The plant-growth-promoting bacterium Klebsiella sp. SBP-8 confers induced systemic tolerance in wheat (Triticum aestivum) under salt stress

Journal of Plant Physiology

Volumn 184, Issue , 2015, Pages 57-67

  Singh, Rajnish Prakash ^a   Jha, Prameela ^a   Jha, Prabhat Nath ^a  

^a BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

Author keywords

ACC deaminase; ERIC PCR; Induced systemic tolerance; Klebsiella sp; PGPR

Indexed keywords

BACTERIA (MICROORGANISMS); KLEBSIELLA; KLEBSIELLA SP.; SORGHUM BICOLOR; TRITICUM AESTIVUM;

BACTERIAL PROTEIN; CHLOROPHYLL;

BIOMASS; DNA SEQUENCE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEAT; INDIA; ISOLATION AND PURIFICATION; KLEBSIELLA; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SALINITY; SALT TOLERANCE; WHEAT;

BACTERIAL PROTEINS; BIOMASS; CHLOROPHYLL; HOT TEMPERATURE; INDIA; KLEBSIELLA; MOLECULAR SEQUENCE DATA; PHYLOGENY; SALINITY; SALT-TOLERANCE; SEQUENCE ANALYSIS, DNA; TRITICUM;

EID: 84938057356     PISSN: 01761617     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jplph.2015.07.002     Document Type: Article

References (74)

1. Abeles F.B., Morgan P.W., Saltveit M.E. Ethylene in Plant Biology 1992, Academic press, San Diego.
2. Ahmad M., Zahir Z.A., Asghar H.N., Ashgar M. Inducing salt tolerance in mung bean through coinoculation with rhizobia and plant growth promoting rhizobacteria containing 1-aminocyclopropane- 1-carboxylate deaminase. Can. J. Microbiol. 2011, 57:578-589.
3. Ali S.F., Rawat L.S., Meghvansi M.K., Mahna S.K. Selection of stress tolerant-rhizobial isolates of wild legumes growing in dry regions of Rajasthan India. ARPN J. Agric. Biol. Sci. 2009, 4:13-16.
4. Alizadeh O., Namazi L. Effect of different irrigation levels on nutrient uptake by mycorrhizal and non-mycorrhizal corn plants as affected by different soil phosphorus content. Adv. Environ. Biol. 2011, 5:2317-2321.
5. Allakhverdiev S.I., Sakamoto A., Nishiyama Y., Inaba M., Murata N. Ionic and osmotic effects of NaCl induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol. 2000, 123:1047-1056.
6. Ames B.N. Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol. 1964, 8:115-118.
7. Ashraf M., Hasnain S., Berge O., Mahmood T. Inoculating wheat seedlings with exopolysaccharide-producing bacteria restricts sodium uptake and stimulates plant growth under salt stress. Biol. Fertil. Soil 2004, 40:157-162.
8. Barka A.E., Nowk J., Clement C. Enhancement of chilling resistance of inoculated grapevine plantlets with plant growth promoting rhizobacteria Burkholderia phytofermans strain PsJN. Appl. Environ. Microbiol. 2006, 72:7246-7252.
9. Bray E.A., Bailey-Serres J., Weretilnyk E. Responses to abiotic stresses. Biochemistry and Molecular Biology of Plants 2000, 1158-1249. American Society of Plant Physiologists, Rockville, MD. W. Gruissem, B. Buchannan, R. Jones (Eds.).
10. Bui E.N. Soil salinity: a neglected factor in plant ecology and biogeography. J. Arid. Environ. 2013, 92:14-25.
11. Cappuccino J.G., Sherman N. Biochemical activities of microorganisms. Microbiology, A Laboratory Manual 1992, The Benjamin/Cummings Publishing Co., California, USA.
12. Castellanos T., Rueda-Puente E., Troyo-Dieguez E., Diaz de Leon-Alvarez J.L., Murillo-Amador B. Effects of a nitrogen-fixing indigenous bacterium (Klebsiella pneumoniae) on the growth and development of the halophyte Salicornia bigelovii as a new crop for saline environments. J. Agron. Crop Sci. 2003, 189.
13. Cheng Z., Park E., Lick G.B.R. 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of sal. Can. J. Microbiol. 2007, 53:912-918.
14. Compant S., Duffy B., Nowak J., Clément C., Barka E.A. Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl. Environ. Microbiol. 2005, 71:4951-4959.
15. Connelly M.B., Young G.M., Sloma A. Extracellular proteolytic activity plays a central role in swarming motility in Bacillus subtilis. J. Bacteriol. 2004, 186:4159-4167.
16. Contesto C., Desbrosses G., Lefoulon C., Béna G., Borel F., Galland M., Gamet L., Varoquaux F., Touraine B. Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci. 2008, 175:178-189.
17. Dimkpa C., Weinan T., Asch F. Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ. 2009, 32:1682-1694.
18. Duan J., Muller K.M., Charles T.C., Vesely S., lick G.B.R. 1-Aminocyclopropane-1-carboxylate (ACC) deaminase genes in rhizobia from Southern Saskatchewan. Microb. Ecol. 2009, 57:423-436.
19. Duxbury A.C., Yentsch C.S. Plankton pigment monographs. J. Mar. Res. 1956, 15:91-101.
20. Dworkin M., Foster J. Experiments with some microorganisms which utilize ethane and hydrogen. J. Bacteriol. 1958, 75:503-592.
21. Falkenmark M. Growing water scarcity in agriculture: future challenge to global water security. Philos. Trans. R. Soc. A 2013, 371:20120410.
22. FAO, 2008. FAO land and plant nutrition management service. http://www.fao.org/ag/agl/agll/spush.
23. Forchetti G., Masciarelli O., Alemano S., Alvarez D., Abdala G. Endophytic bacteria in sunflower (Helianthus annuus L.) isolation, characterization, and production of jasmonates and abscisic acid in culture medium. Appl. Microbiol. Biotechnol. 2007, 76:1145-1152.
24. Gehlot H.S., Panwar D., Tak A., Tak A., Sankhla I.S., Poonar N., Parihar R., Shekhawat N.S., Kumar M., Tiwari R., Ardley J., James E.K., Sprent J.I. Nodulation of legumes from the Thar desert of India and molecular characterization of their rhizobia. Plant Soil 2012, 357:227-243.
25. Geddie J.L., Sutherland I.W. Uptake of metals by bacterial polysaccharides. J. Appl. Bacteriol. 1993, 74:467-472.
26. Glick B.R. Promotion of plant growth by bacterial ACC deaminase. Crit. Rev. Plant Sci. 2007, 26:227-242.
27. Gordon S.A., Weber R.P. Colorimetric estimation of indole acetic acid. Plant Physiol. 1951, 26:192-195.
28. Gupta G., Panwar J., Jha P.N. Natural occurrence of Pseudomonas aeruginosa, a dominant cultivable diazotrophic endophytic bacterium colonizing Pennisetum glaucum (L.) R. Br. Appl. Soil Ecol. 2013, 64:252-261.
29. Han H.S., Lee K.D. Plant growth promoting rhizobacteria effect on antioxidant status, photosynthesis, mineral uptake and growth of lettuce under soil stress. Res. J. Agri. Biol. Sci. 2005, 1:210-215.
30. Harley J.P., Prescott L.M. Laboratory Exercises in Microbiology 2002, McGraw-Hill Publishers, USA. 5th ed.
31. Hoagland D.R., Boyer T.C. General nature and process of salt accumulation by roots with description of experimental methods. Plant Physiol. 1936, 11:471-507.
32. Holbrook A., Edge W., Bailey F. Spectrophotometric method for determination of gibberellic acid. Adv. Chem. Ser. 1961, 28:159-167.
33. Honma M., Shimomura T. Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric. Biol. Chem. 1978, 42:1825-1831.
34. Horie T., et al. Functions of HKT transporters in sodium transport in roots and in protecting leaves from salinity stress. Plant Biotech. 2008, 25:233-239.
35. Iniguez A.L., Dong Y., Triplett E.W. Nitrogen fixation in wheat provided by Klebsiella pneumoniae 342. Mol. Plant Microbe Interact. 2004, 17:1078-1085.
36. Jackson M.L. Soil Chemical Analysis 1967, Prentice Hall of Indian Private Limited, New Delhi.
37. Jha B., Gontia I., Hartmann A. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil 2011, 356:265-277.
38. Jha C.K., Annapurna K., Saraf M. Isolation of Rhizobacteria from Jatropha curcas and characterization of produced ACC deaminase. J. Basic Microbiol. 2012, 52:85-95.
39. Kalra A., Barnawal D., Bharti N., Maji D., Chanotiya C.S. ACC deaminase-containing Arthrobacter protophormiae induces NaCl stress tolerance through reduced ACC oxidase activity and ethylene production resulting in improved nodulation and mycorrhization in P. sativum. Plant Physiol. 2014, 171:884-894.
40. Karthikeyan B., Joe M.M., Islam M.R., Sa T. ACC deaminase containing diazotrophic endophytic bacteria ameliorate salt stress in Catharanthus roseus through reduced ethylene levels and induction of antioxidative defense systems. Symbiosis 2012, 56:77-86.
41. Li J., Ovakim D.H., Charles T.C., Glick B.R. An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Curr. Microbiol. 2000, 41:101-105.
42. Li W., Raoult D., Fournier P. Bacterial strain typing in the genomic era. FEMS Microbiol. Rev. 2009, 33:892-916.
43. Liu W., Yuan X., Zhang Y., Xuan Y., Yan Y. Effects of salt stress and exogenous Ca2+ on Na+ compartmentalization, ion pump activities of tonoplast and plasma membrane in Nitraria tangutorum Bobr. leaves. Acta Physiol. Plant 2014, 36:2183-2193.
44. Lugtenberg B.J., Dekkers L., Bloemberg G.V. Molecular determinants of rhizosphere colonization by Pseudomonas. Annu. Rev. Phytopathol. 2001, 39:461-490.
45. Maathuis F.J.M., Ahmad I., Patishtan J. Regulation of Na+ fluxes in plants. Front. Plant Sci. 2014, 5. 467.
46. Mayak S., et al. Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol. Biochem. 2004, 42:565-572.
47. Mehta S., Nautiyal C.S. An efficient method for qualitative screening of phosphate solubilizing bacteria. Curr. Microbiol. 2001, 43:51-56.
48. Morris C.E., Monier J., Jacques M. Methods for observing microbial biofilms directly onleaf surfaces and recovering them for isolation of culturable microorganisms. Appl. Environ. Microbiol. 1997, 63:1570-1576.
49. Nadeem S.M., Zahir Z.A., Naveed M., Arshad M., Shahzad S.M. Variation in growth and ion uptake of maize due to inoculation with plant growth promoting rhizobacteria under salt stress. Soil Environ. 2006, 25:78-84.
50. Nascimento F.X., Rossi M.J., Soares C.R.F.S., McConkey B.J., Glick B.R. New insights into 1-aminocyclopropane-1-carboxylate (ACC) deaminase phylogeny, evolution and ecological significance. PLoS One 2014, 9(6):e99168.
51. Olsen S.R., Cole C.V., Watanabe F.S., Dean L.A. Estimation of Available Phosphorus in Soils by Extraction with Sodium Bicarbonate 1954, Circular 939 US Department of Agriculture, Washington DC, USA.
52. Onofre-Lemus Janette, Hernández-Lucas Ismael, Girard Lourdes, Caballero-Mellado Jesús ACC (1-aminocyclopropane-1-carboxylate) deaminase activity, a widespread trait in Burkholderia species, and its growth-promoting effect on tomato plants. Appl. Environ. Microbiol. 2009, 75:6581-6590.
53. Parida S.K., Das A.B. Salt tolerance and salinity effects on plants. Ecotoxicol. Environ. Saf. 2005, 60:324-349.
54. Penrose D.M., Glick B.R. Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol. Plant. 2003, 118:10-15.
55. Rashid S., Charles T.C., Glick B.R. Isolation and characterization of new plant growth- promoting bacterial endophytes. App. Soil Ecol. 2012, 61:217-224.
56. Rodriguez-Rosales M.P., Jiang X., Galvez F.J., Aranda M.N., Cubero B., Venema K. Overexpression of the tomato K+/H+ antiporter LeNHX2 confers salt tolerance by improving potassium compartmentalization. New Phytol. 2008, 179:366-377.
57. Sachdev D.P., Chaudhari H.G., Kasture V.M., Dhavale D.D., Chopade B.A. Isolation and characterization of indole acetic acid (IAA) producing Klebsiella pneumoniae strains from rhizosphere of wheat (Triticum aestivum) and their effect on plant growth. Indian J. Exp. Biol. 2009, 447:993-1000.
58. Saravanakumar D., Samiyappan R. ACC deaminase from Pseudomonas Xuorescens mediated saline resistance in groundnut (Arachis hypogea) plants. J. Appl. Microbiol. 2007, 102:1283-1292.
59. Schwyn B., Neilands J.B. Universal chemical assay for the detection and determination of siderophores. Anal. Biochem. 1987, 160:47-56.
60. Shabala S., Cuin T.A. Potassium transport and plant salt tolerance. Physiol. Plant. 2008, 133:651-669.
61. Shaharoona B., Arshad M., Khalid A. Differential response of etiolated pea seedling to 1-aminocyclopropane-1-carboxylate and/or l-methionine utilizing rhizobacteria. Microbiol 2007, 45:15-20.
62. Sheng Q., Zhang Y.J., Yuan B., Xu P.Y., Xing K., Wang J., Jiang J.H. 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 2014, 374:753-766.
63. Siddikee M.A., Glick B.R., Chauhan P.S., Yim W.J., Sa Ta Enhancement of growth and salt tolerance of red pepper seedlings (Capsicum annuum L.) by regulating stress ethylene synthesis with halotolerant bacteria containing 1-aminocyclopropane-1-carboxylic acid deaminase activity. Plant Physiol. Biochem. 2011, 49:427-434.
64. Siddikee M.A., Chauhan P.S., Sa T. 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. 2012, 31:265-272.
65. Shrivastava U.P., Kumar A. Characterization and optimization of 1-aminocyclopropane-1-carboxylate deaminase (ACCD) activity in different rhizospheric PGPR with microbacterium sp. strain ECI-12A. Int. J. Appl. Sci. Biotechnol. 2013, vol. 1:11-15.
66. Syrmis M.W., O'Carroll M.R., Sloots T.P., Coulter C., Wainwright C.E., Bell S.C., Nissen M.D. Rapid genotyping of Pseudomonas aeruginosa isolates harboured by adult and paediatric patients with cystic fibrosis using repetitive-elementbased PCR assays. J. Med. Microbiol. 2004, 53:1089-1096.
67. Tamura K., Stecher G., Peterson D., Filipski A., Kumar S. MEGA6: molecular evolutionary genetics analysis version 6. 0. Mol. Biol. Evol. 2013, 30:2725-2729.
68. Tittabutr P., Piromyou P., Longtonglang A., Noisa-Ngiam R., Boonkerd N., Teaumroong N. Alleviation of the effect of environmental stresses using co-inoculation of mungbean by Bradyrhizobium and rhizobacteria containing stress-induced ACC deaminase enzyme. Soil Sci. Plant Nutr. 2013, 59:559-571.
69. Venkateswarlu B., Desai S., Prasad Y.G. Agriculturally important microorganisms for stressed ecosystems: challenges in technology development and application. Agriculturally Important Microorganisms 2008, vol. 1:225-246. Academic World, Bhopal.
70. Walkley A.J., Black I.A. Estimation of soil organic carbon by the chromic acid titration method. Soil Sci. 1934, 37:29-38.
71. Wang W.X., Barak T., Vinocur B., Shoseyov O., Altman A. A Biotic Resistance and Chaperones: Possible Physiological Role of SP1, a Stable and Stabilizing Protein from Populus 2003, 439-443. Kluwer, Dordrecht.
72. Yang J., Kloepper J.W., Ryu C.M. Rhizosphere bacteria help plants tolerate abiotic stress. Trends Plant Sci. 2009, 14:1-4.
73. Zhang H., Kim M.-S., Sun Y., Dowd S.E., Shi H., Pare P.W. Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol. Plant Microbe Interact. 2008, 21:737-744.
74. Zhang J.L., Shi H. Physiological and molecular mechanisms of plant salt tolerance. Photosynth. Res. 2013, 115:1-22.