34 research outputs found
Variation in plant Toll/Interleukin-1 receptor domain protein dependence on ENHANCED DISEASE SUSCEPTIBILITY 1
Toll/Interleukin-1 receptor (TIR) domains are integral to immune systems across all kingdoms. In plants, TIRs are present in nucleotide-binding leucine-rich repeat (NLR) immune receptors, NLR-like, and TIR-only proteins. Although TIR-NLR and TIR signaling in plants require the ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) protein family, TIRs persist in species that have no EDS1 members. To assess whether particular TIR groups evolved with EDS1, we searched for TIR-EDS1 co-occurrence patterns. Using a large-scale phylogenetic analysis of TIR domains from 39 algal and land plant species, we identified 4 TIR families that are shared by several plant orders. One group occurred in TIR-NLRs of eudicots and another in TIR-NLRs across eudicots and magnoliids. Two further groups were more widespread. A conserved TIR-only group co-occurred with EDS1 and members of this group elicit EDS1-dependent cell death. In contrast, a maize (Zea mays) representative of TIR proteins with tetratricopeptide repeats was also present in species without EDS1 and induced EDS1-independent cell death. Our data provide a phylogeny-based plant TIR classification and identify TIRs that appear to have evolved with and are dependent on EDS1, while others have EDS1-independent activity
Genome and time-of-day transcriptome of Wolffia australiana link morphological minimization with gene loss and less growth control.
Rootless plants in the genus Wolffia are some of the fastest growing known plants on Earth. Wolffia have a reduced body plan, primarily multiplying through a budding type of asexual reproduction. Here, we generated draft reference genomes for Wolffia australiana (Benth.) Hartog & Plas, which has the smallest genome size in the genus at 357 Mb and has a reduced set of predicted protein-coding genes at about 15,000. Comparison between multiple high-quality draft genome sequences from W. australiana clones confirmed loss of several hundred genes that are highly conserved among flowering plants, including genes involved in root developmental and light signaling pathways. Wolffia has also lost most of the conserved nucleotide-binding leucine-rich repeat (NLR) genes that are known to be involved in innate immunity, as well as those involved in terpene biosynthesis, while having a significant overrepresentation of genes in the sphingolipid pathways that may signify an alternative defense system. Diurnal expression analysis revealed that only 13% of Wolffia genes are expressed in a time-of-day (TOD) fashion, which is less than the typical ∼40% found in several model plants under the same condition. In contrast to the model plants Arabidopsis and rice, many of the pathways associated with multicellular and developmental processes are not under TOD control in W. australiana, where genes that cycle the conditions tested predominantly have carbon processing and chloroplast-related functions. The Wolffia genome and TOD expression data set thus provide insight into the interplay between a streamlined plant body plan and optimized growth
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A wheat kinase and immune receptor form host-specificity barriers against the blast fungus
Since emerging in Brazil in 1985, wheat blast has spread throughout South America and recently appeared in Bangladesh and Zambia. Here we show that two wheat resistance genes, Rwt3 and Rwt4, acting as host-specificity barriers against non-Triticum blast pathotypes encode a nucleotide-binding leucine-rich repeat immune receptor and a tandem kinase, respectively. Molecular isolation of these genes will enable study of the molecular interaction between pathogen effector and host resistance genes
Characterization of defense responses against bacterial pathogens in duckweeds lacking EDS1
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The conservation and divergence of angiosperm immune signaling pathways
Achieving sufficient food production for a growing population is a major challenge that requires innovative solutions. One approach towards increasing crop yield is to reduce disease related losses. Plants have developed a sophisticated innate immune system to recognize pathogens and exert an effective immune response. Pathogen presence can result in intracellular changes which are sensed by nucleotide-binding leucine-rich repeat (NLR) proteins that subsequently trigger an immune response. NLRs belong to a complex gene family with diversity similar to the mammalian Major Histocompatibility Complex (MHC). While high allelic diversity is a common feature of NLR genes, NLR proteins fold into a conserved architecture consisting of a nucleotide-binding-domain (NB), leucine rich repeats (LRR), and commonly a coiled-coil (CC) or Toll-Interleukin-1 Receptor domain (TIR). Their conserved domain structure makes the gene family amenable to identification by bioinformatics. There are numerous cloned NLR genes, for which we understand their activation, redundancy, and specificity to various degrees. For each cloned NLR, there are many more NLRs that are yet to be studied. Furthermore, the downstream signaling enacted by these receptors, despite being highly conserved, is still poorly understood due to complex networks of positive and negative feedback loops between pathways. Established plant model systems were adopted for the study of plant immunity due to the large amount of community resources available and ease of genetics. However, traditional model plant species have often been difficult to utilise for studying immunity with discoveries often limited to large effect single copy hubs or pathogen specific receptors largely due to redundancy and complex interactions underlying counterintuitive phenotypes. An alternative approach to studying immunity is to apply the same techniques to systems with much reduced immune complexity, regardless of their model status. In doing so, the reduced redundancy could reveal receptor and signaling hubs with a disproportionate impact on the immune system. In order to focus on plant species with lower complexity immune pathways, it was necessary to catalogue the diversity in immune pathways across plant species. To do this, I compiled available genomes of plant species and investigated variation in the number of NLR receptors (Chapter 2). Those species with low numbers of NLRs proportional to the proteome size could be divided into two categories: those with genes known to be involved in classical immune signalling pathways (Chapter 2 & 3), and those without (Chapter 2 & 4). The independent loss of NLRs and signaling pathways across the plant phylogeny allowed prediction of co-occurring genes with classical immune pathways (Chapter 2). In all species we have studied thus far, we observed a strikingly conserved protein family called TIR-NBARC-like-β-propeller/TPRs (TNPs) present even in species without a classical immune pathway. However, no clear role in immunity was evident for TNPs when investigating their expression in model plant species, despite their similar architecture to NLRs (Chapter 3). The development of duckweed as a model for plant immunity allowed us to study an immune response in the absence of classical components of an immune signaling pathway (Chapter 4). This revealed the conservation of hormone and transcriptional control of the immune response and expansion of antimicrobial proteins. However, duckweed in controlled laboratory conditions was regularly killed by bacterial infections. To reconcile how duckweeds are a widespread invasive species, despite high susceptibility to disease in the laboratory, we studied the effect of duckweed inhabited pond water filtrates on disease resistance (Chapter 5). This led to the discovery of bacterial species in duckweeds' natural environment that can protect duckweeds from pathogen infection. Taken together, these studies reveal a picture of necessary components for a minimal immune system in plants, several candidates for signal pathway genes and atypical defence mechanisms
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Characterization of defense responses against bacterial pathogens in duckweeds lacking EDS1
ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1) mediates the induction of defense responses against pathogens in most angiosperms. However, it has recently been shown that a few species have lost EDS1. It is unknown how defense against disease unfolds and evolves in the absence of EDS1. We utilize duckweeds; a collection of aquatic species that lack EDS1, to investigate this question. We established duckweed-Pseudomonas pathosystems and used growth curves and microscopy to characterize pathogen-induced responses. Through comparative genomics and transcriptomics, we show that the copy number of infection-associated genes and the infection-induced transcriptional responses of duckweeds differ from other model species. Pathogen defense in duckweeds has evolved along different trajectories than in other plants, including genomic and transcriptional reprogramming. Specifically, the miAMP1 domain-containing proteins, which are absent in Arabidopsis, showed pathogen responsive upregulation in duckweeds. Despite such divergence between Arabidopsis and duckweed species, we found conservation of upregulation of certain genes and the role of hormones in response to disease. Our work highlights the importance of expanding the pool of model species to study defense responses that have evolved in the plant kingdom independent of EDS1
Convergent loss of an EDS1/PAD4 signaling pathway in several plant lineages reveals coevolved components of plant immunity and drought response
Plant innate immunity relies on nucleotide binding leucine-rich repeat receptors (NLRs) that recognize pathogen-derived molecules and activate downstream signaling pathways. We analyzed the variation in NLR gene copy number and identified plants with a low number of NLR genes relative to sister species. We specifically focused on four plants from two distinct lineages, one monocot lineage (Alismatales) and one eudicot lineage (Lentibulariaceae). In these lineages, the loss of NLR genes coincides with loss of the well-known downstream immune signaling complex ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)/PHYTOALEXIN DEFICIENT 4 (PAD4). We expanded our analysis across whole proteomes and found that other characterized immune genes were absent only in Lentibulariaceae and Alismatales. Additionally, we identified genes of unknown function that were convergently lost together with EDS1/PAD4 in five plant species. Gene expression analyses in Arabidopsis (Arabidopsis thaliana) and Oryza sativa revealed that several homologs of the candidates are differentially expressed during pathogen infection, drought, and abscisic acid treatment. Our analysis provides evolutionary evidence for the rewiring of plant immunity in some plant lineages, as well as the coevolution of the EDS1/PAD4 pathway and drought responses
The NLR-annotator tool enables annotation of the intracellular immune receptor repertoire
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 a detailed study of its NLR complement. However, low NLR expression and high intrafamily sequence homology hinder their accurate annotation. Here, we developed NLR-Annotator, a software tool for in silico NLR identification independent of transcript support. Although developed for wheat, we demonstrate the universal applicability of NLR-Annotator across diverse plant taxa. We applied our tool to wheat and combined it with a transcript-validated subset of genes from the reference gene annotation to characterize the structure, phylogeny, and expression profile of the NLR gene family. We detected 3,400 full-length NLR loci, of which 1,560 were confirmed as expressed genes with intact open reading frames. NLRs with integrated domains mostly group in specific subclades. Members of another subclade predominantly locate in close physical proximity to NLRs carrying integrated domains, suggesting a paired helper function. Most NLRs (88%) display low basal expression (in the lower 10 percentile of transcripts). In young leaves subjected to biotic stress, we found up-regulation of 266 of the NLRs To illustrate the utility of our tool for the positional cloning of resistance genes, we estimated the number of NLR genes within the intervals of mapped rust resistance genes. Our study will support the identification of functional resistance genes in wheat to accelerate the breeding and engineering of disease-resistant varieties