Hypersensitive Cell Death and Papilla Formation in Barley Attacked by the Powdery Mildew Fungus Are Associated with Hydrogen Peroxide but Not with Salicylic Acid Accumulation1

Hückelhoven, Ralph; Fodor, József; Preis, Christine; Kogel, Karl Heinz

doi:10.1104/pp.119.4.1251

Cited by 372 publications

(350 citation statements)

References 45 publications

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“…This finding is surprising because apoplastic oxidative microbursts (revealed by hydrogen peroxide accumulation) are known to take place underneath both primary and AGTs, demonstrating that each germ tube is capable of eliciting a subcellular defense response at the cell periphery of attacked host cells (17,23). Although the enzyme(s) generating these oxidative microbursts have not been conclusively identified in barley (24,25), it is interesting that treatment of tobacco BY2 cells with cryptogein, a 10-kDa protein secreted by the phytoparasitic oomycete Phytophthora cryptogea, resulted in the accumulation of the NADPH oxidase NtrbohD and its presumed negative regulator, NtRac5, components of the oxi- dative burst machinery, in PM lipid rafts (22).…”

Section: Discussionmentioning

confidence: 66%

Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain

Bhat

Miklis

Schmelzer

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

327

256

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Many fungal pathogens must enter plant cells for successful colonization. Barley mildew resistance locus o (Mlo) is required for host cell invasion upon attack by the ascomycete powdery mildew fungus, Blumeria graminis f.sp. hordei, and encodes the founder of a family of heptahelical integral membrane proteins unique to plants. Recessively inherited loss-of-function mutant alleles (mlo) result in effective penetration resistance to all isolates of the biotrophic parasite. We used noninvasive fluorescence-based imaging to show that fluorescently tagged MLO protein becomes redistributed in the plasma membrane (PM) and accumulates beneath fungal appressoria coincident with the initiation of pathogen entry into host cells. Polarized MLO accumulation occurs once upon attack and appears to be independent of actin cytoskeleton function. Likewise, barley ROR2 syntaxin, a genetically defined component of penetration resistance to B. graminis f.sp. hordei, and a subset of predicted PM-resident proteins become redistributed to fungal entry sites. We previously identified calmodulin, a cytoplasmic calcium sensor, as an interactor and positive regulator of MLO activity and demonstrate here by FRET microscopy an increase in MLO͞calmodulin FRET around penetration sites coincident with successful host cell entry. Our data provide evidence for the formation of a pathogen-triggered PM microdomain that is reminiscent of membrane microdomains (lipid rafts) induced upon attempted entry of pathogenic bacteria in animal cells.

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Section: Discussionmentioning

confidence: 66%

Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain

Bhat

Miklis

Schmelzer

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

327

256

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“…In a previous study, we showed that a barley BI-1 homologue is expressed in early response to attack by Bgh (5). Here, we studied BI-1 expression during compatible and incompatible interactions of nearisogenic barley backcross Pallas (BCP) lines bearing no functional resistance gene, the major resistance gene Mla12 mediating the HR after race-specific recognition of AvrMla12 from fungal race BghA6 (6,24), or the recessive null mutant mlo allele mlo5 mediating broad penetration resistance (13, 17, 19, 24). Comparison of deduced amino acid sequences of barley (H. vulgare, GenBank accession no.…”

Section: Resultsmentioning

confidence: 99%

Overexpression of barley BAX inhibitor 1 induces breakdown of mlo -mediated penetration resistance to Blumeria graminis

Hückelhoven

Dechert²,

Kögel³

2003

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

175

137

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Cell death regulation is linked to pathogen defense in plants and animals. Execution of apoptosis as one type of programmed cell death in animals is irreversibly triggered by cytochrome c release from mitochondria via pores formed by BAX proteins. This type of programmed cell death can be prevented by expression of BAX inhibitor 1 (BI-1), a membrane protein that protects cells from the effects of BAX by an unknown mechanism. In barley, a homologue of the mammalian BI-1 is expressed in response to inoculation with the barley powdery mildew fungus Blumeria graminis f.sp. hordei (Bgh). We found differential expression of BI-1 in response to Bgh in susceptible and resistant plants. Chemical induction of resistance to Bgh by soil drench treatment with 2,6-dichloroisonicotinic acid led to down-regulation of the expression level of BI-1. Importantly, single-cell transient overexpression of BI-1 in epidermal leaf tissue of susceptible barley cultivar Ingrid led to enhanced accessibility, resulting in a higher penetration efficiency of Bgh on BI-1-transformed cells. In Bgh-resistant mlo5 genotypes, which do not express the negative regulator of defense and cell death MLO, overexpression of BI-1 almost completely reconstituted susceptibility to fungal penetration. We suggest that BI-1 is a regulator of cellular defense in barley sufficient to substitute for MLO function in accessibility to fungal parasites.

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“…This compartment was seen to accumulate in the vicinity of papillae. We speculate that this PEN1-related compartment might correspond to the "large vesicles" described previously in the defense literature (Zeyen and Bushnell, 1979;Hü ckelhoven et al, 1999) and that PEN1 might mediate its fusion at infection sites during papilla formation.…”

Section: A Role For Pen1 In Papilla Formationmentioning

confidence: 99%

“…The latter possibility, though unexpected, is consistent with the observation of GFP-PEN1 fluorescence in the apparent interior of the papillar structure. Unusual trafficking and fusion events, involving the fusion of unusually large "vesicles" 1 m in diameter at the papillae, have been reported during papilla formation (Zeyen and Bushnell, 1979), and such compartments have been shown to target reactive oxygen species toward infection sites (Hü ckelhoven et al, 1999). Collins et al (2003) report a decrease in the number of large vesicles observed at sites of failed penetration by the fungus in pen1 mutants.…”

Section: A Role For Pen1 In Papilla Formationmentioning

confidence: 99%

The PEN1 Syntaxin Defines a Novel Cellular Compartment upon Fungal Attack and Is Required for the Timely Assembly of Papillae

Assaad

Qiu

Youngs

et al. 2004

MBoC

360

388

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Attack by the host powdery mildew Erysiphe cichoracearum usually results in successful penetration and rapid proliferation of the fungus on Arabidopsis. By contrast, the nonhost 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-h 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.

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Hypersensitive Cell Death and Papilla Formation in Barley Attacked by the Powdery Mildew Fungus Are Associated with Hydrogen Peroxide but Not with Salicylic Acid Accumulation1

Cited by 372 publications

References 45 publications

Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain

Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain

Overexpression of barley BAX inhibitor 1 induces breakdown of mlo -mediated penetration resistance to Blumeria graminis

The PEN1 Syntaxin Defines a Novel Cellular Compartment upon Fungal Attack and Is Required for the Timely Assembly of Papillae

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