Contrasting Mechanisms of Defense Against Biotrophic and Necrotrophic Pathogens
TL;DR: This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens.
Abstract: It has been suggested that effective defense against biotrophic pathogens is largely due to programmed cell death in the host, and to associated activation of defense responses regulated by the salicylic acid-dependent pathway. In contrast, necrotrophic pathogens benefit from host cell death, so they are not limited by cell death and salicylic acid-dependent defenses, but rather by a different set of defense responses activated by jasmonic acid and ethylene signaling. This review summarizes results from Arabidopsis-pathogen systems regarding the contributions of various defense responses to resistance to several biotrophic and necrotrophic pathogens. While the model above seems generally correct, there are exceptions and additional complexities.
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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
TL;DR: Evidence is emerging that beneficial root-inhabiting microbes also hijack the hormone-regulated immune signaling network to establish a prolonged mutualistic association, highlighting the central role of plant hormones in the regulation of plant growth and survival.
Abstract: Plant hormones have pivotal roles in the regulation of plant growth, development, and reproduction. Additionally, they emerged as cellular signal molecules with key functions in the regulation of immune responses to microbial pathogens, insect herbivores, and beneficial microbes. Their signaling pathways are interconnected in a complex network, which provides plants with an enormous regulatory potential to rapidly adapt to their biotic environment and to utilize their limited resources for growth and survival in a cost-efficient manner. Plants activate their immune system to counteract attack by pathogens or herbivorous insects. Intriguingly, successful plant enemies evolved ingenious mechanisms to rewire the plant’s hormone signaling circuitry to suppress or evade host immunity. Evidence is emerging that beneficial root-inhabiting microbes also hijack the hormone-regulated immune signaling network to establish a prolonged mutualistic association, highlighting the central role of plant hormones in the regulation of plant growth and survival.
2,132 citations
Cites background from "Contrasting Mechanisms of Defense A..."
...…molecule of microbe or insect that binds to a host protein, commonly to suppress host immunity PGPR: plant-growthpromoting rhizobacteria Innate Immunity to Plant Pathogens According to their lifestyles, plant pathogens are generally divided into necrotrophs and biotrophs (Glazebrook 2005)....
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...The SA response pathway is typically (but not exclusively) effective against microbial biotrophic pathogens (Glazebrook 2005)....
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TL;DR: Recent advances made in understanding the role of salicylic acid, jasmonates and ethylene in modulating plant defence responses against various diseases and pests are reviewed.
Abstract: Plant hormones play important roles in regulating developmental processes and signaling networks involved in plant responses to a wide range of biotic and abiotic stresses. Significant progress has been made in identifying the key components and understanding the role of salicylic acid (SA), jasmonates (JA) and ethylene (ET) in plant responses to biotic stresses. Recent studies indicate that other hormones such as abscisic acid (ABA), auxin, gibberellic acid (GA), cytokinin (CK), brassinosteroids (BR) and peptide hormones are also implicated in plant defence signaling pathways but their role in plant defence is less well studied. Here, we review recent advances made in understanding the role of these hormones in modulating plant defence responses against various diseases and pests.
2,072 citations
TL;DR: Genetic studies reveal an increasingly complex network of proteins required for SA-mediated defense signaling, and this process is amplified by several regulatory feedback loops.
Abstract: For more than 200 years, the plant hormone salicylic acid (SA) has been studied for its medicinal use in humans. However, its extensive signaling role in plants, particularly in defense against pathogens, has only become evident during the past 20 years. This review surveys how SA in plants regulates both local disease resistance mechanisms, including host cell death and defense gene expression, and systemic acquired resistance (SAR). Genetic studies reveal an increasingly complex network of proteins required for SA-mediated defense signaling, and this process is amplified by several regulatory feedback loops. The interaction between the SA signaling pathway and those regulated by other plant hormones and/or defense signals is also discussed.
2,030 citations
Cites background from "Contrasting Mechanisms of Defense A..."
...SA and JA control resistance against pathogens with different infection strategies; SA signaling predominantly combats biotrophic pathogens and viruses, whereas JA signaling protects against necrotrophic pathogens and insects (61)....
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TL;DR: 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.
Abstract: 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.
2,027 citations
Cites background from "Contrasting Mechanisms of Defense A..."
...Jasmonates are also involved in the regulation of tritrophic interactions (28, 128, 136), host plant resistance to phloem-feeding insects (27, 32, 87, 145), trichome-based defenses (15, 77), priming of direct and indirect defenses (28, 132), pathogen resistance (36), and systemic transmission of defense signals (109)....
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References
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TL;DR: A model describing the sequence of events leading from initial infection to the induction of defense genes is presented and exciting new data suggest that the mobile signal for SAR might be a lipid molecule.
Abstract: Systemic acquired resistance (SAR) is a mechanism of induced defense that confers long-lasting protection against a broad spectrum of microorganisms. SAR requires the signal molecule salicylic acid (SA) and is associated with accumulation of pathogenesis-related proteins, which are thought to contribute to resistance. Much progress has been made recently in elucidating the mechanism of SAR. Using the model plant Arabidopsis, it was discovered that the isochorismate pathway is the major source of SA during SAR. In response to SA, the positive regulator protein NPR1 moves to the nucleus where it interacts with TGA transcription factors to induce defense gene expression, thus activating SAR. Exciting new data suggest that the mobile signal for SAR might be a lipid molecule. We discuss the molecular and genetic data that have contributed to our understanding of SAR and present a model describing the sequence of events leading from initial infection to the induction of defense genes.
2,744 citations
TL;DR: An Arabidopsis thaliana leaf cell system based on the induction of early-defence gene transcription by flagellin, a highly conserved component of bacterial flagella that functions as a PAMP in plants and mammals is developed, suggesting that signalling events initiated by diverse pathogens converge into a conserved MAPK cascade.
Abstract: There is remarkable conservation in the recognition of pathogen-associated molecular patterns (PAMPs) by innate immune responses of plants, insects and mammals. We developed an Arabidopsis thaliana leaf cell system based on the induction of early-defence gene transcription by flagellin, a highly conserved component of bacterial flagella that functions as a PAMP in plants and mammals. Here we identify a complete plant MAP kinase cascade (MEKK1, MKK4/MKK5 and MPK3/MPK6) and WRKY22/WRKY29 transcription factors that function downstream of the flagellin receptor FLS2, a leucine-rich-repeat (LRR) receptor kinase. Activation of this MAPK cascade confers resistance to both bacterial and fungal pathogens, suggesting that signalling events initiated by diverse pathogens converge into a conserved MAPK cascade.
2,480 citations
"Contrasting Mechanisms of Defense A..." refers background in this paper
...Recognition of flagellin activates a MAP kinase cascade that culminates in expression of the transcription factors WRKY22 and WRKY29 (6)....
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TL;DR: By cloning and characterizing an Arabidopsis defence-related gene (SID2) defined by mutation, it is shown that SA is synthesized from chorismate by means of ICS, and that SA made by this pathway is required for LAR and SAR responses.
Abstract: Salicylic acid (SA) mediates plant defences against pathogens, accumulating in both infected and distal leaves in response to pathogen attack. Pathogenesis-related gene expression and the synthesis of defensive compounds associated with both local and systemic acquired resistance (LAR and SAR) in plants require SA. In Arabidopsis, exogenous application of SA suffices to establish SAR, resulting in enhanced resistance to a variety of pathogens. However, despite its importance in plant defence against pathogens, SA biosynthesis is not well defined. Previous work has suggested that plants synthesize SA from phenylalanine; however, SA could still be produced when this pathway was inhibited, and the specific activity of radiolabelled SA in feeding experiments was often lower than expected. Some bacteria such as Pseudomonas aeruginosa synthesize SA using isochorismate synthase (ICS) and pyruvate lyase. Here we show, by cloning and characterizing an Arabidopsis defence-related gene (SID2) defined by mutation, that SA is synthesized from chorismate by means of ICS, and that SA made by this pathway is required for LAR and SAR responses.
2,089 citations
"Contrasting Mechanisms of Defense A..." refers background in this paper
...However, it is possible that there is some synthesis through PAL, and that this is important for limiting the local spread of B. cinerea (43)....
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...SID2 encodes isochorismate synthase, and SA production is drastically reduced in sid2 plants, indicating that the majority of SA in Arabidopsis is produced from isochorismate rather than from the phenylalanine pathway described previously (22, 72, 82, 95, 122, 127)....
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...However, inhibitors that block phenylalanine ammonia lyase (PAL) activity do result in enhanced susceptibility (43, 53)....
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...However, there is some SA present in sid2 mutants, and this may well be synthesized through the phenylalanine pathway (122)....
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...Most of the SA produced in Arabidopsis is made through a pathway that requires isochorismate synthase, the product of SID2, and is thought not to require PAL (122)....
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TL;DR: Salicylic acid is essential for the development of systemic acquired resistance in tobacco and was investigated in transgenic tobacco plants harboring a bacterial gene encoding salicylate hydroxylase.
Abstract: It has been proposed that salicylic acid acts as an endogenous signal responsible for inducing systemic acquired resistance in plants. The contribution of salicylic acid to systemic acquired resistance was investigated in transgenic tobacco plants harboring a bacterial gene encoding salicylate hydroxylase, which converts salicylic acid to catechol. Transgenic plants that express salicylate hydroxylase accumulated little or no salicylic acid and were defective in their ability to induce acquired resistance against tobacco mosaic virus. Thus, salicylic acid is essential for the development of systemic acquired resistance in tobacco.
1,731 citations
"Contrasting Mechanisms of Defense A..." refers background in this paper
...Transgenic plants expressing NahG were important for providing the first demonstrations that SA is required for expression of defense effector genes such as PR-1, and for the phenomenon of systemic acquired resistance (SAR; discussed below) (27, 46)....
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TL;DR: Transgenic tobacco and Arabidopsis thaliana expressing the bacterial enzyme salicylate hydroxylase cannot accumulate salicylic acid, which makes the plants unable to induce systemic acquired resistance, but also leads to increased susceptibility to viral, fungal, and bacterial pathogens.
Abstract: Transgenic tobacco and Arabidopsis thaliana expressing the bacterial enzyme salicylate hydroxylase cannot accumulate salicylic acid (SA). This defect not only makes the plants unable to induce systemic acquired resistance, but also leads to increased susceptibility to viral, fungal, and bacterial pathogens. The enhanced susceptibility extends even to host-pathogen combinations that would normally result in genetic resistance. Therefore, SA accumulation is essential for expression of multiple modes of plant disease resistance.
1,662 citations
"Contrasting Mechanisms of Defense A..." refers background in this paper
...Transgenic plants expressing NahG were important for providing the first demonstrations that SA is required for expression of defense effector genes such as PR-1, and for the phenomenon of systemic acquired resistance (SAR; discussed below) (27, 46)....
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