A SNARE‐protein has opposing functions in penetration resistance and defence signalling pathways

Abstract

SummaryPenetration resistance is often the first line of defence against fungal pathogens. Subsequently induced defences are mediated by the programmed cell death (PCD) reaction pathway and the salicylic acid (SA), jasmonic acid (JA) and ethylene (ET) signalling pathways. We previously demonstrated that full penetration resistance in Arabidopsis against the non-host barley powdery mildew fungus (Blumeria graminis f.sp. hordei) requires the syntaxin SYP121 (PEN1). Here we report that SYP121, together with SYP122, functions as a negative regulator of subsequently induced defence pathways. The SA level in the syntaxin double mutant syp121-1 syp122-1 is dramatically elevated, resulting in necrosis and dwarfism. This phenotype is partially rescued by introducing the SA-signalling mutations eds1-2, eds5-3, sid2-1 and npr1-1 as well as the NahG transgene. These partially rescued triple mutants have an unknown defence to Pseudomonas syringae pv. tomato, and have increased HR-like responses to non-host and host powdery mildew fungi. The HR-like responses cause efficient resistance to the latter. These defence pathways are SA-independent. Furthermore, the JA/ET signalling marker, PDF1.2, is highly upregulated in the triple mutants. Thus SYP121 and SYP122 are negative regulators of PCD, SA, JA and ET pathways through a molecular function distinct from that of SYP121 in penetration resistance. Our data suggest that individual cells preferentially express either penetration resistance or the subsequently induced defences.

Requirement of Vesicle-Associated Membrane Protein 721 and 722 for Sustained Growth during Immune Responses in Arabidopsis

“…3A), it is suggested that SYP132 rather than PEN1 is engaged in the secretion of growth-related cargo transported by VAMP721/722 endomembrane containers. However, it was reported that the pen1 syp122 plants are dwarfed (Zhang et al, 2007), indicating the importance of PEN1 and SYP122 in plant growth. We therefore suggest that the three PM syntaxins PEN1, SYP122 and SYP132 are involved in plant growth and development by forming SNARE complexes with VAMP721/722, although whether VAMP721/722 interact with different PM syntaxins simultaneously or distinctly depending on a cue is unknown.…”

“…Similarly, the VAMP721/722-cosilenced plants are dwarfed, and the snap33 and the vamp721 vamp722 double mutant genotypes are lethal at early seedling stage (Assaad et al, 2004;Heese et al, 2001;Kwon et al, 2008c;Zhang et al, 2007), suggesting that the PEN1-SNAP33-VAMP721/722 pathway also serves a role in constitutive secretion during plant growth, transporting materials required for cellular viability to the PM. We here describe a function of VAMP721/722 in sustained growth during immune responses in plants.…”

Binding of SEC11 Indicates Its Role in SNARE Recycling after Vesicle Fusion and Identifies Two Pathways for Vesicular Traffic to the Plasma Membrane

“…Along with the Qa-SNARE SYP132, which is constitutively expressed and present at low levels (Enami et al, 2009), these proteins mediate secretory vesicle traffic, contributing to cellular homeostasis, expansion, and growth (Blatt, 2000;Shope et al, 2003;Campanoni and Blatt, 2007). Functional differences between SYP121 and SYP122 are known (Leyman et al, 1999;Zhang et al, 2007;Rehman et al, 2008;Honsbein et al, 2009Honsbein et al, , 2011Grefen et al, 2010a;Eisenach et al, 2012), but as these Qa-SNAREs share cognate partners Karnik et al, 2013b;Yun et al, 2013), studies to date have offered few clues to the mechanistic basis for the differences in their regulation and function. Among other factors, SM proteins are widely recognized to be key components that regulate SNARE-mediated vesicle traffic, both in stabilizing the cognate SNARE complex and in controlling the availability of several Qa-SNAREs for binding (Südhof and Rothman, 2009;Rizo and Südhof, 2012).…”

“…In Arabidopsis thaliana, two of these SNAREs, SYP121 (=SYR1/PEN1) and SYP122, show a high degree of structural homology and overlap in function (Assaad et al, 2004;Tyrrell et al, 2007;Bassham and Blatt, 2008;Rehman et al, 2008). Single mutations of these Qa-SNAREs have little effect on plant growth under many conditions, and reduced growth is normally evident only in the syp121/syp122 double mutant (Assaad et al, 2004;Zhang et al, 2007). Both SYP121 and SYP122 are expressed throughout the development of the plant and in most, if not all, tissues (Uemura et al, 2004;Enami et al, 2009).…”

“…In plant cells, SNARE-mediated vesicle traffic delivers wall materials and membrane to the cell surface, making essential contributions to homeostasis, cell expansion, and growth (Blatt, 2000;Shope et al, 2003;Campanoni and Blatt, 2007). It also plays important roles in resistance to pathogens (Kalde et al, 2007;Zhang et al, 2007) and responses to abiotic stress (Grefen and Blatt, 2008;Eisenach et al, 2012). Cognate SNAREs localize to vesicle and target membranes, and during the SNARE cycle, their assembly in a stable heteromeric core complex draws vesicle and target membranes together for fusion of the two bilayers.…”