The Roles Of Auxin During Plant-microbe Interactions

Among all the phytohormones, auxin likely plays the most roles in plant physiology. With an intricate biosynthesis pathway and a complex gene signaling cascade, auxin is involved in many biological processes, including plant growth and responses against potential pathogens. It has been extensively documented that some microorganisms are capable of synthesizing this phytohormone, especially indole-3-acetic acid (IAA), the major naturally occurring auxin. In an environmental scenario consisting of bacteria and fungi interacting with plants, the production of auxin by such microorganisms may lead to hormonal imbalances in the host. This disturbance in plant hormonal status can modulate plant metabolism and defense systems, favoring symbiosis or pathogenesis. The basic mechanism of IAA as a modulator of plant gene expression is well understood, and new evidence about the mechanisms by which microbes affect plant auxin activities is now emerging. This review focuses on the effects of auxins produced by microorganisms during plant-microbe interactions. The routes of auxin biosynthesis in bacteria and fungi are described for some organisms. We also give examples of the effects of microbe-produced auxin in symbiotic and pathogenic events and describe how plants modulate IAA signaling to counteract infection by biotrophic pathogens. © 2012 Nova Science Publishers, Inc. All rights reserved.3151Abreu, M.E., Munné-Bosch, S., Salicylic acid deficiency in NahG transgenic lines and sid2 mutants increases seed yield in the annual plant Arabidopsis thaliana (2009) Journal of Experimental Botany, 60, pp. 1261-1271Arteca, R.N., Arteca, J.M., Effects of brassinosteroid, auxin, and cytokinin on ethylene production in Arabidopsis thaliana plants (2008) Journal of Experimental Botany, 59, pp. 3019-3026Bari, R., Jones, J.D., Role of plant hormones in plant defence responses (2009) Plant Mol Biol, 69, pp. 473-488Barker, S.J., Tagu, D., The Roles of Auxins and Cytokinins in Mycorrhizal Symbioses (2000) Journal of Plant Growth Regulation, 19, pp. 144-154Bashan, Y., Holguin, G., Azospirillum-plant relationships: environmental and physiological advances (1990-1996) (1997) Canadian Journal of Microbiology, 43, pp. 103-121Basse, C.W., Lottspeich, F., Steglich, W., Kahmann, R., Two potential indole-3-acetaldehyde dehydrogenases in the phytopathogenic fungus Ustilago maydis (1996) European Journal of Biochemistry, 242, pp. 648-656Berg, G., Plant-microbe interactions promoting plant growth and health: perspectives for controlled use of microorganisms in agriculture (2009) Applied Microbiology and Biotechnology, 84, pp. 11-18Bianco, C., Imperlini, E., Calogero, R., Senatore, B., Amoresano, A., Carpentieri, A., Pucci, P., Defez, R., Indole-3-acetic acid improves Escherichia coli defences to stress (2006) Archives of Microbiology, 185, pp. 373-382Bölker, M., Basse, C.W., Schirawski, J., Ustilago maydis secondary metabolism-from genomics to biochemistry (2008) Fungal Genetics and Biology, 45 (SUPPL. 1), pp. S88-93Cernadas, R.A., Camillo, L.R., Benedetti, C.E., Transcriptional analysis of the sweet orange interaction with the citrus canker pathogens Xanthomonas axonopodis pv. citri and Xanthomonas axonopodis pv. aurantifolii (2008) Molecular Plant Pathology, 9, pp. 609-631Chung, K.R., Shilts, T., Ertürk, U., Timmer, L.W., Ueng, P.P., Indole derivatives produced by the fungus Colletotrichum acutatum causing lime anthracnose and postbloom fruit drop of citrus (2003) FEMS Microbiology Letters, 226, pp. 23-30Darwin, C., The power of movement in plants (1880), London: John MurrayDing, X., Cao, Y., Huang, L., Zhao, J., Xu, C., Li, X., Wang, S., Activation of the indole-3-acetic acid-amido synthetase GH3-8 suppresses expansin expression and promotes salicylate-and jasmonate-independent basal immunity in rice (2008) The Plant Cell, 20, pp. 228-240Dobbelaere, S., Croonenborghs, A., Thys, A., Vande Broek, A., Vanderleyden, J., Phytostimulatory effect of Azospirillum brasilense wild type and mutant strains altered in IAA production on wheat (1999) Plant and Soil, 212, pp. 155-164Felten, J., Kohler, A., Morin, E., Bhalerao, R.P., Palme, K., Martin, F., Ditengou, F.A., Legué, V., The ectomycorrhizal fungus Laccaria bicolor stimulates lateral root formation in poplar and Arabidopsis through auxin transport and signaling (2009) Plant Physiology, 151, pp. 1991-2005Felten, J., Legué, V., Ditengou, F.A., Lateral root stimulation in the early interaction between Arabidopsis thaliana and the ectomycorrhizal fungus Laccaria bicolor is fungal auxin the trigger? (2010) Plant Signaling and Behavior, 5, pp. 864-867Fu, J., Liu, H., Li, Y., Yu, H., Li, X., Xiao, J., Wang, S., Manipulating broad-spectrum disease resistance by suppressing pathogen-induced auxin accumulation in rice (2011) Plant Physiology, 155, pp. 589-602Fukuhara, H., Minakawa, Y., Akao, S., Minamisawa, K., The involvement of indole-3-acetic acid produced by Bradyrhizobium elkanii in nodule formation (1994) Plant Cell and Physiology, 35, pp. 1261-1265Ghosh, S., Basu, P.S., Production and metabolism of indole acetic acid in roots and root nodules of Phaseolus mungo (2006) Microbiological Research, 161, pp. 362-366Gruen, H.E., Auxins and fungi (1959) Annual Review of Plant Physiology, 10, pp. 405-440Grunewald, W., Cannoot, B., Friml, J., Gheysen, G., Parasitic nematodes modulate PIN-mediated auxin transport to facilitate infection (2009) PLoS Pathogens, 5 (1), pp. e1000266Kämper, J., Kahmann, R., Bölker, M., Ma, L.J., Brefort, T., Saville, B.J., Banuett, F., Birren, B.W., Insights from the genome of the biotrophic fungal plant pathogen Ustilago maydis (2006) Nature, 444, pp. 97-101Karabaghli, C., Frey-Klett, P., Sotta, B., Bonnet, M., Le Tacon, F., Vitro effects of Laccaria bicolor S238N and Pseudomonas fluorescens strain BBc6 on rooting of de-rooted shoot hypocotyls of Norway spruce (1998) Tree Physiology, 18, pp. 103-111Kazan, K., Manners, J.M., Linking development to defense: auxin in plant-pathogen interactions (2009) Trends in Plant Science, 14, pp. 373-382Kilaru, A., Bailey, B.A., Hasenstein, K.H., Moniliophthora perniciosa produces hormones and alters endogenous auxin and salicylic acid in infected cocoa leaves (2007) FEMS Microbiology Letters, 274, pp. 238-244Kunkel, B.N., Brooks, D.M., Cross talk between signaling pathways in pathogen defense (2002) Current Opinion in Plant Biology, 5, pp. 325-331Lambrecht, M., Okon, Y., Vande Broek, A., Vanderleyden, J., Indole-3-acetic acid: a reciprocal signalling molecule in bacteria-plant interactions (2000) Trends in Microbiology, 8, pp. 298-300Liu, P., Nester, E.W., Indoleacetic acid, a product of transferred DNA, inhibits vir gene expression and growth of Agrobacterium tumefaciens C58 (2006) Proceedings of the National Academy of Sciences of the United States of America, 103, pp. 4658-4662Llorente, F., Muskett, P., Sánchez-Vallet, A., López, G., Ramos, B., Sánchez-Rodríguez, C., Jordá, L., Molina, A., Repression of the auxin response pathway increases Arabidopsis susceptibility to necrotrophic fungi (2008) Molecular Plant, 1, pp. 496-509López, M.A., Bannenberg, G., Castresana, C., Controlling hormone signaling is a plant and pathogen challenge for growth and survival (2008) Current Opinion in Chemical Biology, 11, pp. 420-427Maor, R., Haskin, S., Levi-Kedmi, H., Sharon, A., Planta production of indole-3-acetic acid by Colletotrichum gloeosporioides f. sp. aeschynomene (2004) Applied and Environmental Microbiology, 70, pp. 1852-1854Marois, E., Van den Ackerveken, G., Bonas, U., The Xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host (2002) Molecular Plant Microbe Interactions, 15, pp. 637-646Mathesius, U., Auxin: at the root of nodule development? (2008) Functional Plant Biology, 35, pp. 651-668McQueen-Mason, S., Durachko, D.M., Cosgrove, D.J., Two endogenous proteins that induce cell wall extension in plants (1992) The Plant Cell, 4, pp. 1425-1433Mondego, J.M., Carazzolle, M.F., Costa, G.G., Formighieri, E.F., Parizzi, L.P., Rincones, J., Cotomacci, C., Pereira, G.A., A genome survey of Moniliophthora perniciosa gives new insights into Witches' Broom Disease of cacao (2008) BMC Genomics, 9, p. 548Navarro, L., Dunoyer, P., Jay, F., Arnold, B., Dharmasiri, N., Estelle, M., Voinnet, O., Jones, J.D., A plant miRNA contributes to antibacterial resistance by repressing auxin signaling (2006) Science, 312, pp. 436-439Nielsen, N., Materials which hasten the growth of Avena coleoptiles (1928) Planta, 6, pp. 376-378Normanly, J., Approaching cellular and molecular resolution of auxin biosynthesis and metabolism (2010) Cold Spring Harbor Perspectives in Biology, 2 (1), pp. a001594Park, J.-E., Park, J.-Y., Kim, Y.-S., Staswick, P.E., Jeon, J., Yun, J., Kim, S.-Y., Park, C.-M., GH3-mediated auxin homeostasis links growth regulation with stress adaptation response in Arabidopsis (2007) The Journal of Biological Chemistry, 282, pp. 10036-10046Patten, C.L., Glick, B.R., Bacterial biosynthesis of indole-3-acetic acid (1996) Canadian Journal of Microbiology, 42 (3), pp. 207-220Perley, J.E., Stowe, B.B., On the ability of Taphrina deformans to produce indoleacetic acid from tryptophan by way of tryptamine (1966) Plant Physiology, 41, pp. 234-237Persello-Cartieaux, F., Nussaume, L., Robaglia, C., Tales from the underground: molecular plant-rhizobacteria interactions (2003) Plant, Cell and Environment, 26, pp. 189-199Pii, Y., Crimi, M., Cremonese, G., Spena, A., Pandolfini, T., Auxin and nitric oxide control indeterminate nodule formation (2007) BMC Plant Biology, 7, p. 21Prusty, R., Hunter, A., Kashpur, O., Normanly, J., Aberrant synthesis of Indole-3-acetic Acid in Saccharomyces cerevisiae triggers morphogenic transition, a virulence trait of pathogenic fungi (2010) Genetics, 220, pp. 211-220Prusty, R., Grisafi, P., Fink, G.R., The plant hormone indoleacetic acid induces invasive growth in Saccharomyces cerevisiae (2004) Proceedings of the National Academy of Sciences of the United States of America, 101, pp. 4153-4157Reineke, G., Heinze, B., Schirawski, J., Buettner, R., Indole-3-acetic acid (IAA) biosynthesis in the smut fungus Ustilago maydis and its relevance for increased IAA levels in infected tissue (2008) Molecular Plant Pathology, 9, pp. 339-355Remans, R., Spaepen, S., Vanderleyden, J., Auxin signaling in plant defense (2006) Science, 313, p. 171Robert-Seilaniantz, A., Navarro, L., Bari, R., Jones, J.D.G., Pathological hormone imbalances (2007) Current Opinion in Plant Biology, 10, pp. 372-379Robinette, D., Matthysse, A.G., Inhibition by Agrobacterium tumefaciens and Pseudomonas savastanoi of development of the hypersensitive response elicited by Pseudomonas syringae pv. phaseolicola (1990) Journal of Bacteriology, 172, pp. 5742-5749Robinson, M., Riov, J., Sharon, A., Indole-3-acetic acid biosynthesis in Colletotrichum gloeosporioides f. sp. aeschynomene (1998) Applied and Environmental Microbiology, 64, pp. 5030-5032Santner, A., Calderon-Villalobos, L., Estelle, M., Plant hormones are versatile chemical regulators of plant growth (2009) Nature Chemical Biology, 5, pp. 301-307Spaepen, S., Vanderleyden, J., Auxin and plant-microbe interactions (2011) Cold Spring Harbor Perspectives in Biology, 1 (4), p. 3Spaepen, S., Vanderleyden, J., Remans, R., Indole-3-acetic acid in microbial and microorganism-plant signaling (2007) FEMS Microbiological Reviews, 31, pp. 425-448Splivallo, R., Fischer, U., Göbel, C., Feussner, I., Karlovsky, P., Truffles regulate plant root morphogenesis via the production of auxin and ethylene (2009) Plant Physiology, 150, pp. 2018-2029Staswick, P.E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M.T., Maldonado, M.C., Suza, W., Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid (2005) The Plant Cell, 17, pp. 616-627Steenhoudt, O., Vanderleyden, J., Azospirillum, a free living nitrogen-fixing bacterium closely associated with grasses: genetic, biochemical and ecological aspects (2000) FEMS Microbiological Reviews, 24, pp. 487-506Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.-Y., Dolezal, K., Schlereth, A., Alonso, J.M., TAA1-Mediated Auxin Biosynthesis Is Essential for Hormone Crosstalk and Plant Development (2008) Cell, 133, pp. 177-191Tanaka, E., Tanaka, C., Ishihara, A., Kuwahara, Y., Tsuda, M., Indole-3-acetic acid biosynthesis in Aciculosporium take, a causal agent of witches' broom of bamboo (2003) Journal of General Plant Pathology, 69, pp. 1-6Tiryaki, I., Staswick, P.E., An Arabidopsis Mutant Defective in Jasmonate Response Is Allelic to the Auxin-Signaling Mutant axr1 (2002) Plant Physiology, 130, pp. 887-894van Noorden, G.E., Kerim, T., Goffard, N., Wiblin, R., Pellerone, F.I., Rolfe, B.G., Mathesius, U., Overlap of proteome changes in Medicago truncatula in response to auxin and Sinorhizobium meliloti (2007) Plant Physiology, 144, pp. 1115-1131Vande Broek, A., Lambrecht, M., Eggermont, K., Vanderleyden, J., Auxins upregulate expression of the indole-3-pyruvate decarboxylase gene in Azospirillum brasilense (1999) Journal of Bacteriology, 181, pp. 1338-1342Vande Broek, A., Gysegom, P., Ona, O., Hendrickx, N., Prinsen, E., Impe, J.V., Vanderleyden, J., Transcriptional Analysis of the Azospirillum brasilense Indole-3-Pyruvate Decarboxylase Gene and Identification of a cis-Acting Sequence Involved in Auxin Responsive Expression (2005) Molecular Plant Microbe Interactions, 18, pp. 311-323Vandeputte, O., Oden, S., Mol, A., Vereecke, D., Goethals, K., El Jaziri, M., Prinsen, E., Biosynthesis of auxin by the gram-positive phytopathogen Rhodococcus fascians is controlled by compounds specific to infected plant tissues (2005) Applied and Environmental Microbiology, 71, pp. 1169-1177Verstrepen, K., Klis, F., Flocculation, adhesion and biofilm formation in yeasts (2006) Molecular Microbiology, 60, pp. 5-15Wang, D., Pajerowska-Mukhtar, K., Culler, A.H., Dong, X., Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway (2007) Current Biology, 17, pp. 1784-1790Woltering, E.J., Balk, P., Nijenhuis-Devries, M., Faivre, M., Ruys, G., Somhorst, D., Philosoph-Hadas, S., Friedman, H., An auxin-responsive 1-aminocyclopropane-1-carboxylate synthase is responsible for differential ethylene production in gravistimulated Antirrhinum majus L. flower stems (2005) Planta, 220, pp. 403-413Woodward, A.W., Bartel, B., Auxin: Regulation, action, and interaction (2005) Annals of Botany, 95, pp. 707-735Zambryski, P., Tempe, J., Schell, J., Transfer and function of T-DNA genes from Agrobacterium Ti-plasmid and Ri-plasmid in plants (1989) Cell, 56, pp. 193-201Yang, S., Zhang, Q., Guo, J., Charkowski, A.O., Glick, B.R., Ibekwe, A.M., Cooksey, D.A., Yang, C.-H., Global effect of indole-3-acetic acid biosynthesis on multiple virulence factors of Erwinia chrysanthemi 3937 (2007) Applied and Environmental Microbiology, 73, pp. 1079-108