ROLE OF SIDEROPHORE IN CONTROL OF PLANT DISEASE

Plant pathogens such as bacteria and fungi compete for space or nutrients and this may be a key feature for biocontrol mechanism (Whipps 2001) in rhizosphere.  The iron requirement of the plant influences the rhizosphere microbial community structure (Yang and Crowley 2000). Iron is abundant but its bioavailability in the soil is limited due to the insoluble form of ferric hydroxide.

Micromolar concentration of iron is required by bacteria and fungi for their growth. Therefore  they evolve high affinity iron uptake system the siderophore and a membrane–bound system for transport and utilization of chelated iron (Neilands and Nakamura 1991).  Siderophore (Greek: “iron carrier”) are low molecular weight compounds that chelates ferric ion and serve as a vehicle to transport iron into the cell and are produced by bacteria and fungi growing under iron stress. The role of these compounds is to scavenge iron from the environment and make it available to microbial cell. Transport of iron into the cell is mediated by specific membrane receptor. Siderophore mediated competition for iron deprive pathogen of iron resulting in decrease incidence of disease. These bacterial iron chelators sequester the limited supply of iron available in the rhizosphere making it unavailable to pathogenic fungi, thereby restricting their growth (O’Sullivan and O’Gara 1992; Loper and Henkels 1999). Certain plant growth-promoting pseudomonads inhibit deleterious and pathogenic rhizosphere bacteria and fungi by producing siderophores (Buyer and Sikora 1990; Kloepper et al., 1980). Microorganisms growing under aerobic condition need iron for  various metabolic functions, such as reduction of oxygen for synthesis of ATP, formation of heme etc. (Neilands 1995). Ferric-siderophore complexes on being recognized are bound to outer receptor proteins and iron is transported into the microbial cell where it becomes available for metabolic function.

Interesting aspect is diverse organisms can use same type of siderophore (Handelsman and Stabb 1996). The fluorescent pseudomonads produce a class of siderophores known as pseudobactins which are structurally complex iron-binding molecules. Plants too can acquire iron from certain pseudobactins (Duijff et al., 1994 a, b). The siderophore pseudobactin 358 (PSB358) produced by Pseudomonas putida WCS358 is involved in suppression of fusarial wilt disease of carnation (Lemanceau et al., 1992). Matthijs et al. (2007) studied thioquinolobactin siderophore produced by Pseudomonas which showed anti-Pythium activity. Pseudomonas putida and Pseudomonas fluorescens are soil inhabitants, and certain strains promote plant growth and health by suppressing diseases caused by soil borne pathogens. The capacity of these strains to produce pyoverdines is linked, in some cases, with disease suppression (Loper and Buyer 1991).

Role of the pyoverdine siderophore produced by many Pseudomonas species biologically control Pythium and Fusarium species (Loper and Buyer 1991). Pseudomonas aeruginosa 7NSK2 produces three siderophores: the yellow-green fluorescent pyoverdin, the salicylate derivative pyochelin, and salicylic acid. Role of pyochelin and pyoverdin was shown to suppress Pythium causing damping–off   of tomato by Pseudomonas aeruginosa 7NSK2 (Buysens et al., 1996).

Pseudomonas aeruginosa needs iron to sustain growth. Two siderophores pyoverdine and pyochelin are produced by this bacterium characterized by high and low affinities for iron respectively. P. aeruginosa is able to utilize different siderophores from other microorganisms (Cornelis and Dingemans 2013). Some siderophore can be used only by the bacteria that produce them (Ongena et al., 1999) whereas, Pseudomonas spp. can utilize siderophore produced by many different bacteria and fungi (Loper and Henkels 1999). Various environmental factors can also influence the quantity of siderophores produced (Duffy and Défago 1999). Siderophore is an important aspect of microorganisms. The solubilization of iron of different composition   present in soil is brought about by bacteria and fungi by dissolution and chelation through organic acid or siderophores.

 

References:

Buyer, J. S. and Sikora, L. J. 1990 Rhizosphere Interactions and Siderophores. Plant and Soil 129 (1): 101-107

Buysens, S., Heungens, K., Poppe, J. and Höfte, M. 1996   Involvement of Pyochelin and Pyoverdin in Suppression of Pythium-Induced Damping-Off of Tomato by Pseudomonas aeruginosa 7NSK2. Appl. Environ. Microbiol. 62(3): 865–871

Cornelis, P. and Dingemans, J.  2013 Pseudomonas aeruginosa Adapts its Iron Uptake Strategies in Function of the Type of Infections. Front Cell Infect. Microbiol. 3: 75

doi:  10.3389/fcimb.2013.00075

Duffy, B. K. and Défago, G. 1999 Environmental Factors Modulating Antibiotic and Siderophore Biosynthesis by Pseudomonas fluorescens Biocontrol Strains. Appl. Environ. Microbiol. 65(6): 2429–2438

Duijff, B. J., Bakker, P. A. H. M. and Schippers, B. 1994a Ferric Pseudobactin 358 as an Iron Source for Carnation. J. Pl. Nutri. 17(12): 2069 -2078

 DOI: 10.1080/01904169409364866

Duijff, B. J., De Kogel, W. J., Bakker, P. A. H. M. and Schippers, B. 1994b lnfluence of Pseudobactin 358 on the Iron Nutrition of Barley. Soil Biol. Biochem. 26(12): 1681-1688

 Handelsman, J.  and Stabb, E. V. 1996 Biocontrol of Soilborne Plant Pathogens. The Plant Cell 8: 1855-1869

Kloepper, J. W., Leong, J., Teintze, M. and Schroth, M. N. 1980 Enhanced Plant Growth by Siderophores Produced by Plant Growth-Promoting Rhizobacteria. Nature 286: 885–886

doi:10.1038/286885a0

Lemanceau, P., Bakker, P. A., De Kogel, W. J., Alabouvette, C.  and Schippers, B.  1992 Effect of Pseudobactin 358 Production by Pseudomonas putida WCS358 on Suppression of Fusarium Wilt of Carnations by Nonpathogenic Fusarium oxysporum Fo47. Appl. Environ. Microbiol. 58 (9): 2978-2982

Loper, J.  E. and Buyer, J. S. 1991 Siderophores in Microbial Interactions on Plant Surfaces. Mol. Plant-Microbe Interact. 4(1): 5–13

Loper, J.  E. and Henkels, M. D. 1999 Utilization of Heterologous Siderophores Enhances Levels of Iron Available to Pseudomonas putida in the Rhizosphere. Appl. Environ. Microbiol. 65(12): 5357-5363

Neilands, J. B. 1995 Siderophores: Structure and Function of Microbial Iron Transport Compounds.  J. Biol. Chem. 270 (45): 26723 – 26726

doi: 10.1074/jbc.270.45.26723

Neilands, J. B. and Nakamura, K. 1991 Regulation of Iron Assimilation in Microorganisms. Nutri. Rev. 43(7): 193-197

doi: 10.1111/j.1753-4887.1985.tb02419.x

Matthijs, S., Tehrani,  K. A.,  Laus,  G.,  Jackson, R. W., Cooper,  R. M. and  Cornelis,  P. 2007 Thioquinolobactin, a Pseudomonas Siderophore with Antifungal and Anti-Pythium Activity. Environ. Microbiol. 9(2): 425-34

doi: 10.1111/j.1462-2920.2006.01154.x

Ongena, M., Daayf, F., Jacques, P., Thonart, P., Benhamou, N., Paulitz, T. C., Cornelis,  P., Koedam,  N. and  Belanger, R. R. 1999 Protection of Cucumber Against Pythium Root Rot by Fluorescent Pseudomonads: Predominant Role of Induced Resistance Over Siderophores and Antibiosis. Plant Pathol.  48: 66–76

O’Sullivan, D. J. and O’Gara, F. 1992 Traits of Fluorescent Pseudomonas spp. Involved in Suppression of Plant Root Pathogens. Microbiol. Rev. 56(4): 662 – 676

Yang, C-H. and  Crowley, D. E. 2000  Rhizosphere Microbial Community Structure in Relation to Root Location and Plant Iron Nutritional Status. Appl. Environ.  Microbiol. 66: 345–351

Whipps, J. M. 2001 Microbial Interactions and Biocontrol in the Rhizosphere. J.  Exp.  Bot.  52 (1): 487 – 511

doi.org/10.1093/jexbot/52.suppl_1.487

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