bioRxiv Science⌕ Search

bioRxiv · 10.1101/171868

Heterologous expression of the immune receptor EFR in Medicago truncatula reduces pathogenic infection, but not rhizobial symbiosis

Abstract

Interfamily transfer of plant pattern recognition receptors (PRRs) represents a promising biotechnological approach to engineer broad-spectrum, and potentially durable, disease resistance in crops. It is however unclear whether new recognition specificities to given pathogen-associated molecular patterns (PAMPs) affect the interaction of the recipient plant with beneficial microbes. To test this in a direct reductionist approach, we transferred the Brassicaceae-specific PRR ELONGATION FACTOR-THERMO UNSTABLE RECEPTOR (EFR) from Arabidopsis thaliana to the legume Medicago truncatula, conferring recognition of the bacterial EF-Tu protein. Constitutive EFR expression led to EFR accumulation and activation of immune responses upon treatment with the EF-Tu-derived elf18 peptide in leaves and roots. The interaction of M. truncatula with the bacterial symbiont Sinorhizobium meliloti is characterized by the formation of root nodules that fix atmospheric nitrogen. Although nodule numbers were slightly reduced at an early stage of the infection in EFR-Medicago when compared to control lines, nodulation was similar in all lines at later stages. Furthermore, nodule colonization by rhizobia, and nitrogen fixation were not compromised by EFR expression. Importantly, the M. truncatula lines expressing EFR were substantially more resistant to the root bacterial pathogen Ralstonia solanacearum. Our data suggest that the transfer of EFR to M. truncatula does not impede root nodule symbiosis, but has a positive impact on disease resistance against a bacterial pathogen. In addition, our results indicate that Rhizobium can either avoid PAMP recognition during the infection process, or is able to actively suppress immune signaling.\n\nSignificance StatementCrop engineering helps reducing the economic and environmental costs of plant disease. The genetic transfer of immune receptors across plant species is a promising biotechnological approach to increase disease resistance. Surface-localized pattern-recognition receptors (PRRs), which detect conserved characteristic microbial features, are functional in heterologous taxonomically-diverse plant species, and confer broad-spectrum disease resistance. It was unclear whether PRR transfer negatively impacts the association of the recipient plants with symbiotic microbes. Here, we show that a legume engineered with a novel PRR recognizing a conserved bacterial protein becomes more resistant to an important bacterial pathogen without significant impact on nitrogen-fixing symbiosis with rhizobia. This finding is of particular relevance as attempts to transfer this important symbiosis into non-legume plants are ongoing.

Explore related subjects

Keep this discovery

Explore connections, maps & timelines

BibTeXRIS

Pfeilmeier, S., George, J., Morel, A., Roy, S., Smoker, M., Stansfeld, L., Downie, A., Peeters, N., Malone, J., Zipfel, C.. 2017-08-02. Heterologous expression of the immune receptor EFR in Medicago truncatula reduces pathogenic infection, but not rhizobial symbiosis. https://doi.org/10.1101/171868

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

Specialisation of photosynthetic biochemistry in C4 chloroplasts potentiates distinct cell-specific functionality of different chloroplast-to-nucleus retrograde signalling pathways.

Chloroplasts are key environmental sensors for plant cells. Upon exposure to abiotic stresses such as excess sunlight and heat, reactive oxygen species (ROS) in chloroplasts are sensed to trigger chloroplast-to-nucleus signalling pathways for acclimatory nuclear gene expression. There is extensive biochemical- and cell type-specialisation of chloroplasts, such as those in heat-resilient plants performing C4 photosynthesis, but how these specialisations intersect with chloroplast-to-nucleus signalling remains unclear. Here we show that specific chloroplast-to-nucleus signalling networks are functional in specialised leaf cell types of the C4 model species, Setaria viridis. RNA-sequencing, electron paramagnetic resonance (EPR) spectroscopy and metabolomics on cell type-enriched fractions, complemented with mutant analyses provided evidence for cell-specific enrichment of chloroplast-to-nucleus retrograde signalling pathways correlating with the photosynthetic specialisation in these cell types. Singlet oxygen (1O2)-responsive beta-cyclocitral ({beta}-CC) /dihydroactinidiolide (DHA) signalling and hydrogen peroxide (H2O2)-responsive 3'-phosphoadenosine 5'-phosphate (PAP) signalling pathways were specific to mesophyll cells, in line with enrichment of photosystem II and linear electron flow to photosystem I, respectively in this cell type. In contrast, bundle sheath cells were enriched for the rapid, ROS-independent retrograde signalling pathway mediated by the Calvin cycle product, dihydroxyacetone phosphate (DHAP), consistent with the exclusive localisation of the Calvin cycle to C4 bundle sheath cells. Taken together, our results provide insights into how chloroplast- and cell type-specialisation intersect with stress signalling in plant cells and identify photosynthetic biochemistry as a key driver of cell-specific cellular signalling.

plant biology↗

The periplasmic substrate-binding protein ThuE is required for sucrose uptake and multiplication of Pseudomonas syringae pv. tomato DC3000 in tomato leaves

Phytopathogenic bacteria depend on host-derived carbon for successful colonization of plant tissue. While sucrose is among the most abundant sugars in the leaf apoplast, the steps that limit its acquisition by Pseudomonas syringae are not known. In this study, we used base editing to generate mutants of six candidate sucrose utilization genes in P. syringae pv. tomato DC3000 (Pto). Loss of either the sucrose hydrolase ScrB or both levansucrases had no detectable effect, whereas the growth defect in the loss of the outer membrane porin mutant scry was overcome by raising external sucrose. Loss of the periplasmic substrate-binding protein ThuE impaired growth both in vitro and in planta, reducing bacterial populations to approximately two orders of magnitude lower in tomato leaves. Sucrose import through a single non-redundant inner membrane ABC transporter is therefore required for Pto multiplication in planta and serves as a potential target for controlling bacterial speck disease.

plant biology↗

Spatial expression evolution of duplicated genes post-whole genome duplication in cultivated tomato

The mechanisms by which whole genome duplication contributes to expression divergence of duplicate genes, which can impact the evolution of form and function, has been a long-standing question in evolutionary biology. We compared expression patterns of paralogs derived from the most recent Solanaceae-specific genome triplication event across 23 tissues and inferred ancestral expression states to investigate patterns of expression evolution. While the partitioning of ancestral expression states is traditionally considered the second most common (after the gene loss) trajectory of duplicate expression evolution, we found that the ancestral expression states tended to be retained by most (~66%) duplicates, with ~6% of gene lineages experiencing expression gain events and ~20% experiencing expression losses. The genes that gained expression in fruit tissues are significantly enriched with functions associated with fruit quality. Notably, asymmetrical expression divergence is prevalent among duplicates, especially when ancestral genes were either not expressed or were highly expressed. Our study demonstrates the utility of integrating paralog expression comparisons with phylogenetic analyses to document the potential evolutionary history of spatial expression patterns and gain insight into how expression divergence contributes to the evolution of function across tissues.

plant biology↗