque C, Suarez C, Rodrıguez MX, Barea JM (2010) Evaluation of actinomycete strains for key traits related to plant growth promotion and mycorrhiza helping activities. Appl Soil Ecol 45:209–217CrossRefGoogle Scholar
  42. Franke R, Humphreys JM, Hemm MR, Denault JW, Ruegger MO, Cusumano JC, Chapple C (2002) The Arabidopsis, R.E.F. and 8 genes encodes the 3-hydroxylase of phenylpropanoid metabolism. Plant J 30:33–45PubMedCrossRefGoogle Scholar
  43. Frantzios G, Galatis B, Apostolakos P (2001) Aluminium effects on microtubule organization in dividing root-tip cells of Triticum turgidum II. Cytokinetic cells. J Plant Res 114:157–170CrossRefGoogle Scholar
  44. Frey SD, Knorr M, Parrent JL, Simpson RT (2004) Chronic nitrogen enrichment affects the structure and function of the soil microbial community in temperate hardwood and pine forests. For Ecol Manag 196:159–171CrossRefGoogle Scholar
  45. Gassmann W, Schroeder JI (1994) A mechanism for aluminum-sensitive low-affinity K+ uptake and membrane potential control. Plant Physiol 105:1399–1408PubMedPubMedCentralCrossRefGoogle Scholar
  46. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117CrossRefGoogle Scholar
  47. Glick BR, Bashan Y (1997) Genetic manipulation of plant growth promoting bacteria to enhance biocontrol of fungal phytopathogens. Biotechnol Adv 15:353–378PubMedCrossRefGoogle Scholar
  48. Gomes LH, Duarte KMR, Andrino FG, Cesar F, Tavares A (2000) A simple method for DNA isolation from Xanthomonas spp. Sci Agric 57:553–555CrossRefGoogle Scholar
  49. Gray EJ, Smith DL (2005) Intracellular and extracellular PGPR: commonalities and distinctions in the plant-bacterium signaling processes. Soil Biol Biochem 37:395–412CrossRefGoogle Scholar
  50. Guo JH, Qi HY, Guo YH, Ge HL, Gong LY, Zhang LX et al (2004a) Biocontrol of tomato wilt by plant growth-promoting rhizobacteria. Biol Control 29:66–72CrossRefGoogle Scholar
  51. Guo T, Zhang G, Zhou M, Wu F, Chen J (2004b) Effects of aluminum and cadmium toxicity on growth and antioxidant enzyme activities of two barley genotypes with different Al resistance. Plant Soil 258:241–248CrossRefGoogle Scholar
  52. Guo TR, Yao PC, Zhang ZD, Wang JJ, Mei WANG (2012) Involvement of antioxidative defense system in rice seedlings exposed to aluminum toxicity and phosphorus deficiency. Rice Sci 19:207–212CrossRefGoogle Scholar
  53. Gupta N, Gaurav SG, Kumar A (2013) Molecular basis of aluminum toxicity in plants: a review. Am J Plant Sci 4:21–37CrossRefGoogle Scholar
  54. Halder AK, Misra AK, Chakrabarty PK (1991) Solubilization of inorganic phosphates by Bradyrhizobium. Indian J Exp Biol 29:28–31Google Scholar
  55. Hartman WH, Richardson CJ, Vilgalys R, Bruland GL (2008) Environmental and anthropogenic control of bacterial communities in wetland soils. PNAS 105:17842–17847PubMedCrossRefGoogle Scholar
  56. Hayat R, Ali S, Amara U, Khalid R, Ahmed I (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598CrossRefGoogle Scholar
  57. Horst WJ, Puschel AK, Schmohl N (1997) Induction of callose formation is a sensitive marker for genotypic aluminium sensitivity in maize. Plant Soil 192:23–30CrossRefGoogle Scholar
  58. Horst WJ, Schmohl N, Kollmeier M, Baluska F, Sivaguru M (1999) Does aluminum affect root growth of maize through interaction with the cell wall plasma membrane-cytoskeleton continuum? Plant Soil 215:163–174CrossRefGoogle Scholar
  59. Hossain MA, Hossain AZ, Kihara T, Koyama H, Hara T (2005) Aluminum-induced lipid peroxidation and lignin deposition are associated with an increase in H2O2 generation in wheat seedlings. Soil Sci Plant Nutr 51:223–230CrossRefGoogle Scholar
  60. Huang JW, Shaff JE, Grunes DL, Kochian LV (1992) Aluminum effects on calcium fluxes at the root apex of aluminum-tolerant and aluminium-sensitive wheat cultivars. Plant Physiol 98:230–237PubMedPubMedCentralCrossRefGoogle Scholar
  61. Ishikawa S, Wagatsuma T (1998) Plasma membrane permeability of root-tip cells following temporary exposure to Al ions is a rapid measure of Al tolerance among plant species. Plant Cell Physiol 39:516–525CrossRefGoogle Scholar
  62. Ishikawa S, Wagatsuma T, Takano T, Tawaraya K, Oomata K (2001) The plasma membrane intactness of root tip cells is a primary factor for Al-tolerance in cultivars of five species. Soil Sci Plant Nutr 47:489–501CrossRefGoogle Scholar
  63. Jenkins SN, Waite IS, Blackburn A, Husband R, Rushton SP, Manning DC et al (2009) Actinobacterial community dynamics in long-term managed grasslands. Antonie van Leeuwenhoek 95:319–334PubMedCrossRefGoogle Scholar
  64. Jetiyanon K, Kloepper JW (2002) Mixtures of plant growth-promoting rhizobacteria for induction of systemic resistance against multiple plant diseases. Biol Control 24:285–291CrossRefGoogle Scholar
  65. Jones DL, Gilroy S, Larsen PB, Howell SH, Kochian LV (1998) Effect of aluminum on cytoplasmic Ca2+ homeostasis in root hairs of Arabidopsis thaliana (L.). Planta 206:378–387PubMedCrossRefGoogle Scholar
  66. Kidd PS, Proctor J (2000) Effects of aluminium on the growth and mineral composition of Betula pendula Roth. J Exp Bot 51:1057–1066PubMedCrossRefGoogle Scholar
  67. Kiegle E, Gilliham M, Haseloff J, Tester M (2000) Hyperpolarisation activated calcium currents found only in cells from the elongation zone of Arabidopsis thaliana roots. Plant J 21:225–229PubMedCrossRefGoogle Scholar
  68. Kloepper JW, Schroth MN (1978) Plant growth promoting rhizobacteria on radishes. In: Proceeding of the 4th international conference on plant pathogenic bacteria, vol 2. Plant Pathology and Phytobacteriology Station, INRA, Angers, pp 879–882Google Scholar
  69. Kochian LV, Hoekenga AO, Piñeros MA (2004) How do plants tolerate acid soils? Mechanisms of aluminum tolerance and phosphorous efficiency. Annu Rev Plant Physiol Plant Mol Biol 55:459–493CrossRefGoogle Scholar
  70. Kochian LV, Piñeros MA, Hoekenga OA (2005) The physiology, genetics and molecular biology of plant aluminum resistance and toxicity. Plant Soil 274:175–195CrossRefGoogle Scholar
  71. Krstic D, Djalovic I, Nikezic D, Bjelic D (2012) Aluminium in acid soils: chemistry, toxicity and impact on maize plants. In: Anna A (ed) Food production – approaches, challenges and tasks. InTech, pp 231–242Google Scholar
  72. Kuo MC, Kao CH (2003) Aluminum effects on lipid peroxidation and antioxidative enzyme activities in rice leaves. Biol Plant 46:149–152CrossRefGoogle Scholar
  73. Lauber CL, Strickland MS, Bradford MA, Fierer N (2008) The influence of soil properties on the structure of bacterial and fungal communities across land-use types. Soil Biol Biochem 40:2407–2415CrossRefGoogle Scholar
  74. Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community composition at the continental scale. Appl Environ Microbiol 75:5111–5120PubMedPubMedCentralCrossRefGoogle Scholar
  75. Lazof DB, Goldsmith JG, Rufty TW, Linton RW (1994) Rapid uptake of aluminum into cells of intact soybean root tip: a microanalytical study using secondary ion mass spectrometry. Plant Physiol 106:1107–1114PubMedPubMedCentralCrossRefGoogle Scholar
  76. Lemire J, Mailloux R, Auger C, Whalen D, Appanna VD (2010) Pseudomonas fluorescens orchestrates a fine metabolic-balancing act to counter aluminium toxicity. Environ Microbiol 12:1384–1390PubMedGoogle Scholar
  77. Li QQ, Dong BD, Qiao YZ, Liu MY, Zhang JW (2010) Root growth, available soil water, and water-use efficiency of winter wheat under different irrigation regimes applied at different growth stages in North China. Agric Water Manag 97:1676–1682CrossRefGoogle Scholar
  78. Li Y, Yang G, X Luo LT (2008) Aluminium sensitivity and tolerance in model and elite wheat varieties. Cereal Res Commun 36:257–267CrossRefGoogle Scholar
  79. Lindberg S, Szynkier K, Greger M (1991) Aluminium effects on transmembrane potential in cells of fibrous roots of sugar beet. Physiol Plant 83:54–62CrossRefGoogle Scholar
  80. Lucas García JA, Probanza A, Ramos B, Barriuso J, Gutierrez Mañero FJ (2004) Effects of inoculation with plant growth promoting rhizobacteria (PGPR) and Sinorhizobium fredii on biological nitrogen fixation, nodulation and growth of Glycine max cv. Osumi. Plant Soil 267:143–153CrossRefGoogle Scholar
  81. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–555CrossRefPubMedPubMedCentralGoogle Scholar
  82. Ma Z, Walk TC, Marcus A, Lynch JP (2001) Morphological synergism in root hair length, density, initiation and geometry for phosphorus acquisition in Arabidopsis thaliana: a modeling approach. Plant Soil 236:221–235CrossRefGoogle Scholar
  83. Malekzadeh P, Mehr RS, Hatamnia AA (2015) Effects of aluminum toxicity on maize (Zea mays L.) seedlings. Iran J Plant Physiol 5:1289–1296Google Scholar
  84. Mandal N (1997) Nutritive values of tree leaves of some tropical species for goats. Small Rumin Res 24:95–105CrossRefGoogle Scholar
  85. Marienfeld S, Schmohl N, Klein M, Schröder WH, Kuhn AJ, Horst WJ (2000) Localisation of aluminium in root tips of Zea mays and Vicia faba. J Plant Physiol 156:666–671CrossRefGoogle Scholar
  86. Marschner H (1995) Mineral nutrition of higher plants. Academic, LondonGoogle Scholar
  87. Massot N, Llugany M, Poschenrieder C, Barceló J (1999) Callose production as indicator of aluminum toxicity in bean cultivars. J Plant Nutr 22:1–10CrossRefGoogle Scholar
  88. Matsumoto H (1988) Inhibition of proton transport activity of microsomal membrane vesicles of barley roots by aluminum. Soil Sci Plant Nutr 34:499–506CrossRefGoogle Scholar
  89. Matsumoto H, Morimura S, Takahashi E (1977a) Less involvement of pectin in the precipitation of aluminum in pea root. Plant Cell Physiol 18:325–335CrossRefGoogle Scholar
  90. Matsumoto H, Morimura S, Takahashi E (1977b) Binding of aluminium to DNA of DNP (deoxyribonucleoprotein) in pea root nuclei. Plant Cell Physiol 18:987–993Google Scholar
  91. Mena-Violante HG, Olalde-Portugal V (2007) Alteration of tomato fruit quality by root inoculation with plant growth-promoting rhizobacteria (PGPR): Bacillus subtilis BEB- 13bs. Sci Hortic 113:103–106CrossRefGoogle Scholar
  92. Merzaeva OV, Shirokikh IG (2006) Colonization of plant rhizosphere by actinomycetes of different genera. Microbiology 75:226–230CrossRefGoogle Scholar
  93. Miyasaka SC, Kochian LV, Shaff JE, Foy CD (1989) Mechanism of aluminium tolerance in wheat: an investigation of genotypic differences in rhizosphere pH, K+, and H+ transport, and root cell membrane potentials. Plant Physiol 91:1188–1196PubMedPubMedCentralCrossRefGoogle Scholar
  94. Mora ML, Demaneta R, Acuñaa JJ, Viscardia S, Jorqueraa M, Rengelb Z, Durán P (2017) Aluminum-tolerant bacteria improve the plant growth and phosphorus content in ryegrass grown in a volcanic soil amended with cattle dung manure. Appl Soil Ecol 115:19–26CrossRefGoogle Scholar
  95. Naderifar M, Daneshian J (2012) Effect of different nitrogen and biofertilizers effect on growth and yield of Brassica napus L. Int J Agric Crop Sci 8:478–482Google Scholar
  96. Nichol BE, Oliveira LA, Glass ADM, Siddiqi MY (1993) The effects of aluminum on the influx of calcium, potassium, ammonium, nitrate, and phosphate in an aluminum sensitive cultivar of barley (Hordeum vulgare L.). Plant Physiol 101:1263–1266PubMedPubMedCentralCrossRefGoogle Scholar
  97. Nilsson LO, Bååth E, Falkengren-Grerup U, Wallander H (2007) Growth of ectomycorrhizal mycelia and composition of soil microbial communities in oak forest soils along a nitrogen deposition gradient. Oecologia 153:375–384PubMedCrossRefGoogle Scholar
  98. Ofei-Manu P, Ishikawa S, Wagatsuma T, Tawaraya K (2001) The plasma membrane strength of root tip cells and root phenolic compounds are correlated with Al tolerance in several common woody plants. Soil Sci Plant Nutr 47:359–375CrossRefGoogle Scholar
  99. Panda SK, Yamamoto Y, Kondo H, Matsumoto H (2008) Mitochondrial alterations related to programmed cell death in tobacco cells under aluminium stress. Compt Rend Biol 331:597–610CrossRefGoogle Scholar
  100. Panda SK, Baluska F, Matsumoto H (2009) Aluminum stress signaling in plants. Plant Signal Behav 4:592–597PubMedPubMedCentralCrossRefGoogle Scholar
  101. Panda SK, Sahoo L, Katsuhara M, Matsumoto H (2013) Overexpression of alternative oxidase gene confers aluminum tolerance by altering the respiratory capacity and the response to oxidative stress in tobacco cells. Mol Biotechnol 54:551–563PubMedCrossRefGoogle Scholar
  102. Panhwar QA, Naher UA, Jusop S, Othman R, Latif MA et al (2014) Biochemical and molecular characterization of potential phosphate-solubilizing bacteria in acid sulfate soils and their beneficial effects on rice growth. PLoS One 9(10):e97241. Scholar
  103. Papernik LA, Kochian LV (1997) Possible involvement of Al-induced electrical signals in Al tolerance in wheat. Plant Physiol 115:657–667PubMedPubMedCentralCrossRefGoogle Scholar
  104. Parker DR, Bertsch EM (1992) Formation of the Al13 tridecameric polycation under diverse synthesis conditions. Environ Sci Technol 26:914–921CrossRefGoogle Scholar
  105. Peixoto PHP, Cambria J, Sant’Anna R, Mosquim PR, Moreira MA (1999) Aluminum effects on lipid peroxidation and on the activities of enzymes of oxidative metabolism in sorghum. Braz J Plant Physiol 11:137–143Google Scholar
  106. Philippot L, Raaijmakers JM, Lemanceau P, Putten WHV (2013) Going back to the roots: the microbial ecology of the rhizosphere. Nat Rev Microbiol 11:789–799PubMedCrossRefGoogle Scholar
  107. Piñeros M, Tester M (1995) Characterization of a voltage-dependent Ca2+-selective channel from wheat roots. Planta 195:478–488CrossRefGoogle Scholar
  108. Piñeros M, Tester M (1997) Calcium channels in plant cells: selectivity, regulation and pharmacology. J Exp Bot 48:551–577PubMedCrossRefGoogle Scholar
  109. Piňeros MA, Kochian LV (2001) A patch-clamp study on the physiology of aluminum toxicity and aluminium tolerance in maize. Identification and characterization of Al3+-induced anion channels. Plant Physiol 125:292–305PubMedPubMedCentralCrossRefGoogle Scholar
  110. Prabagar S, Hodson MJ, Evans DE (2011) Silicon amelioration of aluminium toxicity and cell death in suspension cultures of Norway spruce (Picea abies (L.) Karst.). Environ Exp Bot 70:266–276CrossRefGoogle Scholar
  111. Rengel Z, Elliott DC (1992) Mechanism of aluminum inhibition of Net45 Ca2+ uptake by Amaranthus protoplasts. Plant Physiol 98:632–638PubMedPubMedCentralCrossRefGoogle Scholar
  112. Rincón M, Gonzales RA (1992) Aluminum partitioning in intact roots of aluminum-tolerant and aluminum-sensitive wheat (Triticum aestivum L.) cultivars. Plant Physiol 99:1021–1028PubMedPubMedCentralCrossRefGoogle Scholar
  113. Rousk J, Bååth E, Brookes PC, Lauber CL, Lozupone C, Caporaso JG et al (2010) Soil bacterial and fungal communities across a pH gradient in an arable soil. ISME 4:1340–1351CrossRefGoogle Scholar
  114. Ryan PR, Kochian LV (1993) Interaction between aluminium toxicity and calcium uptake at the root apex in near-isogenic lines of wheat (Triticum aestivum L.) differing in aluminium tolerance. Plant Physiol 102:975–982PubMedPubMedCentralCrossRefGoogle Scholar
  115. Ryan PR, DiTomaso JM, Kochian LV (1993) Aluminium toxicity in roots: an investigation of spatial sensitivity and the role of the root cap. J Exp Bot 44:437–446CrossRefGoogle Scholar
  116. Sade H, Meriga B, Surapu V, Gadi J, Sunita MSL, Suravajhala P et al (2016) Toxicity and tolerance of aluminium in plants: tailoring plants to suit to acid soils. Biometals 29:187–210PubMedCrossRefGoogle Scholar
  117. Saravanakumar D, Lavanya N, Muthumeena B, Raguchander T, Suresh S, Samiyappan R (2008) Pseudomonas fluorescens enhances resistance and natural enemy population in rice plants against leaffolder pest. J Appl Entomol 132:469–479CrossRefGoogle Scholar
  118. Sasaki M, Kasai M, Yamamoto Y, Matsumoto H (1994) Comparison of the early response to aluminium stress between tolerant and sensitive wheat cultivars: root growth, aluminium content and efflux of K+. J Plant Nutr 17:1275–1288CrossRefGoogle Scholar
  119. Schippers B, Scheffer RJ, Lugtenberg BJJ, Weisbeck PJ (1995) Biocoating of seeds with plant growth promoting rhizobacteria to improve plant establishment. Outlook Agric 24:179–185CrossRefGoogle Scholar
  120. Schmohl N, Horst WJ (2000) Cell wall pectin content modulates aluminum sensitivity of Zea mays (L.) cells grown in suspension culture. Plant Cell Environ 23:735–742CrossRefGoogle Scholar
  121. Siddiqui ZA, Baghel G, Akhtar MS (2007) Biocontrol of Meloidogyne javanica by rhizobium and plant growth-promoting rhizobacteria on lentil. World J Microbiol Biotechnol 23:435–441CrossRefGoogle Scholar
  122. Silva S (2012) Aluminium toxicity targets in plants. J Bot. Scholar
  123. Silva IR, Smyth TJ, Moxley DF, Carter TE, Allen NS, Rufty TW (2000) Aluminum accumulation at nuclei of cells in the root tip. Fluorescence detection using lumogallion and confocal laser scanning microscopy. Plant Physiol 123:543–552PubMedPubMedCentralCrossRefGoogle Scholar
  124. Silva S, Pinto-Carnide O, Martins-Lopes P, Matos M, Guedes-Pinto H, Santos C (2010) Differential aluminium changes on nutrient accumulation and root differentiation in an Al-sensitive vs. tolerant wheat. Environ Exp Bot 68:91–98CrossRefGoogle Scholar
  125. Singh B, Satyanarayana T (2011) Microbial phytases in phosphorus acquisition and plant growth promotion. Physiol Mol Biol Plants 17:93–103PubMedPubMedCentralCrossRefGoogle Scholar
  126. Sivaguru M, Fujiwara T, Samaj J, Baluska F, Yang Z, Osawa H, Maeda T et al (2000) Aluminum-induced 1→3-β-D-glucan inhibits cell-to-cell trafficking of molecules through plasmodesmata. A new mechanism of aluminum toxicity in plants. Plant Physiol 124:991–1005PubMedPubMedCentralCrossRefGoogle Scholar
  127. Slugenová K, Ditmarová L, Kurjak D, Válka J (2011) Drought and aluminum as stress factors in Norway spruce (Picea abies [L.] Karst) seedlings. J For Sci 57:547–554CrossRefGoogle Scholar
  128. Smitha E, Naidu R, Alstonb AM (2002) Chemistry of Inorganic Arsenic in Soils: II. Effect of Phosphorus, Sodium, and Calcium on Arsenic Sorption. J Environ Qual 31:557–563CrossRefGoogle Scholar
  129. Sousa CS, Soares ACF, Garrido MS (2008) Characterization of streptomycetes with the potential to promote plant growth and biocontrol. Sci Agric 65:50–55CrossRefGoogle Scholar
  130. Sudha SN, Jayakumar R, Sekar V (1999) Introduction and expression of the cry1Ac gene of Bacillus thuringiensis in a cereal-associated bacterium Bacillus polymyxa. Curr Microbiol 38:163–167PubMedCrossRefGoogle Scholar
  131. Tabuchi A, Matsumoto H (2001) Changes in cell-wall properties of wheat (Triticum aestivum) roots during aluminum-induced growth inhibition. Physiol Plant 112:353–358PubMedCrossRefGoogle Scholar
  132. Tamás L, Budíková S, Huttová J, Mistrik I, Šimonovičová M, Široká B (2005) Aluminum-induced cell death of barley-root border cells is correlated with peroxidase-and oxalate oxidase-mediated hydrogen peroxide production. Plant Cell Rep 24:189–194PubMedCrossRefGoogle Scholar
  133. Thion L, Mazars C, Thuleau P, Graziana A, Rossignol M, Moreau M et al (1996) Activation of plasma membrane voltage-dependent calcium-permeable channels by disruption of microtubules in carrot cells. FEBS Lett 393:13–18PubMedCrossRefGoogle Scholar
  134. Thuleau P, Ward JM, Ranjeva R, Schroeder JI (1994) Voltage-dependent calcium-permeable channels in the plasma membrane of a higher plant cell. EMBO J 13:2970–2975PubMedPubMedCentralCrossRefGoogle Scholar
  135. Tokizawa M, Kobayashi Y, Saito T, Kobayashi M, Iuchi S, Nomoto M et al (2015) Sensitive to proton rhizotoxicity1, calmodulin binding transcription activator2, and other transcription factors are involved in aluminum-activated malate transporter1 expression. Plant Physiol 167:991–1003PubMedPubMedCentralCrossRefGoogle Scholar
  136. Very AA, Davies JM (2000) Hyperpolarization-activated calcium channels at the tip of Arabidopsis root hairs. PNAS 97:9801–9806PubMedCrossRefGoogle Scholar
  137. Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586CrossRefGoogle Scholar
  138. Vitorello VA, Haug A (1996) Short-term aluminum uptake by tobacco cells: growth dependence and evidence for internalization in a discrete peripheral region. Physiol Plant 97:536–544CrossRefGoogle Scholar
  139. Vitorello VA, Capaldi FR, Stefanuto VA (2005) Recent advances in aluminum toxicity and resistance in higher plants. Braz J Plant Physiol 17:129–143CrossRefGoogle Scholar
  140. von Uexküll HR, Mutert E (1995) Global extent, development and economic impact of acid soils. In: Date RA, Grundon NJ, Raymet GE, Probert ME (eds) Plant–soil interactions at low pH: principles and management. Kluwer Academic Publishers, Dordrecht, pp 5–19CrossRefGoogle Scholar
  141. Wagatsuma T, Ishikawa S, Obata H, Tawaraya K, Katohda S (1995) Plasma membrane of younger and outer cells is the primary specific site for aluminum toxicity in roots. Plant Soil 171(1):105–112CrossRefGoogle Scholar
  142. Wang T, Liu MQ, Li HX (2014) Inoculation of phosphate solubilizing bacteria Bacillus thuringiensis B1 increases available phosphorus and growth of peanut in acidic soil. Soil Plant Sci 64:252–259Google Scholar
  143. Weller DM, Raaijmakers JM, Mcspadden BB, Thomashow LS (2002) Microbial populations responsible for specific soil suppressiveness to plant pathogens. Annu Rev Phytopathol 40:309–348PubMedPubMedCentralCrossRefGoogle Scholar
  144. Wu Y, Zeng J, Zhu Q, Zhang Z, Lin X (2017) pH is the primary determinant of the bacterial community structure in agricultural soils impacted by polycyclic aromatic hydrocarbon pollution. Sci Rep 7:40093. Scholar
  145. Yamamoto Y, Kobayashi Y, Matsumoto H (2001) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Plant Physiol 125:199–208PubMedPubMedCentralCrossRefGoogle Scholar
  146. Zahir AZ, Arshad M, Frankenberger WT (2004) Plant growth promoting rhizobacteria: applications and perspectives in agriculture. Adv Agron 81:97–168CrossRefGoogle Scholar
  147. Zerrouk IZ, Benchabane M, Khelifi L, Yokawa K, Ludwig-Muller J, Baluska F (2016) A Pseudomonas strain isolated from date-palm rhizospheres improves root growth and promotes root formation in maize exposed to salt and aluminum stress. J Plant Physiol 191:111–119CrossRefGoogle Scholar
  148. Zhang H, Jiang Z, Qin R, Zhang H, Zou J, Jiang W, Liu D (2014) Accumulation and cellular toxicity of aluminum in seedling of Pinus massoniana. BMC Plant Biol 14:264. Scholar
  149. Zheng SJ (2010) Crop production on acidic soils: overcoming aluminum toxicity and phosphorus deficiency. Ann Bot 106:183–184PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Jintu Dutta
    • 1
  • Utpal Bora
    • 2
  1. 1.Centre for the EnvironmentIndian Institute of Technology GuwahatiGuwahatiIndia
  2. 2.Department of Biosciences and BioengineeringIndian Institute of Technology GuwahatiGuwahatiIndia

Personalised recommendations