Systemic acquired resistance (SAR) is a mechanism of induced defense that confers long-lasting protection against a broad spectrum of microorganisms. SAR requires the signal molecule salicylic acid (SA) and is associated with accumulation of pathogenesis-related proteins, which are thought to contribute to resistance. Much progress has been made recently in elucidating the mechanism of SAR. Using the model plant Arabidopsis, it was discovered that the isochorismate pathway is the major source of SA during SAR. In response to SA, the positive regulator protein NPR1 moves to the nucleus where it interacts with TGA transcription factors to induce defense gene expression, thus activating SAR. Exciting new data suggest that the mobile signal for SAR might be a lipid molecule. We discuss the molecular and genetic data that have contributed to our understanding of SAR and present a model describing the sequence of events leading from initial infection to the induction of defense genes.

The tomato Cf-9 gene confers resistance to races of the fungal pathogen Cladosporium fulvum expressing the Avr9 gene. cDNA amplified fragment length polymorphism analysis was used to display transcripts whose expression is rapidly altered during the Avr9-and Cf-9 -mediated defense response in tobacco cell cultures. Diphenyleneiodonium was used to abolish the production of active oxygen species during gene induction. Of 30,000 fragments inspected, 290 showed altered abundance, of which 263 were induced independently of active oxygen species. cDNA clones were obtained for 13 ACRE (for Avr9/Cf-9 rapidly elicited) genes. ACRE gene induction occurred in the presence of cycloheximide. Avr9 induced ACRE gene expression in leaves. Surprisingly, ACRE genes were also rapidly but transiently induced in leaves in response to other stresses. The amino acid sequences of some ACRE proteins are homologous to sequences of known proteins such as ethylene response element binding protein transcription factors, the N resistance protein, a calcium binding protein, 13-lipoxygenase, and a RING-H2 zinc finger protein. Rapid induction of ACRE genes suggests that they play a pivotal role during plant defense responses. INTRODUCTIONDisease resistance in plants often involves recognition of invading pathogens followed by activation of a defense response. Such incompatible interactions are dependent on the presence of a resistance ( R ) gene in the host and an avirulence ( Avr ) gene in the pathogen (Flor, 1971;Keen, 1990). Many plant R genes have been identified. Their products have motifs consistent with potential roles in pathogen detection and subsequent signal transduction (Bent, 1996). However, the signal transduction activated by R gene products is still poorly understood.Cladosporium fulvum is a biotrophic fungus that causes leaf mold disease of tomato. The tomato Cf-9 gene confers resistance to C. fulvum races expressing the corresponding Avr9 gene . The Avr9 protein is secreted by the fungus and is processed to a cystine knot peptide of 28 amino acids, which can be retrieved in intercellular washing fluid (IF) from infected leaves (De Wit and Spikman, 1982;Van den Ackerveken et al., 1993). Infiltration of Cf9 tomato or transgenic Cf9 tobacco with Avr9 leads to necrosis within 24 hr.This response is faster in tobacco than it is in tomato (Hammond-Kosack et al., 1998). Cell suspension cultures derived from Cf9 tobacco plants, when challenged with Avr9, rapidly produce active oxygen species (AOS) (Piedras et al., 1998) and activate two mitogen-activated protein (MAP) kinases (Romeis et al., 1999) and a calcium-dependent protein kinase (Romeis et al., 2000).The mode of action of the Cf-9 protein is not known. Changes in gene expression are likely to be important for activation of defense mechanisms, and transcriptional changes have been reported in several plant-pathogen interaction systems (Rushton and Somssich, 1998). The nonhost resistance responses of parsley and tobacco cells to elicitors from cultures of Phytophthora spp have be...

Tomato (Lycopersicon esculentum) Cf genes confer resistance to the fungal pathogen Cladosporium fulvum through recognition of secreted avirulence (Avr) peptides. Plant defense responses, including rapid alterations in gene expression, are immediately activated upon perception of the pathogen. Previously, we identified a collection of Avr9/Cf-9 rapidly (15 to 30 min) elicited (ACRE) genes from tobacco (Nicotiana tabacum). Many of the ACRE genes encode putative signaling components and thus may play pivotal roles in the initial development of the defense response. To assess the requirement of 42 of these genes in the hypersensitive response (HR) induced by Cf-9/Avr9 or by Cf-4/Avr4, we used virus-induced gene silencing (VIGS) in N. benthamiana. Three genes were identified that when silenced compromised the Cf-mediated HR. We further characterized one of these genes, which encodes a Ser/Thr protein kinase called Avr9/Cf-9 induced kinase 1 (ACIK1). ACIK1 mRNA was rapidly upregulated in tobacco and tomato upon elicitation by Avr9 and by wounding. Silencing of ACIK1 in tobacco resulted in a reduced HR that correlated with loss of ACIK1 transcript. Importantly, ACIK1 was found to be required for Cf-9/Avr9- and Cf-4/Avr4-mediated HRs but not for the HR or resistance mediated by other resistance/Avr systems, such as Pto/AvrPto, Rx/Potato virus X, or N/Tobacco mosaic virus. Moreover, VIGS of LeACIK1 in tomato decreased Cf-9–mediated resistance to C. fulvum, showing the importance of ACIK1 in disease resistance.

SUMMARY DNA damage is normally detrimental to living organisms. Here we show that it can also serve as a signal to promote immune responses in plants. We found that the plant immune hormone salicylic acid (SA) can trigger DNA damage in the absence of a genotoxic agent. The DNA damage sensor proteins, RAD17 and ATR, are required for effective immune responses. These sensor proteins are negatively regulated by a key immune regulator SNI1 (suppressor of npr1-1, inducible 1), which we discovered as a missing subunit of the Structural Maintenance of Chromosome (SMC) 5/6 complex required for controlling DNA damage. Elevated DNA damage caused by the sni1 mutation or treatment with a DNA-damaging agent markedly enhances SA-mediated defense gene expression. Our study suggests that activation of DNA damage responses is an intrinsic component of the plant immune responses.