Transcriptome Analysis of the Rhizosphere Bacterium Azospirillum brasilense Reveals an Extensive Auxin Response

Abstract

The rhizosphere bacterium Azospirillum brasilense produces the auxin indole-3-acetic acid (IAA) through the indole-3-pyruvate pathway. As we previously demonstrated that transcription of the indole-3-pyruvate decarboxylase (ipdC) gene is positively regulated by IAA, produced by A. brasilense itself or added exogenously, we performed a microarray analysis to study the overall effects of IAA on the transcriptome of A. brasilense. The transcriptomes of A. brasilense wild-type and the ipdC knockout mutant, both cultured in the absence and presence of exogenously added IAA, were compared.Interfering with the IAA biosynthesis/homeostasis in A. brasilense through inactivation of the ipdC gene or IAA addition results in much broader transcriptional changes than anticipated. Based on the multitude of changes observed by comparing the different transcriptomes, we can conclude that IAA is a signaling molecule in A. brasilense. It appears that the bacterium, when exposed to IAA, adapts itself to the plant rhizosphere, by changing its arsenal of transport proteins and cell surface proteins. A striking example of adaptation to IAA exposure, as happens in the rhizosphere, is the upregulation of a type VI secretion system (T6SS) in the presence of IAA. The T6SS is described as specifically involved in bacterium-eukaryotic host interactions. Additionally, many transcription factors show an altered regulation as well, indicating that the regulatory machinery of the bacterium is changing.

Characterization of a Nitrilase and a Nitrile Hydratase from Pseudomonas sp. Strain UW4 That Converts Indole-3-Acetonitrile to Indole-3-Acetic Acid

“…Bacterial effector proteins are injected into host cells via type III secretion systems to facilitate pathogenicity (19). Altogether, these studies show that IAA acts as a signaling molecule for a variety of different bacterial genes that play a role in both beneficial and deleterious plant-microbe interactions (16).…”

“…In Azospirillum brasilense Sp245, interfering with IAA biosynthesis affects the expression of ribosomal proteins, which are involved in protein synthesis. IAA also affects aerobic denitrification and adaptation to an anaerobic metabolism, cell respiration, and carbohydrate uptake (16). In the phytopathogen Agrobacterium tumefaciens C58, exogenous IAA leads to the upregulation of genes involved in amino acid synthesis and carbon metabolism (17).…”

“…In both A. brasilense and Dickeya dadantii, exposure to exogenous IAA leads to increased expression of a type VI secretion system, which may be used to directly interact with plant cells. IAA is also required for the expression of effectors secreted by the type III secretion system in Erwinia chrysanthemi (16,18). Bacterial effector proteins are injected into host cells via type III secretion systems to facilitate pathogenicity (19).…”

Nitric Oxide in Azospirillum and Related Bacteria: Production and Effects

“…Boscari et al ( 2013 ) showed the transcriptomic profi les during nodule development in M. truncatula-S. meliloti symbiosis and how the expression pattern is modulated by NO. In a similar manner, Van Puyvelde et al ( 2011 ) studied the transcriptomic response of A. brasilense wt and Faj009 to exogenous and endogenous auxin. They found evidence of a putative connection between the IAA and NO biosynthetic pathways since the Nap operon was up-regulated in the ipdC − mutant.…”

Not Just Sweet Talkers

“…Azospirillum brasilense also shows an extensive transcriptional response to auxin indole-3-acetic acid (IAA), a phytohormone produced both by that bacterium and the plant. Since many various genes such as those from secretion systems are involved in this response, it suggests that IAA acts as a signalling molecule in the planteAzospirillum interaction (Van Puyvelde et al, 2011).…”