Plant disease resistance protects plants from pathogens in two ways: by pre-formed structures and chemicals, and by infection-induced responses of the immune system. Relative to a susceptible plant, disease resistance is the reduction of pathogen growth on or in the plant (and hence a reduction of disease), while the term disease tolerance describes plants that exhibit little disease damage despite substantial pathogen levels. Disease outcome is determined by the three-way interaction of the pathogen, the plant, and the environmental conditions (an interaction known as the disease triangle).
Defense-activating compounds can move cell-to-cell and systematically through the plant's vascular system. However, plants do not have circulating immune cells, so most cell types exhibit a broad suite of antimicrobial defenses. Although obvious qualitative differences in disease resistance can be observed when multiple specimens are compared (allowing classification as "resistant" or "susceptible" after infection by the same pathogen strain at similar inoculum levels in similar environments), a gradation of quantitative differences in disease resistance is more typically observed between plant strains or genotypes. Plants consistently resist certain pathogens but succumb to others; resistance is usually specific to certain pathogen species or pathogen strains.
Background
Plant disease resistance is crucial to the reliable production of food, and it provides significant reductions in agricultural use of land, water, fuel, and other inputs. Plants in both natural and cultivated populations carry inherent disease resistance, but this has not always protected them.
The late blight Great Famine of Ireland of the 1840s was caused by the oomycete Phytophthora infestans. The world's first mass-cultivated banana cultivar Gros Michel was lost in the 1920s to Panama disease caused by the fungus Fusarium oxysporum. The current wheat stem rust, leaf rust, and yellow stripe rust epidemics spreading from East Africa into the Indian subcontinent are caused by rust fungi Puccinia graminis and P. striiformis. Other epidemics include chestnut blight, as well as recurrent severe plant diseases such as rice blast, soybean cyst nematode, and citrus canker.
Plant pathogens can spread rapidly over great distances, vectored by water, wind, insects, and humans. Across large regions and many crop species, it is estimated that diseases typically reduce plant yields by 10% every year in more developed nations or agricultural systems, but yield loss to diseases often exceeds 20% in less developed settings.
However, disease control is reasonably successful for most crops. Disease control is achieved by use of plants that have been bred for good resistance to many diseases, and by plant cultivation approaches such as crop rotation, pathogen-free seed, appropriate planting date and plant density, control of field moisture, and pesticide use.
Common disease resistance mechanisms
Pre-formed structures and compounds
Plant cuticle/surface Plant cell walls Antimicrobial chemicals (for example: polyphenols, sesquiterpene lactones, saponins) Antimicrobial peptides Enzyme inhibitors Detoxifying enzymes that break down pathogen-derived toxins Receptors that perceive pathogen presence and activate inducible plant defences
Inducible post-infection plant defenses
Cell wall reinforcement (cellulose, lignin, suberin, callose, cell wall proteins) Antimicrobial chemicals, including reactive oxygen species such as hydrogen peroxide or peroxynitrite, or more complex phytoalexins such as genistein or camalexin Antimicrobial proteins such as defensins, thionins, or PR-1 Antimicrobial enzymes such as chitinases, beta-glucanases, or peroxidases Hypersensitive response – a rapid host cell death response associated with defence induction.
Immune system
The plant immune system carries two interconnected tiers of receptors, one most frequently sensing molecules outside the cell and the other most frequently sensing molecules inside the cell. Both systems sense the intruder and respond by activating antimicrobial defenses in the infected cell and neighboring cells. In some cases, defense-activating signals spread to the rest of the plant or even to neighboring plants. The two systems detect different types of pathogen molecules and classes of plant receptor proteins.
The first tier is primarily governed by pattern recognition receptors that are activated by recognition of evolutionarily conserved pathogen or microbial–associated molecular patterns (PAMPs or MAMPs). Activation of PRRs leads to intracellular signaling, transcriptional reprogramming, and biosynthesis of a complex output response that limits colonization. The system is known as PAMP-triggered immunity or as pattern-triggered immunity (PTI).
The second tier, primarily governed by resistant gene products, or R gene products, is often termed effector-triggered immunity (ETI). ETI is typically activated by the presence of specific pathogen "effectors" and then triggers strong antimicrobial responses (see R gene section below).
In addition to PTI and ETI, plant defenses can be activated by the sensing of damage-associated compounds (DAMP), such as portions of the plant cell wall released during pathogenic infection.
Responses activated by PTI and ETI receptors include ion channel gating, oxidative burst, cellular redox changes, or protein kinase cascades that directly activate cellular changes (such as cell wall reinforcement or antimicrobial production), or activate changes in gene expression that then elevate other defensive responses.
Plant immune systems show some mechanistic similarities with the immune systems of insects and mammals, but also exhibit many plant-specific characteristics. The two above-described tiers are central to plant immunity but do not fully describe plant immune systems. In addition, many specific examples of apparent PTI or ETI violate common PTI/ETI definitions, suggesting a need for broadened definitions and/or paradigms. Currently, the term exoToxin-Triggered Immunity (TTI) has been introduced as an exotoxin associated immune response. This is separate to ETI or PTI due to the exotoxin's ability to trigger an immune response in plants alone. This immune pathway was only described in Arabidopsis thaliana, and with a specific exotoxin associated with Pseudomonas syringae (Syringomycin, or SYR), requiring further studies to expand the definition/role in plant immunity. Other papers have shown plant immune responses following various Cyclic Lipopeptides (CLPs) treatment, but have not described the response under a specific immune pathway (ETI, PTI, or TTI).
The term quantitative resistance (discussed below) refers to plant disease resistance that is controlled by multiple genes and multiple molecular mechanisms that each have small effects on the overall resistance trait. Quantitative resistance is often contrasted to ETI resistance mediated by single major-effect R genes.
Pattern-triggered immunity
PAMPs, conserved molecules that inhabit multiple pathogen genera, are referred to as MAMPs by many researchers. The defenses induced by MAMP perception are sufficient to repel most pathogens. However, pathogen effector proteins (see below) are adapted to suppress basal defenses such as PTI. Many receptors for MAMPs (and DAMPs) have been discovered. MAMPs and DAMPs are often detected by transmembrane receptor-kinases that carry LRR or LysM extracellular domains.
PTI has also been shown to control and suppress portions of the ETI pathway, acting as an immune control element for plant cells.
Effector triggered immunity
Effector triggered immunity (ETI) is activated by the presence of pathogen effectors. The ETI response is reliant on R genes, in which the effector products produced by pathogens bind to R protein receptors in the cell. Compared to PTI, ETI has a larger response, however, transcriptional regulation is largely conserved between PTI and ETI pathways.
Pathogens use effectors as a way to evade the plant PTI response, however plants can induce both PTI and ETI responses to pathogen invasion, rather than purely independent pathways. Plant ETI often causes an apoptotic hypersensitive response.
R genes and R proteins
Plants have evolved R genes (resistance genes) whose products mediate resistance to specific virus, bacteria, oomycete, fungus, nematode or insect strains. R gene products are proteins that allow recognition of specific pathogen effectors, either through direct binding or by recognition of the effector's alteration of a host protein. Many R genes encode NB-LRR proteins (proteins with nucleotide-binding and leucine-rich repeat domains, also known as NLR proteins or STAND proteins, among other names). Most plant immune systems carry a repertoire of 100–600 different R gene homologs. Individual R genes have been demonstrated to mediate resistance to specific virus, bacteria, oomycete, fungus, nematode or insect strains. R gene products control a broad set of disease resistance responses whose induction is often sufficient to stop further pathogen growth/spread.
Studied R genes usually confer specificity for particular strains of a pathogen species (those that express the recognized effector). As first noted by Harold Flor in his mid-20th century formulation of the gene-for-gene relationship, a plant R gene has specificity for a pathogen avirulence gene (Avr gene). Avirulence genes are now known to encode effectors. The pathogen Avr gene must have matched specificity with the R gene for that R gene to confer resistance, suggesting a receptor/ligand interaction for Avr and R genes. Alternatively, an effector can modify its host cellular target (or a molecular decoy of that target), and the R gene product (NLR protein) activates defenses when it detects the modified form of the host target or decoy.
Effector biology
Effectors are central to the pathogenic or symbiotic potential of microbes and microscopic plant-colonizing animals such as nematodes. Effectors typically are proteins that are delivered outside the microbe and into the host cell. These colonist-derived effectors manipulate the host's cell physiology and development. As such, effectors offer examples of co-evolution (example: a fungal protein that functions outside of the fungus but inside of plant cells has evolved to take on plant-specific functions). Pathogen host range is determined, among other things, by the presence of appropriate effectors that allow colonization of a particular host. Pathogen-derived effectors are a powerful tool to identify plant functions that play key roles in disease and in disease resistance. Apparently most effectors function to manipulate host physiology to allow disease to occur. Well-studied bacterial plant pathogens typically express a few dozen effectors, often delivered into the host by a Type III secretion apparatus. Fungal, oomycete and nematode plant pathogens apparently express a few hundred effectors.
So-called "core" effectors are defined operationally by their wide distribution across the population of a particular pathogen and their substantial contribution to pathogen virulence. Genomics can be used to identify core effectors, which can then be used to discover new R gene alleles, which can be used in plant breeding for disease resistance.
Small RNAs and RNA interference