Skip to main content

Arabidopsis as a Model System to Decipher the Diversity and Complexity of Plant Responses to Plant-Growth-Promoting Rhizobacteria

  • Chapter
  • First Online:
Book cover Bacteria in Agrobiology: Plant Probiotics

Abstract

The mechanisms involved in the stimulation of plant growth by plant-growth-promoting rhizobacteria (PGPR) remained obscure until the very end of twentieth century. In the last decade, investigations on the plant partner of plant–PGPR interaction have begun to unveil the diversity and complexity of mechanisms behind growth promotion. These studies that used the model plant Arabidopsis to identify plant signaling pathways modulated by PGPR provide new paradigms on how rhizobacteria modify plant development and nutrition. This chapter presents insights on PGPR-elicited developmental and nutritional regulations that have been obtained. Overall, the emerging picture is the concomitant elicitation of a variety of regulatory mechanisms that only begin to be identified as mediators of plant responses. It leaves large gaps in our knowledge, especially on primary PGPR targets and molecular events linking PGPR with individual plant regulatory pathways, and on the integration of these regulations within a probably complex cross talk network.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Abeles FB, Morgan PW, Salveit MEJ (1992) Ethylene in plant biology, 2nd edn. Academic, San Diego, CA, p 414

    Google Scholar 

  • Babalola O (2010) Beneficial bacteria of agricultural importance. Biotechnol Lett 32:1559–1570

    Article  PubMed  CAS  Google Scholar 

  • Barbieri P, Galli E (1993) Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Res Microbiol 144:69–75

    Article  PubMed  CAS  Google Scholar 

  • Bashan Y, Holguin G, de-Bashan LE (2004) Azospirillum-plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577

    Article  PubMed  CAS  Google Scholar 

  • Benjamins R, Scheres B (2008) Auxin: the looping star in plant development. Annu Rev Plant Biol 59:443–465

    Article  PubMed  CAS  Google Scholar 

  • Berthomieu P, Conejero G, Nublat A, Brackenbury WJ, Lambert C, Savio C, Uozumi N, Oiki S, Yamada K, Cellier F, Gosti F, Simonneau T, Essah PA, Tester M, Very A-A, Sentenac H, Casse F (2003) Functional analysis of AtHKT1 in Arabidopsis shows that Na+ recirculation by the phloem is crucial for salt tolerance. EMBO J 22:2004–2014

    Article  PubMed  CAS  Google Scholar 

  • Bertrand H, Plassard C, Pinochet X, Touraine B, Normand P, Cleyet-Marel J-C (2000) Stimulation of the ionic transport system in Brassica napus by a plant growth-promoting rhizobacterium (Achromobacter sp.). Can J Bot 46:229–236

    CAS  Google Scholar 

  • Bertrand H, Nalin R, Bally R, Cleyet-Marel J-C (2001) Isolation and identification of the most efficient plant growth-promoting bacteria associated with canola (Brassica napus). Biol Fertil Soils 33:152–156

    Article  Google Scholar 

  • Blaha D, Prigent-Combaret C, Mirza MS, Moenne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470

    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 

  • Bloemberg GV, Lugtenberg BJJ (2001) Molecular basis of plant growth promotion and biocontrol by rhizobia. Curr Opin Plant Biol 4:343–350

    Article  PubMed  CAS  Google Scholar 

  • Cartieaux F, Thibaud MC, Zimmerli L, Lessard P, Sarrobert C, David P, Gerbaud A, Robaglia C, Sommerville S, Nussaume L (2003) Transcriptome analysis of Arabidopsis colonized by a plant-growth promoting rhizobacterium reveals a general effect on disease resistance. Plant J 36:177–188

    Article  PubMed  CAS  Google Scholar 

  • Colangelo EP, Guerinot ML (2004) The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16:3400–3412

    Article  PubMed  CAS  Google Scholar 

  • Contesto C, Desbrosses G, Lefoulon C, Béna G, Borel F, Galland M, Gamet L, Varoquaux F, Touraine B (2008) Effects of rhizobacterial ACC deaminase activity on Arabidopsis indicate that ethylene mediates local root responses to plant growth-promoting rhizobacteria. Plant Sci 175:178–189

    Article  CAS  Google Scholar 

  • Contesto C, Milesi S, Mantelin S, Zancarini A, Desbrosses G, Varoquaux F, Bellini C, Kowalczyk M, Touraine B (2010) The auxin-signaling pathway is required for the lateral root response of Arabidopsis to the rhizobacterium Phyllobacterium brassicacearum. Planta 232:1455–1470

    Article  PubMed  CAS  Google Scholar 

  • Costacurta A, Keijers V, Vanderleyden J (1994) Molecular cloning and sequence analysis of an Azospirillum brasilense indole-3-pyruvate decarboxylase gene. Mol Gen Genet 243:463–472

    PubMed  CAS  Google Scholar 

  • Curie C, Briat JF (2003) Iron transport and signaling in plants. Annu Rev Plant Biol 54:183–206

    Article  PubMed  CAS  Google Scholar 

  • del Pozo JC, Dharmasiri S, Hellmann H, Walker L, Gray WM, Estelle M (2002) AXR1-ECR1-dependent conjugation of RUB1 to the Arabidopsis cullin AtCUL1 is required for auxin response. Plant Cell 14:421–433

    Article  PubMed  Google Scholar 

  • Desbrosses G, Contesto C, Varoquaux F, Galland M, Touraine B (2009) PGPR-Arabidopsis interactions is a useful system to study signaling pathways involved in plant developmental control. Plant Signal Behav 4:321–323

    Article  PubMed  CAS  Google Scholar 

  • Dharmasiri S, Swarup R, Mockaitis K, Dharmasiri N, Singh SK, Kowalchyk M, Marchant A, Mills S, Sandberg G, Bennett MJ, Estelle M (2006) AXR4 is required for localization of the auxin influx facilitator AUX1. Science 312:1218–1220

    Article  PubMed  CAS  Google Scholar 

  • Dobbelaere S, Croonenborghs A, Thys A, Vande Broek A, Vanderleyden J (1999) Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat. Plant Soil 212:155–164

    Article  CAS  Google Scholar 

  • Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149

    Article  CAS  Google Scholar 

  • Estelle M, Somerville S (1987) Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol Gen Genet 206:200–206

    Article  CAS  Google Scholar 

  • Farag MA, Ryu CM, Sumner LW, Paré PW (2006) GC-MS SPME profiling of rhizobacterial volatiles reveals prospective inducers of growth promotion and induced systemic resistance in plants. Phytochemistry 67:2262–2268

    Article  PubMed  CAS  Google Scholar 

  • Farmer EE (2001) Surface-to-air signals. Nature 411:854–856

    Article  PubMed  CAS  Google Scholar 

  • Forde BG, Lorenzo H (2001) The nutritional control of root development. Plant Soil 232:51–68

    Article  CAS  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  PubMed  CAS  Google Scholar 

  • Glick BR, Jacobson CB, Schwarze MMK, Pasternak JJ (1994) 1-Aminocyclopropane-1-carboxylic acid deaminase mutants of the plant growth promoting rhizobacterium Pseudomonas putida GR12-2 do not stimulate canola root elongation. Can J Microbiol 40:911–915

    Article  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 

  • Gutiérrez-Luna F, López-Bucio J, Altamirano-Hernández J, Valencia-Cantero E, de la Cruz H, Macías-Rodríguez L (2010) Plant growth-promoting rhizobacteria modulate root-system architecture in Arabidopsis thaliana through volatile organic compound emission. Symbiosis 51:75–83

    Article  Google Scholar 

  • Guzman P, Ecker JR (1990) Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2:513–523

    Article  PubMed  CAS  Google Scholar 

  • Imsande J, Touraine B (1994) N demand and the regulation of nitrate uptake. Plant Physiol 105:3–7

    PubMed  CAS  Google Scholar 

  • Kai M, Piechulla B (2009) Plant growth promotion due to rhizobacterial volatiles – an effect of CO2? FEBS Lett 583:3473–3477

    Article  PubMed  CAS  Google Scholar 

  • Kai M, Crespo E, Cristescu SM, Harren FJM, Francke W, Piechulla B (2010) Serratia odorifera: analysis of volatile emission and biological impact of volatile compounds on Arabidopsis thaliana. Appl Microbiol Biotechnol 88:965–976

    Article  PubMed  CAS  Google Scholar 

  • Khalid A, Arshad M, Zahir Z (2004) Screening plant growth-promoting rhizobacteria for improving growth and yield of wheat. J Appl Microbiol 96:473–480

    Article  PubMed  CAS  Google Scholar 

  • Kishore GK, Pande S, Podile AR (2005) Phylloplane bacteria increase seedling emergence, growth and yield of field-grown groundnut (Arachis hypogaea L.). Lett Appl Microbiol 40:260–268

    Article  PubMed  CAS  Google Scholar 

  • Kloepper JW, Lifshitz R, Zablotowicz RM (1989) Free-living bacterial inocula for enhancing crop productivity. Trends Biotechnol 7:39–44

    Article  Google Scholar 

  • Kloepper JW, Zablotowicz RM, Tipping EM, Lifshitz R (1991) Plant growth promotion mediated by bacterial rhizosphere colonizers. In: Keister KL, Cregan PB (eds) The rhizosphere and plant growth. Kluwer Academic, Dordrecht, pp 315–326

    Google Scholar 

  • Kloepper JW, Ryu CM, Zhang S (2004) Induced systemic resistance and promotion of plant growth by Bacillus spp. Phytopathology 94:1259–1266

    Article  PubMed  CAS  Google Scholar 

  • Lappartient AG, Touraine B (1996) Demand-driven control of root ATP sulfurylase activity and SO 2−4 uptake in intact canola. The role of phloem-translocated glutathione. Plant Physiol 111:147–157

    PubMed  CAS  Google Scholar 

  • Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B (1999) Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J 18:89–95

    Article  PubMed  CAS  Google Scholar 

  • Larcher M, Muller B, Mantelin S, Rapior S, Cleyet-Marel J-C (2003) Early modifications of Brassica napus root system architecture induced by a plant growth-promoting Phyllobacterium strain. New Phytol 160:119–125

    Article  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 

  • Loper JE, Schroth MN (1986) Influence of bacterial sources of indole-3-acetic acid on root elongation of sugar beet. Phytopathology 76:386–389

    Article  CAS  Google Scholar 

  • Lopez-Bucio J, Campos-Cuevas JC, Hernandez-Calderon E, Velasquez-Becerra C, Farias-Rodriguez R, Macias-Rodriguez LI, Valencia-Cantero E (2007) Bacillus megaterium rhizobacteria promote growth and alter root-system architecture through an auxin- and ethylene-independent signaling mechanism in Arabidopsis thaliana. Mol Plant Microbe Interact 20:207–217

    Article  PubMed  CAS  Google Scholar 

  • Mantelin S, Touraine B (2004) Plant growth-promoting bacteria and nitrate availability: impacts on root development and nitrate uptake. J Exp Bot 394:27–34

    Google Scholar 

  • Mantelin S, Desbrosses G, Larcher M, Tranbarger TJ, Cleyet-Marel J-C, Touraine B (2006a) Nitrate-dependent control of root architecture and N nutrition are altered by a plant growth-promoting Phyllobacterium sp. Planta 223:591–603

    Article  PubMed  CAS  Google Scholar 

  • Mantelin S, Fisher-Le Saux M, Zakhia F, Béna G, Bonneau S, Jeder H, de Lajudie P, Cleyet-Marel J-C (2006b) Emended description of the genus Phyllobacterium and description of four novel species associated with plant roots: Phyllobacterium bourgognense sp. nov., Phyllobacterium ifriqiyense sp. nov., Phyllobacterium leguminum sp. nov. and Phyllobacterium brassicacearum sp. nov. Int J Syst Evol Microbiol 56:827–839

    Article  PubMed  CAS  Google Scholar 

  • Nazoa P, Vidmar JJ, Tranbarger TJ, Mouline K, Damiani I, Tillard P, Zhuo D, Glass ADM, Touraine B (2003) Regulation of the nitrate transporter gene AtNRT2.1 in Arabidopsis thaliana: responses to nitrate, amino acids and developmental stage. Plant Mol Biol 52:689–703

    Article  PubMed  CAS  Google Scholar 

  • Paré PW, Tumlinson JH (1999) Plant volatiles as a defense against insect herbivores. Plant Physiol 121:325–332

    Article  PubMed  Google Scholar 

  • Patten CL, Glick BR (2002) Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol 68:3795–3801

    Article  PubMed  CAS  Google Scholar 

  • Persello-Cartieaux F, David P, Sarrobert C, Thibaud MC, Achouak W, Robaglia C, Nussaume L (2001) Utilization of mutants to analyze the interaction between Arabidopsis thaliana and its naturally root-associated Pseudomonas. Planta 212:190–198

    Article  PubMed  CAS  Google Scholar 

  • Piechulla B, Pott MB (2003) Plant scents-mediators of inter- and intraorganismic communication. Planta 217:687–689

    Article  PubMed  CAS  Google Scholar 

  • Pitts RJ, Cernac A, Estelle M (1998) Auxin and ethylene promote root hair elongation in Arabidopsis. Plant J 16:553–560

    Article  PubMed  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  PubMed  CAS  Google Scholar 

  • Rus A, Yokoi S, Sharkhuu A, Reddy M, Lee B-h, Matsumoto TK, Koiwa H, Zhu J-K, Bressan RA, Hasegawa PM (2001) AtHKT1 is a salt tolerance determinant that controls Na+ entry into plant roots. Proc Natl Acad Sci USA 98:14150–14155

    Article  PubMed  CAS  Google Scholar 

  • Ryu C-M, Farag MA, Hu C-H, Reddy MS, Wei H-X, Paré PW, Kloepper JW (2003) Bacterial volatiles promote growth in Arabidopsis. Proc Natl Acad Sci USA 100:4927–4932

    Article  PubMed  CAS  Google Scholar 

  • Scheible WR, Gonzalez Fontes A, Lauerer M, Mueller Roeber B, Caboche M, Stitt M (1997) Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9:783–798

    Article  PubMed  CAS  Google Scholar 

  • Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448

    Article  PubMed  CAS  Google Scholar 

  • Spaepen S, Dobbelaere S, Croonenborghs A, Vanderleyden J (2008) Effects of Azospirillum brasilense indole-3-acetic acid production on inoculated wheat plants. Plant Soil 312:15–23

    Article  CAS  Google Scholar 

  • Stotzky G, Schenck S (1976) Volatile organic compounds and microorganisms. CRC Crit Rev Microbiol 4:333–382

    Article  PubMed  CAS  Google Scholar 

  • Touraine B (2004) Nitrate uptake by roots – transporters and root development. In: De Kok LJ, Stulen I (eds) Plant ecophysiology, vol 3, Nitrogen acquisition and assimilation in higher plants. Kluwer Academic, Dordrecht, pp 1–34

    Google Scholar 

  • Tranbarger TJ, Al-Ghazi Y, Muller B, Teyssendier de la Serve B, Doumas P, Touraine B (2003) Transcription factor genes with expression correlated to nitrate-related root plasticity of Arabidopsis thaliana. Plant Cell Environ 26:459–469

    Article  CAS  Google Scholar 

  • Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9:1963–1971

    Article  PubMed  CAS  Google Scholar 

  • van Loon L (2007) Plant responses to plant growth-promoting rhizobacteria. Eur J Plant Pathol 119:243–254

    Article  Google Scholar 

  • Van Loon LC, Bakker PAHM, Pieterse CMJ (1998) Systemic resistance induced by rhizospheric bacteria. Annu Rev Phytopathol 36:453–483

    Article  PubMed  Google Scholar 

  • Vansuyt G, Robin A, Briat J, Curie C, Lemanceau P (2007) Iron acquisition from Fe-pyoverdine by Arabidopsis thaliana. Mol Plant Microbe Interact 20:441–447

    Article  PubMed  CAS  Google Scholar 

  • Vespermann A, Kai M, Piechulla B (2007) Rhizobacterial volatiles affect the growth of fungi and Arabidopsis thaliana. Appl Environ Microbiol 73:5639–5641

    Article  PubMed  CAS  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Walch-Liu P, Ivanov II, Filleur S, Gan Y, Remans T, Forde BG (2006) Nitrogen regulation of root branching. Ann Bot 97:875–881

    Article  PubMed  CAS  Google Scholar 

  • Wang W, Vinocur B, Altman A (2003) Plant responses to drought, salinity and extreme temperatures: towards genetic engineering for stress tolerance. Planta 218:1–14

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proc Natl Acad Sci USA 96:6529–6534

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Kim MS, Krishnamachari V, Payton P, Sun Y, Grimson M, Farag MA, Ryu C-M, Allen R, Melo IS, Paré PW (2007) Rhizobacterial volatile emissions regulate auxin homeostasis and cell expansion in Arabidopsis. Planta 226:839–851

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Kim MS, Sun Y, Dowd SE, Shi H, Paré PW (2008a) Soil bacteria confer plant salt tolerance by tissue-specific regulation of the sodium transporter HKT1. Mol Plant Microbe Interact 21:737–744

    Article  PubMed  Google Scholar 

  • Zhang H, Xie X, Kim MS, Kornyeyev DA, Holaday S, Paré PW (2008b) Soil bacteria augment Arabidopsis photosynthesis by decreasing glucose sensing and abscisic acid levels in planta. Plant J 56:264–273

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Sun Y, Xie X, Kim MS, Dowd SE, Paré PW (2009) A soil bacterium regulates plant acquisition of iron via deficiency-inducible mechanisms. Plant J 58:568–577

    Article  PubMed  CAS  Google Scholar 

  • Zhang H, Murzello C, Sun Y, Kim MS, Xie X, Jeter RM, Zak JC, Dowd SE, Paré PW (2010) Choline and osmotic-stress tolerance induced in Arabidopsis by the soil microbe Bacillus subtilis (GB03). Mol Plant Microbe Interact 23:1097–1104

    Article  PubMed  CAS  Google Scholar 

  • Zhuang X, Chen J, Shim H, Bai Z (2007) New advances in plant growth-promoting rhizobacteria for bioremediation. Environ Int 33:406–413

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Bruno Touraine .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2012 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Desbrosses, G., Varoquaux, F., Touraine, B. (2012). Arabidopsis as a Model System to Decipher the Diversity and Complexity of Plant Responses to Plant-Growth-Promoting Rhizobacteria. In: Maheshwari, D. (eds) Bacteria in Agrobiology: Plant Probiotics. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27515-9_13

Download citation

Publish with us

Policies and ethics