Random mutagenesis of the nucleotide‐binding domain of <scp>NRC</scp>1 (<scp>NB</scp>‐<scp>LRR</scp> Required for Hypersensitive Response‐Associated Cell Death‐1), a downstream signalling nucleotide‐binding, leucine‐rich repeat (<scp>NB</scp>‐<scp>LRR</scp>) protein, identifies gain‐of‐function mutations in the nucleotide‐binding pocket

Sueldo, D.J.; Shimels, Mahdere; Spiridon, Laurentiu N.; Caldararu, Octav; Petrescu, Andrei‐Jose; Joosten, M.H.A.J.; Tameling, W.I.L.

doi:10.1111/nph.13459

Cited by 41 publications

(40 citation statements)

References 92 publications

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“…Mutation of this conserved lysine residue results in the abolition of function in numerous plant NLRs Downstream of the P-loop motif is the 'RNBS-B/sensor 1 motif', thought to be involved in the differentiation of bound nucleotides, with a proposed role in interacting with the c-phosphate of ATP bound to the NB domain (Ogura and Wilkinson, 2001;Takken et al, 2006). Both gain-of-function and loss-offunction mutations have been described for this motif, dependent on the nature of the substitution (Salmeron et al, 1996;Dinesh-Kumar et al, 2000;Tornero et al, 2002;Sueldo et al, 2015). It has been proposed, based on structural modelling of the NB-ARC domain of the tomato NLR NRC1 (using the structure of CED-4 as the template), that the arginine in the RNBS-B motif interacts with c-phosphate of the ATP molecule (Sueldo et al, 2015).…”

Section: Progress Towards a Mechanistic Understanding Of Plant Nlr Fumentioning

confidence: 99%

“…Both gain-of-function and loss-offunction mutations have been described for this motif, dependent on the nature of the substitution (Salmeron et al, 1996;Dinesh-Kumar et al, 2000;Tornero et al, 2002;Sueldo et al, 2015). It has been proposed, based on structural modelling of the NB-ARC domain of the tomato NLR NRC1 (using the structure of CED-4 as the template), that the arginine in the RNBS-B motif interacts with c-phosphate of the ATP molecule (Sueldo et al, 2015).…”

Section: Progress Towards a Mechanistic Understanding Of Plant Nlr Fumentioning

confidence: 99%

“…Structural modelling of plant NB-ARC domains based on the crystal structures of Apaf-1 and CED-4 indicate that GLPL residues are involved in stabilizing the adenosine and ribose backbone of the nucleotide through van der Waals interactions (McHale et al, 2006;Sueldo et al, 2015). Various gain-of-function and loss-of-function mutants have been described in this motif as well, further suggesting that structural changes caused by nucleotide exchange are crucial for NLR auto-inhibition and activation (Dodds et al, 2001;Bendahmane et al, 2002;Sueldo et al, 2015).…”

Section: Progress Towards a Mechanistic Understanding Of Plant Nlr Fumentioning

confidence: 99%

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Animal NLRs provide structural insights into plant NLR function

Bentham

Burdett

Anderson

et al. 2016

Ann Bot

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Background The plant immune system employs intracellular NLRs (nucleotide binding [NB], leucine-rich repeat [LRR]/nucleotide-binding oligomerization domain [NOD]-like receptors) to detect effector proteins secreted into the plant cell by potential pathogens. Activated plant NLRs trigger a range of immune responses, collectively known as the hypersensitive response (HR), which culminates in death of the infected cell. Plant NLRs show structural and functional resemblance to animal NLRs involved in inflammatory and innate immune responses. Therefore, knowledge of the activation and regulation of animal NLRs can help us understand the mechanism of action of plant NLRs, and vice versa.Scope This review provides an overview of the innate immune pathways in plants and animals, focusing on the available structural and biochemical information available for both plant and animal NLRs. We highlight the gap in knowledge between the animal and plant systems, in particular the lack of structural information for plant NLRs, with crystal structures only available for the N-terminal domains of plant NLRs and an integrated decoy domain, in contrast to the more complete structures available for animal NLRs. We assess the similarities and differences between plant and animal NLRs, and use the structural information on the animal NLR pair NAIP/NLRC4 to derive a plausible model for plant NLR activation.Conclusions Signalling by cooperative assembly formation (SCAF) appears to operate in most innate immunity pathways, including plant and animal NLRs. Our proposed model of plant NLR activation includes three key steps: (1) initially, the NLR exists in an inactive auto-inhibited state; (2) a combination of binding by activating elicitor and ATP leads to a structural rearrangement of the NLR; and (3) signalling occurs through cooperative assembly of the resistosome. Further studies, structural and biochemical in particular, will be required to provide additional evidence for the different features of this model and shed light on the many existing variations, e.g. helper NLRs and NLRs containing integrated decoys.

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Section: Progress Towards a Mechanistic Understanding Of Plant Nlr Fumentioning

confidence: 99%

Section: Progress Towards a Mechanistic Understanding Of Plant Nlr Fumentioning

confidence: 99%

Section: Progress Towards a Mechanistic Understanding Of Plant Nlr Fumentioning

confidence: 99%

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Animal NLRs provide structural insights into plant NLR function

Bentham

Burdett

Anderson

et al. 2016

Ann Bot

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“…One cytoplasmic candidate is a downstream NLR, NRC1 (NB-LRR Required for Hypersensitive-Response-Associated Cell Death1). NRC1 has been shown to be required for autoactive Mi-1.2 cell death in N. benthamiana (Gabriëls et al, 2007;Sueldo et al, 2015). N. benthamiana encodes at least four NRC1-like proteins, and silencing specific NRC-like proteins did not compromise the HR-inducing activity of an autoactive Mi-1.2 variant, suggesting that there might be functional redundancy among these NRC-like genes (Wu et al, 2016).…”

Section: Discussionmentioning

confidence: 99%

The Conformation of a Plasma Membrane-Localized Somatic Embryogenesis Receptor Kinase Complex Is Altered by a Potato Aphid-Derived Effector

et al. 2016

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Somatic embryogenesis receptor kinases (SERKs) are transmembrane receptors involved in plant immunity. Tomato (Solanum lycopersicum) carries three SERK members. One of these, SlSERK1, is required for Mi-1.2-mediated resistance to potato aphids (Macrosiphum euphorbiae). Mi-1.2 encodes a coiled-coil nucleotide-binding leucine-rich repeat protein that in addition to potato aphids confers resistance to two additional phloem-feeding insects and to root-knot nematodes (Meloidogyne spp.). How SlSERK1 participates in Mi-1.2-mediated resistance is unknown, and no Mi-1.2 cognate pest effectors have been identified. Here, we study the mechanistic involvement of SlSERK1 in Mi-1.2-mediated resistance. We show that potato aphid saliva and protein extracts induce the Mi-1.2 defense marker gene SlWRKY72b, indicating that both saliva and extracts contain a Mi-1.2 recognized effector. Resistant tomato cultivar Motelle (Mi-1.2/Mi-1.2) plants overexpressing SlSERK1 were found to display enhanced resistance to potato aphids. Confocal microscopy revealed that Mi-1.2 localizes at three distinct subcellular compartments: the plasma membrane, cytoplasm, and nucleus. Coimmunoprecipitation experiments in these tomato plants and in Nicotiana benthamiana transiently expressing Mi-1.2 and SlSERK1 showed that Mi-1.2 and SlSERK1 colocalize only in a microsomal complex. Interestingly, bimolecular fluorescence complementation analysis showed that the interaction of Mi-1.2 and SlSERK1 at the plasma membrane distinctively changes in the presence of potato aphid saliva, suggesting a model in which a constitutive complex at the plasma membrane participates in defense signaling upon effector binding.

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“…An interesting nucleotide-binding site (NBS)-LRR protein required for HR signaling mediated by both extra-and intracellular resistance proteins was picked up in this system by PhD student Suzan Gabriëls and was studied in more detail by PhD student Daniela Sueldo (39,85).…”

Section: Avr-triggered Cf-mediated Downstream Defense Signalingmentioning

confidence: 99%

Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato

Wit

2016

Annu. Rev. Phytopathol.

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In this review, I recount my personal history. My drive to study hostpathogen interactions was to find alternatives for agrochemicals, which was triggered after reading the book "Silent Spring" by Rachel Carson. I reflect on my research at the Laboratory of Phytopathology at Wageningen University, where I have worked for my entire career on the interaction between Cladosporium fulvum and tomato, and related gene-for-gene pathosystems. I describe different methods used to identify and sequence avirulence (Avr) genes from the pathogen and resistance (R) genes from the host. The major genes involved in classical gene-for-gene interactions have now been identified, and breeders can produce plants with multiple R genes providing durable and environmentally safe protection against pathogens. In some cases, this might require the use of genetically modified plants when R genes cannot be introduced by classical breeding. MY MOTIVATION TO STUDY PLANT PATHOLOGYI grew up after World War II on a farm in Limburg, the most southern province of The Netherlands. In those days farming was very labor-intensive and still very much dependent on horsepower. I loved to work with horses, but soon they were replaced by tractors. In Limburg, farms were relatively small and not specialized. Apart from growing crops like cereals, sugar beets, and potatoes, most farmers also kept dairy cattle, pigs, and chickens. My eldest brother was going to succeed my father, and I knew that my future would not be in farming. After primary school, I went to high school, where although I spent my time mainly studying languages (Dutch, English, French, German, Greek, and Latin), I was more interested in chemistry and biology. I was fascinated by crop plants that could grow out of tiny seeds into adult plants within one season, and by majestic trees like the chestnut tree that overlooked our farm for more than hundred years. If that chestnut tree could talk, it would have told me how it survived shell bursts during World War II while the farm was completely destroyed. I had a small garden of my own where I experimented with seeds of pea and bean, digging them up from the soil a few days after I had sowed them, curious to find out how far they had developed. My father and my biology teacher at high school stimulated my interest in plant biology. After high school, I went to Wageningen University, where I followed a broad BS program in (bio)chemistry and biology. I did my MS in crop protection, which included three research projects of six months at the Laboratories of Biochemistry, Plant Physiology, and Phytopathology. Apart from these research projects, the MS program included practical training abroad, for which I spent three months at Imperial Chemical Industries (ICI) in Bracknell, UK, working on a bioassay to test the effectiveness of fungicides against powdery mildew of wheat. In those days, protection of crops against fungal pathogens was mainly achieved by applying fungicides. After having read the book "Silent Spring" by Rachel Carson (8),...

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Cited by 41 publications

References 92 publications

Animal NLRs provide structural insights into plant NLR function

Animal NLRs provide structural insights into plant NLR function

The Conformation of a Plasma Membrane-Localized Somatic Embryogenesis Receptor Kinase Complex Is Altered by a Potato Aphid-Derived Effector

Cladosporium fulvum Effectors: Weapons in the Arms Race with Tomato

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