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Journal ArticleDOI

Plant Immune Responses Against Viruses: How Does a Virus Cause Disease?

01 May 2013-The Plant Cell (American Society of Plant Biologists)-Vol. 25, Iss: 5, pp 1489-1505
TL;DR: A summary and update of advances in plant antiviral immune responses, beyond RNA silencing mechanisms, is provided and the rise of Brachypodium and Setaria species as model grasses to study antiviral responses in Poaceae is documented.
Abstract: Plants respond to pathogens using elaborate networks of genetic interactions. Recently, significant progress has been made in understanding RNA silencing and how viruses counter this apparently ubiquitous antiviral defense. In addition, plants also induce hypersensitive and systemic acquired resistance responses, which together limit the virus to infected cells and impart resistance to the noninfected tissues. Molecular processes such as the ubiquitin proteasome system and DNA methylation are also critical to antiviral defenses. Here, we provide a summary and update of advances in plant antiviral immune responses, beyond RNA silencing mechanisms—advances that went relatively unnoticed in the realm of RNA silencing and nonviral immune responses. We also document the rise of Brachypodium and Setaria species as model grasses to study antiviral responses in Poaceae, aspects that have been relatively understudied, despite grasses being the primary source of our calories, as well as animal feed, forage, recreation, and biofuel needs in the 21st century. Finally, we outline critical gaps, future prospects, and considerations central to studying plant antiviral immunity. To promote an integrated model of plant immunity, we discuss analogous viral and nonviral immune concepts and propose working definitions of viral effectors, effector-triggered immunity, and viral pathogen-triggered immunity.

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Citations
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Journal ArticleDOI
01 May 2015-Virology
TL;DR: This work will present host factors implicated in antiviral pathways and summarize the current status of knowledge about the diverse viral suppressors' strategies acting at various steps of antiviral silencing in plants, and consider the multi-functionality of these versatile proteins and related biochemical processes in which they may be involved in fine-tuning the plant-virus interaction.

420 citations


Cites background from "Plant Immune Responses Against Viru..."

  • ...These include hypersensitive reaction (HR) (Mandadi and Scholthof, 2013), systemic acquired resistance (SAR) (Kachroo and Robin, 2013), activation of ubiquitin/26S proteasome system (UPS) (Dielen et al....

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  • ...These include hypersensitive reaction (HR) (Mandadi and Scholthof, 2013), systemic acquired resistance (SAR) (Kachroo and Robin, 2013), activation of ubiquitin/26S proteasome system (UPS) (Dielen et al., 2010) or RNA silencing (RNA interference, RNAi) (Pumplin and Voinnet, 2013)....

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Journal ArticleDOI
TL;DR: Recent findings on the different roles of hormones in the regulation of plant–virus interactions are summarized, which are helping to elucidate the fine tuning of viral and plant systems by hormones.
Abstract: Hormones are tuners of plant responses to biotic and abiotic stresses. They are involved in various complicated networks, through which they modulate responses to different stimuli. Four hormones primarily regulate plant defence to pathogens: salicylic acid (SA), jasmonic acid (JA), ethylene (Et) and abscisic acid (ABA). In susceptible plants, viral infections result in hormonal disruption, which manifests as the simultaneous induction of several antagonistic hormones. However, these antagonistic hormones may exhibit some sequential accumulation in resistant lines. Virus propagation is usually restricted by the activation of the small interfering RNA (siRNA) antiviral machinery and/or SA signalling pathway. Several studies have investigated these two systems, using different model viruses. However, the roles of hormones other than SA, especially those with antagonistic properties, such as ABA, have been neglected. Increasing evidence indicates that hormones control components of the small RNA system, which regulates many processes (including the siRNA antiviral machinery and the microRNA system) at the transcriptional or post-transcriptional level. Consequently, cross-talk between the antagonistic SA and ABA pathways modulates plant responses at multiple levels. In this review, we summarize recent findings on the different roles of hormones in the regulation of plant-virus interactions, which are helping us to elucidate the fine tuning of viral and plant systems by hormones.

280 citations


Cites background from "Plant Immune Responses Against Viru..."

  • ...Work on monocots has focused on breeding for resistance, leaving the underlying mechanisms largely unexplored (Mandadi and Scholthof, 2013)....

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Journal ArticleDOI
TL;DR: This review aims at describing some of the most devastating diseases caused by viruses on crops and summarizes current knowledge about plant–virus interactions, focusing on resistance mechanisms that prevent or limit viral infection in plants.
Abstract: Viruses cause epidemics on all major cultures of agronomic importance, representing a serious threat to global food security. As strict intracellular pathogens, they cannot be controlled chemically and prophylactic measures consist mainly in the destruction of infected plants and excessive pesticide applications to limit the population of vector organisms. A powerful alternative frequently employed in agriculture relies on the use of crop genetic resistances, approach that depends on mechanisms governing plant-virus interactions. Hence, knowledge related to the molecular bases of viral infections and crop resistances is key to face viral attacks in fields. Over the past 80 years, great advances have been made on our understanding of plant immunity against viruses. Although most of the known natural resistance genes have long been dominant R genes (encoding NBS-LRR proteins), a vast number of crop recessive resistance genes were cloned in the last decade, emphasizing another evolutive strategy to block viruses. In addition, the discovery of RNA interference pathways highlighted a very efficient antiviral system targeting the infectious agent at the nucleic acid level. Insidiously, plant viruses evolve and often acquire the ability to overcome the resistances employed by breeders. The development of efficient and durable resistances able to withstand the extreme genetic plasticity of viruses therefore represents a major challenge for the coming years. This review aims at describing some of the most devastating diseases caused by viruses on crops and summarizes current knowledge about plant-virus interactions, focusing on resistance mechanisms that prevent or limit viral infection in plants. In addition, I will discuss the current outcomes of the actions employed to control viral diseases in fields and the future investigations that need to be undertaken to develop sustainable broad-spectrum crop resistances against viruses.

259 citations


Cites background from "Plant Immune Responses Against Viru..."

  • ...…of viral avirulence factors by hostencoded NBS-LRR proteins and leads to HR and SAR (described previously in this review), recent hypotheses advance that it may correspond to antiviral ETI mechanisms (Moffett, 2009; Mandadi and Scholthof, 2013; De Ronde et al., 2014; Nakahara and Masuta, 2014)....

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  • ...…these immune receptors induces a downstream signaling cascade including PRR association with positive regulators, phosphorylation events, successive activation of cytoplasmic kinases (including the MAP kinases) and defense-related transcription factors, as well as specific defense genes expression....

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Journal ArticleDOI
30 Apr 2015-Nature
TL;DR: LIMYB links immune receptor LRR-RLK activation to global translation suppression as an antiviral immunity strategy in plants, which results in protein synthesis inhibition, decreased viral messenger RNA association with polysome fractions and enhanced tolerance to begomovirus.
Abstract: Plants and plant pathogens are subject to continuous co-evolutionary pressure for dominance, and the outcomes of these interactions can substantially impact agriculture and food security. In virus-plant interactions, one of the major mechanisms for plant antiviral immunity relies on RNA silencing, which is often suppressed by co-evolving virus suppressors, thus enhancing viral pathogenicity in susceptible hosts. In addition, plants use the nucleotide-binding and leucine-rich repeat (NB-LRR) domain-containing resistance proteins, which recognize viral effectors to activate effector-triggered immunity in a defence mechanism similar to that employed in non-viral infections. Unlike most eukaryotic organisms, plants are not known to activate mechanisms of host global translation suppression to fight viruses. Here we demonstrate in Arabidopsis that the constitutive activation of NIK1, a leucine-rich repeat receptor-like kinase (LRR-RLK) identified as a virulence target of the begomovirus nuclear shuttle protein (NSP), leads to global translation suppression and translocation of the downstream component RPL10 to the nucleus, where it interacts with a newly identified MYB-like protein, L10-INTERACTING MYB DOMAIN-CONTAINING PROTEIN (LIMYB), to downregulate translational machinery genes fully. LIMYB overexpression represses ribosomal protein genes at the transcriptional level, resulting in protein synthesis inhibition, decreased viral messenger RNA association with polysome fractions and enhanced tolerance to begomovirus. By contrast, the loss of LIMYB function releases the repression of translation-related genes and increases susceptibility to virus infection. Therefore, LIMYB links immune receptor LRR-RLK activation to global translation suppression as an antiviral immunity strategy in plants.

175 citations

Journal ArticleDOI
TL;DR: Current knowledge of the mechanisms that link plant N status to the plant's response to pathogen infection and to the virulence and nutritional status of phytopathogens are described.
Abstract: Nitrogen (N) is essential for life and is a major limiting factor of plant growth. Because soils frequently lack sufficient N, large quantities of inorganic N fertilizers are added to soils for crop production. However, nitrate, urea, and ammonium are a major source of global pollution, because much of the N that is not taken up by plants enters streams, groundwater, and lakes, where it affects algal production and causes an imbalance in aquatic food webs. Many agronomical data indicate that the higher use of N fertilizers during the green revolution had an impact on the incidence of crop diseases. In contrast, examples in which a decrease in N fertilization increases disease severity are also reported, indicating that there is a complex relationship linking N uptake and metabolism and the disease infection processes. Thus, although it is clear that N availability affects disease, the underlying mechanisms remain unclear. The aim of this review is to describe current knowledge of the mechanisms that link plant N status to the plant's response to pathogen infection and to the virulence and nutritional status of phytopathogens.

170 citations

References
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Journal ArticleDOI
16 Nov 2006-Nature
TL;DR: A detailed understanding of plant immune function will underpin crop improvement for food, fibre and biofuels production and provide extraordinary insights into molecular recognition, cell biology and evolution across biological kingdoms.
Abstract: 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.

10,539 citations


"Plant Immune Responses Against Viru..." refers background in this paper

  • ...In fact, antiviral immune concepts are generally excluded from plant innate immunity models (Jones and Dangl, 2006; Bent and Mackey, 2007; Boller and Felix, 2009; Hogenhout et al., 2009; Dodds and Rathjen, 2010; Schwessinger and Ronald, 2012; Spoel and Dong, 2012)....

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  • ...Typical bacterial and fungal effector proteins are encoded by these microbes and delivered into the plant cells, wherein they interfere with PTI or other immune regulators (Jones and Dangl, 2006; Bent and Mackey, 2007; Dodds and Rathjen, 2010; Spoel and Dong, 2012)....

    [...]

  • ...…patterns (P/MAMPs) by plant pattern recognition receptors (PRRs) initiates the so called P/MAMP-triggered immune (PTI) response, which may occasionally result in HR (Jones and Dangl, 2006; Bent and Mackey, 2007; Boller and Felix, 2009; Dodds and Rathjen, 2010; Schwessinger and Ronald, 2012)....

    [...]

  • ...The ETI responses, and to a somewhat lesser extent the PTI responses, are closely associated with or even culminate in HR, thus imparting resistance against the invading pathogen (Jones and Dangl, 2006)....

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  • ...…view of plant–pathogen interactions will be predicated on including viruses that are often overlooked in leading plant innate immunity models (Jones and Dangl, 2006; Bent and Mackey, 2007; Boller and Felix, 2009; Hogenhout et al., 2009; Dodds and Rathjen, 2010; Schwessinger and Ronald,…...

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Journal ArticleDOI
TL;DR: This review discusses recent information on functions and mechanisms of the ubiquitin system and focuses on what the authors know, and would like to know, about the mode of action of ubi...
Abstract: The selective degradation of many short-lived proteins in eukaryotic cells is carried out by the ubiquitin system. In this pathway, proteins are targeted for degradation by covalent ligation to ubiquitin, a highly conserved small protein. Ubiquitin-mediated degradation of regulatory proteins plays important roles in the control of numerous processes, including cell-cycle progression, signal transduction, transcriptional regulation, receptor down-regulation, and endocytosis. The ubiquitin system has been implicated in the immune response, development, and programmed cell death. Abnormalities in ubiquitin-mediated processes have been shown to cause pathological conditions, including malignant transformation. In this review we discuss recent information on functions and mechanisms of the ubiquitin system. Since the selectivity of protein degradation is determined mainly at the stage of ligation to ubiquitin, special attention is focused on what we know, and would like to know, about the mode of action of ubiquitin-protein ligation systems and about signals in proteins recognized by these systems.

7,888 citations

Journal ArticleDOI
14 Jun 2001-Nature
TL;DR: The current knowledge of recognition-dependent disease resistance in plants is reviewed, and a few crucial concepts are included to compare and contrast plant innate immunity with that more commonly associated with animals.
Abstract: Plants cannot move to escape environmental challenges. Biotic stresses result from a battery of potential pathogens: fungi, bacteria, nematodes and insects intercept the photosynthate produced by plants, and viruses use replication machinery at the host's expense. Plants, in turn, have evolved sophisticated mechanisms to perceive such attacks, and to translate that perception into an adaptive response. Here, we review the current knowledge of recognition-dependent disease resistance in plants. We include a few crucial concepts to compare and contrast plant innate immunity with that more commonly associated with animals. There are appreciable differences, but also surprising parallels.

3,814 citations


"Plant Immune Responses Against Viru..." refers background in this paper

  • ...In turn, the resistance responses triggered by such interactions (variously described as the guard hypothesis [Dangl and Jones, 2001], the decoy model [van der Hoorn and Kamoun, 2008], or the bait and switch model [Collier and Moffett, 2009]) culminate in HR and SAR responses via the action of…...

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Journal ArticleDOI
TL;DR: Current evidence indicates that MAMPs, DAMPs, and effectors are all perceived as danger signals and induce a stereotypic defense response, and the importance of MAMP/PRR signaling for plant immunity is highlighted.
Abstract: Microbe-associated molecular patterns (MAMPs) are molecular signatures typical of whole classes of microbes, and their recognition plays a key role in innate immunity. Endogenous elicitors are similarly recognized as damage-associated molecular patterns (DAMPs). This review focuses on the diversity of MAMPs/DAMPs and on progress to identify the corresponding pattern recognition receptors (PRRs) in plants. The two best-characterized MAMP/PRR pairs, flagellin/FLS2 and EF-Tu/EFR, are discussed in detail and put into a phylogenetic perspective. Both FLS2 and EFR are leucine-rich repeat receptor kinases (LRR-RKs). Upon treatment with flagellin, FLS2 forms a heteromeric complex with BAK1, an LRR-RK that also acts as coreceptor for the brassinolide receptor BRI1. The importance of MAMP/PRR signaling for plant immunity is highlighted by the finding that plant pathogens use effectors to inhibit PRR complexes or downstream signaling events. Current evidence indicates that MAMPs, DAMPs, and effectors are all perceived as danger signals and induce a stereotypic defense response.

2,801 citations

Journal ArticleDOI
TL;DR: The recent convergence of molecular studies of plant immunity and pathogen infection strategies is revealing an integrated picture of the plant–pathogen interaction from the perspective of both organisms, suggesting novel biotechnological approaches to crop protection.
Abstract: Plants are engaged in a continuous co-evolutionary struggle for dominance with their pathogens. The outcomes of these interactions are of particular importance to human activities, as they can have dramatic effects on agricultural systems. The recent convergence of molecular studies of plant immunity and pathogen infection strategies is revealing an integrated picture of the plant-pathogen interaction from the perspective of both organisms. Plants have an amazing capacity to recognize pathogens through strategies involving both conserved and variable pathogen elicitors, and pathogens manipulate the defence response through secretion of virulence effector molecules. These insights suggest novel biotechnological approaches to crop protection.

2,666 citations


"Plant Immune Responses Against Viru..." refers background in this paper

  • ...In fact, antiviral immune concepts are generally excluded from plant innate immunity models (Jones and Dangl, 2006; Bent and Mackey, 2007; Boller and Felix, 2009; Hogenhout et al., 2009; Dodds and Rathjen, 2010; Schwessinger and Ronald, 2012; Spoel and Dong, 2012)....

    [...]

  • ...…interactions will be predicated on including viruses that are often overlooked in leading plant innate immunity models (Jones and Dangl, 2006; Bent and Mackey, 2007; Boller and Felix, 2009; Hogenhout et al., 2009; Dodds and Rathjen, 2010; Schwessinger and Ronald, 2012; Spoel and Dong, 2012)....

    [...]

  • ...Typical bacterial and fungal effector proteins are encoded by these microbes and delivered into the plant cells, wherein they interfere with PTI or other immune regulators (Jones and Dangl, 2006; Bent and Mackey, 2007; Dodds and Rathjen, 2010; Spoel and Dong, 2012)....

    [...]

  • ...…patterns (P/MAMPs) by plant pattern recognition receptors (PRRs) initiates the so called P/MAMP-triggered immune (PTI) response, which may occasionally result in HR (Jones and Dangl, 2006; Bent and Mackey, 2007; Boller and Felix, 2009; Dodds and Rathjen, 2010; Schwessinger and Ronald, 2012)....

    [...]

  • ...Together, the SGT1/RAR1/HSP90/R protein complex mediates downstream MAP kinase activation and changes in defense gene expression and hormone levels (Dodds and Rathjen, 2010)....

    [...]