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Auxin and Plant-Microbe Interactions Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Auxin and Plant-Microbe Interactions Stijn Spaepen and Jos Vanderleyden Centre of Microbial and Plant Genetics, Department of Microbial and Molecular Systems, Katholieke Universiteit Leuven, B-3001 Leuven, Belgium Correspondence: [email protected] Microbial synthesis of the phytohormone auxin has been known for a long time. This property is best documented for bacteria that interact with plants because bacterial auxin can cause interference with the many plant developmental processes regulated by auxin. Auxin biosynthesis in bacteria can occur via multiple pathways as has been observed in plants. There is also increasing evidence that indole-3-acetic acid (IAA), the major naturally occurring auxin, is a signaling molecule in microorganisms because IAA affects gene expression in some microorganisms. Therefore, IAA can act as a reciprocal signaling mol- ecule in microbe-plant interactions. Interest in microbial synthesis of auxin is also increasing in yet another recently discovered property of auxin in Arabidopsis. Down-regulation of auxin signaling is part of the plant defense system against phytopathogenic bacteria. Exogenous application of auxin, e.g., produced by the pathogen, enhances susceptibility to the bacterial pathogen. he phytohormone auxin (from the Greek (Persello-Cartieaux et al. 2003; Spaepen et al. T“auxein,” meaning to grow) regulates a 2007a). The term rhizobacteria refers to the whole repertoire of plant developmental proc- fact that their numbers are highly enriched in esses, as documented in previous articles on the rhizosphere, i.e., the narrow band of soil this topic. Perhaps less well known is the fact that surrounds the root (Hiltner 1904; Smalla that some microorganisms also produce au- et al. 2006; van Loon 2007). Of more recent xin (Costacurta and Vanderleyden 1995; Patten date is the observation that auxin (indole-3- and Glick 1996). In their interaction with acetic acid or IAA) is a signaling molecule in plants, these microorganisms can interfere some microorganisms (Spaepen et al. 2007a). with plant development by disturbing the auxin Bringing these data together, it follows that balance in plants. This is best documented for auxin can have a major impact in microorgan- phytopathogenic bacteria like Agrobacterium ism-plant interactions. This is the main theme spp. and Pseudomonas savastanoi pv. savastanoi, addressed in this article. Finally, the recent find- causing tumors and galls, respectively (Jameson ing that auxin signaling in plants is also part of 2000; Mole et al. 2007), and plant growth pro- the Arabidopsis defense response against a leaf moting rhizobacteria (PGPR) such as Azospiril- pathogen (Navarro et al. 2006) is discussed in lum spp. that impact on plant root development relation to bacterial IAA synthesis. Editors: Mark Estelle, Dolf Weijers, Ottoline Leyser, and Karin Ljung Additional Perspectives on Auxin Signaling available at www.cshperspectives.org Copyright # 2011 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a001438 Cite this article as Cold Spring Harb Perspect Biol 2011;3:a001438 1 Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press S. Spaepen and J. Vanderleyden BIOSYNTHESIS PATHWAYS IN BACTERIA been identified using several genetic and bio- chemical methods. However, not all genes, Production of IAA has been reported for many enzymes encoded, or intermediates have been bacteria. It is even assumed that over 80% of the characterized. Especially, the use of feeding ex- bacteria isolated from the rhizosphere are capa- periments with labeled precursors in combina- ble to synthesize IAA (Patten and Glick 1996; tion with the identification of intermediates Khalid et al. 2004). The main precursor for has been a major source for the identification the synthesis of IAA is tryptophan. Addition of biosynthetic pathways. The pathways de- of tryptophan to culture media results in all scribed in literature are illustrated in Figure 1 cases in higher IAA production. Biosynthesis and are mostly named according to a key inter- of tryptophan starts from the metabolic node mediate of the given pathway. In several studied chorismate in a five-step reaction encoded by microorganisms, redundancy of IAA biosyn- the trp genes. The branch point compound thetic pathways is observed, meaning that mul- chorismate is synthesized starting from phos- tiple pathways are present and active in one phoenolpyruvate and erythrose 4-phosphate single microorganism. This observation is main- in the shikimate pathway, a common pathway ly based on knockout studies in which some for the biosynthesis of aromatic amino acids IAA production could still be observed after and many secondary metabolites (Dosselaere inactivation of a single pathway. In the follow- and Vanderleyden 2001; Merino et al. 2008). ing sections, an overview of the IAA biosyn- Starting with tryptophan, at least five dif- thetic pathways in bacteria is given. ferent pathways have been described for the synthesis of IAA, and most pathways show sim- Indole-3-Acetamide Pathway ilarity to those described in plants, although some intermediates can differ (Patten and Glick As the indole-3-acetamide (IAM) pathway is 1996; Woodward and Bartel 2005; Spaepen et al. present in several pathogens and can contribute 2007a). The IAA biosynthetic pathways have to the virulence of these strains by producing OH N N N N H H Nitrilase Indole-3-acetaldoxime Indole-3-acetonitrile Glucobrassicin Nitrile hydratase H2N O N OH Trp mono- H IAM-hydrolase HO O Indole-3-acetamide oxygenase O NH 2 N N H Tryptophan side-chain oxidase H Chorismate Anthranilate Tryptophan Indole-3-acetic acid OH O IAAId O O N N dehydrogenase Amino transferase H IPDC H Indole-3-pyruvate Indole-3-acetaldehyde NH 2 N Trp decarboxylase H Amine-oxidase Tryptamine Trp-independent biosynthesis pathway OH HO O OH N N H H Indole-3-lactate Tryptophol Figure 1. Overview of IAA biosynthetic pathways in bacteria. Dashed lines refer to the name of pathways, mostly named after an intermediate. IAAld, indole-3-acetaldehyde; IAM, indole-3-acetamide; IPDC, indole-3- pyruvate decarboxylase; Trp, tryptophan. Adapted from Spaepen et al. (2007). 2 Cite this article as Cold Spring Harb Perspect Biol 2011;3:a001438 Downloaded from http://cshperspectives.cshlp.org/ on September 27, 2021 - Published by Cold Spring Harbor Laboratory Press Auxin and Plant-Microbe Interactions high amounts of IAA (Jameson 2000; Persello- iaaH could be isolated from B. japonicum Cartieaux et al. 2003), the genes/proteins and (Sekine et al. 1988; Sekine et al. 1989). Later, their regulation involved in this pathway are the presence of the IAM pathway was also con- well characterized. The pathway consists of firmed for Rhizobium sp. strain NGR234 by two distinct steps. In the first step tryptophan LC-MS detection of intermediates (Theunis monooxygenase (encoded by iaaM gene) con- et al. 2004). verts tryptophan to IAM; in the second step IAM is hydrolyzed to IAA and ammonia by an Indole-3-Pyruvate Pathway IAM hydrolase (encoded by iaaH gene). Both genes have been characterized from many phy- The indole-3-pyruvate (IPA) pathway is a major topathogens such as Agrobacterium tumefaciens, auxin pathway in plants. The IPA pathway could P. savastanoi, Pseudomonas syringae, Pantoea be shown in many bacteria such as phytopatho- agglomerans, but also in symbiotic nitrogen- gens (P. agglomerans), plant beneficial bacteria fixing bacteria belonging to Rhizobium and (Azospirillum, Bacillus, Bradyrhizobium, Enter- Bradyrhizobium species (Sekine et al. 1989; Clark obacter cloacae, Paenibacillus, Pseudomonas, et al. 1993; Morris 1995; Theunis et al. 2004). In and Rhizobium), and even cyanobacteria. The A. tumefaciens, these genes are located in the pathway consists of three steps. In a first step T-DNA region of the pTi plasmid together the precursor tryptophan is transaminated to with the ipt gene (coding for dimethylallyl- IPA by an aminotransferase. Aminotransferase pyrophosphate:AMP dimethylallyltransferase), activity has been shown in different IAA-pro- involved in cytokinin production (for reviews ducing bacteria such as Azospirillum brasilense see Hooykaas and Beijersbergen 1994; Costa- and Azospirillum lipoferum (Ruckda¨schel et al. curta and Vanderleyden 1995). A. tumefaciens 1988; Baca et al. 1994). In the rate-limiting can infect dicotyledonous plants at wound sites step IPA is decarboxylated to indole-3-acetalde- by transferring the T-DNA inside the plant cells hyde (IAAld), which is then oxidized to IAA by a (genetic colonization), where it is stably inte- dehydrogenase. The decarboxylation step is cat- grated into the genome. Several genes encoded alyzed by the key enzyme indole-3-pyruvate on the T-DNA are expressed in the plant nu- decarboxylase (encoded by ipdC gene). Based cleus, causing an imbalance in the hormonal on phylogenetic and biochemical analysis, this status of the plant cells and thereby inducing group of enzymes could be divided into two crown gall tumors (for reviews see Zambryski subgroups, indicating a distinct origin of the et al. 1989; Zambryski 1992; Hooykaas and encoding genes (Spaepen et al. 2007b). Several Beijersbergen 1994). In the plant pathogen members have been isolated and characterized P. savastanoi pv. savastanoi, which produces from diverse bacteria such as A. brasilense, A. high amounts of IAA in culture medium lipoferum, E. cloacae, Pseudomonas putida, and (Glickmann et al. 1998; Manulis et al. 1998; P. agglomerans (Koga et al. 1991; Costacurta Buell et al. 2003), the iaaM and iaaH genes et al. 1994; Brandl and Lindow 1996; Patten are located on plasmid pIAA1 (Comai and and Glick 2002b). Inactivation of these genes Kosuge 1982). Both genes are clustered in the results in impaired IAA production (sometimes iaa operon, and loss of the pIAA1 plasmid .90%), indicating the importance of the results in the loss of IAA production in free liv- encoded enzymes and consequently the IPA ing cultures. Strains without the pIAA1 plasmid pathway in the IAA biosynthesis (Prinsen et al.
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