Journal of Plant Growth Regulation

, Volume 33, Issue 3, pp 654–670 | Cite as

Bacterial Biosynthesis of 1-Aminocyclopropane-1-Carboxylate (ACC) Deaminase and Indole-3-Acetic Acid (IAA) as Endophytic Preferential Selection Traits by Rice Plant Seedlings

  • Hassan Etesami
  • Hossein Mirsyed Hosseini
  • Hossein Ali Alikhani
  • Leila Mohammadi
Article

Abstract

In this study, bacteria were isolated from the rhizosphere and inside the roots and nodules of berseem clover plants grown in the field in Iran. Two hundred isolates were obtained from the rhizosphere (120 isolates), interior roots (57 isolates), and nodules (23 isolates) of clover plants grown in rotation with rice plants. Production of chitinase, pectinase, cellulase, siderophore, salicylic acid, hydrogen cyanide, indole acetic acid (IAA), 1-aminocyclopropane-1-carboxylate (ACC) deaminase, solubilization of phosphate, antifungal activity against various rice plant pathogen fungi, N2 fixation, and colonization assay on rice seedlings by these strains was evaluated and compared (endophytic isolates vs. rhizosphere bacteria). The results showed both the number and the ability of plant growth-promoting (PGP) traits were different between endophytic and rhizosphere isolates. A higher percentage of endophytic isolates were positive for production of IAA, ACC deaminase, and siderophore than rhizosphere isolates. Therefore, it is suggested that clover plant may shape its own associated microbial community and act as filters for endophyte communities, and rhizosphere isolates with different (PGP) traits. We also studied the PGP effect of the most promising endophytic and rhizosphere isolates on rice seedlings. A significant relationship among IAA and ACC deaminase production, the size of root colonization, and plant growth (root elongation) in comparison with siderophore production and phosphate solubilization for the isolates was observed. The best bacterial isolates (one endophytic isolate and one rhizosphere isolate), based on their ability to promote rice growth and colonize rice roots, were identified. Based on 16S rDNA sequence analysis, the endophytic isolate CEN7 and the rhizosphere isolate CEN8 were closely related to Pseudomonas putida and Pseudomonas fluorescens, respectively. It seems that PGP trait production (such as IAA, ACC deaminase) may be required for endophytic and rhizosphere competence as compared to other PGP traits in rice seedlings under constant flooded conditions. The study also shows that the presence of diverse rhizobacteria with effective growth-promoting traits associated with clover plants may be used for sustainable crop management under field conditions.

Keywords

Rhizobacteria Berseem clover Rice PGPR PGP traits Endophytic bacteria 

References

  1. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181CrossRefPubMedGoogle Scholar
  2. Arshad M (2007) Perspectives of bacterial ACC deaminase in phytoremediation. Trends Biotechnol 25:356–362CrossRefPubMedGoogle Scholar
  3. Bagwell C, Piceno Y, Ashburne A, Lovell C (1998) Physiological diversity of the rhizosphere diazotroph assemblages of selected salt marsh grasses. Appl Environ Microbiol 66:1609–1616Google Scholar
  4. Belimova AA, Hontzeasb N, Safronovaa VI, Demchinskayaa SV, Piluzzac G, Bullittac S, Glick BR (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biol Biochem 37:241–250CrossRefGoogle Scholar
  5. Benizri E, Baudoin E, Guckert A (2001) Root colonization by inoculated plant growth promoting rhizobacteria. Biocontrol Sci Technol 11:557–574CrossRefGoogle Scholar
  6. Bhattacharjee RB, Singh A, Mukhopadhyay SN (2008) Use of nitrogen-fixing bacteria as biofertiliser for non-legumes: prospects and challenges. Appl Microbiol Biotechnol 80:199–209CrossRefPubMedGoogle Scholar
  7. Bhattacharyya PN, Jha DK (2012) Plant growth promoting rhizobacteria (PGPR): emergence in agriculture. World J Microbiol Biotechnol 28:1327–1350CrossRefPubMedGoogle Scholar
  8. Bhusan Bal H, Das S, Tushar K, Adhya TK (2013) ACC deaminase and IAA producing growth promoting bacteria from the rhizosphere soil of tropical rice plants. J Basic Microbiol 00:1–13Google Scholar
  9. Brandl MT, Lindow SE (1998) Contribution of indole-3-acetic acid production to the epiphytic fitness of Erwinia herbicola. Appl Environ Microbiol 64:3256–3263PubMedCentralPubMedGoogle Scholar
  10. Chanway CP, Shishido M, Nairn J, Jungwirth S, Markham J, Xiao G, Holl FB (2000) Endophytic colonization and field responses of hybrid spruce seedlings after inoculation with plant growth-promoting rhizobacteria. For Ecol Manag 133:81–88CrossRefGoogle Scholar
  11. Cheng ZY (2007) 1-Aminocyclopropane-1-carboxylate deaminase from Pseudomonas putida UW4 facilitates the growth of canola in the presence of salt. Can J Microbiol 53:912–918CrossRefPubMedGoogle Scholar
  12. Chi F, Shen SH, Cheng HP, Jing YX, Yanni YG, Dazzo FB (2005) Ascending migration of endophytic rhizobia, from roots to leaves, inside rice plants and assessment of benefits to rice growth physiology. Appl Environ Microbiol 71:7271–7278PubMedCentralCrossRefPubMedGoogle Scholar
  13. Compant S, Duffy B, Nowak J, Clément C, Barka EA (2005a) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959PubMedCentralCrossRefPubMedGoogle Scholar
  14. Compant S, Reiter B, Sessitsch A, Nowak J, Clement C, Ait Barka E (2005b) Endophytic colonization of Vitis vinifera L. by plant growth-promoting bacterium Burkholderia sp. strain PsJN. Appl Environ Microbiol Res 71:1685–1693CrossRefGoogle Scholar
  15. Dobbelaere S, Croonenborghs A, Thys A, Broek AV, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasiliense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164CrossRefGoogle Scholar
  16. Dobereiner J (1989) Isolation and identification of root associated diazotrophs. Plant Soil 110:207–212CrossRefGoogle Scholar
  17. Elbeltagy A, Nishioka K, Suzuki H, Sato T, Sato Y, Morisaki H, Mitsui H, Minamisawa K (2000) Isolation and characterization of endophytic bacteria from wild and traditionally cultivated rice varieties. Soil Sci Plant Nutr 46:617–629CrossRefGoogle Scholar
  18. Elliot LF, Lynch JM (1984) Pseudomonads as a factor in the growth of winter wheat (Triticum aestivum L.). Soil Biol Biochem 16:69–71CrossRefGoogle Scholar
  19. Elvira-Recuenco M, Van Vuurde JW (2000) Natural incidence of endophytic bacteria in pea cultivars under field conditions. Can J Microbiol 46:1036–1041CrossRefPubMedGoogle Scholar
  20. Gerhardt P, Murray RGE, Costilow RN, Wester EW (1994) Methods for general bacteriology. American Society for Microbiology, New YorkGoogle Scholar
  21. Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 4:109–117CrossRefGoogle Scholar
  22. Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312CrossRefPubMedGoogle Scholar
  23. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012:1–15CrossRefGoogle Scholar
  24. Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796PubMedCentralPubMedGoogle Scholar
  25. Hallmann J (1997) Bacterial endophytes in agricultural crops bacterial endophytes in agricultural crops. Can J Microbiol 43:895–914CrossRefGoogle Scholar
  26. Hardoim PR, van Overbeek LS, Elsas JD (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends Microbiol 16:463–471CrossRefPubMedGoogle Scholar
  27. Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol Res 70:2667–2677CrossRefGoogle Scholar
  28. Iniguez AL, Dong Y, Carter HD, Ahmer BMM, Stone JM, Triplett EW (2005) Regulation of enteric endophytic bacterial colonization by plant defenses. Mol Plant Microbe Interact 18:169–178CrossRefPubMedGoogle Scholar
  29. James EK, Gyaneshwar P, Mathan N, Barraquio WL, Reddy PM, Iannetta PPM, Olivars FL, Ladha JK (2002) Infection and colonization of rice seedlings by the plant growth-promoting bacterium Herbaspirillum seropedicae Z 67. Mol Plant Microbiol Interact 15:894–906CrossRefGoogle Scholar
  30. Jinantana J, Sariah M (1997) Antagonistic effect of Malaysian isolates of Trichoderma harzianum and Gliocladium virens on Sclerotium rolfsii. Pertanika J Trop Agric Sci 20:35–41Google Scholar
  31. Khalid A, Arshad M, Zahir ZA (2005) Screening plant growth promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480CrossRefGoogle Scholar
  32. Kobayashi DY, Palumbo JD (2000) Bacterial endophytes and their effects on plants and uses in agriculture. In: Bacon CW, White JF (eds) Microbial endophytes. Marcel Dekker, New York, pp 199–233Google Scholar
  33. Kucera B (2005) Plant hormone interactions during seed dormancy release and germination. Seed Sci Res 15:281–307CrossRefGoogle Scholar
  34. Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251CrossRefPubMedGoogle Scholar
  35. Loaces I, Ferrando L, Fernández Scavino A (2011) Dynamics, diversity and function of endophytic siderophore-producing bacteria in rice. Microb Ecol 61:606–618CrossRefPubMedGoogle Scholar
  36. Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:142–146CrossRefGoogle Scholar
  37. Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556CrossRefPubMedGoogle Scholar
  38. Madhaiyan M, Poonguzhali S, Senthilkumar M (2004) Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L.) by Methylobacterium sp. Bot Bull Acad Sin 45:315–324Google Scholar
  39. Martinez-Viveros O, Jorquera M, Crowley DE, Gajardo G, Mora ML (2010) Mechanisms and practical considerations involved in plant growth promotion by rhizobacteria. J Soil Sci Plant Nutr 10:293–319CrossRefGoogle Scholar
  40. Mateos PF, Jimenez-Zurdo JI, Chen J, Squartini AS, Haack SK, Martinez-Molina E, Hubbell DH, Dazzo FB (1992) Cell-associated pectinolytic and cellulolytic enzymes in Rhizobium leguminosarum bv. trifolii. Appl Environ Microbiol 58:1816–1822PubMedCentralPubMedGoogle Scholar
  41. Mayak S, Tirosh T, Glick BR (2004) Plant growth promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572CrossRefPubMedGoogle Scholar
  42. Mendes R, Pizzirani-Kleiner AA, Araujo WL, Raaijmakers JM (2007) Diversity of cultivated endophytic bacteria from sugarcane: genetic and biochemical characterization of Burkholderia cepacia complex isolates. Appl Environ Microbiol 73(22):7259–7267PubMedCentralCrossRefPubMedGoogle Scholar
  43. Meyer JM, Azelvandre P, Georges C (1992) Iron metabolism in Pseudomonas: salicylic acid, a siderophore of Pseudomonas fluorescens CHAO. Biofactors 4:23–27PubMedGoogle Scholar
  44. Miethke M, Marahiel M (2007) Siderophore-based iron acquisition and pathogen control. Microbiol Mol Biol 71(3):413–451CrossRefGoogle Scholar
  45. Montealegre JR, Reyes R, Pérez LM, Herrera R, Silva P, Besoain X (2003) Selection of bioantagonistic bacteria to be used in biological control of Rhizoctonia solani in tomato. Electron J Biotechnol 6:115–127CrossRefGoogle Scholar
  46. Oliveira ALM, Urquiaga S, Döbereiner J, Baldani JI (2002) The effect of inoculating endophytic N2-fixing bacteria on micropropagated sugarcane plants. Plant Soil 242:205–215CrossRefGoogle Scholar
  47. Pajand N, Paul AJ (2000) Endophytic bacteria induce growth promotion and wilt disease suppression in oilseed rape and tomato. Biol Control 18:208–215CrossRefGoogle Scholar
  48. Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801PubMedCentralCrossRefPubMedGoogle Scholar
  49. Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth promoting rhizobacteria. Physiol Plant 118:10–15CrossRefPubMedGoogle Scholar
  50. Pikovskaya RI (1948) Mobilization of phosphorus in soil connection with the vital activity of some microbial species. Microbiologiya 17:362–370Google Scholar
  51. Rashid S, Charles TC, Glick BR (2012) Isolation and characterization of new plant growth-promoting bacterial endophytes. Appl Soil Ecol 61:217–224CrossRefGoogle Scholar
  52. Reinhold-Hurek B, Hurek T (1998) Life in grasses: diazotrophic endophytes. Trends Microbiol 6:139–144CrossRefPubMedGoogle Scholar
  53. Richardson AE (2001) Prospects for using soil microorganisms to improve the acquisition of phosphorus by plants. Aust J Plant Physiol 28:897–906Google Scholar
  54. Rosenblueth M, Martinez Romero E (2004) Rhizobium etli maize populations and their competitiveness for root colonization. Arch Microbiol Res 181:337–344CrossRefGoogle Scholar
  55. Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interaction with hosts. Mol Plant Microbe Interact 19:827–837CrossRefPubMedGoogle Scholar
  56. Sandhu A, Halverson LJ, Beattie GA (2009) Identification and genetic characterization of phenol-degrading bacteria from leaf microbial communities. Microb Ecol 57:276–285CrossRefPubMedGoogle Scholar
  57. Schwyn B, Neilands J (1987) Universal chemical assays for the detection and determination of siderophores. Anal Biochem 160:47–56CrossRefPubMedGoogle Scholar
  58. Sessitsch A, Reiter B, Pfeifer U, Wilhelm E (2002) Cultivation-independent population analysis of bacterial endophytes in three potato varieties based on eubacterial and Actinomycetes-specific PCR of 16S rRNA genes. FEMS Microbiol Ecol 39:23–32CrossRefPubMedGoogle Scholar
  59. Shah J (2009) Plants under attack: systemic signals in defence. Curr Opin Plant Biol 12:459–464CrossRefPubMedGoogle Scholar
  60. 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 42:155–159CrossRefPubMedGoogle Scholar
  61. Silva HSA, Silva RDS, Mounteer A (2003) Development of a root colonization bioassay for rapid screening of rhizobacteria for potential biocontrol agents. J Phytopathol 151:42–46CrossRefGoogle Scholar
  62. Sturz AV, Christie BR, Matheson BG, Nowak JB (1997) Diversity of endophytic bacteria which colonize red clover nodules, roots, stems and foliage and their influence on host growth. Biol Fertil Soils 25:13–19CrossRefGoogle Scholar
  63. Teaumroong N, Teamtaisong K, Sooksa-ngun T, Boonkerd N (2001) The dizotrophic endophytic bacteria in Thai rice. In: Suriyaphan O, Hansakdi E, Jongruaysup S, Simons R (eds) Proceeding of the fifth ESAFS international conference on rice environments and rice products, Krabi, pp 147–160Google Scholar
  64. van Loon LC (2000) Systemic acquired resistance. In: Fraser RSS, Van Loon LC, Slusarenko AJ (eds) Mechanisms of resistance to plant diseases. Kluwer, Dordrecht, pp 521–574CrossRefGoogle Scholar
  65. Verma SC, Ladha JK, Tripathi AK (2001) Evaluation of plant growth promoting and colonization ability of endophytic diazotrophs from deep water rice. J Biotechnol 91:127–141CrossRefPubMedGoogle Scholar
  66. Wang LL, Wang ET, Liu JLY, Chen WX (2006) Endophytic occupation of root nodules and roots of Melilotus dentatus by Agrobacterium tumefaciens. Microb Ecol 52:436–443CrossRefPubMedGoogle Scholar
  67. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009) Phytoremediation: planteendophyte partnerships take the challenge. Curr Opin Biotechnol 20:248–254CrossRefPubMedGoogle Scholar
  68. Yanni YG, Rizk RY, Corich V, Squartini A, Ninke K, Philip-Hollingsworth S, Orgambide G, deBruijn F, Stoltzfus J, Buckley D, Schmidt TM, Mateos PF, Ladha JK, Dazzo FB (1997) Natural endophytic association between Rhizobium leguminosarum bv. trifolii and rice roots and assessment of its potential to promote rice growth. Plant Soil 194:99–114CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Hassan Etesami
    • 1
  • Hossein Mirsyed Hosseini
    • 1
  • Hossein Ali Alikhani
    • 1
  • Leila Mohammadi
    • 1
  1. 1.Soil Science Department, Faculty of Agricultural Engineering and Technology, College of Agriculture & Natural ResourcesUniversity of TehranKarajIran

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