Resistance protein Pit interacts with the GEF OsSPK1 to activate OsRac1 and trigger rice immunity

Wang, Qiong; Li, Yuying; Ishikawa, Kazuya; Kosami, Ken ichi; Uno, Kazumi; Nagawa, Shingo; Li, Tan; Du, Jiamu; Shimamoto, Ko; Kawano, Yoji

doi:10.1073/pnas.1813058115

Cited by 44 publications

(60 citation statements)

References 61 publications

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“…Next, we wondered whether PID3 recruits other component(s) in the signalling pathway. The CC domains of some NLR proteins are key for interactions with downstream signalling components (Shen et al ., ; Inoue et al ., ; Wang et al ., ); indeed, our experiments indicated that the CC domain‐deleted PID3 failed to convey blast resistance (data not shown). We therefore performed yeast two‐hybrid screening with PID3‐CC as bait.…”

Section: Resultsmentioning

confidence: 66%

“…We therefore used OsRac1 RNAi kd plants rather than knockout plants. Similarly, an investigation of the function of OsSPK1 in OsRac1 activation (Wang et al ., ) used OsRac1 kd lines. We surmise that, in addition to its role in regulating immunity, OsRac1 is essential for rice growth and development and, therefore, that OsRac1 knockout mutants are lethal.…”

Section: Discussionmentioning

confidence: 99%

“…Lipid modification of Pit helps localize it to areas of the PM where OsRac1 activation occurs (Kawano et al ., 2014a). Furthermore, OsSPK1, a DOCK family guanine nucleotide exchange factor (GEF) protein, is attracted by Pit to the PM, where it converts OsRac1 from its inactive (guanosine diphosphate bound) to its active (guanosine triphosphate bound) form (Wang et al ., ). These studies provide direct evidence that OsRac1 is an important signalling molecule downstream of Pit.…”

Section: Introductionmentioning

confidence: 97%

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Importance of OsRac1 and RAI1 in signalling of nucleotide‐binding site leucine‐rich repeat protein‐mediated resistance to rice blast disease

et al. 2019

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Summary Plants depend on Resistance (R) genes, most of which encode nucleotide‐binding site leucine‐rich repeat (NLR) proteins, for pathogen race‐specific disease resistance. However, only a few immediate downstream targets of R proteins have been characterized, and the signalling pathways for R‐protein‐induced immunity are largely unknown. In rice (Oryza sativa), NLR proteins serve as important immune receptors in the response to rice blast disease caused by the fungus Magnaporthe oryzae. We used site‐directed mutagenesis to create an autoactive form of the NLR protein PID3 that confers blast resistance and used transgenic rice to test the resulting immunity and gene expression changes. We identified OsRac1, a known GTPase, as a signalling molecule in PID3‐mediated blast resistance, implicating OsRac1 as a possible common factor downstream of rice NLR proteins. We also identified RAI1, a transcriptional activator, as a PID3 interactor required for PID3‐mediated blast resistance and showed that RAI1 expression is induced by PID3 via a process mediated by OsRac1. This study describes a new signalling pathway for NLR protein‐mediated blast resistance and shows that OsRac1 and RAI1 act together to play a critical role in this process.

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Section: Resultsmentioning

confidence: 66%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 97%

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Importance of OsRac1 and RAI1 in signalling of nucleotide‐binding site leucine‐rich repeat protein‐mediated resistance to rice blast disease

et al. 2019

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“…In plants, the presence of cofilins has been reported in various species (Hussey et al, 2002), while PP2A-2, an isoform of PP2A, is known to directly regulate ADF/cofilin (and, therefore, F-actin rearrangements) in Arabidopsis thaliana (Wen et al, 2012). In addition, OsRac1 (a rice homolog of Rac1), along with its activator GEF protein OsSPK1, have been recently suggested to be regulators of actin dynamics in rice (Wang et al, 2018).…”

Section: Discussionmentioning

confidence: 99%

The effects of microcystin-LR inOryza sativaroot cells: F-actin as a new target of cyanobacterial toxicity

Pappas

Gkelis

Panteris

2020

Preprint

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ABSTRACTMicrocystins are toxins produced by cyanobacteria, notorious for negatively affecting a wide range of living organisms, among which several plant species. Although microtubules are a well-established target of microcystin toxicity, its effect on filamentous actin (F-actin) in plant cells has not been studied yet.The effects of microcystin-LR (MC-LR) and the extract of a microcystin-producing freshwater cyanobacterial strain (Microcystis flos-aquae TAU-MAC 1510) on the cytoskeleton (F-actin and microtubules) of Oryza sativa (rice) root cells, were studied by light, confocal, and transmission electron microscopy. Considering the role of F-actin in endomembrane system distribution, the endoplasmic reticulum and the Golgi apparatus in extract-treated cells were also examined.F-actin in both MC-LR- and extract-treated meristematic and differentiating root cells exhibited time-dependent alterations, ranging from disorientation and bundling to the formation of ring-like structures, eventually resulting to a collapse of the F-actin network at longer treatments. Disorganization and eventual depolymerization of microtubules, as well as abnormal chromatin condensation were observed following treatment with the extract, effects which could be attributed to microcystins and other bioactive compounds. Moreover, cell cycle progression was inhibited in extract-treated roots, specifically affecting the mitotic events. As a consequence of F-actin network disorganization, endoplasmic reticulum elements appeared stacked and diminished, while Golgi dictyosomes appeared aggregated.These results support that F-actin is a prominent target of MC-LR, both in pure form and as an extract ingredient. Endomembrane system alterations can also be attributed to the effects of cyanobacterial bioactive compounds (including microcystins) on F-actin cytoskeleton.

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“…A recent study suggested that the LRR domain of ZAR1 plays an important role in interaction with the decoy RKS1, while also helping to maintain ZAR1 in an autoinhibition state through intramolecular interactions (Wang et al , 2019a). Both the CC and TIR domains have been shown to function as signalling components in plant NLRs (Swiderski et al , 2009; Bernoux et al , 2011; Baudin et al , 2017; Wang et al , 2018; Zhai et al , 2019). Indeed, the CC or TIR domains of numerous NLR proteins can trigger cell death when transiently expressed in Nicotiana benthamiana (Bernoux et al , 2011; Bai et al , 2012; Wang et al , 2015; Cesari et al , 2016; Hamel et al , 2016; Baudin et al , 2017; Kim et al , 2018).…”

Section: Introductionmentioning

confidence: 99%

Pm21 CC domain activity modulated by intramolecular interactions is implicated in cell death and disease resistance

Gao

Gong

et al. 2020

Molecular Plant Pathology

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Molecular Plant Pathology. 2020;21:975-984. | 975 wileyonlinelibrary.com/journal/mpp | INTRODUC TI ONPlants prevent pathogen invasion via a two-layered immune system (Dodds and Rathjen, 2010;Dangl et al., 2013). The first layer is pattern-triggered immunity (PTI) governed by membrane-localized pattern recognition receptors (PRRs). PTI is the basal immune response of plants against infections by pathogens (Couto and Zipfel, 2016;Tang et al., 2017). Once pathogens suppress PTI and enter host cells, plants employ the second layer of the immune system to combat pathogens.In this branch of the immune system, intracellular nucleotide-binding Abstract Nucleotide-binding (NB) leucine-rich repeat (LRR) receptors (NLRs) provide resistance against several plant pathogens. We previously cloned the wheat powdery mildew resistance gene Pm21, which encodes a coiled-coil (CC) NLR that confers broad-spectrum resistance against Blumeria graminis f. sp. tritici. Here, we report comprehensive biochemical and functional analyses of Pm21 CC domain in Nicotiana benthamiana. Transient overexpression assay suggested that only the extended CC (eCC, amino acid residues 1-159) domain has cell-death-inducing activity, whereas the CC-containing truncations, including CC-NB and CC-NB-LRR, do not induce celldeath responses. Coimmunoprecipitation (Co-IP) assay showed that the eCC domain self-associates and interacts with the NB and LRR domains in planta. These results imply that the activity of the eCC domain is inhibited by the intramolecular interactions of different domains in the absence of pathogens. We found that the LRR domain plays a crucial role in D491V-mediated full-length (FL) Pm21 autoactivation. Some mutations in the CC domain leading to the loss of Pm21 resistance to powdery mildew impaired the CC activity of cell-death induction. Two mutations (R73Q and E80K) interfered with D491V-mediated Pm21 autoactivation without affecting the cell-death-inducing activity of the eCC domain. Notably, some susceptible mutants harbouring mutations in the CC domain still exhibited cell-death-inducing activity. Taken together, these results implicate the CC domain of Pm21 in cell-death signalling and disease-resistance signalling, which are potentially independent of each other. K E Y W O R D S CC domain, cell death, disease resistance, intramolecular interaction, Pm21 S U PP O RTI N G I N FO R M ATI O N Additional supporting information may be found online in the Supporting Information section. How to cite this article: Gao A, Hu M, Gong Y, et al. Pm21 CC domain activity modulated by intramolecular interactions is implicated in cell death and disease resistance. Molecular Plant Pathology. 2020;21:975-984.

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Resistance protein Pit interacts with the GEF OsSPK1 to activate OsRac1 and trigger rice immunity

Cited by 44 publications

References 61 publications

Importance of OsRac1 and RAI1 in signalling of nucleotide‐binding site leucine‐rich repeat protein‐mediated resistance to rice blast disease

Importance of OsRac1 and RAI1 in signalling of nucleotide‐binding site leucine‐rich repeat protein‐mediated resistance to rice blast disease

The effects of microcystin-LR inOryza sativaroot cells: F-actin as a new target of cyanobacterial toxicity

Pm21 CC domain activity modulated by intramolecular interactions is implicated in cell death and disease resistance

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