The Role ofNDR1in Avirulence Gene-Directed Signaling and Control of Programmed Cell Death in Arabidopsis

Abstract

Arabidopsis plants containing the ndr1-1 mutation are incapable of mounting a hypersensitive response to bacteria carrying avrRpt2, but show an exaggerated cell death response to bacteria carrying avrB (Century et al., 1995). We show here that ndr1-1 plants are severely impaired in induction of systemic acquired resistance and PR1-driven transcription of a reporter gene in response to Pseudomonas syringae strains carrying avrRpt2 but not in response to P. syringae carrying avrB. The ndr1-1 mutation also impaired salicylic acid (SA) accumulation in response to treatments that produced reactive oxygen species (ROS) and impaired induction of systemic acquired resistance in response to in situ production of ROS. Hydrogen peroxide accumulated in wild-type Arabidopsis leaves beginning 4 to 7 h postinoculation with P. syringae carrying either avrRpt2 or avrB. In ndr1-1 plants, P. syringae carrying avrRpt2 elicited no detectable hydrogen peroxide production. Hydrogen peroxide production in response to bacteria carrying avrB was similar to that of Columbia in kinetics but of lesser intensity at early time points. These data are interpreted to indicate that NDR1 links ROS generation to SA production and that the phenotypic consequences of the ndr1-1 mutation are caused by a reduced ability to accumulate SA upon pathogen infection.Exquisite specificity is a hallmark of gene-for-gene disease resistance. Individual plant lines carry a specific complement of disease resistance (R) genes. Plants resist infection only if the pathogen carries a specific avirulence (avr) gene that is the matched cognate of one of these plant R genes. Mutant plants with nonfunctional alleles of a particular R gene fail to recognize a pathogen carrying the corresponding avr gene, and disease ensues (Parker et al., 2000;Staskawicz, 2001). With bacterial pathogens, this specificity of molecular recognition in at least some cases is associated with direct binding of the plant R gene product to the bacterial avr gene product (Scofield et al., 1996; Tang et al., 1996). Recognition takes place inside the plant cell (Gopalan et al., 1996;Leister et al., 1996) following export of the avr gene product from the bacteria via a type III secretion system (Pirhonen et al., 1996;Mudgett and Staskawicz, 1998).In contrast to the specificity of upstream molecular recognition processes, downstream plant responses to pathogen infection often bear strong similarities despite being elicited by vastly different types of pathogen. Gene-for-gene disease resistance is usually accompanied by rapid cell death (the hypersensitive response [HR]; Klement, 1982) in plant cells that are in direct contact with pathogen (Turner and Novacky, 1974). Uninoculated regions of the plant are induced to display an immunity to further pathogen challenge termed systemic acquired resistance (SAR). SAR protects plants from a broad spectrum of pathogens including those very different from the original (Ryals et al., 1994). A set of genes termed "pathogenesis related" (PR) are induced both locall...

Programmed cell death in the plant immune system

“…Two separate signaling modules regulate NB-LRR proteins: nonrace-specific disease resistance 1 (NDR1) regulates in most cases immune responses mediated by CC-NB-LRR proteins, whereas the enhanced disease susceptibility 1 (EDS1)/ phytoalexin deficient 4 (PAD4)/senescence-associated gene 101 (SAG101) complex mediates TIR-NB-LRR signaling. 69 These two systems integrate redox signals downstream of NADPH oxidase 49 leading to SA accumulation, 70,71 which has a central role in defense responses. ROS and SA act synergistically to drive HR.…”

VASCULAR ASSOCIATED DEATH1, a Novel GRAM Domain–Containing Protein, Is a Regulator of Cell Death and Defense Responses in Vascular Tissues

“…Our observations are in agreement with these novel functions proposed for EDS1 and NDR1 in plant defense potentiation. In addition, the fact that the cell death phenotype of vad1 was differentially affected by the two regulators also could be related, at least in part, through ROS generation or independently of them, to their ability to differentially modulate SA levels (Shapiro and Zhang, 2001;our work). Consistent with these results, PR1 gene expression is clearly (A) VAD1 and PR1 transcript accumulation in wild-type plants (Col-0) at different times after inoculation with an avirulent (Xcc147) strain of X. campestris pv campestris (squares), an avirulent (DC3000/avrRpm1) strain of P. syringae pv tomato (diamonds), or after treatment with water (triangles).…”

Root-Secreted Malic Acid Recruits Beneficial Soil Bacteria

“…Four days after inoculation, the plants were stained for GUS assay using a GUS staining kit (obtained from SigmaAldrich) according to manufacturer's instructions. The control and treated plants were imaged for the expression of PR1::GUS in the leaves as per the published protocol (Shapiro and Zhang, 2001). A representative image of at least 12 leaves was presented for each treatment.…”