Jonathan Dallas Jones

The Sainsbury Laboratory | TSL

Excessive activation of effector-triggered immunity (ETI) in plants inhibits plant growth and activates cell death. ETI mediated by intracellular Toll/Interleukin-1 receptor/Resistance protein (TIR) nucleotide-binding leucine-rich-repeat receptors (NLRs) involves two partially redundant signalling nodes in Arabidopsis, EDS1-PAD4-ADR1 and EDS1-SAG10...

Arabidopsis Col-0 RPP2A and RPP2B confer recognition of Arabidopsis downy mildew ( Hyaloperonospora arabidopsidis [ Hpa ]) isolate Cala2, but the identity of the recognized ATR2 Cala2 effector was unknown. To reveal ATR2 Cala2 , an F 2 population was generated from a cross between Hpa -Cala2 and Hpa -Noks1. We identified ATR2 Cala2 as a non-canonic...

Greenhouse gas (GHG) emissions have created a global climate crisis which requires immediate interventions to mitigate the negative effects on all aspects of life on this planet. As current agriculture and land use contributes up to 25% of total GHG emissions, plant scientists take center stage in finding possible solutions for a transition to sust...

Plants have powerful defence mechanisms, and extensive immune receptor repertoires, yet crop monocultures are prone to epidemic diseases. Rice is susceptible to many diseases, such as rice blast caused by Magnaporthe oryzae. Varietal resistance of rice to blast relies on intracellular nucleotide binding, leucine-rich repeat (NLR) receptors that rec...

Here we identified cell-surface (LRR-RLKs, LRR-RLPs, LysM-RLKs and LysM-RLPs) and intracellular immune receptors (NB-ARCs) from the genomes of 350 plant species. Zip file contains: Folder 'Immune_receptor_sequences' - FASTA files of the identified LRR-RLPs, Lys-RLKs, LysM-RLPs and NB-ARCs. Folder 'RLK_sequences' - FASTA files of the identified...

Late blight caused by the oomycete pathogen Phytophthora infestans continues to cause major worldwide losses in potato and tomato. Most accessions of Solanum americanum, a globally distributed, wild Solanaceae plant, are highly resistant to late blight. We generated high-quality reference genomes of four S. americanum accessions, re-sequenced 52 ac...

To safeguard bread wheat against pests and diseases, breeders have introduced over 200 resistance genes into its genome, thus nearly doubling the number of designated resistance genes in the wheat gene pool. Isolating these genes facilitates their fast-tracking in breeding programs and incorporation into polygene stacks for more durable resistance....

Plant disease resistance involves both detection of microbial molecular patterns by cell-surface pattern recognition receptors and detection of pathogen effectors by intracellular NLR immune receptors. NLRs are classified as sensor NLRs, involved in effector detection, or helper NLRs required for sensor NLR signalling. TIR-domain-containing sensor...

Knowledge of the immune mechanisms responsible for viral recognition is critical for understanding durable disease resistance and successful crop protection. We determined how potato virus Y (PVY) coat protein (CP) is recognised by Rysto, a TNL immune receptor. We applied structural modelling, site‐directed mutagenesis, transient overexpression, co...

Understanding the plant immune system is crucial for using genetics to protect crops from diseases. Plants resist pathogens via a two-tiered innate immune detection-and-response system. The first plant Resistance (R) gene was cloned in 1992 (Johal and Briggs, 1992). Since then, many cell-surface pattern recognition receptors (PRRs) have been identi...

Recent reports suggest that cell-surface and intracellular immune receptors function synergistically to activate robust defence against pathogens, but whether or not they co-evolve is unclear. Here we determined the copy numbers of cell-surface and intracellular immune receptors in 208 species. Surprisingly, these receptor gene families contract an...

Plants use intracellular immune receptors (NLRs) to detect pathogen-derived effector proteins. The Arabidopsis NLR pair RRS1-R/RPS4 confers disease resistance to different bacterial pathogens by perceiving structurally distinct effectors AvrRps4 from Pseudomonas syringae pv . pisi and PopP2 from Ralstonia solanacearum via an integrated WRKY domain...

Diverse pathogens from the genus Phytophthora 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 domain, leucine-rich repeat- cont...

Potyviruses are the largest group of plant RNA viruses, causing significant losses in many crops. Among them, potato virus Y (PVY) is particularly important, and enhances the severity of infections by other viruses. The Ry sto gene confers PVY resistance and encodes a TIR-NLR intracellular immune receptors that recognizes PVY coat protein (CP). To...

The oomycete Albugo candida causes white rust of Brassicaceae, including vegetable and oilseed crops, and wild relatives such as Arabidopsis thaliana . Novel White Rust Resistance ( WRR )-genes from Arabidopsis enable new insights into plant/parasite co-evolution. WRR4A from Arabidopsis accession Col-0 provides resistance to many but not all white...

Activation of cell Surface and Intracellular Receptor-Mediated Immunity (SRMI and IRMI) results in rapid transcriptional reprogramming that underpins disease resistance. However, the mechanisms by which SRMI and IRMI lead to transcriptional changes are not clear. Here, we combine RNA-seq and ATAC-seq to define changes in gene expression and chromat...

Late blight caused by Phytophthora infestans greatly constrains potato production. Many Resistance ( R ) genes were cloned from wild Solanum species and/or introduced into potato cultivars by breeding. However, individual R genes have been overcome by P. infestans evolution; durable resistance remains elusive. We positionally cloned a new R gene, R...

The plant immune system involves cell-surface receptors that detect intercellular pathogen-derived molecules, and intracellular receptors that activate immunity upon detection of pathogen-secreted effectors that act inside the plant cell. Surface receptor-mediated immunity has been extensively studied but in authentic interactions between plants an...

Disease resistance genes encoding nucleotide-binding and leucine-rich repeat (NLR) intracellular immune receptor proteins detect pathogens by the presence of pathogen effectors. Plant genomes typically contain hundreds of NLR-encoding genes. The availability of the hexaploid wheat (Triticum aestivum) cultivar Chinese Spring reference genome allows...

Sequence capture followed by next-generation sequencing has broad applications in cost-effective exploration of biological processes at high resolution [1, 2]. Genome-wide RNA sequencing (RNA-seq) over a time course can reveal the dynamics of differential gene expression. However, in many cases, only a limited set of genes are of interest, and are...

Potato virus Y (PVY) is a major potato (Solanum tuberosum L.) pathogen that causes severe annual crop losses worth billions of dollars worldwide. PVY is transmitted by aphids, and successful control of virus transmission requires the extensive use of environmentally damaging insecticides to reduce vector populations. Rysto, from the wild relative S...

Plant nucleotide-binding domain, leucine-rich repeat receptor (NLR) proteins play important roles in recognition of pathogen-derived effectors. However, the mechanism by which plant NLRs activate immunity is still largely unknown. The paired Arabidopsis NLRs RRS1-R and RPS4, that confer recognition of bacterial effectors AvrRps4 and PopP2, are well...

Potato virus Y (PVY) is a major potato pathogen that causes annual losses of billions of dollars. Control of its transmission requires extensive use of environmentally damaging insecticides. Ry sto confers extreme resistance (ER) to PVY and is a valuable trait in resistance breeding programs. We isolated Ry sto using Resistance gene enrichment sequ...

The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. To colonize its host, Hpa translocates effector proteins that suppress plant immunity into infected host cells. Here, we investigate the relevance of the interaction between one of these effectors, HaRxL106, and Arabidopsis RADICAL‐INDUCED CELL DE...

Background ATAC-cap-seq is a high-throughput sequencing method that combines ATAC-seq with targeted nucleic acid enrichment of precipitated DNA fragment. There are increased analytical difficulties arising from working with a set of regions of interest that may be small in number and biologically dependent. Common statistical pipelines for RNAseq m...

Disease resistance genes encoding intracellular immune receptors of the nucleotide-binding and leucine-rich repeat (NLR) class of proteins detect pathogens by the presence of pathogen effectors. Plant genomes typically contain hundreds of NLR encoding genes. The availability of the hexaploid wheat cultivar Chinese Spring reference genome now allows...

Key message: A broad-spectrum late blight disease-resistance gene from Solanum verrucosum has been mapped to potato chromosome 9. The gene is distinct from previously identified-resistance genes. We have identified and characterised a broad-spectrum resistance to Phytophthora infestans from the wild Mexican species Solanum verrucosum. Diagnostic r...

Plant and animal cells share similar malate-mediated cell death processes, but plants have evolved a unique intracellular communication between organelles in regulating programmed cell death in response to specific photoperiods.

The tomato PROCERA gene encodes a DELLA protein, and loss‐of‐function mutations derepress growth. We used CRISPR/Cas9 and a single guide RNAs (sgRNA) to target mutations to the PROCERA DELLA domain, and recovered several loss‐of‐function mutations and a dominant dwarf mutation that carries a deletion of one amino acid in the DELLA domain. This is t...

Supplementary Fig. 1. Cell death responses upon expressing of AVR2 on Désirée-Rpi-mcq1 and Désirée-Rpi-blb3. Agroinfiltration using A. tumefaciens strain carrying pK7WG2: AVR2, pK7WG2: empty and co-infiltrations of R3a/AVR3a on Désirée-Rpi-mcq1 (A), Désirée-Rpi-blb3 (B), and untransformed ‘Désirée’ (Wild type) (C). Each effector is tested twice on...

Late blight caused by the oomycete pathogen Phytophthora infestans is the most devastating disease in potato. For sustainable management of this economically important disease, resistance breeding relies on the availability of resistance (R) genes. Such R genes against P. infestans have evolved in wild tuber-bearing Solanum species from North, Cent...

MutRenSeq is a method to clone disease resistance (R) genes in plants. Tips and detailed experimental protocols for the pipeline, including the complexity reduction by R gene targeted enrichment sequencing, and computational analysis based on comparative genomics are provided in this chapter.

Background The Oxford Nanopore Technologies MinION™ sequencer is a small, portable, low cost device that is accessible to labs of all sizes and attractive for in-the-field sequencing experiments. Selective breeding of crops has led to a reduction in genetic diversity, and wild relatives are a key source of new genetic resistance to pathogens, usual...

Key message: We identified two novel wheat stem rust resistance genes, Sr-1644-1Sh and Sr-1644-5Sh in Aegilops sharonensis that are effective against widely virulent African races of the wheat stem rust pathogen. Stem rust is one of the most important diseases of wheat in the world. When single stem rust resistance (Sr) genes are deployed in wheat...

Plant NLR (Nucleotide-binding domain and Leucine-rich Repeat) immune receptor proteins are encoded by Resistance (R) genes and confer specific resistance to pathogen races that carry the corresponding recognized effectors. Some NLR proteins function in pairs, forming receptor complexes for the perception of specific effectors. We show here that the...

RPS4 nucleolus localization is altered by RRS1 co-expression in N. benthamiana. (A) Overexpression of N-terminally YFP-tagged RPS4 with mCherry and GUS-HF results in nucleocytoplasmic localization. YFP-RPS4 mainly localizes to the nucleolus. The experiment was repeated three times with nearly identical results. Scale bar = 10 μm. (B) When co-expres...

EDS1 associates with both RPS4 and RRS1 proteins in planta. Co-IP was performed with transiently expressed RRS1-R-HF or RPS4-HF with GFP-EDS1 or GFP in N. benthamiana leaves. After 2 dpi, samples were harvested and then immunoprecipitated with anti-GFP beads. The samples were then analyzed by immunoblotting with anti-FLAG and anti-GFP antibodies. A...

EDS1 interacts with AvrRps4. (A-B) Both N- and C-terminally Myc tagged EDS1 co-immunoprecipitate with AvrRps4 in planta. The 35S::Myc-EDS1 or the 35S::EDS1-Myc were co-infiltrated with the 35S::PAD4-GFP, 35S::AvrRps4-GFP or 35S::GFP in N. benthamiana leaves and samples were harvested at 2 dpi. Immunoprecipitations were performed using anti-GFP and...

BiFC verification of the interaction between EDS1 and AvrRps4. The AvrRps4-cCFP and nVenus EDS1 constructs were transiently co-expressed in N. benthamiana leaves. The combination of AvrRps4-cCFP with nVenus-PAD4 was used as a negative control. The functionality of nVenus-PAD4 construct was verified by co-expression with cCFP-EDS1. Red or blue fluor...

AvrRps4 does not affect RPS4/EDS1/PAD4 association in the nucleus in the presence RRS1. (A-B) Multi-color BiFC analysis between RRS1, RPS4, EDS1 and PAD4 in the presence or absence of AvrRps4. RRS1-HF, nCerulean-RPS4, cCFP-EDS1 and nVenus-PAD4 were transiently co-expressed with AvrRps4-E187A-mCherry or AvrRps4-mCherry, in N. benthamiana leaves. Co-...

RPS4 protein accumulation in Arabidopsis and N. benthamiana. (A-B) Western blot analysis of RPS4-HS, RRS1-R-HF, and RPS4-HS/RRS1-R-HF transgenic lines. Total proteins were extracted from each plant and western blot was performed with anti-PR1 (A), anti-HA, and anti-FLAG (B) antibodies. (C) Reduced RPS4 accumulation is not due to reduced T-DNA trans...

RPS4 self-associates only in the presence of RRS1 in co-IP assays. (A) Agrobacterium-mediated transient co-expression of RRS1-GFP/RPS4-HF/RPS4-Myc or GFP/ RPS4-HF/RPS4-Myc was performed in N. benthamiana leaves. Anti-FLAG co-IPs were performed with total protein extracts and probed with anti-GFP, -FLAG, and -Myc antibodies. (B) Co-IPs show that RRS...

AvrRps4 does not affect RPS4/EDS1 association in the nucleus in the presence or absence of RRS1. BiFC assays of RPS4/EDS1 association in the presence of RRS1 or both RRS1 and AvrRps4 or AvrRps4E187A. N. benthamiana leaves were co-infiltrated with nVenus-RPS4/nCFP-EDS1/RRS1-R-HF/AvrRps4E187A or nVenus-RPS4/nCFP-EDS1/RRS1-R-HF/AvrRps4-mCherry, recons...

AvrRps4KRVY/AAAA mutant and EDS1 association in BiFC assay. BiFC reveals that interaction between of EDS1 and AvrRps4KRVY/AAAA mutant forms cytoplasmic aggregations that are reduced in the presence of PAD4-HA but not in the presence of SAG101. BiFC assays were performed by co-expression of the indicated proteins in N. benthamiana. Scale bar = 15 μm...

Plant immunity protects plants from numerous potentially pathogenic microbes. The biological network that controls plant inducible immunity must function effectively even when network components are targeted and disabled by pathogen effectors. Network buffering could confer this resilience by allowing different parts of the network to compensate fo...

The timecourses of the activity levels (A, C, E, and G) and responses (B, D, F, and H) of the JA (A and B), ET (C and D), PAD4 (E and F), and SA (G and H) signaling sectors in 17 genotypes. The lines for the genotypes are color coded for combinations of the active signaling sectors: JA (red), ET (yellow), PAD4 (green), and SA (blue), except for JEP...

Signaling allocations with different stringency of regularization. Heatmaps of the signaling allocations based on the models with no regularization (A) and with the regularization stringency selected by BIC (B) are shown. The orders of the genes in the rows of the heatmaps are the same as that in Fig 2 to facilitate comparisons among these two pane...

Genes selected for the SA single sector dominance are likely regularization artifacts. Heatmaps of the signaling allocations based on the AICc-selected regularization (A) and no regularization (B) for seven genes that passed the filter for the SA single sector dominance are shown. Since there is no evidently consistent pattern between (A) and (B),...

Signaling allocation for alternative ET and PAD4 sector activity markers, AT3G16530 (A) and AT4G21840 (B). Heatmaps for the signaling allocations are shown. The allocation patterns are similar to those of the ET and PAD4 sector activity markers of our selection, ARGOS and AT4G04500, respectively (Fig 5B and 5C). The allocations were scaled for visu...

Transcript response timecourse comparisons of ein2-sensitive genes between wild type (JEPS) and ein2 (JePS). (A) The timecourses of 100 genes randomly selected from 1270 genes whose transcript responses were significantly changed in JePS compared to JEPS. Each trace represents one of the 100 genes. The timecourse is color coded as shown. (B-E) Arti...

An early ethylene spike is evident with other ET marker genes. Mean transcript levels of common ET marker genes, across all genotypes and time points profiled. (A) ARL (AT2G44080) and (B) EBF2 (AT5G25350). The lines for the genotypes are color coded for combinations of the active signaling sectors: JA (red), ET (yellow), PAD4 (green), and SA (blue)...

Raw hormone data. They are in pmol/g dry weight. U.Q., under quantification limit. (TXT)

Supporting methods. (DOCX)

The transcript levels of the flg22-resonsive, network-dependent (A, 5259 genes) or network-independent (B, 2659 genes) genes. The heatmaps after clustering based on the Pearson correlation coefficient are shown. The log2-transformed transcript level data from the genotypes fls2, JEPS, and jeps at all the time points were used. See Fig 1 for selecti...

Infiltration schedules. (ZIP)

FLS2 transcript levels in the ein2-containing genotypes. FLS2 transcript levels in the ein2-containing genotypes are increased to nearly wild type levels within 1 hour after flg22 treatment. (A and B) Transcript level time courses of AT5G46330 (FLS2) for 17 genotypes are shown. The lines for the genotypes are color coded for combinations of the act...

The oomycete pathogen Hyaloperonospora arabidopsidis (Hpa) causes downy mildew disease on Arabidopsis. During infection, Hpa like other biotrophic pathogens, suppresses activation of plant innate immunity by translocating effector proteins into host cells. Some of these effectors localize to the host cell nucleus where they may manipulate transcrip...

Reader Comments The white paper reports the deliberations of a workshop focused on biotic challenges to plant health held in Washington, D.C. in September 2016. Ensuring health of food plants is critical to maintaining the quality and productivity of crops and for sustenance of the rapidly growing human population. There is a close linkage between...

Background Plants are exposed to diverse pathogens and pests, yet most plants are resistant to most plant pathogens. Non-host resistance describes the ability of all members of a plant species to successfully prevent colonization by any given member of a pathogen species. White blister rust caused by Albugo species can overcome non-host resistance...

Mammals, in addition to their adaptive immune system based on somatic evolution of antibodies, carry an innate immune system based on both cell surface and intracellular immune receptors (1). In animals ranging from insects to mammals, Toll-like receptors (TLRs), with extracellular leucine-rich repeats (LRRs) and an intracellular Toll/interleukin-1...

Structural Rearrangements can have unexpected effects on quantitative phenotypes. Surprisingly, these rearrangements can also be considered as... To understand the population genetics of structural variants and their effects on phenotypes, we developed an approach to mapping structural variants that segregate in a population sequenced at low covera...

Plants control nutrient availability in intercellular spaces (the apoplast) via transporters, channels, and vesicular transport. Recent papers in Science and Nature from two groups have highlighted how plants control sugar to restrict bacterial growth (Yamada et al., 2016) and how increased water availability enhances pathogenesis (Xin et al., 2016...

Supporting info item

Shared logic in diverse immune systems The innate immune systems of both plants and animals depend on the ability to recognize pathogen-derived molecules and stimulate a defense response. Jones et al. review how that common function is achieved in such diverse kingdoms by similar molecules. The recognition system is built for hair-trigger sensitivi...

Targeted capture provides an efficient and sensitive means for sequencing specific genomic regions in a high-throughput manner. To date, this method has mostly been used to capture exons from the genome (the exome) using short insert libraries and short-read sequencing technology, enabling the identification of genetic variants or new members of la...

To understand the population genetics of structural variants (SVs), and their effects on phenotypes, we developed an approach to mapping SVs, particularly transpositions, segregating in a sequenced population, and which avoids calling SVs directly. The evidence for a potential SV at a locus is indicated by variation in the counts of short-reads tha...

The oomycete pathogen Phytophthora infestans causes potato late blight, and as a potato and tomato specialist pathogen, is seemingly poorly adapted to infect plants outside the Solanaceae. Here, we report the unexpected finding that P. infestans can infect Arabidopsis thaliana when another oomycete pathogen, Albugo laibachii, has colonized the host...