Evolution of views on plant immunity: from Flor’s “gene-for-gene” theory to the “zig-zag model” developed by Jones and Dangl

The study of plant defence mechanisms in response to pathogens in the mid-20th century resulted in Harold Flor’s gene-for-gene interaction hypothesis, which became recognised as central to the study of phytoimmunity. According to this theory, the outcome of interactions in plant – pathogen phytopathosystems – i.e. compatibility or incompatibility – is controlled genetically in interacting organisms and determined by the presence of specific genes in both pathogen and plant: resistance genes in the plant and avirulence genes in pathogen. The latest achievements in phytoimmunology, obtained with the help of modern molecular biology and bioinformatics methods, have made a significant contribution to the classical understanding of plant immunity and provided grounds for a modern concept of phytoimmunity consisting in the “zig-zag model” developed by Jonathan Jones and Jefferey Dangl. Plant immunity is currently understood as being determined by an innate multi-layer immune system involving various structures and mechanisms of specific and non-specific immunity. Recognition by plant membrane receptors of conservative molecular patterns associated with microorganisms, as well as molecules produced during cell wall disruption by pathogen hydrolytic enzymes forms a basic non-specific immune response in the plant. Detection of pathogen effector molecules by plant intra-cellular receptors triggers a specific effector-triggered immunity, resulting in the development of the hypersensitive response, systemic resistance and immune memory of the plant. Virulence factors and pathogen attack strategies on the one hand, and mechanisms of plant immune protection on the other, are the result of one form of constant co-evolution, often termed an “evolutionary arms race”. This paper discusses the main principles of Flor's classical “gene-for-gene interaction” theory as well as the molecular-genetic processes of plant innate immunity, their mechanisms and participants in light of contemporary achievements in phytoimmunology.

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Salicylic acid signalling: new insights and prospects at a quarter-century milestone

Essays in Biochemistry ◽

10.1042/bse0580101 ◽

2015 ◽

Vol 58 ◽

pp. 101-113 ◽

Cited By ~ 25

Author(s):

Xiaoyu Liu ◽

Kristin S. Rockett ◽

Camilla J. Kørner ◽

Karolina M. Pajerowska-Mukhtar

Keyword(s):

Salicylic Acid ◽

Molecular Mechanisms ◽

Plant Immunity ◽

Plant Defence ◽

Immune Memory ◽

Quarter Century ◽

Modern Agriculture ◽

Signalling Network ◽

Defence Responses ◽

Plant Defence Responses

The plant hormone salicylic acid (SA) plays an essential role in the regulation of diverse biological processes throughout the entire lifespan of the plant. Twenty-five years ago, SA first emerged as an endogenous signal capable of inducing plant defence responses both at the site of infection and in the systemic tissue of the plant. Since then, SA-mediated signalling pathways have been extensively characterized and dissected using genetic and biochemical approaches. Current research is largely focused on the identification of novel SA downstream signalling genes, in order to understand their precise contributions to the phytohormonal cross-talk and signalling network. This will subsequently help us to identify novel targets that are important for plant health, and contribute to advances in modern agriculture. In this chapter we highlight recent advances in the field of SA biosynthesis and the discovery of candidates for systemic mobile signals. We also discuss the molecular mechanisms underlying SA perception. In addition, we review the novel SA signalling components that expand the scope of SA functions beyond plant immunity to include plant growth and development, endoplasmic reticulum (ER) stress, DNA repair and homologous recombination. Finally, we shed light on the roles of SA in epigenetically controlled transgenerational immune memory that has long-term benefits for plants.

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The plant endoplasmic reticulum is both receptive and responsive to pathogen effectors

10.1101/2020.06.09.142141 ◽

2020 ◽

Author(s):

Emily Breeze ◽

Victoria Vale ◽

Hazel McLellan ◽

Laurence Godiard ◽

Murray Grant ◽

...

Keyword(s):

Endoplasmic Reticulum ◽

Pseudomonas Syringae ◽

Secretory Pathway ◽

Temporal Dynamics ◽

De Novo ◽

Morphological Changes ◽

Plant Immunity ◽

Plant Defence ◽

Pathogen Effectors ◽

Pathogen Effector

AbstractThe endoplasmic reticulum (ER) is the entry point to the secretory pathway and, as such, is critical for adaptive responses to biotic stress, when the demand for de novo synthesis of immunity-related proteins and signalling components increases significantly. Comprised of a network of interconnected tubules and cisternae, the architecture of the ER is highly pleomorphic and dynamic, rapidly remodelling to meet new cellular requirements. During infection with the hemi-biotrophic phytopathogen, Pseudomonas syringae pv. tomato DC3000, the ER in cells immediately adjacent to established bacterial colonies condenses into ‘knot-like’ structures, reminiscent of fenestrated sheets. Based on known temporal dynamics of pathogen effector delivery and initial bacterial multiplication, the timing of these observed morphological changes is rapid and independent of classical elicitor activation of pathogen-triggered immunity. To further investigate a role for ER reconfiguration in suppression of plant immunity we identified a conserved C-terminal tail-anchor domain in a set of pathogen effectors known to localize to the ER and used this protein topology in an in silico screen to identify putative ER-localised effectors within the effectorome of the oomycete Phytophthora infestans. Subsequent characterization of a subset of 15 candidate tail-anchored P. infestans effectors revealed that 11 localised to the ER and/or Golgi. Notably, transient expression of an ER-localised effector from the closely related oomycete, Plasmopara halstedii, reconfigured the ER network, revealing intimate association of labelled ER with perinuclear chloroplasts and clusters of chloroplasts, potentially facilitating retrograde signalling during plant defence.

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Deciphering the mode of action and host recognition of bacterial type III effectors

Functional Plant Biology ◽

10.1071/fp10085 ◽

2010 ◽

Vol 37 (10) ◽

pp. 926 ◽

Cited By ~ 2

Author(s):

Selena Gimenez-Ibanez ◽

Dagmar R. Hann ◽

John P. Rathjen

Keyword(s):

Mode Of Action ◽

Pathogenic Bacteria ◽

Plant Immunity ◽

Plant Defence ◽

Host Recognition ◽

Type Iii Effectors ◽

Host Cytoplasm ◽

Host Plasma Membrane ◽

Defence Responses ◽

Bacterial Effectors

Plant pathogenic bacteria adhere to cell walls and remain external to the cell throughout the pathogenic lifecycle, where they elicit host immunity through host plasma membrane localised receptors. To be successful pathogens, bacteria must suppress these defence responses, which they do by secreting a suite of virulence effector molecules into the host cytoplasm. However, effectors themselves can act as elicitors after perception by intracellular host immune receptors, thus, re-activating plant immunity. Bacterial effectors generally target host molecules through specific molecular activities to defeat plant defence responses. Although effectors can be used as tools to elucidate components of plant immunity, only a handful of these molecular targets are known and much remains to be learnt about effector strategies for bacterial pathogenicity. This review highlights recent advances in our understanding of the mode of action of bacterial effectors, which in the future will lead to improvements in agriculture.

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Rhodopseudomonas palustris quorum sensing molecule pC-HSL induces systemic resistance to TMV infection via up-regulation of NbSIPK/NbWIPK expressions in Nicotiana benthamiana

Phytopathology ◽

10.1094/phyto-05-20-0177-r ◽

2020 ◽

Author(s):

Xiaohua Du ◽

Renyan Huang ◽

Zhuo Zhang ◽

Deyong Zhang ◽

Ju`e Cheng ◽

...

Keyword(s):

Quorum Sensing ◽

Nicotiana Benthamiana ◽

Biological Activities ◽

Plant Immunity ◽

Rhodopseudomonas Palustris ◽

Photosynthetic Bacterium ◽

Homoserine Lactone ◽

Systemic Resistance ◽

Marker Genes ◽

Ros Scavenging

G-negative bacteria produce a myriad of N-acyl-homoserine lactones (AHLs) that can function as quorum sensing (QS) signaling molecules. AHLs are also known to regulate various plant biological activities. p-Coumaroyl-homoserine lactone (pC-HSL) is the only QS molecule produced by a photosynthetic bacterium, Rhodopseudomonas palustris (R. palustris). The role of pC-HSL in the interaction between R. palustris and plant has not been investigated. In this study, we investigated the effect of pC-HSL on plant immunity and have found that this QS molecule can induce a systemic resistance to Tobacco mosaic virus (TMV) infection in Nicotiana benthamiana (N. benthamiana). The results show that pC-HSL treatment can prolong the activation of two mitogen-associated protein kinase (MAPK) genes (i.e., NbSIPK and NbWIPK) and enhance the expression of transcription factor WRKY8 as well as immune response marker genes NbPR1 and NbPR10, leading to an increased accumulation of reactive oxygen species (ROS) in the TMV infected plants. Our results also show that pC-HSL treatment can increase activities of two ROS-scavenging enzymes, POD and SOD. Knockdown of NbSIPK or NbWIPK expression in N. benthamiana plants through VIGS nullified or attenuated pC-HSL-induced systemic resistance, indicating that the functioning of pC-HSL relies on the activity of those two kinases. Meanwhile, pC-HSL pre-treated plants also showed a strong induction of kinase activities of NbSIPK and NbWIPK post TMV inoculation. Taken together, our results demonstrate that pC-HSL treatment results in enhanced plant resistance to TMV infection, which is helpful to uncover the outcome of interaction between R. palustris and its host plants.

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Modes of action of non-pathogenic strains of Fusarium oxysporum in controlling Fusarium wilts

Plant Protection Science ◽

10.17221/10354-pps ◽

2002 ◽

Vol 38 (SI 1 - 6th Conf EFPP 2002) ◽

pp. 195-199 ◽

Cited By ~ 2

Author(s):

C. Alabouvette ◽

Ch. Olivain

Keyword(s):

Fusarium Oxysporum ◽

Plant Defence ◽

Root Surface ◽

Systemic Resistance ◽

Induce Systemic Resistance ◽

Biocontrol Efficacy ◽

Modes Of Action ◽

Defence Reactions ◽

Chlamydospore Germination ◽

Fusarium Wilts

Many studies have demonstrated the capacity of non-pathogenic strains of F. oxysporum to control Fusarium diseases. These non-pathogenic strains show several modes of action contributing to their biocontrol capacity. They are able to compete for nutrients in the soil, affecting the rate of chlamydospore germination and the saprophytic growth of the pathogen, diminishing the probability for the pathogen to reach the root surface. They are competing with the pathogen at the root surface for colonization of infection sites, and inside the root where they induce plant defence reactions. By triggering the defence reactions, they induce systemic resistance of the plant. Depending on the strain, and on the plant species, these mechanisms are more or less important, leading to a more or less efficient biocontrol efficacy.

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Arbuscular Mycorrhizal Symbiosis Affects Plant Immunity to Viral Infection and Accumulation

Viruses ◽

10.3390/v11060534 ◽

2019 ◽

Vol 11 (6) ◽

pp. 534 ◽

Cited By ~ 8

Author(s):

Zhipeng Hao ◽

Wei Xie ◽

Baodong Chen

Keyword(s):

Viral Infection ◽

Plant Immunity ◽

Arbuscular Mycorrhizal ◽

Am Fungi ◽

Plant Viruses ◽

Limiting Factors ◽

Systemic Resistance ◽

Mycorrhizal Symbiosis ◽

Complex Nature ◽

Terrestrial Plants

Arbuscular mycorrhizal (AM) fungi, as root symbionts of most terrestrial plants, improve plant growth and fitness. In addition to the improved plant nutritional status, the physiological changes that trigger metabolic changes in the root via AM fungi can also increase the host ability to overcome biotic and abiotic stresses. Plant viruses are one of the important limiting factors for the commercial cultivation of various crops. The effect of AM fungi on viral infection is variable, and considerable attention is focused on shoot virus infection. This review provides an overview of the potential of AM fungi as bioprotection agents against viral diseases and emphasizes the complex nature of plant–fungus–virus interactions. Several mechanisms, including modulated plant tolerance, manipulation of induced systemic resistance (ISR), and altered vector pressure are involved in such interactions. We propose that using “omics” tools will provide detailed insights into the complex mechanisms underlying mycorrhizal-mediated plant immunity.

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The role of oomycete effectors in plant - pathogen interactions

Functional Plant Biology ◽

10.1071/fp10073 ◽

2010 ◽

Vol 37 (10) ◽

pp. 919 ◽

Cited By ~ 22

Author(s):

Adrienne R. Hardham ◽

David M. Cahill

Keyword(s):

Plant Cell ◽

Plant Pathogens ◽

Plant Defence ◽

Effector Proteins ◽

Plant Structure ◽

Cell Wall Degrading Enzymes ◽

Cell Cytoplasm ◽

Diverse Range ◽

Successful Infection ◽

Pathogen Effector

Plants constantly come into contact with a diverse range of microorganisms that are potential pathogens, and they have evolved multi-faceted physical and chemical strategies to inhibit pathogen ingress and establishment of disease. Microbes, however, have developed their own strategies to counteract plant defence responses. Recent research on plant–microbe interactions has revealed that an important part of the infection strategies of a diverse range of plant pathogens, including bacteria, fungi and oomycetes, is the production of effector proteins that are secreted by the pathogen and that promote successful infection by manipulating plant structure and metabolism, including interference in plant defence mechanisms. Pathogen effector proteins may function either in the extracellular spaces within plant tissues or within the plant cell cytoplasm. Extracellular effectors include cell wall degrading enzymes and inhibitors of plant enzymes that attack invading pathogens. Intracellular effectors move into the plant cell cytoplasm by as yet unknown mechanisms where, in incompatible interactions, they may be recognised by plant resistance proteins but where, in compatible interactions, they may suppress the plant’s immune response. This article presents a brief overview of our current understanding of the nature and function of effectors produced by oomycete plant pathogens.

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Genome-wide transcriptomic analysis reveals correlation between higher WRKY61 expression and reduced symptom severity in Turnip crinkle virus infected Arabidopsis thaliana

Scientific Reports ◽

10.1038/srep24604 ◽

2016 ◽

Vol 6 (1) ◽

Cited By ~ 11

Author(s):

Ruimin Gao ◽

Peng Liu ◽

Yuhan Yong ◽

Sek-Man Wong

Keyword(s):

Arabidopsis Thaliana ◽

Transcriptome Analysis ◽

Plant Immunity ◽

Plant Defence ◽

Enrichment Analysis ◽

Global Gene Expression ◽

Chemical Stimulus ◽

Turnip Crinkle Virus ◽

Rna Seq ◽

Genome Wide

Abstract Turnip crinkle virus (TCV) is a carmovirus that infects many Arabidopsis ecotypes. Most studies mainly focused on discovery of resistance genes against TCV infection and there is no Next Generation Sequencing based comparative genome wide transcriptome analysis reported. In this study, RNA-seq based transcriptome analysis revealed that 238 (155 up-regulated and 83 down-regulated) significant differentially expressed genes with at least 15-fold change were determined. Fifteen genes (including upregulated, unchanged and downregulated) were selected for RNA-seq data validation using quantitative real-time PCR, which showed consistencies between these two sets of data. GO enrichment analysis showed that numerous terms such as stress, immunity, defence and chemical stimulus were affected in TCV-infected plants. One putative plant defence related gene named WRKY61 was selected for further investigation. It showed that WRKY61 overexpression plants displayed reduced symptoms and less virus accumulation, as compared to wild type (WT) and WRKY61 deficient lines, suggesting that higher WRKY61 expression level reduced TCV viral accumulation. In conclusion, our transcriptome analysis showed that global gene expression was detected in TCV-infected Arabidopsis thaliana. WRKY61 gene was shown to be negatively correlated with TCV infection and viral symptoms, which may be connected to plant immunity pathways.

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