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Updates from the group of Sophien Kamoun at The Sainsbury Lab
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Nature Food: Near- to long-term measures to stabilize global wheat supplies and food security (2022)

Nature Food: Near- to long-term measures to stabilize global wheat supplies and food security (2022) | Publications | Scoop.it

The Ukraine–Russia war will impact global food security over months if not years. In the wake of COVID-19 and in the face of increasing climate change, we propose responses to a multi-layered global food crisis that mitigate near-term food security risks, stabilize wheat supplies and transition towards long-term agri-food system resilience.

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Molecular Plant: A potato late blight resistance gene protects against multiple Phytophthora species by recognizing a broadly conserved RXLR-WY effector (2022)

Molecular Plant: A potato late blight resistance gene protects against multiple Phytophthora species by recognizing a broadly conserved RXLR-WY effector (2022) | Publications | Scoop.it
Species of the genus Phytophthora - the plant killer - cause disease and reduce yields in many crop plants. Although many Resistance to Phytophthora infestans (Rpi) genes effective against potato late blight have been cloned, few have been cloned against other Phytophthora species. Most Rpi genes encode nucleotide-binding, leucine-rich repeat- containing (NLR) immune receptor proteins, that recognize RXLR effectors. However, whether NLR proteins can recognize RXLR effectors from multiple Phytophthora species has rarely been investigated. Here, we identified a new RXLR-WY effector AVRamr3 from P. infestans that is recognized by Rpi-amr3 from a wild Solanaceae species Solanum americanum. Rpi-amr3 associates with AVRamr3 in planta. AVRamr3 is broadly conserved in many different Phytophthora species, and the recognition of AVRamr3 homologs by Rpi-amr3 activates resistance against multiple Phytophthora pathogens, including the tobacco black shank disease and cacao black pod disease pathogens P. parasitica and P. palmivoraRpi-amr3 is thus the first characterized resistance gene that acts against P. parasitica or P. palmivora. These findings suggest a novel path to redeploy known R genes against different important plant pathogens.

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PNAS: A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution (2022)

PNAS: A genetically linked pair of NLR immune receptors shows contrasting patterns of evolution (2022) | Publications | Scoop.it

Throughout their evolution, plant nucleotide-binding leucine-rich-repeat receptors (NLRs) have acquired widely divergent unconventional integrated domains that enhance their ability to detect pathogen effectors. However, the functional dynamics that drive the evolution of NLRs with integrated domains (NLR-IDs) remain poorly understood. Here, we reconstructed the evolutionary history of an NLR locus prone to unconventional domain integration and experimentally tested hypotheses about the evolution of NLR-IDs. We show that the rice (Oryza sativa) NLR Pias recognizes the effector AVR-Pias of the blast fungal pathogen Magnaporthe oryzae. Pias consists of a functionally specialized NLR pair, the helper Pias-1 and the sensor Pias-2, that is allelic to the previously characterized Pia pair of NLRs: the helper RGA4 and the sensor RGA5. Remarkably, Pias-2 carries a C-terminal DUF761 domain at a similar position to the heavy metal-associated (HMA) domain of RGA5. Phylogenomic analysis showed that Pias-2/RGA5 sensor NLRs have undergone recurrent genomic recombination within the genus Oryza, resulting in up to six sequence-divergent domain integrations. Allelic NLRs with divergent functions have been maintained transspecies in different Oryza lineages to detect sequence-divergent pathogen effectors. By contrast, Pias-1 has retained its NLR helper activity throughout evolution and is capable of functioning together with the divergent sensor-NLR RGA5 to respond to AVR-Pia. These results suggest that opposite selective forces have driven the evolution of paired NLRs: highly dynamic domain integration events maintained by balancing selection for sensor NLRs, in sharp contrast to purifying selection and functional conservation of immune signaling for helper NLRs.


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bioRxiv: Effector target-guided engineering of an integrated domain expands the disease resistance profile of a rice NLR immune receptor (2022)

bioRxiv: Effector target-guided engineering of an integrated domain expands the disease resistance profile of a rice NLR immune receptor (2022) | Publications | Scoop.it

A subset of plant intracellular NLR immune receptors detect effector proteins, secreted by phytopathogens to promote infection, through unconventional integrated domains which resemble the effector's host targets. Direct binding of effectors to these integrated domains activates plant defences. The rice NLR receptor Pik-1 binds the Magnaporthe oryzae effector AVR-Pik through an integrated heavy metal-associated (HMA) domain. However, the stealthy alleles AVR-PikC and AVR-PikF avoid interaction with Pik-HMA and evade host defences. Here, we exploited knowledge of the biochemical interactions between AVR-Pik and its host target, OsHIPP19, to engineer novel Pik-1 variants that respond to AVR-PikC/F. First, we exchanged the HMA domain of Pikp-1 for OsHIPP19-HMA, demonstrating that effector targets can be incorporated into NLR receptors to provide novel recognition profiles. Second, we used the structure of OsHIPP19-HMA to guide mutagenesis of Pikp-HMA to expand its recognition profile. We demonstrate that the extended recognition profiles of engineered Pikp-1 variants correlate with effector binding in planta and in vitro, and with the gain of new contacts across the effector/HMA interface. Crucially, transgenic rice producing the engineered Pikp-1 variants were resistant to blast fungus isolates carrying AVR-PikC or AVR-PikF. These results demonstrate that effector target-guided engineering of NLR receptors can provide new-to-nature disease resistance in crops.


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Essays in Biochemistry: Show me your ID: NLR immune receptors with integrated domains in plants (2022)

Essays in Biochemistry: Show me your ID: NLR immune receptors with integrated domains in plants (2022) | Publications | Scoop.it

Abstract. Nucleotide-binding and leucine-rich repeat receptors (NLRs) are intracellular plant immune receptors that recognize pathogen effectors secreted into the plant cell. Canonical NLRs typically contain three conserved domains including a central nucleotide binding (NB-ARC) domain, C-terminal leucine-rich repeats (LRRs) and an N-terminal domain. A subfamily of plant NLRs contain additional noncanonical domain(s) that have potentially evolved from the integration of the effector targets in the canonical NLR structure. These NLRs with extra domains are thus referred to as NLRs with integrated domains (NLR-IDs). Here, we first summarize our current understanding of NLR-ID activation upon effector binding, focusing on the NLR pairs Pik-1/Pik-2, RGA4/RGA5, and RRS1/RPS4. We speculate on their potential oligomerization into resistosomes as it was recently shown for certain canonical plant NLRs. Furthermore, we discuss how our growing understanding of the mode of action of NLR-ID continuously informs engineering approaches to design new resistance specificities in the context of rapidly evolving pathogens.


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Science Advances: Genome evolution of a nonparasitic secondary heterotroph, the diatom Nitzschia putrida (2022)

Science Advances: Genome evolution of a nonparasitic secondary heterotroph, the diatom Nitzschia putrida (2022) | Publications | Scoop.it

Secondary loss of photosynthesis is observed across almost all plastid-bearing branches of the eukaryotic tree of life. However, genome-based insights into the transition from a phototroph into a secondary heterotroph have so far only been revealed for parasitic species. Free-living organisms can yield unique insights into the evolutionary consequence of the loss of photosynthesis, as the parasitic lifestyle requires specific adaptations to host environments. Here, we report on the diploid genome of the free-living diatom Nitzschia putrida (35 Mbp), a nonphotosynthetic osmotroph whose photosynthetic relatives contribute ca. 40% of net oceanic primary production. Comparative analyses with photosynthetic diatoms and heterotrophic algae with parasitic lifestyle revealed that a combination of gene loss, the accumulation of genes involved in organic carbon degradation, a unique secretome, and the rapid divergence of conserved gene families involved in cell wall and extracellular metabolism appear to have facilitated the lifestyle of a free-living secondary heterotroph.

 

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Medium: When to preprint? (2022)

Medium: When to preprint? (2022) | Publications | Scoop.it

At what stage in the life of a research paper should you preprint it? It depends on the circumstances of the study, but there are roughly four options.

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Medium: Even in a great orchestra, you will only hear the bad player (2022)

Medium: Even in a great orchestra, you will only hear the bad player (2022) | Publications | Scoop.it

To be a successful scientist, a balanced skill set is important. Overachievers in just one area will struggle in academia.

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Medium: Don’t be a deliveroo student (2022)

Medium: Don’t be a deliveroo student (2022) | Publications | Scoop.it

Humor can help bring focus to serious topics. Controls, controls, and more controls…

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Medium: Open science: a letter to a friend (2022)

Medium: Open science: a letter to a friend (2022) | Publications | Scoop.it

I’m deeply touched and honored to be invited to write these few words on behalf of the Institute of Biotechnology and Genetic Engineering Alumni Association (IBGEAA) to celebrate the 12 years of professional life of Prof. Md. Tofazzal Islam at Bangabandhu Sheikh Mujibur Rahman Agricultural University (BSMRAU).

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Medium: The knee that broke Neymar’s back — Is academia that harsh? (2022)

Medium: The knee that broke Neymar’s back — Is academia that harsh? (2022) | Publications | Scoop.it

The chances of success in academia are definitely better than in elite sports. And there are many ways of having a satisfying and fulfilling career.

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bioRxiv: Sensor NLR immune proteins activate oligomerization of their NRC helper (2022)

bioRxiv: Sensor NLR immune proteins activate oligomerization of their NRC helper (2022) | Publications | Scoop.it

Nucleotide-binding domain and leucine-rich repeat (NLR) immune receptors are important components of plant and metazoan innate immunity that can function as individual units or as pairs or networks. Upon activation, NLRs form multiprotein complexes termed resistosomes or inflammasomes. Whereas metazoan paired NLRs, such as NAIP/NLRC4, activate into hetero-complexes, the molecular mechanisms underpinning activation of plant paired NLRs, especially whether they associate in resistosome hetero-complexes is unknown. In asterid plant species, the NLR required for cell death (NRC) immune receptor network is composed of multiple resistance protein sensors and downstream helpers that confer immunity against diverse plant pathogens. Here, we show that pathogen effector-activation of the NLR proteins Rx (confers virus resistance) and Bs2 (confers bacterial resistance) leads to oligomerization of the helper NLR NRC2. Activated Rx does not oligomerize or enter into a stable complex with the NRC2 oligomer and remains cytoplasmic. In contrast, activated NRC2 oligomers accumulate in membrane-associated puncta. We propose an activation-and-release model for NLRs in the NRC immune receptor network. This points to a distinct activation model compared to mammalian paired NLRs.


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bioRxiv: SNP calling parameters have minimal impact on population structure and divergence time estimates for the rice blast fungus (2022)

bioRxiv: SNP calling parameters have minimal impact on population structure and divergence time estimates for the rice blast fungus (2022) | Publications | Scoop.it

Objectives Accurate single-nucleotide polymorphisms (SNP) calls are crucial for robust evolutionary and population genetic inferences in genomic analyses. Such inferences can reveal the time-scales and processes associated with the emergence and spread of pandemic plant pathogens, such as the rice blast fungus Magnaporthe oryzae (Syn. Pyricularia oryzae). However, the specificity and sensitivity of SNP calls depend on the filtering parameters applied to the data. Here, we used a benchmarking approach to evaluate the impact of SNP calling on different population genetic analyses of the rice blast fungus, namely genetic clustering, topology of phylogenetic reconstructions and estimation of evolutionary rates. Results To benchmark SNP calling parameters, we generated a gold standard set of validated SNPs by sequencing nine M. oryzae genomes with both Illumina short-reads and Oxford Nanopore Technologies (ONT). We used the gold standard set of SNPs to identify the SNP calling parameter configuration that maximizes sensitivity and specificity. We found that the choice of parameter configurations can substantially change the number of ascertained SNPs, preferentially affecting SNPs segregating at low population frequency. However, SNP calling parameter configurations did not significantly affect the clustering of isolates in clonal lineages, the monophyly of each clonal lineage, and the estimation of evolutionary rates. We leverage the evolutionary rates obtained from each SNP calling parameter configuration to generate divergence time estimates that take into account the uncertainty associated with both the estimation of evolutionary rates and SNP calling. Our analysis indicates that M. oryzae clonal lineage expansions took place ~300 years ago.


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Plant and Cell Physiology: Activation and Regulation of NLR Immune Receptor Networks (2022)

Plant and Cell Physiology: Activation and Regulation of NLR Immune Receptor Networks (2022) | Publications | Scoop.it

Plants have many types of immune receptors that recognize diverse pathogen molecules and activate the innate immune system. The intracellular immune receptor family of nucleotide-binding domain leucine-rich repeat-containing proteins (NLRs) perceive translocated pathogen effector proteins and execute a robust immune response, including programmed cell death. Many plant NLRs have functionally specialized to sense pathogen effectors (sensor NLRs) or to execute immune signalling (helper NLRs). Sub-functionalized NLRs form a network-type receptor system known as the NLR network. In this review, we highlight the concept of NLR networks, discussing how they are formed, activated, and regulated. Two main types of NLR networks have been described in plants: the ADR1/NRG1 network and the NRC network. In both networks, multiple helper NLRs function as signalling hubs for sensor NLRs and cell surface-localized immune receptors. Additionally, the networks are regulated at the transcriptional and posttranscriptional levels, as well as being modulated by other host proteins to ensure proper network activation and prevent autoimmunity. Plant pathogens in turn have converged on suppressing NLR networks, thereby facilitating infection and disease. Understanding the NLR immune system at the network level could inform future breeding programs by highlighting the appropriate genetic combinations of immunoreceptors to use while avoiding deleterious autoimmunity and suppression by pathogens.


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bioRxiv: Tangled gene-for-gene interactions mediate co-evolution of the rice NLR immune receptor Pik and blast fungus effector proteins (2022)

bioRxiv: Tangled gene-for-gene interactions mediate co-evolution of the rice NLR immune receptor Pik and blast fungus effector proteins (2022) | Publications | Scoop.it

Studies focused solely on single organisms can fail to identify the networks underlying host-pathogen gene-for-gene interactions. Here, we integrate genetic analyses of rice (Oryza sativa, host) and rice blast fungus (Magnaporthe oryzae, pathogen) and uncover a new pathogen recognition specificity of the rice nucleotide-binding domain and leucine-rich repeat protein (NLR) immune receptor Pik, which mediates resistance to M. oryzae expressing the avirulence effector gene AVR-Pik. Rice Piks-1, encoded by an allele of Pik-1, recognizes a previously unidentified effector encoded by the M. oryzae avirulence gene AVR-Mgk1, which is found on a mini-chromosome. AVR-Mgk1 has no sequence similarity to known AVR-Pik effectors, and is prone to deletion from the mini-chromosome mediated by repeated Inago2 retrotransposon sequences. AVR-Mgk1 is detected by Piks-1 and by other Pik-1 alleles known to recognize AVR-Pik effectors; recognition is mediated by AVR-Mgk1 binding to the integrated heavy metal-associated domain of Piks-1 and other Pik-1 alleles. Our findings highlight how complex gene-for-gene interaction networks can be disentangled by applying forward genetics approaches simultaneously to the host and pathogen. We demonstrate dynamic co-evolution between an NLR integrated domain and multiple families of effector proteins.


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bioRxiv: Binding of a blast fungus Zinc-finger fold effector to a hydrophobic pocket in the host exocyst subunit Exo70 modulates immune recognition in rice (2022)

bioRxiv: Binding of a blast fungus Zinc-finger fold effector to a hydrophobic pocket in the host exocyst subunit Exo70 modulates immune recognition in rice (2022) | Publications | Scoop.it

Exocytosis plays an important role in plant-microbe interactions, both in pathogenesis and symbiosis. Exo70 proteins are integral components of the exocyst, an octameric complex that mediates tethering of vesicles to membranes in eukaryotes. Although plant Exo70s are known to be targeted by pathogen effectors, the underpinning molecular mechanisms and the impact of this interaction on infection is poorly understood. Here, we show the molecular basis of the association between the effector AVR- Pii of the blast fungus Maganaporthe oryzae and rice Exo70 alleles OsExo70F2 and OsExo70F3, which is sensed by the immune receptor pair Pii via an integrated RIN4/NOI domain. The crystal structure of AVR-Pii in complex with OsExo70F2 reveals that the effector binds to a conserved hydrophobic pocket in Exo70, defining a new effector/target binding interface. Structure-guided and random mutagenesis validates the importance of AVR-Pii residues at the Exo70 binding interface to sustain protein association and disease resistance in rice when challenged with fungal strains expressing effector mutants. Further, the structure of AVR-Pii defines a novel Zinc- finger effector fold (ZiF) distinct from the MAX fold previously described for the majority of characterized M. oryzae effectors. Our data suggests that blast fungus ZiF effectors bind a conserved Exo70 interface to manipulate plant exocytosis and that these effectors are also baited by plant immune receptors, pointing to new opportunities for engineering disease resistance.

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bioRxiv: A pandemic clonal lineage of the wheat blast fungus (2022)

bioRxiv: A pandemic clonal lineage of the wheat blast fungus (2022) | Publications | Scoop.it

Wheat, the most important food crop, is threatened by a blast disease pandemic. Here, we show that a clonal lineage of the wheat blast fungus recently spread to Asia and Africa following two independent introductions from South America. Through a combination of genome analyses and laboratory experiments, we show that the decade-old blast pandemic lineage can be controlled by the Rmg8 disease resistance gene and is sensitive to strobilurin fungicides. However, we also highlight the potential of the pandemic clone to evolve fungicide-insensitive variants and sexually recombine with African lineages. This underscores the urgent need for genomic surveillance to track and mitigate the spread of wheat blast outside of South America, and to guide pre-emptive wheat breeding for blast resistance.


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Essays in Biochemistry: NLR receptor networks in plants (2022)

Essays in Biochemistry: NLR receptor networks in plants (2022) | Publications | Scoop.it

To fight off diverse pathogens and pests, the plant immune system must recognize these invaders; however, as plant immune receptors evolve to recognize a pathogen, the pathogen often evolves to escape this recognition. Plant–pathogen co-evolution has led to the vast expansion of a family of intracellular immune receptors-nucleotide-binding domain and leucine-rich repeat proteins (NLRs). When an NLR receptor recognizes a pathogen ligand, it activates immune signaling and thus initiates defense responses. However, in contrast with the model of NLRs acting individually to activate resistance, an emerging paradigm holds that plants have complex receptor networks where the large repertoire of functionally specialized NLRs function together to act against the large repertoire of rapidly evolving pathogen effectors. In this article, we highlight key aspects of immune receptor networks in plant NLR biology and discuss NLR network architecture, the advantages of this receptor network system, and the evolution of the NLR network in asterid plants.


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Medium: #DeathByPowerpoint — ban the two-title slides now (2022)

Medium: #DeathByPowerpoint — ban the two-title slides now (2022) | Publications | Scoop.it

There is plenty of good advice on how to prepare a slide show, yet poorly crafted slides with multiple messages keep showing up. Let’s start by ditching the two-title slides once for all. Cite as…

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Medium: OpenPlantPathology Interview — Embrace open science to advance your career (2022)

Medium: OpenPlantPathology Interview — Embrace open science to advance your career (2022) | Publications | Scoop.it

This post is adapted from an OpenPlantPathology (OPP) interview with Emerson Del Ponte (Nov. 12, 2018). Here is a link to the original.

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Medium: Open science to tackle plant health emergencies: enough excuses, please! (2022)

Medium: Open science to tackle plant health emergencies: enough excuses, please! (2022) | Publications | Scoop.it

The thorny politics of the global food trade are often an excuse against the application of open science principles to plant disease epidemics. But scientists have often themselves to blame for the slow release of information and data, and there are ways around some of the issues.

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Medium: Three biologists and a social scientist go to Yellowstone… (2022)

Medium: Three biologists and a social scientist go to Yellowstone… (2022) | Publications | Scoop.it

…they ponder whether there are any moose in the National Park.

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Medium: Worried about scooping? What scooping? (2022)

Medium: Worried about scooping? What scooping? (2022) | Publications | Scoop.it

I’m surprised at how many in the biology community don’t seem to know about the “scooping Protection” policy that many journals have adopted. It’s the most progressive development in scientific publishing since preprints. Check it out.

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Medium: Time management for academics— forget about the Eisenhower method (2022)

Medium: Time management for academics— forget about the Eisenhower method (2022) | Publications | Scoop.it

I recently came to realize that I don’t follow the famed Eisenhower method for time management. Instead, I like to Shuffle. Let me tell you how.

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bioRxiv: Effector-dependent activation and oligomerization of NRC helper NLRs by Rpi-amr3 and Rpi-amr1 (2022)

bioRxiv: Effector-dependent activation and oligomerization of NRC helper NLRs by Rpi-amr3 and Rpi-amr1 (2022) | Publications | Scoop.it

Plant pathogens compromise crop yields. Plants have evolved robust innate immunity that depends in part on intracellular Nucleotide-binding, Leucine Rich-Repeat (NLR) immune receptors that activate defense responses upon detection of pathogen-derived effectors. Most sensor NLRs that detect effectors require the activity of helper NLRs, but how helper NLRs support sensor NLR function is poorly understood. Many Solanaceae NLRs require the NRC (NLR-Required for Cell death) class of helper NLRs. We show here that Rpi-amr3, a sensor NLR from Solanum americanum, detects AVRamr3 from the potato late blight pathogen, Phytophthora infestans, and activates oligomerization of the helper NLR NRC2 into a high-molecular weight resistosome. The NRC2 resistosome also forms upon recognition of P. infestans effector AVRamr1 by another sensor NLR, Rpi-amr1. The ATP-binding motif of Rpi-amr3 is required for NRC2 resistosome formation, but not for interaction with the cognate effector. The NRC2 resistosome can be activated by AVRamr3 homologs from other Phytophthora species. Mechanistic understanding of NRC resistosome formation will underpin engineering crops with durable disease resistance.


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