Global Effect of Indole-3-Acetic Acid Biosynthesis on Multiple Virulence Factors of Erwinia chrysanthemi 3937

Abstract

Production of the plant hormone indole-3-acetic acid (IAA) is widespread among plant-associated microorganisms. The non-gall-forming phytopathogen Erwinia chrysanthemi 3937 (strain Ech3937) possesses iaaM (ASAP16562) and iaaH (ASAP16563) gene homologues. In this work, the null knockout iaaM mutant strain Ech138 was constructed. The IAA production by Ech138 was reduced in M9 minimal medium supplemented with L-tryptophan. Compared with wild-type Ech3937, Ech138 exhibited reduced ability to produce local maceration, but its multiplication in Saintpaulia ionantha was unaffected. The pectate lyase production of Ech138 was diminished. Compared with wild-type Ech3937, the expression levels of an oligogalacturonate lyase gene, ogl, and three endopectate lyase genes, pelD, pelI, and pelL, were reduced in Ech138 as determined by a green fluorescent protein-based fluorescence-activated cell sorting promoter activity assay. In addition, the transcription of type III secretion system (T3SS) genes, dspE (a putative T3SS effector) and hrpN (T3SS harpin), was found to be diminished in the iaaM mutant Ech138. Compared with Ech3937, reduced expression of hrpL (a T3SS alternative sigma factor) and gacA but increased expression of rsmA in Ech138 was also observed, suggesting that the regulation of T3SS and pectate lyase genes by IAA biosynthesis might be partially due to the posttranscriptional regulation of the Gac-Rsm regulatory pathway.Erwinia chrysanthemi is an opportunistic phytopathogen that causes soft rot, wilt, and blight diseases on a wide range of plant host species (18, 39). Several virulence determinants have been discovered in E. chrysanthemi including the type III secretion system (T3SS) and well-studied extracellular enzymes such as pectate lyase and pectinase (35,97).In E. chrysanthemi, the pectinases (Pel), which are secreted through the type II secretion system, attack the plant cell wall pectin and lead to the loss of plant cell wall structural integrity (1,44,91,93,98,99). The production of pectinases is induced by pectin and its derivatives including polygalacturonate (PGA) and is tightly regulated by environmental conditions (5, 39, 40). Several transcriptional regulators, including Fur, HNS, KdgR, PecS, PecT, cyclic AMP receptor protein, ExpR, and Pir, have been shown to modulate the expression of the genes encoding Pel enzymes (12,13,19,20,29,39,67,68,70,74,83,84,85,86,95). In addition, several interconnections between these regulatory systems have been observed (39,67,69,71,72,73,74). Consequently, this complex regulatory network allows E. chrysanthemi to use pectin as a sole carbon and energy source for growth as well as to finely adjust the synthesis of its virulence factors during pathogenesis.The T3SS is considered one of the major pathogenic factors in many bacterial pathogens (14,21,31,32,35,103,104). Recently, a T3SS regulatory pathway of strain Ech3937 was elucidated (105). Similarly to Pseudomonas syringae and Erwinia and Pantoea spp., the T3SS of Ech3937 is regulated by HrpX/HrpY, a two-component...

The Conjugated Auxin Indole-3-Acetic Acid–Aspartic Acid Promotes Plant Disease Development

“…Indeed, several studies have demonstrated the importance of the different components of the auxin signaling pathway in resistance against biotrophs and necrotrophs (El Oirdi and Bouarab, 2007;Yang et al, 2007;Spoel and Dong, 2008;Cuzick et al, 2009;Truman et al, 2010;Kidd et al, 2011). Nevertheless, a direct, major role for IAA in plant susceptibility has not yet been demonstrated.…”

“…A role for auxin in plant disease has long been suspected since many pathogens produce auxin during interaction with their host and because auxin can modulate the plant defense response (Yamada, 1993;Yang et al, 2007;Kazan and Manners, 2009). Auxin signaling has also been shown to promote disease caused by a number of pathogens (Grant and Jones, 2009;Kazan and Manners, 2009), and several auxin signaling mutants are more resistant to necrotrophic and biotrophic pathogens than are wildtype plants (Navarro et al, 2006;Chen et al, 2007;El Oirdi and Bouarab, 2007;Wang et al, 2007;Cuzick et al, 2009;Kidd et al, 2011).…”

Indole-3-acetic acid in plant–pathogen interactions: a key molecule for in planta bacterial virulence and fitness

“…Regarding plant-associated bacteria, IAA has been shown to determine changes in bacterial gene expression in the nongall-forming phytopathogen D. dadantii (formerly Erwinia herbicola) 3937 [57], in Agrobacterium tumefaciens [58,59] and in the plant growth-stimulating rhizobacterium A. brasilense [60], in which its ipdC gene has been the only bacterial gene reported to possess an AuxRE in its promoter, as observed in the auxin-responsive genes of plants [48]. Similarly, in the yeast Saccharomyces cerevisiae, several IAA-inducible genes are regulated at high IAA concentrations by the fungal transcriptional activator YAP-1, which is able to bind to their promoters to induce a switch towards invasive behavior, together with an arrest of cell growth.…”

Production of the Phytohormone Indole-3-Acetic Acid by Estuarine Species of the Genus Vibrio

“…Microorganisms that produce IAA can influence the host plant and function as pathogens, symbionts, or growth regulators, depending on how their IAA production influences the concentration of the plant's endogenous IAA pool and on the sensitivity of the plant to auxin. Organisms such as Erwinia chrysanthemi, Pseudomonas savastanoi, and Agrobacterium tumefaciens are phytopathogens of many host plants (11,21,23,46). Other organisms, including Azospirillum brasilense and Pseudomonas putida GR12-2, have proven beneficial to plants, and many IAA producers have been shown to stimulate increases in root mass and/or length (20,37,44).…”