Cooperative functioning between phenylalanine ammonia lyase and isochorismate synthase activities contributes to salicylic acid biosynthesis in soybean

Abstract

Salicylic acid (SA), an essential regulator of plant defense, is derived from chorismate via either the phenylalanine ammonia lyase (PAL) or the isochorismate synthase (ICS) catalyzed steps. The ICS pathway is thought to be the primary contributor of defense-related SA, at least in Arabidopsis. We investigated the relative contributions of PAL and ICS to defense-related SA accumulation in soybean (Glycine max). Soybean plants silenced for five PAL isoforms or two ICS isoforms were analyzed for SA concentrations and SA-derived defense responses to the hemibiotrophic pathogens Pseudomonas syringae and Phytophthora sojae. We show that, unlike in Arabidopsis, PAL and ICS pathways are equally important for pathogen-induced SA biosynthesis in soybean. Knock-down of either pathway shuts down SA biosynthesis and abrogates pathogen resistance. Moreover, unlike in Arabidopsis, pathogen infection is associated with the suppression of ICS gene expression. Pathogen-induced biosynthesis of SA via the PAL pathway correlates inversely with phenylalanine concentrations. Although infections with either virulent or avirulent strains of the pathogens increase SA concentrations, resistance protein-mediated response to avirulent P. sojae strains may function in an SA-independent manner. These results show that PAL- and ICS-catalyzed reactions function cooperatively in soybean defense and highlight the importance of PAL in pathogen-induced SA biosynthesis.

Maize phenylalanine ammonia‐lyases contribute to resistance to Sugarcane mosaic virus infection, most likely through positive regulation of salicylic acid accumulation

“…In Arabidopsis thaliana and barley ( Hordeum vulgare ), most SA biosynthesis is dependent on isochorismate synthase (ICS) activity (Hao et al ., ; Wildermuth et al ., ). In tobacco ( Nicotiana tabacum ) SA is predominantly synthesized from benzoic acid derived from the phenylpropanoid pathway (phenylalanine) (Lee et al ., ), in peach ( Prunus persica ) SA is also produced from benzoic acid derived from phenylalanine via an alternative pathway (Diaz‐Vivancos et al ., ), whilst in soybean ( Glycine max ) the isochorismate and phenylpropanoid pathways are equally important in supplying the carbon skeletons for SA biosynthesis (Shine et al ., ). The phenylpropanoid pathway is also involved in the biosynthesis of many plant defensive compounds, including flavonoids, lignin, condensed tannins, hydroxycinnamic acid, coumarins and stilbenes (An and Mou, ; Yu and Jez, ).…”

“…In rice, OsPAL6 ‐knockout mutant plants were highly susceptible to Magnaporthe oryzae and susceptibility was associated with decreased flavonoid, phytoalexin and SA accumulation (Duan et al ., ). Knockdown of PAL expression in soybean inhibits SA biosynthesis and resistance to P. syringae and Phytophthora sojae (Shine et al ., ; Zhang et al ., ).…”

MgO‐induced defence against bacterial wilt disease in Arabidopsis thaliana

“…The data showed that SA was synthesized significantly within 1 day in the roots of A. thaliana upon treatment with MgO. In A. thaliana , ICS1, one of the two functional ICS isoforms, is known to be the major contributor to pathogen‐induced SA biosynthesis (Shine et al ., ). Considerable ICS1 induction was also observed in the present study, suggesting a pivotal role of ICS1 in the SA production in A. thaliana roots treated with MgO.…”

The biochemical properties of the twoArabidopsis thalianaisochorismate synthases

“…The existence of two ICS genes, most probably by gene duplication, in a plant such as Arabidopsis that has a relatively small genome is puzzling, but possession of two genes encoding ICS proteins with such highly similar sequences, structures and near-identical enzymological properties (as shown in the present study) suggests that this redundancy must confer some advantage on this plant. Duplication of ICS genes has also occurred independently in Brassica napus and soybean ([13,24] and data not shown). For poplar, which has only a single ICS gene, the primary ICS transcript undergoes alternative splicing to allow production of alternative isoforms of the enzyme [24].…”

“…Subsequently, the discovery of the SA induction-deficient 2 ( sid2 ) mutant in Arabidopsis thaliana (hereafter referred to as Arabidopsis ) and the identification of isochorismate synthase 1 (ICS1; AtICS1:EC 5.4.4.2, also known as isochorismate hydroxymutase) as the enzyme encoded by the wild-type SID2 allele showed that, in this plant, SA is synthesised from chorismic acid, derived from the shikimic acid pathway, and that SA biosynthesis occurs in the plastid [5,10–12]. In some plants, as shown in soybean ( Glycine max ), there can be redundancy in SA biosynthesis with both the shikimic acid pathway and the phenylpropanoid pathway being required to generate sufficient SA for effective pathogen defence [13]. However, in Arabidopsis , SA biosynthesis appears to be solely dependent on the shikimic acid pathway and follows a similar route to that which occurs in bacteria.…”