The PEN1 syntaxin defines a novel cellular compartment upon fungal attack and is required for the timely assembly of papilla

Attack by the host powdery mildew Erysiphe cichoracearum usually results in successful penetration and rapid proliferation of the fungus on Arabidopsis. By contrast, the non-host barley powdery mildew Blumeria graminis f. sp. hordei (Bgh) typically fails to penetrate Arabidopsis epidermal cells. In both instances the plant secretes cell wall appositions or papillae beneath the penetration peg of the fungus. Genetic screens for mutations that result in increased penetration of Bgh on Arabidopsis have recently identified the PEN1 syntaxin. Here we examine the role of PEN1 and of its closest homologue, SYP122, identified as a syntaxin whose expression is responsive to infection. pen1 syp122 double mutants are both dwarfed and necrotic, suggesting that the two syntaxins have overlapping functions. Although syp122-1 and the cell wall mur mutants have considerably more pronounced primary cell wall defects than pen1 mutants, these have relatively subtle or no effects on penetration resistance. Upon fungal attack, PEN1 appears to be actively recruited to papillae, and there is a 2-hour delay in papillae formation in the pen1-1 mutant. We conclude that SYP122 may have a general function in secretion, including a role in cell wall deposition. By contrast, PEN1 appears to have a basal function in secretion and a specialized defense-related function, being required for the polarized secretion events that give rise to papilla formation. Introduction Fungi typically initiate an invasion of plant tissues by penetrating the plant cell wall. If the intruding pathogen can be intercepted at this early stage, cellular integrity and homeostasis are maintained, and damage to plant tissues is greatly reduced. In numerous studies of cereals attacked by powdery mildew, resistance to fungal penetration has been intimately associated with the papilla response (see Belanger and Bushnell, 2002). Papillae are dome shaped appositions deposited by the epidermal cell in the apoplasm (between the cell wall and plasma membrane) directly subtending the appressorium and penetration peg of the fungus. Degenerate penetration pegs are often found trapped in the papilla matrix (Ebrahim-Nesbat et al., 1986; Hippe-Sanwald et al., 1992; Kunoh et al., 1996) and the phenolics, reactive oxygen species and hydrolases found to accumulate in papillae are likely to constitute effective barriers to fungal penetration (Belanger and Bushnell, 2002). Although there has been extensive research on papillae in the grasses, very little is known about the genes that regulate papilla formation aside from the MLO locus of barley. The wild-type MLO gene product is a negative …