Pathogen Resistance Signalling in Plants


Within natural ecosystems, most plants are resistant to most pathogens. At a fundamental level, this seemingly simply truth may hold the key to our understanding of how plants have evolved to survive under a myriad of environmental conditions and their associated stresses. Indeed, in defining how plants evolve, adapt and maintain broad spectrum resistance to most pathogens – typically referred to as non‐host resistance – we may not only reveal the mechanisms that underpin plant resistance signalling but also the precise manner in which plants regulate these processes under various environmental conditions. Herein lies the greatest challenge and unanswered question in the field of agriculture today: How do we feed 9 billion people by the year 2050? To address this, one of the first hurdles that must be overcome is a full understanding of the processes that regulate stress (i.e. abiotic and biotic) signalling in plants, as well as the processes that define pathogen and host specificity, including the performance of these processes under rapidly changing environmental conditions. In the case of pathogen infection, plants utilise a broad suite of innate and inducible mechanisms to resist invasion. In large part, these processes are governed by the activity of resistance (R) proteins, which are evolutionarily conserved and highly evolved proteins that function not only in pathogen recognition but also in the activation of the cellular processes necessary to defend against proliferation and the elicitation of disease. Furthermore, recent data supports the hypothesis that numerous processes, such as the balance between growth and defence, also contribute to the host resistance and pathogen virulence.

Key Concepts

  • Most plants are resistant to most pathogens.
  • Modern agriculture practices positively impact crop yield and durability. These practices can also have a negative impact on the unintended selection and enrichment of virulent pathogens.
  • Plants defend against pathogen invasion using a suite of highly conserved resistance (R) genes.
  • Pathogens have evolved to recognise and respond to the activity of plant R proteins through the deployment of secreted virulence factors.
  • Immune signalling in plants utilises various pre‐formed and inducible processes to defend against pathogen infection.
  • Many basic physiological processes, including response to light, temperature and water availability, are associated with, and required for, immune signalling.
  • The development of advanced genome sequencing technologies has increased the speed at which the development and selection of elite breeding lines are deployed into cropping systems.
  • Current plant breeding approaches utilise a hybrid of molecular genomics and classical breeding techniques to identify and introduce desirable traits into crops to enhance plant performance (e.g. resistance) and yield.

Keywords: biotic stress; immune signalling; pathogen; disease resistance; disease control; disease management; molecular biology; genomics; plant pathology

Figure 1. Illustration of the interactions between plants, pathogens, humans and the environment. As an expansion of the ‘Disease Triangle’ paradigm, human influence on modern agricultural practices has significantly impacted not only the performance of cropping systems as a function of biotic stress performance but also the inadvertent selection of enhanced, often hyper‐virulent pathogen races. As environmental conditions and abiotic stressors become more taxing on both plants and their pathogens, the influence of high temperatures, for example, has opposing effectors. For example, at high temperatures, the growth and selection of microbes with enhanced virulence is often observed. Conversely, at high temperatures, plant performance is often negatively affected, with plant resources and signalling processes shifted to abiotic stress tolerance/response signalling. As a result, plants are ‘forced to choose’ between survival due to abiotic stress and to allocate signalling to support immunity and defence signalling. As a key feature of the interaction of plants with environmental and microbes, human influence on this process is also becoming more evident. As populations increase, there is also an increase in the need to produce crops that generate higher yields, as well as perform under what are typically limiting environmental conditions (i.e. high temperature and drought). As a result, plant breeders must often choose between a balance of phenotypic traits and genotypes to introduce lines with elite performance under one or the other conditions, including the introduction of lines with enhanced nutritional or horticultural qualities. As a function of disease management, chemical treatment of crops with pesticides/fungicides influences not only plant performance under biotic stress conditions but can often times have a negative – unintended – influence on the selection and propagation of hyper‐virulent, pathogenic microbes. As a combination of each of these factors, we present an updated model of the classical ‘Disease Triangle’ to highlight the influence of humans on agricultural systems and plant performance: the ‘Disease Diamond’. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 2. Plants recognise a myriad of biotic conditions, pathogens and stresses and respond using complex, highly specific immune signalling cascades. The recognition of pathogenic organisms by plants is typically initiated through the perception of evolutionarily conserved features by pattern recognition receptors, and co‐receptors (represented by the blue and red transmembrane proteins, respectively), present on the cell surface of the invading organisms; in short, these molecules are perceived as ‘non‐self’ by the host plant. This form of immune signalling, termed pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI) results in the activation of a broad, non‐specific, defence signalling response that initiates a number of conserved and highly effective pathogen resistance mechanisms, including mitogen‐activated protein kinase (MAPK) signalling, the deposition of callose and the induction of defence‐responsive genes. As a more robust, sustained immune response, following the perception of pathogen‐secreted effector proteins [represented by black circles (bacterial effectors) and orange stars (oomycete effectors)], plants initiate a second, amplified, defence response, termed effector‐triggered immunity (ETI). This form of immune signalling relies on the specific interaction – either direct or indirect – between plant resistance (R) proteins and pathogen‐derived avirulence (Avr) proteins – broadly referred to as effectors. Similar to the activation of PTI, ETI initiates a series of similar, shared, signalling cascades whose outcome results in localised cell death responses, termed the hypersensitive response, which is similar in function to apoptosis. The outcome of this process is the abrogation of pathogen growth, and in most cases, the survival of the host. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 3. Immune signalling in plants and animals share a number of functionally similar pathogen perception and host signalling processes. The perception of pathogens in both plants and animals uses similar signalling mechanisms to induce changes in gene expression and cellular response to biotic stress. As a first response to pathogen invasion, plants and animals utilise a highly conserved immune signalling process – PTI – to initiate broad, non‐specific defence signalling cascades, including the generation of reactive oxygen species (ROS), activation of MAPK signalling and changes in gene expression associated with host defence. In plants, the induction of a second, amplified response – ETI – is initiated in response to the perception of secreted pathogen avirulence/effector proteins, which are recognised by host‐specific R proteins. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 4. Classical illustration of the genetic foundation for the ‘Gene‐for‐Gene’ interaction. Proposed by Flor in the 1940s, this foundational hypothesis describing the inheritance of resistance in plants and the maintenance of virulence in pathogens posits that for every gene in a plant that confers resistance, there is a corresponding, host‐recognised, gene in the pathogen that confers avirulence. In the presence of both genes (i.e. R + Avr), plants are resistance. When either gene is lacking (i.e. r + avr), plants are susceptible. This basic process has been used to define a number of R/Avr interactions in plants in the 70+ years since it was first discovered, and moreover, it provided a tractable mechanism to guide a number of plant breeding outcomes aimed at the generation and selection of plants with broad pathogen resistance. Image reproduced from Hammond‐Kosack and Kanyuka (2007).
Figure 5. R protein classes and their cellular location. The predicted domains of R proteins which confer either race‐specific or race‐non‐specific resistance are presented schematically: CC, coiled‐coil domain; TIR, Toll and Interleukin 1 receptor‐like motif; NB, nucleotide binding site; LRD, leucine‐rich domain; LRR, leucine‐rich repeat; NLS, nuclear localisation signal; ECS, endocytosis signal; PEST, Pro‐Glu‐Ser‐Ther‐like sequence; WRKY, motif characteristic of some plant transcription factors; 1, 2, 3, 4 – novel domains that lack significant homology to known proteins; 5, domain with homology to a B‐lectin; 6, structure with a weak similarity to a PAN domain; 7, structure with homology to epidermal growth factor (EGF)‐like domain; Cf‐2, Cf‐4 and Cf‐5 confer resistance to Cladosporium fulvum races expressing, respectively, Avr2, Avr4 and Avr5; L6 flax rust resistance 6; Mla10, resistance to Blumeria graminis f. sp. hordei expressing Avra10; RPM1, resistance to P. syringae pv. maculicola expressing AvrRpm1 or AvrB; RPP5, resistance to Hyaloperonospora parasitica expressing ATR5. Image reproduced from Hammond‐Kosack and Kanyuka (2007).


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Corrion, Alex, and Day, Brad(Jun 2015) Pathogen Resistance Signalling in Plants. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0020119.pub2]