ReviewGenes controlling expression of defense responses in Arabidopsis — 2001 status
Introduction
Plants defend themselves from attack by microbial pathogens by activating a battery of defense responses after infection. Provided that they are activated with sufficient speed, these responses are generally quite effective in preventing disease. Consequently, there is considerable interest in understanding the signal transduction networks that control the activation of defense responses in plants. One approach to this problem is to use the powerful Arabidopsis genetic system to identify plant genes that have crucial roles in regulating the activation of defense responses. This article summarizes progress made using this system since the previous review of this topic was written [1]. A model describing the circuitry of the signal transduction network is presented in Fig. 1.
Gene-for-gene resistance is a particularly strong form of plant disease resistance. Plants carry specific resistance (R) genes that are able to recognize pathogens carrying corresponding avirulence (avr) genes. This reaction triggers a rapid defense response that generally includes the programmed cell death of plant cells that are in contact with the pathogen, a phenomenon called the hypersensitive response (HR). Widespread difficulties in detecting direct interactions between R and avr proteins have led to the hypothesis that R proteins ‘guard’ plant proteins (i.e. ‘guardees’) that are the targets of pathogen avr proteins, triggering the HR and other responses when avr–guardee interactions are detected [2]. The detection of an in vivo complex containing an R protein, an avr protein, and an unidentified plant protein is consistent with this hypothesis [3]. This article does not discuss the extensive literature concerning function of R proteins, but does describe signaling downstream from R protein function.
Activation of the HR triggers a systemic resistance response known as systemic acquired resistance (SAR). This response includes the accumulation of the signal molecule salicylic acid (SA) throughout the plant and the consequent expression of a characteristic set of defense genes, including PR-1. Plants expressing SAR are more resistant to subsequent attack by a variety of otherwise virulent pathogens. Many defense responses that are characteristic of SAR also contribute to local resistance that is mediated by some R genes, and to the local growth limitation of moderately virulent pathogens. In a large expression profiling experiment, at 48 hours after infection, the spectra of plant genes expressed in response to a virulent Peronospora parasitica isolate and an isolate that triggers gene-for-gene resistance were similar [4••]. Responses triggered by R genes generally occur much faster than responses to virulent pathogens; this presumably explains why virulent pathogens; this presumably explains why R-gene-mediated resistance is so effective.
Some defense responses are activated by signal transduction networks that require jasmonic acid (JA) and ethylene (ET) as signal molecules. Different pathogens are limited to different extents by SA-dependent responses and by JA/ET-dependent responses. There appears to be con-siderable cross-talk between these signal transduction networks, with at least some SA-dependent responses limited by JA/ET-dependent responses and vice versa.
Section snippets
R-gene signal transduction
Mutations in PBS1, NDR1, EDS1, PAD4, and PBS2 block gene-for-gene resistance that is mediated by some R genes. The only R gene known to be affected by PBS1 mutations is RPS5 [5]. This observation raises the intriguing possibility that PBS1 encodes the ‘guardee’ monitored by RPS5. As RPS5 and the corresponding avr gene, avrPphB, have both been isolated, it should be possible to test this hypothesis in the near future when PBS1 has been isolated.
R genes known to require NDR1 belong to the
SA-dependent signaling
SA-dependent signaling is important for some gene-for-gene resistance responses, for local responses that limit the growth of virulent pathogens, and for SAR. SAR is a resistance response that is activated throughout the plant in response to local infection by necrotizing pathogens. As described above, EDS1 and PAD4 act upstream of SA to promote SA accumulation. The ankyrin-repeat protein NPR1; also known as NIM1 (NON-INDUCIBLE IMMUNITY 1) and SAI1 (SALICYLIC ACID INSENSITIVE 1) acts downstream
Jasmonic acid/ethylene-dependent signaling
The role of JA and ET in the activation of disease resistance mechanisms was demonstrated by the observation that expression of the PDF1.2 gene and other genes was prevented by mutations that block JA signaling (i.e. coi1) or ethylene signaling (i.e. ein2). JA and ET seem to be required simultaneously, as PDF1.2 expression is not activated by either ET treatment of coi1 plants or JA treatment of ein2 plants [40]. Furthermore, resistance to the fungal pathogen Alternaria brassicicola is
Induced systemic resistance
Colonization of roots by certain rhizosphere bacteria confers a form of disease resistance called induced systemic resistance (ISR). ISR occurs in nahG plants, so it is not an SA-dependent phenomenon. No significant changes in plant gene expression have been associated with ISR. Nonetheless, progress has been made in the genetic dissection of this phenomenon. Several years ago, it was found that ISR requires NPR1. This is interesting as it implies that NPR1 is involved in perception of more
Genes not yet placed into pathways
Several interesting mutants have been described that probably affect disease resistance signaling but that are not yet characterized in sufficient detail to allow them to be placed in particular positions in the network. Two genes, HXC2 (Hypersensitivity to Xanthomonas campestris pv. campestris 2) and RXC5 (Resistance to Xanthomonas campestris 5), are required for resistance to a particular isolate of Xanthomonas campestris, implying that they may be part of a gene-for-gene resistance mechanism
Conclusions and future prospects
A major area of progress in the past year has been in elucidating the relative sites of action of signaling components in signal transduction cascades. On the basis of the different requirements of various R genes for other genes to mediate resistance, R-gene-dependent signaling has been resolved into at least three different pathways. New genes have been defined in the SA signaling pathway, and constitutive mutants have been useful in ordering components of the pathway.
There is still much work
Acknowledgements
I apologize to scientists whose work I overlooked or was not able to include because of length limitations.
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
•of special interest
••of outstanding interest
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