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Effect of Fe deficiency on alfalfa plants grown in the presence of Pseudomonas

Published online by Cambridge University Press:  14 June 2013

D. CAMEJO ,
M. C. MARTÍ ,
I. MARTÍNEZ-ALCALÁ ,
J. I. MEDINA-BELLVER ,
S. MARQUÉS  and
A. JIMÉNEZ
D. CAMEJO
Affiliation:
Department of Stress Biology and Plant Pathology, CEBAS-CSIC, P.O. Box 164, E-30100, Murcia, Spain
M. C. MARTÍ
Affiliation:
Department of Stress Biology and Plant Pathology, CEBAS-CSIC, P.O. Box 164, E-30100, Murcia, Spain
I. MARTÍNEZ-ALCALÁ
Affiliation:
Department of Stress Biology and Plant Pathology, CEBAS-CSIC, P.O. Box 164, E-30100, Murcia, Spain
J. I. MEDINA-BELLVER
Affiliation:
Department of Environmental Protection, EEZ-CSIC, Profesor Albareda 1, E-18008, Granada, Spain
S. MARQUÉS
Affiliation:
Department of Environmental Protection, EEZ-CSIC, Profesor Albareda 1, E-18008, Granada, Spain
A. JIMÉNEZ*
Affiliation:
Department of Stress Biology and Plant Pathology, CEBAS-CSIC, P.O. Box 164, E-30100, Murcia, Spain
*
*To whom all correspondence should be addressed. Email: [email protected]
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Summary

Alfalfa is a model plant defined as less sensitive than others to iron (Fe) deficiency. In the present work, some mechanisms induced in low Fe availability conditions were studied, including the effect of inoculation of alfalfa seeds with Pseudomonas putida. The effect of different Fe contents in the nutrient solution on the growth parameters was evaluated at 3 and 10 days, observing that low Fe conditions promoted biomass accumulation. Activation in the mechanisms of Fe acquisition, through acidification of the media and an increase in the ferric chelate reductase (FCR) activity, was observed in the absence of Fe at 10 days. The presence of P. putida KT2442 in the rhizosphere eliminated FCR activation through the excretion of siderophores. The effect of the siderophores on the modulation of FCR activity was demonstrated using a ppsD mutant strain, unable to segregate them, observing an activation of the activity similar to that observed in the absence of the bacteria. This, together with the demonstrated mechanisms to increase Fe availability, contributed to the conclusion that alfalfa can be used for recovery programmes of soils with low Fe availability.

Type
Crops and Soils Research Papers
Information
The Journal of Agricultural Science , Volume 152 , Issue 5 , October 2014 , pp. 731 - 740
Copyright
Copyright © Cambridge University Press 2013 

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References

Abril, M. A., Michan, C., Timmis, K. N. & Ramos, J. L. (1989). Regulator and enzyme specificities of the TOL plasmid-encoded upper pathway for degradation of aromatic hydrocarbons and expansion of the substrate range of the pathway. Journal of Bacteriology 171, 6782–6790.Google Scholar
Alcaraz, C. F., Hellín, E., Sevilla, F. & Martínez-Sánchez, F. (1985). Influence of the leaf iron contents on the ferredoxin levels in citrus plants. Journal of Plant Nutrition 8, 603–611.Google Scholar
Almansa, M. S., Palma, J. M., Yáñez, J., Del Río, L. A. & Sevilla, F. (1991). Purification of an iron-containing superoxide dismutase from a citrus plant, Citrus limonum R. Free Radical Research Communications 12–13, 319–328.CrossRefGoogle Scholar
Camejo, D., Martí, M. C., Nicolás, E., Alarcón, J. J., Jiménez, A. & Sevilla, F. (2007). Response of superoxide dismutase isoenzymes in tomato plants (Lycopersicon esculentum) during thermo-acclimation of the photosynthetic apparatus. Physiologia Plantarum 131, 367–377.CrossRefGoogle ScholarPubMed
Carrillo-Castañeda, G., Juarez Muñoz, J., Ramon Peralta-Videa, J., Gómez, E. & Gardea-Torresdey, J. L. (2002). Plant growth-promoting bacteria promote copper and iron translocation from root to shoot in alfalfa seedlings. Journal of Plant Nutrition 26, 1801–1814.CrossRefGoogle Scholar
Cesco, S., Rombola, A. D., Tagliavini, M., Varanini, Z. & Pinton, R. (2006). Phytosiderophores released by graminaceous species promote 59Fe-uptake in citrus. Plant and Soil 287, 223–233.Google Scholar
Chaney, R. L., Brown, J. C. & Tiffin, L. O. (1972). Obligatory reduction of ferric chelates in iron uptake by soybeans. Plant Physiology 50, 208–213.Google Scholar
Connolly, E. L., Campbell, N. H., Grotz, N., Prichard, C. L. & Guerinot, M. L. (2003). Overexpression of the FRO2 ferric chelate reductase confers tolerance to growth on low iron and uncovers posttranscriptional control. Plant Physiology 133, 1102–1110.Google Scholar
Dasgan, H. Y., Römheld, V., Cakmak, I. & Abak, K. (2002). Physiological root responses of iron deficiency susceptible and tolerant tomato genotypes and their reciprocal F-1 hybrids. Plant and Soil 241, 97–104.CrossRefGoogle Scholar
Dell'Orto, M., Santi, S., De Nisi, P., Cesco, S., Varanini, Z., Zocchi, G. & Pinton, R. (2000). Development of Fe-deficiency responses in cucumber (Cucumis sativus L.) roots: involvement of plasma membrane H+-ATPase activity. Journal of Experimental Botany 51, 695–701.Google Scholar
Del Río, L. A., Sevilla, F., Sandalio, L. M. & Palma, J. M. (1991). Nutritional effect and expression of SODs: induction and gene expression; diagnostics; prospective protection against oxygen toxicity. Free Radical Research Communications 12–13, 819–827.CrossRefGoogle Scholar
Dertz, E. A., Stintzi, A. & Raymond, K. N. (2006). Siderophore-mediated iron transport in Bacillus subtilis and Corynebacterium glutamicum. Journal of Biological Inorganic Chemistry 11, 1087–1097.Google Scholar
Devescovi, G., Aguilar, C., Majolini, M. B., Marugg, J., Weisbeek, P. & Venturi, V. (2001). A siderophore peptide synthetase gene from plant-growth-promoting Pseudomonas putida WCS358. Systematic and Applied Microbiology 24, 321–330.CrossRefGoogle ScholarPubMed
Espinosa-Urgel, M., Kolter, R. & Ramos, J. L. (2002). Root colonization by Pseudomonas putida: love at first sight. Microbiology 148, 341–343.CrossRefGoogle ScholarPubMed
Franklin, F. C., Bagdasarian, M., Bagdasarian, M. M. & Timmis, K. N. (1981). Molecular and functional analysis of the TOL plasmid pWWO from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta cleavage pathway. Proceedings of the National Academy of Sciences USA 78, 7458–7462.CrossRefGoogle ScholarPubMed
Gogorcena, Y., Abadía, J. & Abadía, A. (2000). Induction of in vivo root ferric chelate reductase activity in fruit tree rootstock. Journal of Plant Nutrition 23, 9–21.Google Scholar
Guerinot, M. L. & Yi, Y. (1994). Iron-nutritious, noxious, and not readily available. Plant Physiology 104, 815–820.Google Scholar
Hell, R. & Stephan, U. W. (2003). Iron uptake, trafficking and homeostasis in plants. Planta 216, 541–551.Google Scholar
Hellín, E., Llorente, S., Piquer, V. & Sevilla, F. (1984). Actividad peroxidasa inducida como indicator de la efectividad de compuestos organicos de hierro en la corrección de deficiencia de Fe en el limonero (Peroxidase activity as indicator of efficiency of organic compounds of iron for the correction of iron deficiency in lemon trees). Agrochimica 28, 432–441.Google Scholar
Hellín, E., Ureña, R., Sevilla, F. & Alacaraz, C. F. (1987). Comparative study on the effectiveness of several iron compounds in the iron chlorosis correction in Citrus plants. Journal of Plant Nutrition 10, 411–421.CrossRefGoogle Scholar
Hellín, E., Hernández-Cortes, J. A., Piqueras, A., Olmos, E. & Sevilla, F. J. (1995). The influence of the iron content on the superoxide dismutase activity and chloroplast ultrastructure of Citrus limon. In Iron Nutrition in Soils and Plant (Ed. Abadia, J.), pp. 247–254. Dordecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Hinsinger, P., Plassard, C., Tang, C. & Jaillard, B. (2003). Origins of root-mediated pH changes in the rhizosphere and their responses to environmental constraints. Plant and Soil 248, 43–59.Google Scholar
Hoagland, D. R. & Arnon, D. I. (1950). The Water-culture Method for Growing Plants without Soil. California Agricultural Experiment Station Circular 347. Berkeley, CA, USA: University of California.Google Scholar
Hoel, B. O. & Solhaug, K. A. (1998). Effect of irradiance on chlorophyll estimation with the Minolta SPAD-502 leaf chlorophyll meter. Annals of Botany 82, 389–392.Google Scholar
Houlden, A., Timms-Wilson, T. M., Day, M. J. & Bailey, M. J. (2008). Influence of plant developmental stage on microbial community structure and activity in the rhizosphere of three field crops. FEMS Microbiology Ecology 65, 193–201.Google Scholar
Iturbe-Ormaetxe, I., Morán, J. F., Arrese-Igor, C., Gogorcena, Y., Klucas, R. V. & Becana, M. (1995). Activated oxygen and antioxidant defences in iron-deficient pea plants. Plant Cell and Environment 18, 421–429.Google Scholar
Ji, C., Juarez-Hernández, R. E. & Miler, M. J. (2012). Exploiting bacterial iron acquisition: siderophore conjugates. Future Medicinal Chemistry 4, 297–313.Google Scholar
Jin, C. W., Chen, W. W., Meng, Z. B. & Zheng, S. J. (2008). Iron deficiency-induced increase of root branching contributes to the enhanced root ferric chelate reductase activity. Journal of Integrative Plant Biology 50, 1557–1562.Google Scholar
Jin, C. W., Li, G. X., Yu, X. H. & Zheng, S. J. (2010). Plant Fe status affects the composition of siderophore-secreting microbes in the rhizosphere. Annals of Botany 105, 835–841.CrossRefGoogle ScholarPubMed
Kirk, J. L., Klironomos, J. N., Lee, H. & Trevors, J. T. (2005). The effects of perennial ryegrass and alfalfa on microbial abundance and diversity in petroleum contaminated soil. Environmental Pollution 133, 455–465.Google Scholar
Martí, M. C., Camejo, D., Fernández-García, N., Rellán-Álvarez, R., Marques, S., Sevilla, F. & Jiménez, A. (2009). Effect of oil refinery sludges on the growth and antioxidant system of alfalfa plants. Journal of Hazardous Materials 171, 879–885.CrossRefGoogle ScholarPubMed
Martínez-Alcalá, I., Walker, D. J. & Bernal, M. P. (2010). Chemical and biological properties in the rhizosphere of Lupinus albus alter soil heavy metal fractionation. Ecotoxicology and Environmental Safety 73, 595–602.CrossRefGoogle ScholarPubMed
Masalha, J., Kosegarten, H., Elmaci, O. & Mengel, K. (2000). The central role of microbial activity for iron acquisition in maize and sunflower. Biology and Fertility of Soils 30, 433–439.Google Scholar
Matthijs, S., Laus, G., Meyer, J. M., Abbaspour-Tehrani, K., Schäfer, M., Budzikiewicz, H. & Cornelis, P. (2009). Siderophore-mediated iron acquisition in the entomopathogenic bacterium Pseudomonas entomophila L48 and its close relative Pseudomonas putida KT2440. Biometals 22, 951–964.Google Scholar
Meyer, J. M. (2000). Pyoverdines: pigments, siderophores and potential taxonomic markers of fluorescent Pseudomonas species. Archives of Microbiology 174, 135–142.Google Scholar
Miller, G. W., Huang, I. J., Welkie, G. W. & Pushnik, J. C. (1995). Function of iron in plants with special emphasis on chloroplasts and photosynthetic activity. In Iron Nutrition in Soils and Plant (Ed. Abadia, J.), pp. 19–28. Dordecht, The Netherlands: Kluwer Academic Publishers.Google Scholar
Mordukhava, E. A., Skvortsova, N. P., Kochetkov, V. V., Dubeikovskii, A. N. & Boronin, A. M. (1991). Synthesis of the phytohormone indole-3-acetic acid by rhizosphere bacteria of the genus Pseudomonas. Microbiology 60, 345–349.Google Scholar
Morrissey, J. & Guerinot, M. L. (2009). Iron uptake and transport in plants: The good, the bad, and the ionome. Chemical Reviews 109, 4553–4567.Google Scholar
Negishi, T., Nakanishi, H., Yazaki, J., Kishimoto, N., Fujii, F., Shimbo, K., Yamamoto, K., Sakata, K., Sasaki, T., Kikuchi, S., Mori, S. & Nishizawa, N. K. (2002). cDNA microarray analysis of gene expression during Fe-deficiency stress in barley suggests that polar transport of vesicles is implicated in phytosiderophore secretion in Fe-deficient barley roots. Plant Journal 30, 83–94.Google Scholar
Peralta-Videa, J. R., De La Rosa, G., González, J. H. & Gardea-Torresdey, J. L. (2004). Effects of the growth stage on the heavy metal tolerance of alfalfa plants. Advances in Environmental Research 8, 679–685.Google Scholar
Podile, A. R. & Krishna Kishore, G. (2006). Plant growth-promoting rhizobacteria. In Plant-Associated Bacteria (Ed. Gnanamanickam, S. S.), pp. 195–230. Dordrecht, The Netherlands: Springer.Google Scholar
Rabotti, G. & Zocchi, G. (1994). Plasma membrane-bound H+-ATPase and reductase activities in Fe-deficient cucumber roots. Physiologia Plantarum 90, 779–785.Google Scholar
Richens, D. T. (2005). Ligand substitution reactions at inorganic centers. Chemical Reviews 105, 1961–2002.Google Scholar
Robinson, N. J., Procter, C. M., Connolly, E. L. & Guerinot, M. L. (1999). A ferric-chelate reductase for iron uptake from soils. Nature 397, 694–697.Google Scholar
Romano, J. D. & Kolter, R. (2005). Pseudomonas-Saccharomyces interactions: influence of fungal metabolism on bacterial physiology and survival. Journal of Bacteriology 187, 940–948.Google Scholar
Römheld, V. (1991). The role of phytosiderophores in acquisition of iron and other micronutrients in graminaceous species: an ecological approach. Plant and Soil 130, 127–134.Google Scholar
Schmidt, W. (2003). Iron solutions: acquisition strategies and signaling pathways in plants. Trends in Plant Science 8, 188–193.Google Scholar
Sevilla, F., Del Río, L. A. & Hellín, E. (1984). Superoxide dismutases from a Citrus plant: presence of two iron-containing isoenzymes in leaves of lemon trees. Journal of Plant Physiology 116, 381–387.CrossRefGoogle ScholarPubMed
Sharma, A., Johri, B. N., Sharma, A. K. & Glick, B. R. (2003). Plant growth-promoting bacterium Pseudomonas sp strain GRP(3) influences iron acquisition in mung bean (Vigna radiata L. Wilzeck). Soil Biology and Biochemistry 35, 887–894.Google Scholar
Tomasi, N., Kretzschmar, T., Espen, L., Weisskopf, L., Fuglsang, A. T., Palmgren, M. G., Neumann, G., Varanini, Z., Pinton, R., Martinoia, E. & Cesco, S. (2009). Plasma membrane H+-ATPase-dependent citrate exudation from cluster roots of phosphate-deficient white lupin. Plant Cell and Environment 32, 465–475.Google Scholar
Vanacker, H., Sandalio, L. M., Jiménez, A., Palma, J. M., Corpas, F. J., Meseguer, V., Gómez, M., Sevilla, F., Leterrier, M., Foyer, C. H. & Del Río, L. A. (2006). Roles for redox regulation in leaf senescence of pea plants grown on different sources of nitrogen nutrition. Journal of Experimental Botany 57, 1735–1745.Google Scholar
Vert, G., Grotz, N., Dedaldechamp, F., Gaymard, F., Guerinot, M. L., Briat, J. F. & Curie, C. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223–1233.Google Scholar
Wang, M. Y., Xia, R. X., Hu, L. M., Dong, T. & Wu, Q. S. (2007). Arbuscular mycorrhizal fungi alleviate iron deficient chlorosis in Poncirus trifoliata L. Raf under calcium bicarbonate stress. Journal of Horticultural Science and Biotechnology 82, 776–780.Google Scholar
Weber, G., Von Wiren, N. & Hayen, H. (2008). Investigation of ascorbate-mediated iron release from ferric phytosiderophores in the presence of nicotianamine. Biometals 21, 503–513.CrossRefGoogle ScholarPubMed
Zocchi, G. & Cocucci, S. (1990). Fe uptake mechanism in Fe-efficient cucumber roots. Plant Physiology 92, 908–911.Google Scholar