Skip to main content
Log in

Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

We report the presence of ACC deaminase in Methylobacterium fujisawaense and its lowering of ethylene levels and promotion of root elongation in canola seedlings under gnotobiotic conditions. To test a part of the previous model proposed for ACC deaminase producing bacteria with Methylobacterium, ACC levels and various enzyme activities were monitored in canola. Lower amounts of ACC were present in the tissues of seeds treated with M. fujisawaense strains than in control seeds treated with MgSO4. Though the increased activities of ACC synthase in the tissue extracts of the treated seedlings might be due to bacterial indole-3-acetic acid, the amount of ACC was reduced due to bacterial ACC deaminase activity. The activities of ACC oxidase, the enzyme catalyzing conversion of ACC to ethylene remained lower in M. fujisawaense treated seedlings. This consequently lowered the ethylene in plants and prevented ethylene inhibition of root elongation. Our results collectively suggest that Methylobacterium commonly found in soils, as well as on the surfaces of leaves, seeds, and in the rhizosphere of a wide variety of plants could be better exploited to promote plant growth.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Abbreviations

ACC:

1-aminocyclopropane-1-carboxylate

ACO:

ACC oxidase

ACS:

ACC synthase

AMS:

Ammonium mineral salts

AVG:

l-α-(2-aminoethoxyvinyl) glycine hydrochloride

CFU:

Colony-forming units

IAA:

Indole-3-acetic acid

iPA:

Isopentenyladenosine

MTA:

5′-methylthioadenosine

PGPR:

Plant growth promoting rhizobacteria

PLP:

Pyridoxal phosphate

PPFMs:

Pink-pigmented facultative methylotrophic bacteria

PVPP:

Polyvinylpolypyrrolidone

SAM:

S-adenosyl methionine

t-ZR:

trans-Zeatin riboside

References

  • Abeles FB, Morga PW, Saltveit ME (1992) Ethylene in plant biology. Academic, San Diego

    Google Scholar 

  • Adams DO, Yang SF (1979) Ethylene biosynthesis: identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci USA 76:170–174

    Article  PubMed  CAS  Google Scholar 

  • Bayliss C, Bent E, Culham DE, MacLellan S, Clarke AJ, Brown GL, Wood JM (1997) Bacterial genetic loci implicated in the Pseudomonas putida GR12-2R3-canola mutualism: identification of an exudate-inducible sugar transporter. Can J Microbiol 43:809–818

    Article  PubMed  CAS  Google Scholar 

  • Belimov AA, Safronova VI, Sergeyeva TA, Egorova TN, Matveyeva VA, Tsyganov VE, Borisov AY, Tikhonovich IA, Kluge C, Preisfeld A, Dietz KJ, Stepanok VV (2001) Characterization of plant growth promoting rhizobacteria isolated from polluted soils and containing 1-aminocyclopropane-1-carboxylate deaminase. Can J Microbiol 47:642–652

    Article  PubMed  CAS  Google Scholar 

  • Bleecker AB, Kende H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18

    Article  PubMed  CAS  Google Scholar 

  • Butler HK, Dadson R, Holland MA (2000) Evidence that trans-zeatin riboside produced by a microbial symbiont is physiologically meaningful to its host plant (abstract available at http://www.abstracts.aspb.org/aspp2000/public/P43/0604.html)

  • Dworkin M, Foster J (1958) Experiments with some microorganisms which utilize ethane and hydrogen. J Bacteriol 75:592–601

    PubMed  CAS  Google Scholar 

  • Fluhr R, Mattoo AK (1996) Ethylene: biosynthesis and perception. Crit Rev Plant Sci 15:479–523

    Article  CAS  Google Scholar 

  • Freyermuth SK, Long RLG, Mathur S (1996) Metabolic aspects of plant interaction with commensal methylotrophs. In: Lidstrom ME, Tabita FR (eds) Microbial growth on C1 compounds. Kluwer, The Netherlands, pp 277–284

    Google Scholar 

  • Ghosh S, Penterman JN, Little RD, Chavez R, Glick BR (2003) Three newly isolated plant growth-promoting bacilli facilitate the seedling growth of canola, Brassica campestris. Plant Physiol Biochem 41:277–281

    Article  CAS  Google Scholar 

  • Glick BR (2004) Bacterial ACC deaminase and the alleviation of plant stress. Adv Appl Microbiol 56:291–312

    Article  PubMed  CAS  Google Scholar 

  • Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth-promoting bacteria. J Theor Biol 190:63–68

    Article  PubMed  CAS  Google Scholar 

  • Green PN (1992) The genus Methylobacterium. In: Balows A, Trüper HG, Dworkin M, Harder W, Schleifer KH (eds), The prokaryotes, 2nd edn. vol III. Springer, Berlin Heidelberg New York, pp 2342–2349

  • Holland MA (1997) Methylobacterium and plants. Rec Res Dev Plant Physiol 1:207–213

    Google Scholar 

  • Holland MA, Polacco JC (1992) Urease-null and hydrogenase-null phenotypes of a phylloplane bacterium reveal altered nickel metabolism in two soybean mutants. Plant Physiol 98:942–948

    Article  PubMed  CAS  Google Scholar 

  • Honma M, Shimomura T (1978) Metabolism of 1-aminocyclopropane-1-carboxylic acid. Agric Biol Chem 42:1825–1831

    CAS  Google Scholar 

  • Khalafalla MM, Hattori K (2000) Ethylene inhibitors enhance in vitro root formation on faba bean shoots regenerated on medium containing thidiazuron. Plant Growth Regul 32:59–63

    Article  CAS  Google Scholar 

  • Koenig RL, Morris RO, Polacco JC (2002) tRNA is the source of low-level trans-Zeatin production in Methylobacterium spp. J Bacteriol 184:1832–1842

    Article  PubMed  CAS  Google Scholar 

  • Lehman A, Black R, Ecker JR (1996) HOOKLESS1, an ethylene response gene, is required for differential cell elongation in the Arabidopsis hypocotyl. Cell 85:183–194

    Article  PubMed  CAS  Google Scholar 

  • Li J, Ovakim DH, Charles TC, Glick BR (2000) An ACC deaminase minus mutant of Enterobacter cloacae UW4 no longer promotes root elongation. Curr Microbiol 41:101–105

    Article  PubMed  CAS  Google Scholar 

  • Lizada MCC, Yang SF (1979) A simple and sensitive assay for 1-aminocyclopropane-1-carboxylic acid. Anal Biochem 100:142–147

    Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with folin-phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  • Ma JH, Yao JL, Cohen D, Morris B (1998) Ethylene inhibitors enhance in vitro root formation from apple shoot cultures. Plant Cell Rep 17:211–214

    Article  CAS  Google Scholar 

  • Ma W, Sebestianova SB, Sebestian J, Burd GI, Guinel FC, Glick BR (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Anton Leeuw Int J G 83:285–291

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Senthilkumar M, Seshadri S, Chung HY, Yang JC, Sundaram SP, Sa TM (2004) Growth promotion and induction of systemic resistance in rice cultivar Co-47 (Oryza sativa L.) by Methylobacterium spp. Bot Bull Acad Sin 45:315–324

    Google Scholar 

  • Madhaiyan M, Poonguzhali S, Lee HS, Hari K, Sundaram SP, Sa TM (2005a) Pink-pigmented facultative methylotrophic bacteria accelerate germination, growth and yield of sugarcane clone Co86032 (Saccharum officinarum L.). Biol Fertil Soils 41:350–358

    Article  CAS  Google Scholar 

  • Madhaiyan M, Poonguzhali S, Sundaram SP, Sa TM (2005b) A new insight into foliar applied methanol influencing phylloplane methylotrophic dynamics and growth promotion of cotton (Gossypium hirsutum L.) and sugarcane (Saccharum officinarum L.). Environ Exp Bot (published online 15 September 2005)

  • Malerba M, Crosti P, Armocida D, Bianchetti R (1995) Activation of ethylene production in Acer pseudoplatanus L. cultured cells by fusicoccin. J Plant Physiol 145:93–100

    CAS  Google Scholar 

  • Mattoo AK, Suttle JC (1991) The plant hormone ethylene. CRC Press, Boca Raton, 337 pp

    Google Scholar 

  • Mayak S, Tirosh T, Glick BR (1999) Effect of wild-type and mutant plant growth-promoting rhizobacteria on the rooting of mung bean cuttings. J Plant Growth Regul 18:49–53

    Article  PubMed  CAS  Google Scholar 

  • Penrose DM, Glick BR (2001) Levels of ACC and related compounds in exudate and extracts of canola seeds treated with ACC deaminase containing plant growth-promoting bacteria. Can J Microbiol 47:368–372

    Article  PubMed  CAS  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  PubMed  CAS  Google Scholar 

  • Petruzzelli L, Coraggio I, Leubner-Metzger G (2000) Ethylene promotes ethylene biosynthesis during pea seed germination by positive feedback regulation of 1-aminocyclo-propane-1-carboxylic acid oxidase. Planta 211:144–149

    Article  PubMed  CAS  Google Scholar 

  • SAS Institute Inc. (2001) SAS user’s guide, version 8.2, SAS Institute Inc., Cary, North Carolina

  • Satoh S, Oyamada N, Yoshioka T, Midoh N (1997) 1,1-Dimethyl-4-(phenylsulfonyl)semicarbazide (DPSS) does not inhibit the in vitro activities of 1-aminocyclopropane-1-carboxylate (ACC) oxidase and ACC synthase obtained from senescing carnation (Dianthus caryophyllus L.) petals. Plant Growth Regul 23:191–193

    Article  CAS  Google Scholar 

  • Schaller GE, Kieber JJ (2002) Ethylene. The Arabidopsis book. American Society of Plant Biologists, USA

    Google Scholar 

  • Shah S, Li J, Moffatt BA, Glick BR (1998) Isolation and characterization of ACC deaminase genes from two different plant growth promoting rhizobacteria. Can J Microbiol 44:833–843

    Article  PubMed  CAS  Google Scholar 

  • Stearns JC, Shah S, Greenberg BM, Dixon DG, Glick BR (2005) Tolerance of transgenic canola expressing 1-aminocyclopropane-1-carboxylic acid deaminase to growth inhibition by nickel. Plant Physiol Biochem 43(7):701–708

    Article  PubMed  CAS  Google Scholar 

  • Swarup R, Parry G, Graham N, Allen T, Bennett M (2002) Auxin cross-talk: integration of signalling pathways to control plant development. Plant Mol Biol 49:411–426

    Article  PubMed  CAS  Google Scholar 

  • Trotsenko YA, Ivanova EG, Doronina NV (2001) Aerobic methylotrophic bacteria as phytosymbionts. Microbiology 70:725–736

    Article  PubMed  Google Scholar 

  • Wachter R, Fischer K, Gabler R, Kuhnemann F, Urban W, Bogemann GM, Voesenek LACJ, Blom CWPM, Ullrich CI (1999) Ethylene production and ACC accumulation Agrobacterium tumefaciens-induced plant tumours and their impact on tumour and host stem structure and function. Plant Cell Environ 22:1263–1273

    Article  CAS  Google Scholar 

  • Yi HC, Joo S, Nam KH, Lee JS, Kang BG, Kim WT (1999) Auxin and brassinosteroid differentially regulate the expression of three members of the 1-aminocyclopropane-1-carboxylate synthase gene family in mung bean (Vigna radiata L.). Plant Mol Biol 41:443–454

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Korea Research Foundation, under the Foreign Scientist and Engineers programme research awarded to M. Madhaiyan and Rural Development Administration (RDA), Republic of Korea. The authors wish to thank anonymous referees for their valuable comments on the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Tongmin Sa.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Madhaiyan, M., Poonguzhali, S., Ryu, J. et al. Regulation of ethylene levels in canola (Brassica campestris) by 1-aminocyclopropane-1-carboxylate deaminase-containing Methylobacterium fujisawaense . Planta 224, 268–278 (2006). https://doi.org/10.1007/s00425-005-0211-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-005-0211-y

Keywords

Navigation