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Luedke, D.

Publications and source records attributed to Luedke, D..

7 recordsLinked to original sources

The Pik NLR pair accumulates at the plasma membrane as a hetero-oligomeric sensor-helper immune protein complex prior to activation

Following the perception of pathogen virulence proteins in plants, nucleotide-binding and leucine-rich repeat immune receptors (NLRs) are activated via a wide range of mechanisms. Singleton NLRs can both perceive effectors and trigger an immune response, whereas other NLRs specialise in either pathogen recognition (sensor NLRs) or activation of the immune response (helper NLRs). Sensor and helper NLRs can function as genetically linked pairs or in unlinked receptor networks. Although growing evidence suggests that NLRs conditionally oligomerise upon activation, our understanding of the resting state of NLRs prior to effector perception remains limited. Here, we investigated the oligomeric state of the genetically linked rice (Oryza sativa) sensor Pik-1 and helper Pik-2 NLR pair prior to effector activation when transiently expressed in Nicotiana benthamiana leaves. We show that both wild-type Pikm-1 and engineered Pikm-1Enhancer sensors associate with Pikm-2 and form [~]1 MDa hetero-complexes in the resting state that accumulate at the plasma membrane. Our findings contribute to the growing evidence that pre-activation mechanisms vary widely across NLRs. This knowledge could be leveraged for disease resistance engineering strategies complementary to approaches focussing solely on effector binding. One sentence summaryThe Pik sensor-helper pair of rice immune receptor proteins forms a hetero-oligomer that accumulates at the plasma membrane in its resting state. SynopsisNucleotide-binding and leucine-rich repeat receptors (NLRs) are key players in plant immune systems that recognise and respond to harmful pathogen effector proteins. NLRs can play specialised roles in either detecting effectors (sensor NLRs) or triggering the immune response (helper NLRs) and might function together as pairs or within larger networks. Although many NLRs are known to oligomerise upon the perception of effectors, much less is understood about their resting state prior to pathogen recognition. In this study, we investigated the resting state of a pair of rice NLRs, Pik-1 and Pik-2, transiently expressed in Nicotiana benthamiana leaves. These two proteins formed a sensor/helper complex at the cell membrane even in the absence of the effector protein. This discovery is significant because it reveals a new aspect of how these immune proteins are organised before activation, contributing to our understanding of the diverse ways plants prepare for immune responses. This finding adds to the growing body of evidence that, although many NLR proteins form complexes to respond to pathogens, their resting states and pre-activation mechanisms can vary widely.

plant biology↗

Two genetically linked Arabidopsis TIR-type NLRs are required for immunity and interact with NLRs encoded in a segmentally duplicated genomic region

Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors detect pathogen-secreted effectors inside host cells and induce a robust immune response, typically involving hypersensitive cell death. NLR genes are often genetically linked and can function as pairs or within larger NLR networks. We previously showed that the truncated Toll/Interleukin-1 Receptor (TIR)-type NLR TIR-NB13 (TN13) is required for resistance of Arabidopsis to Pseudomonas syringae pv. tomato (Pst) DC3000 lacking the type-III effector proteins AvrPto and AvrPtoB. TN13 is genetically linked to a full length TIR-NB-LRR (TNL) gene on chromosome 3. Here, we show that TN13, and its genetically linked TNL both localize to the ER membrane via N-terminal transmembrane domains, are required for resistance to Pst DC3000 ({Delta}AvrPto/AvrPtoB) and interact with each other in transient expression assays in Nicotiana benthamiana. In contrast to TN13, the full length TNL, which we named TN13-INTERACTING TNL1 (TNT1), induces an autoactive cell death response when expressed in N. benthamiana that depends on an atypical MHV motif in its NB-ARC domain, as well as the EDS1/SAG101/NRG1 module. TN13 and TNT1 furthermore interact with phylogenetically related NLRs encoded by a segmentally duplicated region on chromosome 5. Our data suggest that both TN13 and the genetically linked TNT1 could be part of a larger TIR-type NLR immune regulatory network, in which TNT1 contributes to basal immunity and might function as an autoactive death switch to induce cell death upon pathogen detection. SIGNIFICANCE STATEMENTThe ER membrane localized truncated TIR-NLR TN13 and the genomically linked full length TNL TNT1 are required for plant disease resistance and form heteromeric associations with phylogenetically related NLRs, encoded by a segmentally duplicated chromosomal region.

plant biology↗

The autoactivity of tomato helper NLR immune proteins of the NRC clade is unaltered in prf mutants of Nicotiana benthamiana

Nucleotide-binding domain and leucine-rich repeat immune receptors (NLRs) can function in networks of sensors and helpers to induce hypersensitive cell death and immunity against pathogens. The tomato sensor NLR Prf guards the Pto kinase from AvrPto and AvrPtoB effector perturbation and activates the downstream helpers NRC2 and NRC3. Prf is conserved across the Solanaceae and its ortholog in the model species Nicotiana benthamiana is also required for detection of AvrPto/AvrPtoB function on Pto. A recent study reported that cell death induction after transient expression of an autoactive mutant of tomato NRC3 is abolished upon RNAi silencing of Prf in N. benthamiana. Here we generated loss-of-function prf mutants in N. benthamiana and demonstrate that autoactive mutants of eight canonical tomato NRCs (NRC0, NRC1, NRC2, NRC3, NRC4a, NRC4b, NRC6, and NRC7) still induce hypersensitive cell death when expressed transiently in the prf mutant background. Autoactive tomato NRCs also triggered cell death when expressed in lettuce (Lactuca sativa), an Asteraceae plant that does not have a Prf ortholog. These results confirm a unidirectional dependency of sensors and helpers in the NRC network and underscore the value of the N. benthamiana and lettuce model systems for studying functional relationships between paired and networked NLRs.

plant biology↗

Speedy benthi: Elongated photoperiods reduce the generation time of the model plant species Nicotiana benthamiana

Nicotiana benthamiana is increasingly gaining prominence as a model plant species with recently published high-quality genome assemblies, which will further enable forward and reverse genetic approaches (Bally et al., 2018; Derevnina et al., 2019; Kourelis et al., 2019; Ranawaka et al., 2023; Vollheyde et al., 2023). However, the generation time of N. benthamiana poses a bottleneck in the creation of mutant and transgenic plant lines. Speed breeding (SB), by extended photoperiods and adjustments to growth parameters, is an efficient way to reduce generation times for many crop and model plant species (Ghosh et al., 2018; Watson et al., 2018; Hickey et al., 2019; Varshney et al., 2021). We hypothesized that an extended photoperiod could reduce the seed to seed generation time of N. benthamiana. We tested this hypothesis by comparing generation times under SB conditions to traditionally used photoperiods in growth chambers and green house settings. We found that a 22h photoperiod reduced the generation time of N. benthamiana by approximately 2 weeks (16-22%). Fertilization in combination with a far-red light spectrum did not yield a further reduction in generation time when combined with SB conditions. Our findings further contribute to the establishment of N. benthamiana as an important model organism for plant research.

plant biology↗

A root-specific NLR network confers resistance to plant parasitic nematodes

Nucleotide-binding domain and leucine-rich repeat immune receptors (NLRs) confer disease resistance to a multitude of foliar and root parasites of plants. However, the extent to which NLR immunity is expressed differentially between plant organs is poorly known. Here, we show that a large cluster of tomato genes, which encodes the cyst and root-knot nematode disease resistance proteins Hero and MeR1 as well as the NLR-helper NRC6, exhibits nearly exclusive expression in the roots. This root-specific gene cluster emerged in Solanum species about 21 million years ago through gene duplication from the ancient NRC network of asterid plants. NLR-sensors in this gene cluster exclusively signal through NRC6 helpers to trigger the hypersensitive cell death immune response. These findings indicate that the NRC6 gene cluster has sub-functionalized from the larger NRC network to specialize for resistance against root pathogens, including cyst and root-knot nematodes. We propose that NLR gene clusters and networks have evolved organ-specific gene expression as an adaptation to particular parasites and to reduce the risk of autoimmunity.

plant biology↗

The cell-wall-localised BETA-XYLOSIDASE 4 contributes to immunity of Arabidopsis against Botrytis cinerea

Plant cell walls constitute physical barriers that restrict access of microbial pathogens to the contents of plant cells. The primary cell wall of multicellular plants predominantly consists of cellulose, hemicellulose and pectin. In Arabidopsis, a cell wall-localised protein, BETA-XYLOSIDASE 4 (BXL4) that belongs to a seven-member BETA-XYLOSIDASE (BXL) gene family was induced upon infection with the necrotrophic fungal pathogen Botrytis cinerea and mechanical wounding in a jasmonoyl isoleucine (JA-Ile) dependent manner. Ectopic expression of the BXL4 gene in Arabidopsis seed coat epidermal cells was able to rescue a bxl1 mutant phenotype suggesting that like BXL1, BXL4, had both xylosidase and arabinosidase activity and acts in mura on cell wall polysaccharides. bxl4 mutants show a compromised resistance to B. cinerea. Upon infection, bxl4 mutants accumulated reduced levels of JA-Ile and camalexin. Conditional overexpression of BXL4 resulted in enhanced expression of PDF1.2 and PAD3 transcripts both before and after B. cinerea infection. This was associated with reduced susceptibility of the transgenic lines to B. cinerea. These data suggest that remodelling or degradation of one or more cell wall polysaccharides is important for plant immunity against B. cinerea and plays a role in pathogen-induced JA-Ile and camalexin accumulation. One-sentence summaryBXL4 is a putative bifunctional xylosidase/arabinofuranisodase localising to the apoplast, important for immunity against the necrotrphic pathogen B. cinerea.

plant biology↗

From isochorismate to salicylate: a new reaction mechanism for salicylic acid biosynthesis

The phytohormone salicylic acid (SA) is a central regulator of plant immunity. Despite such functional importance, our knowledge of its biosynthesis is incomplete. Previous work showed that SA is synthesized from chorismic acid in plastids. The bulk of pathogen-induced SA derives from isochorismate generated by the catalytic activity of ISOCHORISMATE SYNTHASE1 (ICS1). How and in which cellular compartment isochorismate is converted to SA is unknown. Here we show that the pathway downstream of isochorismate requires only two additional proteins: the plastidial isochorismate exporter ENHANCED DISEASE SUSCEPTIBILITY5 (EDS5) and the cytosolic amido-transferase AvrPphB SUSCEPTIBLE3 (PBS3). PBS3 catalyzes the conjugation of glutamate to isochorismate. The reaction product isochorismate-9-glutamate spontaneously decomposes into enolpyruvyl-N-glutamate and SA. This previously unknown reaction mechanism appears to be conserved throughout the plant kingdom.\n\nOne Sentence SummarySalicylic acid is synthesized via isochorismate-9-glutamate by PBS3.

plant biology↗