Dual Regulation Role of GH3.5 in Salicylic Acid and Auxin Signaling during Arabidopsis-Pseudomonas syringae Interaction

Abstract

Salicylic acid (SA) plays a central role in plant disease resistance, and emerging evidence indicates that auxin, an essential plant hormone in regulating plant growth and development, is involved in plant disease susceptibility. GH3.5, a member of the GH3 family of early auxin-responsive genes in Arabidopsis (Arabidopsis thaliana), encodes a protein possessing in vitro adenylation activity on both indole-3-acetic acid (IAA) and SA. Here, we show that GH3.5 acts as a bifunctional modulator in both SA and auxin signaling during pathogen infection. Overexpression of the GH3.5 gene in an activation-tagged mutant gh3.5-1D led to elevated accumulation of SA and increased expression of PR-1 in local and systemic tissues in response to avirulent pathogens. In contrast, two T-DNA insertional mutations of GH3.5 partially compromised the systemic acquired resistance associated with diminished PR-1 expression in systemic tissues. The gh3.5-1D mutant also accumulated high levels of free IAA after pathogen infection and impaired different resistance-gene-mediated resistance, which was also observed in the GH3.6 activation-tagged mutant dfl1-D that impacted the auxin pathway, indicating an important role of GH3.5/GH3.6 in disease susceptibility. Furthermore, microarray analysis showed that the SA and auxin pathways were simultaneously augmented in gh3.5-1D after infection with an avirulent pathogen. The SA pathway was amplified by GH3.5 through inducing SA-responsive genes and basal defense components, whereas the auxin pathway was derepressed through up-regulating IAA biosynthesis and down-regulating auxin repressor genes. Taken together, our data reveal novel regulatory functions of GH3.5 in the plant-pathogen interaction.

Systemic acquired resistance: the elusive signal(s)

“…In spite of heightened SA accumulation and PR gene expression, R gene-mediated resistance in these plants was suppressed, presumably owing to the enhanced susceptibility conferred by elevated IAA levels. In gh3.5 mutants, SAR was partially compromised as indicated by suppressed PR-1 expression in systemic tissues [50 ]. It should be noted that in an independent study, over expression of GH3.5 led to elevated SA levels and PR-1 transcripts and suppression of IAA levels [49].…”

“…Accumulating evidence suggests that SA and auxin perform mutually antagonistic roles in disease resistance [44,45 ], and repression of auxin-related genes was observed in the systemic tissue of SAR-induced Arabidopsis [45 ]. Recently, members of the GH3 family of acyl-adenylate/thioester-forming enzymes involved in the amino acid conjugation of, for example the auxin indole-3-acetic acid (IAA), were implicated in the regulation of basal and R gene-mediated resistance as well as SAR [46][47][48]49,50 ]. GH3.5 can conjugate both SA and IAA [51], and both signaling pathways were upregulated in plants over expressing GH3.5 after pathogen infection [50 ].…”

“…Recently, members of the GH3 family of acyl-adenylate/thioester-forming enzymes involved in the amino acid conjugation of, for example the auxin indole-3-acetic acid (IAA), were implicated in the regulation of basal and R gene-mediated resistance as well as SAR [46][47][48]49,50 ]. GH3.5 can conjugate both SA and IAA [51], and both signaling pathways were upregulated in plants over expressing GH3.5 after pathogen infection [50 ]. In spite of heightened SA accumulation and PR gene expression, R gene-mediated resistance in these plants was suppressed, presumably owing to the enhanced susceptibility conferred by elevated IAA levels.…”

Activation of the Indole-3-Acetic Acid–Amido Synthetase GH3-8 Suppresses Expansin Expression and Promotes Salicylate- and Jasmonate-Independent Basal Immunity in Rice

“…Recent studies have reported that auxin promotes disease susceptibility, and repression of auxin receptors by microRNA is part of an induced immune response in Arabidopsis thaliana (Navarro et al, 2006); auxin-resistant Arabidopsis by mutation of genes functioning in auxin signaling shows enhanced disease resistance (Park et al, 2007;Wang et al, 2007;Zhang et al, 2007). Thus, auxin signaling, which is generally recognized to be involved in plant growth and development (Woodward and Bartel, 2005), is likely involved in the complicated network of plant-pathogen interactions.…”

Abscisic Acid Has a Key Role in Modulating Diverse Plant-Pathogen Interactions

“…This approach has been used to investigate resistance mechanisms with the expectation that elevated expression of defense signaling molecules may lead to a quantitative impact on resistance even where there is significant cross talk and functional redundancy. Thus, several new components have been shown to regulate plant-pathogen interactions (Grant et al, 2003;Xia et al, 2004;Zhang et al, 2007). Aiming to uncover genes involved in SA-mediated signaling mechanisms, we carried out activation tagging in SA-deficient Arabidopsis plants that constitutively express the bacterial salicylate hydroxylase (NahG; Gaffney et al, 1993).…”