ACC Deaminase-Producing Bacteria: A Key Player in Alleviating Abiotic Stresses in Plants

  • Swapnil Sapre
  • Iti Gontia-Mishra
  • Sharad Tiwari


Plants are subjected to many abiotic stresses in the environment. These abiotic stresses may be aggravated in the coming future due to global climate change. Almost all the environmental stress causes the production of ethylene in plants, which is detrimental to plant survival. Therefore, managing ethylene generation in plants is becoming as an attractive strategy to increase crop yields. 1-Aminocyclopropane-1-carboxylic acid is a precursor for production of ethylene in plants. The plant growth-promoting rhizobacteria that possess 1-aminocyclopropane-1-carboxylic acid deaminase activity are known to modulate plant growth under extreme environmental conditions by lowering ethylene concentrations in plants; hence, they can be termed as ‘stress modulator’. Ethylene is also known to reduce the nodule formation in various legumes prevailing under abiotic stress. 1-Aminocyclopropane-1-carboxylic acid deaminase-producing rhizobial strains can intensively promote nodulation in legumes under stress conditions. Another approach for combating abiotic stress in plants is through the incorporation of acdS gene from bacteria to crop plants. The recent molecular biology tools (metagenomics, transcriptomics, proteomics and next-generation sequencing) have been implied to reveal the diversity and application of potential 1-aminocyclopropane-1-carboxylic acid deaminase-producing plant growth-promoting rhizobacteria under various environmental conditions. These rhizobacteria have shown a vital interplay in conferring resistance and adaptation of plants to various abiotic stresses and have immense potential in organic farming and sustainable agriculture.


PGPR ACC deaminase Abiotic stress Ethylene 



The present work was funded by the Science and Engineering Research Board (Grant # SB/FT/LS-374/2012), received by IGM.


  1. Abeles FB, Morgan PW, Saltveit ME Jr (1992) Ethylene in plant biology, 2nd edn. Academic Press, New YorkGoogle Scholar
  2. Ahmad M, Zahir ZA, Asghar HN et al (2011) Inducing salt tolerance in mung bean through co-inoculation with rhizobia and plant-growth promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 57:578–589PubMedCrossRefGoogle Scholar
  3. Ajuzieogu CA, Ibiene AA, Stanley HO (2015) Laboratory study on influence of plant growth promoting rhizobacteria (PGPR) on growth response and tolerance of Zea mays to petroleum hydrocarbon. Afr J Biotechnol 14:2949–2956CrossRefGoogle Scholar
  4. Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167PubMedCrossRefGoogle Scholar
  5. Armad E, Probanza A, Roldanc A et al (2016) Native plant growth promoting bacteria Bacillus thuringiensis and mixed or individual mycorrhizal species improved drought tolerance and oxidative metabolism in Lavandula dentata plants. J Plant Physiol 192:1–12CrossRefGoogle Scholar
  6. Arshad M, Saleem M, Hussain S (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362PubMedCrossRefGoogle Scholar
  7. Barka EA, Nowak J, Clement C (2006) Enhancement of chilling resistance of inoculated grapevine plantlets with a plant growth-promoting rhizobacterium, Burkholderia phytofirmans strain PsJN. Appl Environ Microbiol 72:7246–7252CrossRefGoogle Scholar
  8. Barnawal D, Bharti N, Maji D et al (2012) 1-Aminocyclopropane-1-carboxylic acid (ACC) deaminase-containing rhizobacteria protect Ocimum sanctum plants during waterlogging stress via reduced ethylene generation. Plant Physiol Biochem 58:227–235PubMedCrossRefGoogle Scholar
  9. Barnawal D, Maji D, Bharti N et al (2013) ACC deaminase-containing Bacillus subtilis reduces stress ethylene-induced damage and improves mycorrhizal colonization and rhizobial nodulation in Trigonella foenum-graecum under drought stress. J Plant Growth Regul 32:809–822CrossRefGoogle Scholar
  10. Barnawal D, Bharti N, Maji D et al (2014) ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in Pisum sativum. J Plant Physiol 171:884–894PubMedCrossRefGoogle Scholar
  11. Belimov AA, Dodd IC, Safronova VI et al (2015) Rhizobacteria that produce auxins and contain 1-amino-cyclopropane-1-carboxylic acid deaminase decrease amino acid concentrations in the rhizosphere and improve growth and yield of well-watered and water-limited potato (Solanum tuberosum). Ann Appl Biol 167:11–25CrossRefGoogle Scholar
  12. Bharti N, Barnawal D, Awasthi A et al (2014) Plant growth promoting rhizobacteria alleviate salinity induced negative effects on growth: oil content and physiological status in Mentha arvensis. Acta Physiol Plant 36:45–60CrossRefGoogle Scholar
  13. Bharti N, Pandey SS, Barnawal D et al (2016) Plant growth promoting rhizobacterial Dietzia natronolimnaea modulates the expression of stress responsive genes providing protection of wheat from salinity stress. Sci Rep 6:34768PubMedPubMedCentralCrossRefGoogle Scholar
  14. Brigido C, Nascimento F, Duan J et al (2013) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Mesorhizobium spp. reduces the negative effects of salt stress in chickpea. FEMS Microbiol Lett 349:46–53PubMedGoogle Scholar
  15. Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Appl Environ Microbiol 64:3663–3668PubMedPubMedCentralGoogle Scholar
  16. Carlos MHJ, Stefani PVY, Janette AM et al (2016) Assessing the effects of heavy metals in ACC deaminase and IAA production on plant growth-promoting bacteria. Microbiol Res 188–189:53–61PubMedCrossRefGoogle Scholar
  17. Chakraborty U, Chakraborty BN, Chakraborty AP et al (2013) Water stress amelioration and plant growth promotion in wheat plants by osmotic stress tolerant bacteria. World J Microbiol Biotechnol 29:789–803PubMedCrossRefGoogle Scholar
  18. Chatterjee P, Samaddar S, Anandham R et al (2017) Beneficial soil bacterium Pseudomonas frederiksbergensis OS261 augments salt tolerance and promotes red pepper plant growth. Front Plant Sci 8:705PubMedPubMedCentralCrossRefGoogle Scholar
  19. Chen L, Luo S, Xiao X et al (2010) Application of plant growth-promoting endophytes (PGPE) isolated from Solanum nigrum L. for phytoextraction of Cd-polluted soils. Appl Soil Ecol 46:383–389CrossRefGoogle Scholar
  20. Chen J, Li S, Xu B et al (2017) Characterization of Burkholderia sp. XTB-5 for phenol degradation and plant growth promotion and its application in bioremediation of contaminated soil. Land Degrad Dev 28(3):1091–1099CrossRefGoogle Scholar
  21. Cheng Z, McConkey BJ, Glick BR (2010) Proteomic studies of plant-bacterial interactions. Soil Biol Biochem 42:1673–1684CrossRefGoogle Scholar
  22. Cheng Z, Woody OZ, McConkey BJ et al (2012) Combined effects of the plant growth promoting bacterium Pseudomonas putida UW4 and salinity stress on the Brassica napus proteome. Appl Soil Ecol 61:255–263CrossRefGoogle Scholar
  23. Conforte VP, Echeverria M, Sanchez C et al (2010) Engineered ACC deaminase-expressing free-living cells of Mesorhizobium loti show increased nodulation efficiency and competitiveness on Lotus spp. J Gen Appl Microbiol 56:331–338PubMedCrossRefGoogle Scholar
  24. Drogue B, Sanguin H, Chamam A et al (2014) Plant root transcriptome profiling reveals a strain-dependent response during Azospirillum-rice cooperation. Front Plant Sci 5:607PubMedPubMedCentralCrossRefGoogle Scholar
  25. Duan J, Müller KM, Charles TC et al (2009) 1-aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from Southern Saskatchewan. Microb Ecol 57:423–436PubMedCrossRefGoogle Scholar
  26. Duan J, Jiang W, Cheng Z et al (2013) The complete genome sequence of the plant growth-promoting bacterium Pseudomonas sp.UW4. PLoS One 8(3):e58640PubMedPubMedCentralCrossRefGoogle Scholar
  27. Farwell AJ, Vesely S, Nero V et al (2007) Tolerance of transgenic canola plants (Brassica napus) amended with plant growth-promoting bacteria to flooding stress at a metal contaminated field site. Environ Pollut 147:540–545PubMedCrossRefGoogle Scholar
  28. Gage DJ (2004) Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol Mol Biol Rev 68:280–300PubMedPubMedCentralCrossRefGoogle Scholar
  29. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374PubMedCrossRefGoogle Scholar
  30. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 169:30–39PubMedCrossRefGoogle Scholar
  31. Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68PubMedCrossRefGoogle Scholar
  32. Glick BR, Patten CL, Holguin G et al (1999) Biochemical and genetic mechanisms used by plant growth promoting bacteria. Imperial College Press, LondonCrossRefGoogle Scholar
  33. Gontia I, Kavita K, Schmid M et al (2011) Brachybacterium saurashtrense sp. nov., a halotolerant root associated bacterium with plant growth-promoting potential. Int J Syst Evol Microbiol 61:2799–2804PubMedCrossRefGoogle Scholar
  34. Gontia-Mishra I, Sasidharan S, Tiwari S (2014) Recent developments in use of 1-amino cyclopropane-1-carboxylate (ACC) deaminase for conferring tolerance to biotic and abiotic stress. Biotechnol Lett 36:889–898PubMedCrossRefGoogle Scholar
  35. Gontia-Mishra I, Sapre S, Sharma A et al (2016a) Alleviation of mercury toxicity in wheat by the interaction of mercury-tolerant plant growth-promoting rhizobacteria. J Plant Growth Regul 35:1000–1012CrossRefGoogle Scholar
  36. Gontia-Mishra I, Sapre S, Sharma A et al (2016b) Amelioration of drought tolerance in wheat by the interaction of plant growth promoting rhizobacteria. Plant Biol 18:992–1000PubMedCrossRefGoogle Scholar
  37. Gontia-Mishra I, Sapre S, Kachare S et al (2017a) Molecular diversity of 1-aminocyclopropane-1-carboxylate (ACC) deaminase producing PGPR from wheat (Triticum aestivum L.) rhizosphere. Plant Soil 414:213–227CrossRefGoogle Scholar
  38. Gontia-Mishra I, Sapre S, Tiwari S (2017b) Zinc solubilizing bacteria from the rhizosphere of rice as prospective modulator of zinc biofortification in rice. Rhizosphere 3:185–190CrossRefGoogle Scholar
  39. Grichko VP, Glick BR (2001) Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlled by the 35S, rolD or PRB-1b promoter. Plant Physiol Biochem 39:19–25CrossRefGoogle Scholar
  40. Grichko VP, Filby B, Glick BR (2000) Increased ability of transgenic plants expressing the bacterial enzyme ACC deaminase to accumulate Cd Co, Cu, Ni, Pb, and Zn. J Biotechnol 81:45–53PubMedCrossRefGoogle Scholar
  41. Guinel FC (2015) Ethylene, a hormone at the center-stage of nodulation. Front Plant Sci 6:1121PubMedPubMedCentralCrossRefGoogle Scholar
  42. 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 Soil 375:205–214CrossRefGoogle Scholar
  43. Guo J, Tang S, Ju X et al (2011) Effects of inoculation of a plant growth promoting rhizobacterium Burkholderia sp. D54 on plant growth and metal uptake by a hyperaccumulator Sedum alfredii Hance grown on multiple metal contaminated soil. World J Microbiol Biotechnol 27:2835–2844CrossRefGoogle Scholar
  44. Gururani MA, Upadhyaya CP, Baskar V et al (2013) Plant growth-promoting rhizobacteria enhance abiotic stress tolerance in Solanum tuberosum through inducing changes in the expression of ROS-scavenging enzymes and improved photosynthetic performance. J Plant Growth Regul 32:245258CrossRefGoogle Scholar
  45. Heydarian Z, Yu M, Gruber M et al (2016) Inoculation of soil with plant growth promoting bacteria producing 1-aminocyclopropane-1-carboxylate deaminase or expression of the corresponding acdS gene in transgenic plants increases salinity tolerance in Camelina sativa. Front Microbiol 7:1966PubMedPubMedCentralCrossRefGoogle Scholar
  46. Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 43:1825–1831Google Scholar
  47. Huang XF, Zhou D, Lapsansky ER et al (2017) Mitsuaria sp. and Burkholderia sp. from Arabidopsis rhizosphere enhance drought tolerance in Arabidopsis thaliana and maize (Zea mays L.). Plant Soil 419:523–539CrossRefGoogle Scholar
  48. Illakkiam D, Shankar M, Ponraj P et al (2014) Genome sequencing of a mung bean plant growth promoting strain of P. aeruginosa with biocontrol ability. Int J Genomics 2014:123058PubMedPubMedCentralCrossRefGoogle Scholar
  49. Islam F, Yasmeen T, Ali Q et al (2014a) Influence of Pseudomonas aeruginosa as PGPR on oxidative stress tolerance in wheat under Zn stress. Ecotoxicol Environ Saf 104:285–293PubMedCrossRefGoogle Scholar
  50. Islam F, Yasmeen T, Riaz M et al (2014b) Proteus mirabilis alleviates zinc toxicity by preventing oxidative stress in maize (Zea mays) plants. Ecotoxicol Environ Saf 110:143–152PubMedCrossRefGoogle Scholar
  51. Jacobson CB, Pasternak JJ, Glick BR (1994) Partial purification and characterization of ACC deaminase from the plant growth-promoting rhizobacterium Pseudomonas putida GR12-2. Can J Microbiol 40:1019–1025CrossRefGoogle Scholar
  52. Jha B, Gontia I, Hartmann A (2012) The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 356:265–277CrossRefGoogle Scholar
  53. Jing YX, Yan JL, He HD et al (2014) Characterization of bacteria in the rhizosphere soils of Polygonum pubescens and their potential in promoting growth and Cd, Pb, Zn uptake by Brassica napus. Int J Phytoremediation 16:321–333PubMedCrossRefGoogle Scholar
  54. Johnson PR, Ecker JR (1998) The ethylene gas signal transduction pathway: a molecular perspective. Annu Rev Genet 32:227–254PubMedCrossRefGoogle Scholar
  55. Kamran MA, Syed JH, Eqan SAMAS et al (2015) Effect of plant growth-promoting rhizobacteria inoculation on cadmium (Cd) uptake by Eruca sativa. Environ Sci Pollut Res 22:9275–9283CrossRefGoogle Scholar
  56. Kang BG, Kim WT, Yun HS et al (2010) Use of plant growth-promoting rhizobacteria to control stress responses of plant roots. Plant Biotechnol Rep 4:179–183CrossRefGoogle Scholar
  57. Kaushal M, Wani SP (2016) Plant growth-promoting rhizobacteria: drought stress alleviators to ameliorate crop production in drylands. Ann Microbiol 66:35–42CrossRefGoogle Scholar
  58. Kim K, Park SH, Chae JC et al (2014) Rapid degradation of Pseudomonas fluorescens1-aminocyclopropane-1-carboxylic acid deaminase proteins expressed in transgenic Arabidopsis. FEMS Microbiol Lett 355:193–200PubMedCrossRefGoogle Scholar
  59. Kong Z, Glick BR, Duan J et al (2015) Effects of 1-aminocyclopropane-1-carboxylate (ACC) deaminase-overproducing Sinorhizobium meliloti on plant growth and copper tolerance of Medicago lupulina. Plant Soil 391:383–398CrossRefGoogle Scholar
  60. Kumari S, Vaishnav A, Jain S et al (2016) Induced drought tolerance through wild and mutant bacterial strain Pseudomonas simiae in mung bean (Vigna radiata L.). World J Microbiol Biotechnol 32:4PubMedCrossRefGoogle Scholar
  61. Kwak M-J, Jeong H, Madhaiyan M et al (2014) Genome information of Methylobacterium oryzae, a plant-probiotic methylotroph in the phyllosphere. PLoS One 9(9):e106704PubMedPubMedCentralCrossRefGoogle Scholar
  62. Lee KH, LaRue TA (1992) Exogenous ethylene inhibits nodulation of Pisum sativum L. cv Sparkle. Plant Physiol 100:1759–1763PubMedPubMedCentralCrossRefGoogle Scholar
  63. Leveau JHJ (2007) The magic and menace of metagenomics: prospects for the study of plant growth-promoting rhizobacterial. Eur J Plant Pathol 119:279–300CrossRefGoogle Scholar
  64. Li J, McConkey BJ, Cheng Z et al (2013) Identification of plant growth-promoting rhizobacteria-responsive proteins in cucumber roots under hypoxic stress using a proteomic approach. J Proteome 84:119–131CrossRefGoogle Scholar
  65. Liu JL, Xie BM, Shi XH et al (2015) Effects of two plant growth-promoting rhizobacteria containing 1-aminocyclopropane-1-carboxylate deaminase on oat growth in petroleum-contaminated soil. Int J Environ Sci Technol 12(12):3887–3894CrossRefGoogle Scholar
  66. Loreti E, van Veen H, Perata P (2016) Plant responses to flooding stress. Curr Opin Plant Biol 33:64–71PubMedCrossRefGoogle Scholar
  67. Luo S, Chen L, Chen J et al (2011) Analysis and characterization of cultivable heavy metal-resistant bacterial endophytes isolated from Cd-hyperaccumulator Solanum nigrum L. and their potential use for phytoremediation. Chemosphere 85:1130–1138PubMedCrossRefGoogle Scholar
  68. Ma W, Sebestianova SB, Sebestian J et al (2003a) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Antonie Van Leeuwenhoek 83:285–291PubMedCrossRefGoogle Scholar
  69. Ma W, Guinel FC, Glick BR (2003b) Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69:4396–4402PubMedPubMedCentralCrossRefGoogle Scholar
  70. Ma W, Charles TC, Glick BR (2004) Expression of an exogenous1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891–5897PubMedPubMedCentralCrossRefGoogle Scholar
  71. Maa Y, Rajkumar M, Luo Y et al (2013) Phytoextraction of heavy metal polluted soils using Sedum plumbizincicola inoculated with metal mobilizing Phyllobacterium myrsinacearum RC6b. Chemosphere 93:1386–1392CrossRefGoogle Scholar
  72. Marques APGC, Pires C, Moreira H (2010) Assessment of the plant growth promotion abilities of six bacterial isolates using Zea mays as indicator plant. Soil Biol Biochem 42:1229–1235CrossRefGoogle Scholar
  73. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572PubMedCrossRefGoogle Scholar
  74. Meena KK, Sorty AM, Bitla UM et al (2017) Abiotic stress responses and microbe-mediated mitigation in plants: the omics strategies. Front Plant Sci 8:172PubMedPubMedCentralCrossRefGoogle Scholar
  75. Mesa J, Mateos-Naranjo E, Caviedes MA et al (2015) Scouting contaminated estuaries: heavy metal resistant and plant growth promoting rhizobacteria in the native metal rhizoaccumulator Spartina maritima. Mar Pollut Bull 90:150–159PubMedCrossRefGoogle Scholar
  76. Miller G, Susuki N, Ciftci-Yilmaz S et al (2010) Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant Cell Environ 33:453–467PubMedPubMedCentralCrossRefGoogle Scholar
  77. Motesharezadeh B, Savaghebi-Firoozabadi GR (2011) Study of the increase in phytoremediation efficiency in a nickel polluted soil by the usage of native bacteria: Bacillus safensis FO.036b and Micrococcus roseus M2. Caspian J Environ Sci 9:133–143Google Scholar
  78. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  79. Nascimento F, Brígido C, Alho L et al (2012a) Enhanced chickpea growth promotion ability of a Mesorhizobium strain expressing an exogenous ACC deaminase gene. Plant Soil 353:221–230CrossRefGoogle Scholar
  80. Nascimento F, Brígido C, Glick BR et al (2012b) Mesorhizobium ciceri LMS-1 expressing an exogenous1-aminocyclopropane-1-carboxylate (ACC) deaminase increases its nodulation abilities and chickpea plant resistance to soil constraints. Lett Appl Microbiol 55:15–21PubMedCrossRefGoogle Scholar
  81. Nautiyal CS, Srivastava S, Chauhan PS et al (2013) Plant growth-promoting bacteria Bacillus amyloliquefaciens NBRISN13 modulates gene expression profile of leaf and rhizosphere community in rice during salt stress. Plant Physiol Biochem 66:1–9PubMedCrossRefGoogle Scholar
  82. Niazi A, Manzoor S, Asari S et al (2014) Genome analysis of Bacillus amyloliquefaciens Subsp. plantarum UCMB5113: a rhizobacterium that improves plant growth and stress management. PLoS One 9(8):e104651PubMedPubMedCentralCrossRefGoogle Scholar
  83. Nie L, Shah S, Rashid A et al (2002) Phytoremediation of arsenate contaminated soil by transgenic canola and the plant growth-promoting bacterium Enterobacter cloacae CAL2. Plant Physiol Biochem 40:355–361CrossRefGoogle Scholar
  84. Nikolic B, Schwab H, Sessitsch A (2011) Metagenomic analysis of the 1-aminocyclopropane-1-carboxylate deaminase gene (acdS) operon of an uncultured bacterial endophyte colonizing Solanum tuberosum L. Arch Microbiol 193:665–676PubMedCrossRefGoogle Scholar
  85. Parray JA, Jan S, Kamili AN et al (2016) Current perspectives on plant growth-promoting rhizobacteria. J Plant Growth Regul 35:877–902CrossRefGoogle Scholar
  86. Pereira SIA, Barbosa L, Castro PML (2015) Rhizobacteria isolated from a metal-polluted area enhance plant growth in zinc and cadmium-contaminated soil. Int J Environ Sci Technol 12:2127–2142CrossRefGoogle Scholar
  87. Peters NK, Crist-Estes DK (1989) Nodule formation is stimulated by the ethylene inhibitor amino ethoxy vinyl glycine. Plant Physiol 91:690–693PubMedPubMedCentralCrossRefGoogle Scholar
  88. Płociniczak T, Sinkkonen A, Romantschuk M et al (2014) Characterization of Enterobacter intermedius MH8b and its use for the enhancement of heavy metals uptake by Sinapis alba L. Appl Soil Ecol 63:1–7CrossRefGoogle Scholar
  89. Prapagdee B, Chanprasert M, Mongkolsuk S (2013) Bioaugmentation with cadmium-resistant plant growth-promoting rhizobacteria to assist cadmium phytoextraction by Helianthus annuus. Chemosphere 92:659–666PubMedCrossRefGoogle Scholar
  90. Qiao J, Liu Y, Liang X et al (2014) Draft genome sequence of root-colonizing bacterium Bacillus sp. strain PTS-394. Genome Announc 2(1):e00038–e00014PubMedPubMedCentralCrossRefGoogle Scholar
  91. Qin S, Zhang Y-J, Yuan B et al (2014) Isolation of ACC deaminase-producing habitat-adapted symbiotic bacteria associated with halophyte Limonium sinense (Girard) Kuntze and evaluating their plant growth-promoting activity under salt stress. Plant Soil 374:753–766CrossRefGoogle Scholar
  92. Reed MLE, Glick BR (2005) Growth of canola (Brassica napus) in the presence of plant growth-promoting bacteria and either copper or polycyclic aromatic hydrocarbons. Can J Microbiol 51:1061–1069PubMedCrossRefGoogle Scholar
  93. Sairam RK, Kumutha D, Ezhilmathi K et al (2009) Waterlogging induced oxidative stress and antioxidant enzyme activities in pigeon pea. Biol Planta 53:493–504CrossRefGoogle Scholar
  94. Saleem M, Arshad M, Hussain S et al (2007) Perspective of plant growth promoting rhizobacteria (PGPR) containing ACC deaminase in stress agriculture. J Ind Microbiol Biotechnol 34:635–648PubMedCrossRefGoogle Scholar
  95. Sapre S, Gontia-Mishra I, Tiwari S (2018) Klebsiella sp. confers enhanced tolerance to salinity and plant growth promotion in oat seedlings (Avena sativa). Microbiol Res 206:25–32PubMedCrossRefGoogle Scholar
  96. Saravanakumar D, Samiyappan R (2007) ACC deaminase from Pseudomonas fluorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J Appl Microbiol 102:1283–1292PubMedCrossRefGoogle Scholar
  97. Sarkar A, Ghosh PK, Pramanik K et al (2018) A halotolerant Enterobacter sp. displaying ACC deaminase activity promotes rice seedling growth under salt stress. Res Microbiol 169:20–32PubMedCrossRefGoogle Scholar
  98. Sarma RK, Saikia SR (2014) Alleviation of drought stress in mung bean by strain Pseudomonas aeruginosa GGRJ21. Plant Soil 377:111–126CrossRefGoogle Scholar
  99. Sergeeva E, Shah S, Glick BR (2006) Growth of transgenic canola (Brassica napus cv. Westar) expressing a bacterial 1-aminocyclopropane-1-carboxylate (ACC) deaminase gene on high concentrations of salt. World J Microbiol Biotechnol 22:277–282CrossRefGoogle Scholar
  100. Shagol CC, Subramanian P, Krishnamoorthy R et al (2014) ACC deaminase producing arsenic tolerant bacterial effect on mitigation of stress ethylene emission in maize grown in an arsenic polluted soil. Korean J Soil Sci Fertil 47:213–216CrossRefGoogle Scholar
  101. Shaharoona B, Arshad M, Zahir ZA (2006) Effect of plant growth promoting rhizobacteria containing ACC-deaminase on maize (Zea mays L.) growth under axenic conditions and on nodulation in mung bean (Vigna radiata L.). Lett Appl Microbiol 42:155–159PubMedCrossRefPubMedCentralGoogle Scholar
  102. Shaharoona B, Imran M, Arshad M et al (2011) Manipulation of ethylene synthesis in roots through bacterial ACC deaminase for improving nodulation in legumes. Crit Rev Plant Sci 30:279–291CrossRefGoogle Scholar
  103. Shahzad SM, Khalid A, Arshad M et al (2010) Improving nodulation, growth and yield of Cicer arietinum L. through bacterial ACC-deaminase induced changes in root architecture. Eur J Soil Biol 46:342–347CrossRefGoogle Scholar
  104. Shahzadi I, Khalid A, Mahmood S et al (2013) Effect of bacteria containing ACC deaminase on growth of wheat seedlings grown with chromium contaminated water. Pak J Bot 45:487–494Google Scholar
  105. Sharma P, Khanna V, Kumari P (2013) Efficacy of aminocyclopropane-1-carboxylic acid (ACC)-deaminase-producing rhizobacteria in ameliorating water stress in chickpea under axenic conditions. Afr J Microbiol Res 7(50):5749–5757CrossRefGoogle Scholar
  106. Sharma S, Kulkarni J, Jha B (2016) Halotolerant rhizobacterial promote growth and enhance salinity tolerance in peanut. Front Microbiol 7:1600PubMedPubMedCentralGoogle Scholar
  107. Shukla PS, Agarwal PK, Jha B (2012) Improved salinity tolerance of Arachis hypogaea (L.) by the interaction of halotolerant plant-growth-promoting rhizobacteria. J. Plant Growth Regul 31:195–206CrossRefGoogle Scholar
  108. Siddikee MA, Chauan PS, Anandham R et al (2010) Isolation, characterization, and use for plant growth promotion under salt stress, of ACC deaminase-producing halotolerant bacteria derived from coastal soil. J Microbiol Biotechnol 20:1577–1584PubMedCrossRefPubMedCentralGoogle Scholar
  109. Siddikee MA, Chauhan PS, Sa T (2012) Regulation of ethylene biosynthesis under salt stress in red pepper (Capsicum annuum L.) by 1-aminocyclopropane-1- carboxylic acid (ACC) deaminase-producing halotolerant bacteria. J Plant Growth Regul 31:265–272CrossRefGoogle Scholar
  110. Singh RP, Jha P, Jha PN (2015) The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress. J Plant Physiol 184:57–67PubMedCrossRefGoogle Scholar
  111. Singh N, Marwa N, Mishra SK et al (2016) Brevundimonas diminuta mediated alleviation of arsenic toxicity and plant growth promotion in Oryza sativa L. Ecotoxicol Environ Saf 125:25–34PubMedCrossRefGoogle Scholar
  112. Soussou S, Brunel B, Pervent M et al (2017) Rhizobacterial Pseudomonas spp. strains harbouring acdS gene could enhance metallicolous legume nodulation in Zn/Pb/Cd mine tailings. Water Air Soil Pollut 228:142CrossRefGoogle Scholar
  113. Srinivasan R, Mageswari A, Subramanian P et al (2017) Exogenous expression of ACC deaminase gene in psychrotolerant bacteria alleviates chilling stress and promotes plant growth in millets under chilling conditions. Indian J Exp Biol 55:463–468Google Scholar
  114. Srivastava S, Singh N (2014) Mitigation approach of arsenic toxicity in chickpea grown in arsenic amended soil with arsenic tolerant plant growth promoting Acinetobacter sp. Ecol Eng 70:146–153CrossRefGoogle Scholar
  115. Stearns JC, Shah S, Greenberg BM et al (2005) Tolerance of transgenic canola expressing1-aminocyclopropane-1-carboxylic acid deaminase to growth inhibition by nickel. Plant Physiol Biochem 43:701–708PubMedCrossRefGoogle Scholar
  116. Striker GG (2012) Flooding stress on plants: anatomical, morphological and physiological responses. In: Mworia JK (ed) Botany. InTech, London, pp 3–28Google Scholar
  117. Subramanian P, Krishnamoorthy R, Chanratana M et al (2015) Expression of an exogenous 1-aminocyclopropane-1-carboxylatedeaminase gene in psychrotolerant bacteria modulates ethylene metabolism and cold induced genes in tomato under chilling stress. Plant Physiol Biochem 89:18–23PubMedCrossRefGoogle Scholar
  118. Subramanian P, Kim K, Krishnamoorthy R et al (2016) Cold stress tolerance in psychrotolerant soil bacteria and their conferred chilling resistance in Tomato (Solanum lycopersicum Mill.) under low temperatures. PLoS One 11(8):e0161592PubMedPubMedCentralCrossRefGoogle Scholar
  119. Theocharis A, Bordiec S, Fernandez O et al (2012) Burkholderia phytofirmans PsJN primes Vitis vinifera L. and confers a better tolerance to low nonfreezing temperatures. Mol Plant-Microbe Interact 25:241–249PubMedCrossRefGoogle Scholar
  120. Timmusk S, Paalme V, Pavlicek T et al (2011) Bacterial distribution in the rhizosphere of wild barley under contrasting microclimates. PLoS One 6:e17968PubMedPubMedCentralCrossRefGoogle Scholar
  121. Timmusk S, Abd El-Daim IA, Copolovici L et al (2014) Drought-tolerance of wheat improved by rhizosphere bacteria from harsh environments: enhanced biomass production and reduced emissions of stress volatiles. PLoS One 9(5):e96086PubMedPubMedCentralCrossRefGoogle Scholar
  122. Tiwari S, Lata C, Chauhan PS et al (2016) Pseudomonas putida attunes morphophysiological, biochemical and molecular responses in Cicer arietinum L. during drought stress and recovery. Plant Physiol Biochem 99:108–117PubMedCrossRefGoogle Scholar
  123. Van Oosten MJ, Maggio A (2015) Functional biology of halophytes in the phytoremediation of heavy metal contaminated soils. Environ Exp Bot 111:135–146CrossRefGoogle Scholar
  124. Wang KLC, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:S131–S151PubMedPubMedCentralCrossRefGoogle Scholar
  125. Xun F, Xie B, Liu S et al (2015) Effect of plant growth-promoting bacteria (PGPR) and arbuscular mycorrhizal fungi (AMF) inoculation on oats in saline-alkali soil contaminated by petroleum to enhance phytoremediation. Environ Sci Pollut Res 22:598–608CrossRefGoogle Scholar
  126. Yadav SK (2010) Cold stress tolerance mechanisms in plants: a review. Agron Sustain Dev 30:515–527CrossRefGoogle Scholar
  127. Yang R, Luo C, Chen Y et al (2013) Copper-resistant bacteria enhance plant growth and copper phytoextraction. Int J Phytoremediation 15:573–584PubMedCrossRefGoogle Scholar
  128. Zhang Y, Zhao L, Wang Y et al (2008) Enhancement of heavy metal accumulation by tissue specific co-expression of iaaM and ACC deaminase genes in plants. Chemosphere 72:564–571PubMedCrossRefGoogle Scholar
  129. Zhang Y, He L, Chen Z et al (2011) Characterization of lead-resistant and ACC deaminase-producing endophytic bacteria and their potential in promoting lead accumulation of rape. J Hazard Mater 186:1720–1725PubMedCrossRefGoogle Scholar
  130. Zhang F, Zhang J, Chen L et al (2015) Heterologous expression of ACC deaminase from Trichoderma asperellum improves the growth performance of Arabidopsis thaliana under normal and salt stress conditions. Plant Physiol Biochem 94:41–47PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2019

Authors and Affiliations

  • Swapnil Sapre
    • 1
  • Iti Gontia-Mishra
    • 1
  • Sharad Tiwari
    • 2
  1. 1.Biotechnology CentreJawaharlal Nehru Agriculture UniversityJabalpurIndia
  2. 2.Department of Plant Breeding and GeneticsJawaharlal Nehru Agriculture UniversityJabalpurIndia

Personalised recommendations