Skip to main content
SpringerLink
Log in

The Saharan isolate Saccharothrix algeriensis NRRL B-24137 induces systemic resistance in Arabidopsis thaliana seedlings against Botrytis cinerea

  • Regular Article
  • Published:
Plant and Soil Aims and scope Submit manuscript

Abstract

Background and aim

Saccharothrix algeriensis NRRL B-24137, isolated from a Saharan soil, has been described as a potential biocontrol agent against Botrytis cinerea and other phytopathogens. However, the plant protection mechanisms involved still need to be described. The aim of this study was to determine this protection phenomenon as well as parts of the mechanisms involved, using Arabidopsis thaliana seedlings and B. cinerea.

Methods

The bacterial colonization process was evaluated on A. thaliana seedlings using fluorescence in situ hybridization. Protection of A. thaliana seedlings inoculated with NRRL B-24137 against B. cinerea was then evaluated. Parts of the mechanisms involved in the systemic protection against B. cinerea were evaluated using known mutants of genes involved in jasmonate (JA)/ethylene (ET)/salicylic acid (SA) signaling. Other Arabidopsis mutants, AtrhbohD-3, AtrhbohF-3, and ups1-1 were also screened to determine other parts of the mechanisms involved.

Results

The results showed that the strain NRRL B-24137 colonized, epi- and endophytically, the roots of Arabidopsis seedlings but the strain was not a systemic colonizer during the time of the experiment. The strain NRRL B-24137 also reduced B. cinerea symptoms and the protection was linked to known mechanisms of induced systemic resistance (ISR; JA/ET signaling), as well as to functionality of AtrbohF oxidase and of UPS1. Crosstalk between ET/JA and SA signaling could also be involved.

Conclusions

The isolate NRRL B-24137, after colonizing the root systems of A. thaliana, induces an ISR against B. cinerea, which is JA/ET dependent, but could also require SA crosstalk and protection could also require NAPDH oxidases and UPS1 functionalities.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925

    CAS  PubMed Central  PubMed  Google Scholar 

  • Audenaert K, Pattery T, Cornelis P, Höfte M (2002) Induction of systemic resistance to Botrytis cinerea in tomato by Pseudomonas aeruginosa 7NSK2: role of salicylic acid, pyochelin, and pyocyanin. Mol Plant Microbe Interact 15:1147–1156

    Article  CAS  PubMed  Google Scholar 

  • Bakker PAHM, Pieterse CMJ, Van Loon LC (2007) Induced systemic resistance by fluorescent Pseudomonas spp. Phytopathology 97:239–243

    Article  PubMed  Google Scholar 

  • Barriuso J, Solano BR, Gutiérrez Mañero FJ (2008) Protection against pathogen and salt stress by four plant growth-promoting rhizobacteria isolated from Pinus sp. on Arabidopsis thaliana. Phytopathology 98:666–672

    Article  CAS  PubMed  Google Scholar 

  • Barrow JR, Lucero ME, Reyes-Vera I, Havstad KM (2008) Do symbiotic microbes have a role in plant evolution, performance and response to stress? Com Integr Biol 1:69–73

    Article  Google Scholar 

  • Brandam C, Lebrihi A, Meyer XM, Strub C (2008) Saccharothrix algeriensis, a new antibiotic producer: investigations on its secondary metabolism. In: Industrial Biotechnology International Conferences, 8–11 June 2008, Italy.

  • Cao H, Bowling SA, Gordon AS, Dong X (1994) Characterization of an Arabidopsis mutant that is nonresponsive to inducers of systemic acquired resistance. Plant Cell 6:1583–1592

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cao H, Glazebrook J, Clarke JD, Volko S, Dong X (1997) The Arabidopsis NPR1 gene that controls systemic acquired resistance encodes a novel protein containing ankyrin repeats. Cell 88:57–63

    Article  CAS  PubMed  Google Scholar 

  • Compant S, Clément C, Sessitsch A (2010a) Plant growth-promoting bacteria in the rhizo- and endosphere of plants. Their role, colonization, mechanisms involved and prospects for utilization. Soil Biol Biochem 42:669–678

    Article  CAS  Google Scholar 

  • Compant S, Duffy B, Nowak J, Clément C, Ait Barka E (2005) Use of plant growth-promoting bacteria for biocontrol of plant diseases: principles, mechanisms of action, and future prospects. Appl Environ Microbiol 71:4951–4959

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Compant S, Reiter B, Colli-Mull JG, Gangl H, Sessitsch A (2011) Endophytes of grapevine flowers, berries and seeds: identification of cultivable bacteria, comparison with other plant parts, and visualization of niches of colonization. Microb Ecol 62:188–197

    Article  PubMed  Google Scholar 

  • Compant S, van der Heijden M, Sessitsch A (2010b) Climate change effects on beneficial plant–microbes interactions. FEMS Microbiol Ecol 73:197–214

    CAS  PubMed  Google Scholar 

  • Conn VM, Walker AR, Franco CMM (2008) Endophytic actinobacteria induce defense pathways in Arabidopsis thaliana. Mol Plant-Microbe Interact 21:208–218

    Article  CAS  PubMed  Google Scholar 

  • Daims H, Brühl A, Amann R, Schleifer K-H, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444

    Article  CAS  PubMed  Google Scholar 

  • De Meyer G, Capieau K, Audenaert K, Buchala A, Métraux JP, Höfte M (1999) Nanogram amounts of salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 activate the systemic acquired resistance pathway in bean. Mol Plant Microbe Interact 12:450–458

    Article  PubMed  Google Scholar 

  • De Meyer G, Höfte M (1997) Salicylic acid produced by the rhizobacterium Pseudomonas aeruginosa 7NSK2 induces resistance to leaf infection by Botrytis cinerea on bean. Phytopathology 87:588–593

    Article  PubMed  Google Scholar 

  • Denby KJ, Jason LJM, Murray SL, Last RL (2005) ups1, an Arabidopsis thaliana camalexin accumulation mutant defective in multiple defence signaling pathways. Plant J 41:673–684

    Article  CAS  PubMed  Google Scholar 

  • Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144:367–379

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Glazebrook J, Chen W, Estes B, Chang H-S, Nawrath C, Métraux J-P, Zhu T, Katagiri F (2003) Topology of the network integrating salicylate and jasmonate signal transduction derived from global expression phenotyping. Plant J 34:217–228

    Article  CAS  PubMed  Google Scholar 

  • Hallmann J (2001) Plant interactions with endophytic bacteria. In: Jeger MJ, Spence NJ (eds) Biotic interactions in plant–pathogen associations. CABI, Wallingford, pp 87–119

    Chapter  Google Scholar 

  • Hallmann J, Berg B (2007) Spectrum and population dynamics of bacterial root endophytes. In: Schulz BJE, Boyle CJC, Sieber TN (eds) Microbial root endophytes. Springer, Berlin, pp 15–31

    Google Scholar 

  • Hammerschmidt R (1999) Induced disease resistance: how do induced plants stop pathogens. Physiol Mol Plant Pathol 55:77–84

    Article  CAS  Google Scholar 

  • Hann J, Kamber M (2000) Data mining: concepts and techniques. Morgan Kaufman, San Francisco

  • Heck S, Grau T, Buchala AJ, Metraux JP, Nawrath C (2003) Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis–Pseudomonas syringae pv. tomato interaction. Plant J 36:342–352

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Köberl M, Müller H, Ramadan EM, Berg G (2011) Desert farming benefits from microbial potential in arid soils and promotes diversity and plant health. PLoS ONE 6(9):e24452

    Article  PubMed Central  PubMed  Google Scholar 

  • Lamari L, Zitouni A, Boudjella H, Badjin B, Sabaou N, Lebrihi A, Lefebvre G, Seguin E, Tillequin F (2002a) New dithiolopyrrolones antibiotics from Saccharothrix sp. SA 233: I. Taxonomy, fermentation, isolation and biological activities. J Antibiot 55:696–701

    Article  CAS  PubMed  Google Scholar 

  • Lamari L, Zitouni A, Dob T, Sabaou N, Lebrihi A, Germain P, Seguin E, Tillequin F (2002b) New dithiolopyrrolone antibiotics from Saccharothrix sp. SA 233. II. Physiochemical properties and structure elucidation. J Antibiot 55:702–707

    Article  CAS  PubMed  Google Scholar 

  • Lamari L. (2006) Production de nouveaux antibiotiques du groupe des pyrrothines par une nouvelle espèce dactinomycète, Saccharothrix algeriensis. Thèse de doctorat, E.N.S. de Kouba (Algérie), pp 1–177.

  • Lugtenberg B, Kamilova F (2009) Plant-growth-promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • Marasco R, Rolli E, Ettoumi B, Vigani G, Mapelli F, Borin S, Abou-Hadid AF, El-Behairy UA, Sorlini C, Cherif A, Zocchi G, Daffonchio D (2012) A drought resistance-promoting microbiome is selected by root system under desert farming. PLOS ONE 7(10):e48479

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Maurhofer M, Hase C, Meuwly P, Métraux JP, Défago G (1994) Induction of systemic resistance of tobacco to tobacco necrosis virus by the root-colonizing Pseudomonas fluorescens strain CHA0: influence of the gacA gene and of pyoverdine production. Phytopathology 84:139–146

    Article  CAS  Google Scholar 

  • Maurhofer M, Reimmann C, Schmidli-Sacherer P, Heeb S, Haas D, Défago G (1998) Salicylic acid biosynthetic genes expressed in Pseudomonas fluorescens strain P3 improve the induction of systemic resistance in tobacco against tobacco necrosis virus. Phytopathology 88:678–684

    Article  CAS  PubMed  Google Scholar 

  • Mitter B, Brader G, Afzal M, Compant S, Naveed M, Trognitz F, Sessitsch A (2013) Advances in elucidating plant–soil–microbe (bacteria) interactions. Adv Agron 121:381–445

    Article  CAS  Google Scholar 

  • Muzammil S, Compant S, Yu Z, Mathieu F, Lebrihi A (2011) Saccharothrix algeriensis NRRL B-24137: a new endophyte with high potential to protect grapevine towards Botrytis cinerea in case of high temperature conditions. In: Oeno 2011 - Actes de colloques du 9e symposium international d’oenologie de Bordeaux. Dunod (in press)

  • Oelmüller R, Sherameti I, Tripathi S, Varma A (2009) Piriformospora indica, a cultivable root endophyte with multiple biotechnological applications. Symbiosis 49:1–17

    Article  Google Scholar 

  • Pieterse CM, van der Does D, Zamioudis C, Leon-Reyes A, van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:28–33

    Google Scholar 

  • Pieterse CMJ, Van Loon LC (1999) Salicylic acid-independent plant defence pathways. Trends Plant Sci 4:52–58

    Article  PubMed  Google Scholar 

  • Pieterse CMJ, Van Loon LC (2004) NPR1: the spider in the web of induced resistance signaling pathways. Curr Opinion Plant Biol 7:456–464

    Article  CAS  Google Scholar 

  • Pieterse CMJ, Van Wees SCM, Hoffland E, Van Pelt JA, Van Loon LC (1996) Systemic resistance in Arabidopsis induced by biocontrol bacteria is independent of salicylic acid accumulation and pathogenesis-related gene expression. Plant Cell 8:1225–1237

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pieterse CMJ, Van Wees SCM, Van Pelt JA, Knoester M, Laan R, Gerrits H, Weisbeek PJ, Van Loon LC (1998) A novel signaling pathway controlling induced systemic resistance in Arabidopsis. Plant Cell 10:1571–1580

    CAS  PubMed Central  PubMed  Google Scholar 

  • Pineda A, Zheng SJ, van Loon JJA, Pieterse CM, Dicke M (2010) Helping plants to deal with insects: the role of beneficial soil-borne microbes. Trends Plant Sci 15:507–514

    Article  CAS  PubMed  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opinion Plant Biol 14(4):435–443

    Article  Google Scholar 

  • Roller C, Wagner M, Amann R, Ludwig W, Schleifer KH (1994) In situ probing of gram-positive bacteria with high DNA G+C content using 23S rRNA-targeted oligonucleotides. Microbiology 140:2849–2858

    Article  CAS  PubMed  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interaction with hosts. Mol Plant-Microbe Interact 19:827–837

    Article  CAS  PubMed  Google Scholar 

  • Ryu C-M, Murphy JR, Mysore K, Kloepper JW (2004) Plant growth-promoting rhizobacteria systemically protect Arabidopsis thaliana against cucumber mosaic virus by a salicylic acid and NPR-1 independent and jasmonic acid-dependent pathway. Plant J 39:381–392

    Article  CAS  PubMed  Google Scholar 

  • Ton J, De Vos M, Robben C, Buchala AJ, Métraux J-P, Van Loon LC, Pieterse CMJ (2002) Characterisation of Arabidopsis enhanced disease susceptibility mutants that are affected in systemically induced resistance. Plant J 29:11–21

    Article  CAS  PubMed  Google Scholar 

  • Torres MA, Dangl J (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opinion Plant Biol 8:397–403

    Article  CAS  Google Scholar 

  • van de Mortel JE, de Vos RC, Dekkers E, Pineda A, Guillod L, Bouwmeester K, van Loon JJ, Dicke M, Raaijmakers JM (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160(4):2173–2188

    Article  PubMed Central  PubMed  Google Scholar 

  • Van der Ent S, Van Wees SCM, Pieterse CMJ (2009) Jasmonate signaling in plant interactions with resistance-inducing beneficial microbes. Phytochemistry 70:1581–1588

    Article  PubMed  Google Scholar 

  • Van Loon LC, Bakker PAHM (2004) Signaling in rhizobacteria–plant interactions. In: De Kroon J, Visser EJW (eds) Ecological studies, vol 168, Root ecology. Springer, Berlin, pp 287–330

    Google Scholar 

  • Van Loon LC, Bakker PAHM (2005) Induced systemic resistance as a mechanism of disease suppression by rhizobacteria. In: Siddiqui ZA (ed) PGPR: biocontrol and biofertilization. Springer, Dordrecht, pp 39–66

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • van Loon LC, Van Strien EA (1999) The families of pathogenesis-related proteins, their activities, and comparative analysis of PR-1 type proteins. Physiol Mol Plant Pathol 55:85–97

    Article  Google Scholar 

  • Van Wees SCM, Van der Ent S, Pieterse CMJ (2008) Plant immune responses triggered by beneficial microbes. Curr Opinion Plant Biol 11:443–448

    Article  Google Scholar 

  • Ward ER, Uknes SJ, Williams SC, Dincher SS, Wiederhold DL, Alexander DC, Ahl-Goy P, Métraux J-P, Ryals JA (1991) Coordinate gene activity in response to agents that induce systemic acquired resistance. Plant Cell 3:1085–1094

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yekkour A, Sabaou N, Zitouni A, Errakhi R, Mathieu F, Lebrihi A (2012) Characterization and antagonistic properties of Streptomyces strains isolated from Saharan soils, and evaluation of their ability to control seedling blight of barley caused by Fusarium culmorum. Lett Appl Microbiol 55:427–435

    CAS  Google Scholar 

  • Zamioudis C, Pieterse CMJ (2012) Modulation of host immunity by beneficial microbes. Mol Plant-Microbe Interact 25:139–150

    Article  CAS  PubMed  Google Scholar 

  • Zhou N, Tootle TL, Tsui F, Klessig DF, Glazebrook J (1998) PAD4 functions upstream from salicylic acid to control defense responses in Arabidopsis. Plant Cell 10:1021–1030

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zitouni A (1995) Les genres Nocardiopsis et Saccharothrix (Actinomycetales) dans les sols sahariens: taxonomie numérique, extraction, purification et caractérisation de quelques antibiotiques synthétisés. Magister de microbiologie, E.N.S. de Kouba, Algeria

  • Zitouni A, Boudjella H, Lamari L, Badji B, Mathieu F, Lebrihi A, Sabaou N (2005) Nocardiopsis and Saccharothrix genera in Saharan soils in Algeria: isolation, biological activities and partial characterisation of antibiotics. Res Microbiol 156:984–993

    Article  CAS  PubMed  Google Scholar 

  • Zitouni A, Lamari L, Boudjella H, Badji B, Sabaou N, Gaouar A, Mathieu F, Lebrihi A, Labeda DP (2004) Saccharothrix algeriensis sp. nov., isolated from Saharan soil. Int J Syst Evol Microbiol 54:1377–1381

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by a grant from HEC Pakistan. Additional funding came from CNRS. We would like to thank Ms. Helen Smith (AIT, Wien, Austria) and Dr. Brian Murphy (Trinity College Dublin, Ireland) for the proof reading of the manuscript. Also, special thanks to Livio Antonielli (AIT, Tulln, Austria) for his comments. Additional thanks to the reviewers for their valuable comments.

Author information

Authors and Affiliations

  1. LGC UMR 5503 (CNRS/INPT/UPS), Département Bioprocédés et Systèmes Microbiens, ENSAT-INP de Toulouse, Université de Toulouse, 1 Avenue de l’Agrobiopôle, B.P. 32607, 31326, Castanet-Tolosan Cedex 1, France

    Saima Muzammil, Clotilde Graillon, Rayenne Saria, Florence Mathieu, Ahmed Lebrihi & Stéphane Compant

  2. Bioresources Unit, Health & Environment Départment, AIT Austrian Institute of Technology GmbH, 3430, Tulln, Austria

    Stéphane Compant

Authors
  1. Saima Muzammil
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Clotilde Graillon
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rayenne Saria
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Florence Mathieu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ahmed Lebrihi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Stéphane Compant
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Stéphane Compant.

Additional information

Responsible Editor: Jesus Mercado-Blanco.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table Suppl 1

Results of detection of NRRL B-24137 in WT Col N39005 on and inside roots and leaves with or without Botrytis cinerea. + presence, ND not detectable. (PPT 80 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Muzammil, S., Graillon, C., Saria, R. et al. The Saharan isolate Saccharothrix algeriensis NRRL B-24137 induces systemic resistance in Arabidopsis thaliana seedlings against Botrytis cinerea . Plant Soil 374, 423–434 (2014). https://doi.org/10.1007/s11104-013-1864-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11104-013-1864-0

Keywords

Search

Navigation