Polarized Defense Against Fungal Pathogens Is Mediated by the Jacalin-Related Lectin Domain of Modular Poaceae -Specific Proteins

Abstract

Modular proteins are an evolutionary answer to optimize performance of proteins that physically interact with each other for functionality. Using a combination of genetic and biochemical experiments, we characterized the rice protein OsJAC1, which consists of a jacalin-related lectin (JRL) domain predicted to bind mannose-containing oligosaccharides, and a dirigent domain which might function in stereoselective coupling of monolignols. Transgenic overexpression of OsJAC1 in rice resulted in quantitative broad-spectrum resistance against different pathogens including bacteria, oomycetes, and fungi. Overexpression of this gene or its wheat ortholog TAJA1 in barley enhanced resistance against the powdery mildew fungus. Both protein domains of OsJAC1 are required to establish resistance as indicated by single or combined transient expression of individual domains. Expression of artificially separated and fluorescence-tagged protein domains showed that the JRL domain is sufficient for targeting the powdery mildew penetration site. Nevertheless, co-localization of the lectin and the dirigent domain occurred. Phylogenetic analyses revealed orthologs of OsJAC1 exclusively within the Poaceae plant family. Dicots, by contrast, only contain proteins with either JRL or dirigent domain(s). Altogether, our results identify OsJAC1 as a representative of a novel type of resistance protein derived from a plant lineage-specific gene fusion event for better function in local pathogen defense.

Evolutionary analysis of plant jacalin-related lectins (JRLs) family and expression of rice JRLs in response to Magnaporthe oryzae

“…The transcriptional profiles of Os01g24710, Os06g07250, and Os11g32210 are all elevated after 12 hpi and reached the maximum at 24 hpi. Os12g14440 (also known as OsJAC1) has a much earlier response and reach the peak at 12 hpi, which is consistent with the finding by Jiang (2006) and Weidenbach (2016). Os01g25280, Os05g43240, Os10g04270, and Os12g09720 have similar expression pattern by being up-regulated at 48 hpi.…”

“…Jacalin-related lectin proteins are found in many plants, some of which have been characterized and take roles in enhancing tolerance against environmental stresses and pathogens attacks (Xiao et al 2005;Jiang et al 2006;Xiang et al 2011;Ma et al 2013;Weidenbach et al 2016). In this study, we increase the number of studied plants since more genomes are now available and analyzed the distribution, phylogenic relationship, and domain composition of JRLs in plants across 15 monocots-/dicots-families.…”

“…Another type is NB_ARC-jacalin from wheat, sorghum, barley, and rice. Proteins with Dirigent or disease-response domain exists in plants and have been implicated in plant defense (Ralph et al 2007;Seneviratne et al 2015;Weidenbach et al 2016 Up-regulation (dark red) and down-regulation (dark blue) are described by log 2 fold changes relative to the mean expression of the selected genes in 3 stages: uninoculated rice (0N), inoculated with Guy 11 at 24 hours post inoculation (hpi) (GN24), inoculated with Guy11 at 48 hpi (GN48), inoculated with FJ81278 at 24 hpi (8N24) and inoculated with FJ81278 at 48 hpi (8N48). The type of jacalins are marked with a circle (○) for merojacalin, a triangle (Δ) for holojacalin, and a star (★) for chimeric jacalin.…”

“…Expression of TaJRLL1 in Arabidopsis enhances resistance against fungal diseases (Xiang et al 2011). Transient expression of the wheat JRL gene TaJA1 in barley also confers resistance against the powdery mildew fungus (Weidenbach et al 2016). In rice, SalT protein was first isolated from salt-treated rice tissue of the indica variety Taicheng Native 1 (Claes et al 1990).…”

“…The SalT gene shows organ-specific expression and is induced by drought and hormone treatments. Another jacalin-related lectin protein OsJAC1 accumulates at fungal penetration sites and confers resistance against various rice pathogens (Jiang et al 2006;Weidenbach et al 2016). Jacalin proteins not only recognize carbohydrates for defense in plant, but also have roles during developmental processes.…”