Plant Immune Systems

Omni Magazine, Jan. 1985
Bill Lawren
When the human body is attacked by an invading organism—a virus or bacterium—its immune system organizes itself to repel the attacker. Now a new piece of research from the University of California at Davis indicates that plants may respond in a similar way to invasion by pests.
     Davis entomologists Richard Karban and James Carey placed 16 female spider mites on several cotton seedlings, leaving another group of seedlings mite-free. After five days the mites were killed with a Kelthane pesticide. Twelve days later a new batch of mites was introduced to the plants. After two more weeks the populations were counted. According to Karban and Carey, "fewer mites were found on plants that had been previously exposed than on unexposed controls."
     Karban thinks the presence of pests might generate what he calls a 'wounding response' in plants. This response in turn triggers the production of an unknown substance that, he says, 'has the effect of inhibiting the subsequent population growth' of the pest. If this is true, Karban and Carey speculate that 'it may be possible to inoculate a plant' against both pests and diseases.
     Karban cautions that it will be some time before viable plant vaccines are available to farmers. First the experiments have to be duplicated under field conditions. Then, he says, 'I've got to come up with some easier way to inoculate the plants. can't expect cotton farmers to put mites on their plants and remove them every five days'.

Oecologia, 113(1): 74-81 (Dec 1997)
Specificity of induced resistance in the tomato, Lycopersicon esculentum
Michael J. Stout, Kathi V. Workman, Richard M. Bostock and Sean S. Duffey
Specificity in the induced responses of tomato foliage to arthropod herbivores was investigated. We distinguished between two aspects of specificity: specificity of effect (the range of organisms affected by a given induced response), and specificity of elicitation (ability of the plant to generate distinct chemical responses to different damage types). Specificity of effect was investigated by examining the effect of restricted feeding by Helicoverpa zea on the resistance of tomato plants to an aphid species (Macrosiphum euphorbiae), a mite species (Tetranychus urticae), a noctuid species (Spodoptera exigua), and to a phytopathogen, Pseudomonas syringae pv. tomato. Prior H. zea feeding was found to increase the resistance of tomato plants to all four organisms. Specificity in elicitation was investigated by examining the effect of aphid feeding on the activities of four defense-related proteins and on the suitability of foliage for S. exigua. Aphid feeding was found to induce peroxidase and lipoxygenase activities but not polyphenol oxidase and proteinase inhibitor activities; this response is distinct from the response to H. zea feeding, which induces polyphenol oxidase and proteinase inhibitors but not peroxidase. Leaflets which had been fed upon by aphids were better sources of food for S. exigua than were leaflets which had not been fed upon by aphids. Studies of both these aspects of specificity are needed to understand the way in which plants coordinate and integrate induced responses against insects with other physiological processes.

Pesticide Science 55(2): 193-196. Mar. 26, 1999
Plant immunisation: from myth to SAR
The idea that plants might be able to develop a form of acquired immunity to infection following exposure to a pathogen has been current ever since discovery of the animal immune system in the later years of the nineteenth century. Early attempts to demonstrate a comparable system in plants focused on the detection of precipitating antibodies and hence were doomed to failure. Nevertheless, largely anecdotal evidence for plant immunisation continued to accumulate, culminating in the discovery of phytoalexins in the 1940s. Convincing evidence for systemic changes in plant resistance following an inducer inoculation was not available until 20 years later, when pioneering work on tobacco infected with blue mould (Peronospora tabacina) or tobacco mosaic virus (TMV) showed that tissues remote from the inoculation site were altered in disease reaction type. Increased resistance was expressed as a reduction in lesion numbers and size, and a reduced rate of pathogen reproduction. Systemic acquired resistance (SAR) has now been demonstrated in at least 20 plant species in at least six plant families, although detailed genetic or molecular analysis has mainly been confined to a few models, such as tobacco, cucumber and Arabidopsis. SAR is associated with the coordinate induction of genes encoding defence proteins which can be used as molecular markers of the response. The availability of Arabidopsis mutants altered in the induction and expression of SAR is now providing new insights into the signal transduction pathway(s) involved, and will enable comparison with the molecular mechanisms operating in other plant taxa. Important unresolved questions concern the nature of the translocated signal, the mechanism of defence priming, efficacy of the response against different pathogens, and practical exploitation of SAR in crop protection. The first generation of chemical plant defence activators is now commercially available and optimal use of these SAR inducers in integrated disease control requires further evaluation. The prospects for engineering transgenic crops altered in the regulation or expression of SAR is also a subject for further investigation.

Trends in Genetics 17(1): 449-459 (1 Aug 2001)
RNA silencing as a plant immune system against viruses
Olivier Voinnet
‘RNA silencing’ refers to related processes of post-trancriptional control of gene expression found in plants, animals and fungi. A unifying feature of RNA silencing is that it mediates sequence-specific degradation of target transcripts, recruiting RNA molecules of 21–23 nucleotides as specificity determinants. In higher plants, RNA silencing serves as an adaptive, antiviral defence system, which is transmitted systemically in response to localized virus challenge. Plant viruses have elaborated a variety of counter-defensive measures to overcome the host silencing response. One of these strategies is to produce proteins that target the cell autonomous or signalling steps of RNA silencing. It is not known whether a similar antiviral mechanism also operates in animal cells.

Annals of Botany 89: 503-512, 2002
Induced Systemic Resistance (ISR) Against Pathogens in the Context of Induced Plant Defences
Martin Heil, Richard M. Bostock
Induced systemic resistance (ISR) of plants against pathogens is a widespread phenomenon that has been intensively investigated with respect to the underlying signalling pathways as well as to its potential use in plant protection. Elicited by a local infection, plants respond with a salicylic-dependent signalling cascade that leads to the systemic expression of a broad spectrum and long-lasting disease resistance that is efficient against fungi, bacteria and viruses. Changes in cell wall composition, de novo production of pathogenesis-related-proteins such as chitinases and glucanases, and synthesis of phytoalexins are associated with resistance, although further defensive compounds are likely to exist but remain to be identified. In this Botanical Briefing we focus on interactions between ISR and induced resistance against herbivores that is mediated by jasmonic acid as a central signalling molecule. While many studies report cross-resistance, others have found trade-offs, i.e. inhibition of one resistance pathway by the other. Here we propose a framework that explains many of the thus far contradictory results. We regard elicitation separately from signalling and from production, i.e. the synthesis of defensive compounds. Interactions on all three levels can act independently from each other.

Plant Immune Systems - August 7, 2002
Jeff Schalau, County Director, Agent, Agriculture & Natural Resources
Arizona Cooperative Extension, Yavapai County
Plant scientists call this immune response within plants induced systemic resistance (ISR). ISR was first observed about 100 years ago and has now been identified in over 30 species of plants. Researchers noticed that disease attacks on plants led to a hypersensitive reaction characterized by lesions at the point of entry. The hypersensitive reaction prevented the spread of the disease within the plant. Not only is the disease organism localized, but the rest of the plant is also made resistant to attack by that disease.

Plant immune system's 'take two aspirin' gene, offers hope for disease control - December 2003
From Cornell University News Service
Discovery of the salicylic acid-binding protein 2 (SABP2) gene, by scientists at Boyce Thompson Institute for Plant Research (BTI) at Cornell University, is being called an important step toward new strategies to boost plants' natural defenses against disease and for reducing the need for agricultural pesticides.

The Plant Journal 38(4): 639-649 (May 2004)
Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata
André Kessler and Ian T. Baldwin
A plant's responses to attack from particular pathogens and herbivores may result in resistance to subsequent attack from the same species, but may also affect different species. Such a cross-resistance, called immunization or vaccination, can benefit the plant, if the fitness consequences of attack from the initial attacker are less than those from subsequent attackers. Here, we report an example of naturally occurring vaccination of the native tobacco plant, Nicotiana attenuata, against Manduca hornworms by prior attack from the mirid bug, Tupiocoris notatus (Dicyphus minimus), which results from the elicitation of two categories of induced plant responses. First, attack from both herbivore species causes the plants in nature to release predator-attracting volatile organic compounds (VOCs), and the attracted generalist predator, Geocoris pallens, preferentially attacks the less mobile hornworm larvae. Second, attack from both mirids and hornworms increases the accumulation of secondary metabolites and proteinase inhibitors (PIs) in the leaf tissue, which is correlated with the slow growth of Manduca larvae. Mirid damage does not significantly reduce the fitness of the plant in nature, whereas attack from the hornworm reduces lifetime seed production. Consequently, plants that are attacked by mirids realize a significant fitness advantage in environments with both herbivores. The combination of growth-slowing direct defenses and predator-attracting indirect defenses results in greater hornworm mortality on mirid-attacked plants and provides the mechanism of the vaccination phenomenon.

The Plant Journal 38(4):650-663 (May 2004)
Herbivore-induced plant vaccination. Part II. Array-studies reveal the transience of herbivore-specific transcriptional imprints and a distinct imprint from stress combinations
Claudia Voelckel and Ian T. Baldwin
Microarray technology has given plant biologists the ability to simultaneously monitor changes in the expression of hundreds of genes, and yet, to date, this technology has not been applied to ecological phenomena. In native tobacco (Nicotiana attenuata), prior attack of sap-feeding mirids (Tupiocoris notatus) results in vaccination of the plant against subsequent attacks by chewing hornworms (Manduca sexta). This vaccination is mediated by a combination of direct and indirect defenses and tolerance responses, which act in concert with the attack preferences of a generalist predator. Here, we use microarrays enriched in herbivore-elicited genes with a principal components analysis (PCA) to characterize transcriptional 'imprints' of single, sequential, or simultaneous attacks by these two main herbivores of N. attenuata. The PCA identified distinctly different imprints left by individual attack from the two species after 24 h, but not after 5 days. Moreover, imprints of sequential or simultaneous attacks differed significantly from those of single attack, suggesting the existence of a distinct gene expression program responsive to the combination of biological stressors. A dissection of the transcriptional imprints revealed responses in direct and indirect defense genes that were well correlated with observed increases in defense metabolites. Attack from both herbivores elicits a switch from growth- to defense-related transcriptional processes, and herbivore-specific changes occur largely in primary metabolism and signaling cascades. PCA of these polygenic transcriptional imprints characterizes the ephemeral changes in the transcriptome that occur during the maturation of ecologically relevant phenotypic responses.

Researchers Uncover How Infections Combat Plant Immune Responses (November 2, 2004)
UCR Researcher Part of Team That Identified Three Genetic Suppressors of Immune Response in Plants
RNA silencing is a recently discovered defense mechanism against virus infection in plants and invertebrates. For successful infection to occur, viruses must be able to suppress the RNA silencing’s antiviral response. “Our results demonstrate that citrus tristeza virus (CTV) produces three proteins that are suppressors of RNA silencing and each inhibits RNA silencing in a distinct manner,” said Ding.

Block, A., Schmelz, E.A., O'Donnell, P.J., Jones, J.B., Klee, H.J. 2005. Systemic Acquired Tolerance To Virulent Bacterial Pathogens In Tomato. Plant Physiology. 138:1481-1490.
Plant responses to pathogen attack can vary over a broad range. At one extreme, resistance, a defensive response in the form of rapid tissue death, can limit the further spread of pathogen growth. Alternatively, plants may exhibit tolerance in which pathogens colonize the plant yet result in very little visual disease symptoms. The development of increased widespread plant resistance responses, termed systemic acquired resistance (SAR), to subsequent pathogen attack has been well documented and studied. Surprisingly, how pathogen infection may alter a plants tolerance to subsequent infection is not well understood. Working with the University of Florida (Department of Horticultural Sciences) scientists at the Center for Medical, Agricultural and Veterinary Entomology in Gainesville, FL, have discovered that tomato plants infected by virulent Xanthomonas bacteria display increased tolerance to subsequent infections. This systemic acquired tolerance (SAT) response was characterized by reduced levels of plant cell death with no effect on pathogen growth. The plant hormones ethylene and salicylic acid mediate biochemical systemic responses, such as the production of pathogenesis related proteins, but did not limit pathogen growth in response to virulent Xanthomonas bacteria. This result suggests that a partial or low-level plant defense response represses disease symptom development without affecting bacterial growth. This intermediate plant resistance outcome demonstrates a greater complexity in plant-pathogen interactions than previously appreciated and underscores the importance of understanding how plant defenses are overcome in effort to develop strategies for crop improvement.

Cell, 124(4): 803-814 (Feb 2006)
Host-Microbe Interactions: Shaping the Evolution of the Plant Immune Response
S. Chisholm, G. Coaker, B. Day, B. Staskawicz
The evolution of the plant immune response has culminated in a highly effective defense system that is able to resist potential attack by microbial pathogens. The primary immune response is referred to as PAMP-triggered immunity (PTI) and has evolved to recognize common features of microbial pathogens. In the coevolution of host-microbe interactions, pathogens acquired the ability to deliver effector proteins to the plant cell to suppress PTI, allowing pathogen growth and disease. In response to the delivery of pathogen effector proteins, plants acquired surveillance proteins (R proteins) to either directly or indirectly monitor the presence of the pathogen effector proteins. In this review, taking an evolutionary perspective, we highlight important discoveries over the last decade about the plant immune response.

Nature 444, 323-329 (16 November 2006)
The plant immune system
Jonathan D. G. Jones & Jeffery L. Dangl
Many plant-associated microbes are pathogens that impair plant growth and reproduction. Plants respond to infection using a two-branched innate immune system. The first branch recognizes and responds to molecules common to many classes of microbes, including non-pathogens. The second responds to pathogen virulence factors, either directly or through their effects on host targets. These plant immune systems, and the pathogen molecules to which they respond, provide extraordinary insights into molecular recognition, cell biology and evolution across biological kingdoms. A detailed understanding of plant immune function will underpin crop improvement for food, fibre and biofuels production.

Annual Review of Plant Biology 59: 41-66. (June 2008)
Plant Immunity to Insect Herbivores
Gregg A. Howe and Georg Jander
Herbivorous insects use diverse feeding strategies to obtain nutrients from their host plants. Rather than acting as passive victims in these interactions, plants respond to herbivory with the production of toxins and defensive proteins that target physiological processes in the insect. Herbivore-challenged plants also emit volatiles that attract insect predators and bolster resistance to future threats. This highly dynamic form of immunity is initiated by the recognition of insect oral secretions and signals from injured plant cells. These initial cues are transmitted within the plant by signal transduction pathways that include calcium ion fluxes, phosphorylation cascades, and, in particular, the jasmonate pathway, which plays a central and conserved role in promoting resistance to a broad spectrum of insects. A detailed understanding of plant immunity to arthropod herbivores will provide new insights into basic mechanisms of chemical communication and plant-animal coevolution and may also facilitate new approaches to crop protection and improvement.

Kuska: Temperature effect on Rose mosaic virus behavior (Nov 11, 2014)

Johansson: Plant pathogen defense: Signalling, resistance and cell death (2015)
The plant immune system consists of two main tiers of defense responses; the MAMP triggered im- munity (MTI) and the Effector triggered immunity (ETI). MTI is triggered by recognition of microbe associated molecular patterns MAMPs. MTI strengthens the cell by producing antimicrobial substances, proteins and by fortifying the cell wall. This stops the majority of non-adapted microbes. A subset of microbes have adapted to these measures and evolved effector proteins that subdue the MTI responses. Again, plants have responded, by evolving resistance (R) proteins that recognize effector activity and mount the swift responses that are ETI. The plant responses during ETI are commonly termed the hy- persensitive response (HR) and culminate in programmed cell death of the infected and sometimes sur- rounding cells.