An Extracellular Subtilase Switch for Immune Priming in Arabidopsis

Abstract

In higher eukaryotes, induced resistance associates with acquisition of a priming state of the cells for a more effective activation of innate immunity; however, the nature of the components for mounting this type of immunological memory is not well known. We identified an extracellular subtilase from Arabidopsis, SBT3.3, the overexpression of which enhances innate immune responses while the loss of function compromises them. SBT3.3 expression initiates a durable autoinduction mechanism that promotes chromatin remodeling and activates a salicylic acid(SA)-dependent mechanism of priming of defense genes for amplified response. Moreover, SBT3.3 expression-sensitized plants for enhanced expression of the OXI1 kinase gene and activation of MAP kinases following pathogen attack, providing additional clues for the regulation of immune priming by SBT3.3. Conversely, in sbt3.3 mutant plants pathogen-mediated induction of SA-related defense gene expression is drastically reduced and activation of MAP kinases inhibited. Moreover, chromatin remodeling of defense-related genes normally associated with activation of an immune priming response appear inhibited in sbt3.3 plants, further indicating the importance of the extracellular SBT3.3 subtilase in the establishment of immune priming. Our results also point to an epigenetic control in the regulation of plant immunity, since SBT3.3 is up-regulated and priming activated when epigenetic control is impeded. SBT3.3 represents a new regulator of primed immunity.

Pathogen exploitation of an abscisic acid- and jasmonate-inducible MAPK phosphatase and its interception by Arabidopsis immunity

“…The phosphorylation status of MPK3 and MPK6 changes dynamically during pathogen infection (16)(17)(18)(19). In search of a regulator of MAPK activation during immunity, we found that an ABA-deficient mutant, aba2, shows enhanced activation of MPK3 and MPK6 after treatment with flg22, a bacterial MAMP (Fig.…”

Revisiting Vitis vinifera Subtilase Gene Family: A Possible Role in Grapevine Resistance against Plasmopara viticola

“…Previous studies in plants associated some subtilases with the defense response to pathogen attack, like the subtilase SBT3.3 in A. thaliana (Ramírez et al, 2013), the P69 in S. lycopersicum (Tornero et al, 1996; Jordá et al, 1999) and the cucumisin in grapevine (Figueiredo et al, 2008, 2012). The subtilase genes from V. vinifera were blasted against the A. thaliana genome (TAIR database, https://www.arabidopsis.org/) and the tomato genome (SolGenomics database, https://solgenomics.net/) to retrieve the grapevine sequences presenting higher sequence similarity to A. thaliana SBT3.3 and tomato P69 genes.…”

“…P69 was also the first plant subtilase for which two protein substrates were identified, systemin (Schaller and Ryan, 1994) and the leucine-rich repeat protein (LRP; Tornero et al, 1996), although the consequences of these substrates processing events for plant pathogen interaction still remain unknown. More recently, Ramírez and co-workers have identified a SBT3.3 gene from A. thaliana as encoding a serine protease homolog to the P69C subtilase from tomato and associated its function in immune priming responses (Ramírez et al, 2013). Also, in S. tuberosum , expression profile analysis of detached potato leaves after P. infestans infection or after BABA or BTH treatment highlighted an expression increase of several subtilases genes (Norero et al, 2016).…”

Functional Analogues of Salicylic Acid and Their Use in Crop Protection

“…The process is initiated through the Arabidopsis subtilase SBT3.3, a proteolytic extracellular enzyme, which is involved in activation of chromatin remodeling, covalent histone modifications and defense genes become poised for enhanced activation following pathogen attack [3,134]. During priming, BTH increased acetylation of histone H3 at Lys-9 (H3K9ac) and trimethylation of histone H3 at Lys-4 (H3K4me3) in the promoter regions of the transcription factors WRKY6, WRKY29, and WRKY52 [135]. In addition, DNA methylation and histone modifications are regulated by RNA Polymerase V [136] and are involved in the transmission of a priming state or stress memory, suggesting that plants may inherit priming sensitization [137].…”