Dual role of auxin in regulating plant defense and bacterial virulence gene expression duringPseudomonas syringae PtoDC3000 pathogenesis

Abstract

<jats:title>ABSTRACT</jats:title><jats:p>Modification of host hormone biology is a common strategy used by plant pathogens to promote disease. For example, the bacterial pathogen <jats:italic>Pseudomonas syringae</jats:italic> strain <jats:italic>Pto</jats:italic>DC3000 produces the plant hormone auxin (Indole-3-acetic acid, or IAA) to promote <jats:italic>Pto</jats:italic>DC3000 growth in plant tissue. Previous studies suggest that auxin may promote <jats:italic>Pto</jats:italic>DC3000 pathogenesis through multiple mechanisms, including both suppression of salicylic acid (SA)-mediated host defenses and via an unknown mechanism that appears to be independent of SA. To test if host auxin signaling is important during pathogenesis, we took advantage of <jats:italic>Arabidopsis thaliana</jats:italic> lines impaired in either auxin signaling or perception. We found that disruption of auxin signaling in plants expressing an inducible dominant <jats:italic>axr2-1</jats:italic> mutation resulted in decreased bacterial growth, demonstrating that host auxin signaling is required for normal susceptibility to <jats:italic>Pto</jats:italic>DC3000, and this phenotype was dependent on SA-mediated defenses. However, despite exhibiting decreased auxin perception, <jats:italic>tir1 afb1 afb4 afb5</jats:italic> quadruple mutant plants lacking four of the six known auxin co-receptors supported increased levels of bacterial growth. This mutant also exhibited elevated IAA levels, suggesting that the increased IAA in these plants may promote <jats:italic>Pto</jats:italic>DC3000 growth independent of host auxin signaling, perhaps through a direct effect on the pathogen. In support of this, we found that IAA directly impacted the pathogen, by modulating expression of bacterial virulence genes, both in liquid culture and in planta. Thus, in addition to suppressing host defenses, IAA acts as a microbial signaling molecule that regulates bacterial virulence gene expression.</jats:p>

Manipulation of auxin signalling by plant viruses

“…In contrast, Fusarium oxysporum requires functional auxin signalling and transport to promote disease susceptibility (Kidd et al, 2011). Recent studies support the dual role of auxin during infection, either by enhancing disease susceptibility (Djami-Tchatchou et al, 2020;Fu & Wang, 2011;Mutka et al, 2013) or increasing resistance (Llorente et al, 2008). There is very little evidence whether bacterial and fungal pathogens directly target key regulators of the auxin signalling pathway.…”

Double agent indole-3-acetic acid: mechanistic analysis of indole-3-acetaldehyde dehydrogenase AldA that synthesizes IAA, an auxin that aids bacterial virulence

“…The blast disease of rice is caused by the fungus Magnaporthe oryzae which produces a flattened, hyphal cell from the germinating spore with an infection peg that penetrates the host causing brown diamond-shape lesions on the rice leaves 5 . Interestingly, many plant-associated microbes synthesize a plant hormone or its close mimic to gain entry and establish themselves by modulating the host plant's metabolism as well as their own virulence genes [6][7][8] . An extensively studied example of hormone-mediated plant-microbe pathogenesis is the crown-gall disease caused by the gram-negative soil bacterium Agrobacterium tumefaciens.…”

“…Another intriguing example is that of Pseudomonas syringae, a bacterial plant pathogen that manipulates hormone signaling as a means of breaking the host plant defence 8,11 . It gains entry into the tomato plant by producing the phytotoxin coronatine, a molecular mimic of the plant hormone jasmonic acid-isoleucine, resulting in the bacterial speck disease 7,12,13 .…”

“…IAA produced by P. syringae has been reported to promote the virulence in Arabidopsis thaliana by two different mechanisms -one, it upregulates the virulence gene expression in the bacterium, and second, it suppresses salicylic acid-mediated plant defenses by activating auxin Downloaded from http://portlandpress.com/bioscirep/article-pdf/doi/10.1042/BSR20210598/918652/bsr-2021-0598c.pdf by guest on 16 August 2021 plant host signaling. This results in increased host susceptibility to the pathogen's entry8…”

“…signalling in the host plant (via the TIR1/AFB auxin co-receptor system)8,11 . Studies with tir1/afb mutants show accumulation of IAA in A. thaliana, resulting in the deregulation of…”