Host-Microbe Interactions. Plant Biology.
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A deadly dance: the choreography of host–pathogen interactions, as revealed by single-cell technologies

A deadly dance: the choreography of host–pathogen interactions, as revealed by single-cell technologies | Host-Microbe Interactions. Plant Biology. | Scoop.it
Diane Bolton and colleagues review the impact of single-cell technologies on the study of host–pathogen interaction. They discuss the revolutionary impact these have had for facilitating a greater understanding of the properties of host cells harbouring infection, the pathogen-specific immune responses, and the mechanisms pathogens have evolved to escape host control.
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Arabidopsis thaliana NGATHA1 transcription factor induces ABA biosynthesis by activating NCED3 gene during dehydration stress

Arabidopsis thaliana NGATHA1 transcription factor induces ABA biosynthesis by activating NCED3 gene during dehydration stress | Host-Microbe Interactions. Plant Biology. | Scoop.it
The plant hormone abscisic acid (ABA) is essential for drought-stress responses in plants, and its functions have been well studied; however, the detailed molecular mechanisms of ABA biosynthesis during early drought stress need to be further explored. The present study identified a transcription factor, NGTHA1 (NGA1), which positively regulates ABA accumulation during dehydration stress by activating the NCED3 gene encoding a key ABA biosynthetic enzyme. We also identified a cis -acting element bound by NGA1 in the 5′ untranslated region (5′ UTR) of the NCED3 promoter. The NGA1 protein was degraded under nonstressed conditions, but it was stabilized during dehydration stress in an ABA-independent pathway.

The plant hormone abscisic acid (ABA) is accumulated after drought stress and plays critical roles in the responses to drought stress in plants, such as gene regulation, stomatal closure, seed maturation, and dormancy. Although previous reports revealed detailed molecular roles of ABA in stress responses, the factors that contribute to the drought-stress responses—in particular, regulation of ABA accumulation—remain unclear. The enzyme NINE-CIS-EPOXYCAROTENOID DIOXYGENASE 3 (NCED3) is essential for ABA biosynthesis during drought stress, and the NCED3 gene is highly induced by drought stress. In the present study, we isolated NGATHAs (NGAs) as candidate transcriptional regulators of NCED3 through a screen of a plant library harboring the transcription factors fused to a chimeric repressor domain, SRDX. The NGA proteins were directly bound to a cis -element NGA-binding element (NBE) in the 5′ untranslated region (5′ UTR) of the NCED3 promoter and were suggested to be transcriptional activators of NCED3 . Among the single-knockout mutants of four NGA family genes, we found that the NGATHA1 ( NGA1 ) knockout mutant was drought-stress-sensitive with a decreased expression level of NCED3 during dehydration stress. These results suggested that NGA1 essentially functions as a transcriptional activator of NCED3 among the NGA family proteins. Moreover, the NGA1 protein was degraded under nonstressed conditions, and dehydration stress enhanced the accumulation of NGA1 proteins, even in ABA-deficient mutant plants, indicating that there should be ABA-independent posttranslational regulations. These findings emphasize the regulatory mechanisms of ABA biosynthesis during early drought stress.
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Gene-guided discovery and engineering of branched cyclic peptides in plants

Gene-guided discovery and engineering of branched cyclic peptides in plants | Host-Microbe Interactions. Plant Biology. | Scoop.it
In the past decade, the number of publicly available plant genomes and transcriptomes has steadily increased. Inspired by this genetic resource, we developed a genome-mining approach for the rapid discovery of plant ribosomal peptides from genome-sequenced plants. Herein, we introduce the hypotensive lyciumins as a class of branched cyclic ribosomal peptides in plants and show that they are widely distributed in crop and forage plants. Our results suggest that lyciumin biosynthesis is coupled to plant-specific BURP domains in their precursor peptides and that lyciumin peptide libraries can be generated in planta . This discovery sets the stage for gene-guided discovery of peptide chemistry in the plant kingdom and therapeutic and agrochemical applications of lyciumins.

The plant kingdom contains vastly untapped natural product chemistry, which has been traditionally explored through the activity-guided approach. Here, we describe a gene-guided approach to discover and engineer a class of plant ribosomal peptides, the branched cyclic lyciumins. Initially isolated from the Chinese wolfberry Lycium barbarum , lyciumins are protease-inhibiting peptides featuring an N-terminal pyroglutamate and a macrocyclic bond between a tryptophan-indole nitrogen and a glycine α-carbon. We report the identification of a lyciumin precursor gene from L. barbarum , which encodes a BURP domain and repetitive lyciumin precursor peptide motifs. Genome mining enabled by this initial finding revealed rich lyciumin genotypes and chemotypes widespread in flowering plants. We establish a biosynthetic framework of lyciumins and demonstrate the feasibility of producing diverse natural and unnatural lyciumins in transgenic tobacco. With rapidly expanding plant genome resources, our approach will complement bioactivity-guided approaches to unlock and engineer hidden plant peptide chemistry for pharmaceutical and agrochemical applications.
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BIG regulates stomatal immunity and jasmonate production in Arabidopsis

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Specific recognition of two MAX effectors by integrated HMA domains in plant immune receptors involves distinct binding surfaces

Specific recognition of two MAX effectors by integrated HMA domains in plant immune receptors involves distinct binding surfaces | Host-Microbe Interactions. Plant Biology. | Scoop.it
In this study, we provide insight into the mechanism of effector recognition by plant nucleotide-binding domain and leucine-rich repeat proteins (NLRs), a ubiquitous class of immune receptors that plays a central role in crop protection. By structural and functional analysis of a complex between a fungal effector and an integrated decoy domain (ID) from a rice NLR, we demonstrate the importance of IDs in effector recognition and generate crucial knowledge for future engineering of NLRs to expand their recognition specificities. In addition, we propose, as a hypothesis regarding the diversity of fungal effectors, that in structurally conserved effector families, the molecular mechanisms of host target protein-binding are conserved but not the host target proteins themselves.

The structurally conserved but sequence-unrelated MAX ( Magnaporthe oryzae avirulence and ToxB-like) effectors AVR1-CO39 and AVR-PikD from the blast fungus M. oryzae are recognized by the rice nucleotide-binding domain and leucine-rich repeat proteins (NLRs) RGA5 and Pikp-1, respectively. This involves, in both cases, direct interaction of the effector with a heavy metal-associated (HMA) integrated domain (ID) in the NLR. Here, we solved the crystal structures of a C-terminal fragment of RGA5 carrying the HMA ID (RGA5_S), alone, and in complex with AVR1-CO39 and compared it to the structure of the Pikp1HMA/AVR-PikD complex. In both complexes, HMA ID/MAX effector interactions involve antiparallel alignment of β-sheets from each partner. However, effector-binding occurs at different surfaces in Pikp1HMA and RGA5HMA, indicating that these interactions evolved independently by convergence of these two MAX effectors to the same type of plant target proteins. Interestingly, the effector-binding surface in RGA5HMA overlaps with the surface that mediates RGA5HMA self-interaction. Mutations in the HMA-binding interface of AVR1-CO39 perturb RGA5HMA-binding, in vitro and in vivo, and affect the recognition of M. oryzae in a rice cultivar containing Pi-CO39 . Our study provides detailed insight into the mechanisms of effector recognition by NLRs, which has substantial implications for future engineering of NLRs to expand their recognition specificities. In addition, we propose, as a hypothesis for the understanding of effector diversity, that in the structurally conserved MAX effectors the molecular mechanism of host target protein-binding is conserved rather than the host target proteins themselves.
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Gene expression variability across cells and species shapes innate immunity

Gene expression variability across cells and species shapes innate immunity | Host-Microbe Interactions. Plant Biology. | Scoop.it
Comparison of transcriptomic data from immune-stimulated cells across different species sheds light on the architecture of the innate immune response.
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Holo-Seq: single-cell sequencing of holo-transcriptome

Holo-Seq: single-cell sequencing of holo-transcriptome | Host-Microbe Interactions. Plant Biology. | Scoop.it
Current single-cell RNA-seq approaches are hindered by preamplification bias, loss of strand of origin information, and the inability to observe small-RNA and mRNA dual transcriptomes. Here
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Classifying cells with Scasat, a single-cell ATAC-seq analysis tool | Nucleic Acids Research | Oxford Academic

Classifying cells with Scasat, a single-cell ATAC-seq analysis tool | Nucleic Acids Research | Oxford Academic | Host-Microbe Interactions. Plant Biology. | Scoop.it
Abstract. ATAC-seq is a recently developed method to identify the areas of open chromatin in a cell. These regions usually correspond to active regulatory elem
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Discovery of RNA-binding proteins and characterization of their dynamic responses by enhanced RNA interactome capture

Discovery of RNA-binding proteins and characterization of their dynamic responses by enhanced RNA interactome capture | Host-Microbe Interactions. Plant Biology. | Scoop.it
RNA interactome capture allows the detailed investigation of RNA-bound proteomes. Here the authors describe enhanced RNA-interactome capture using LNA-modified probes for increased sensitivity and specificity.
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Affinity capture of polyribosomes followed by RNAseq (ACAPseq), a discovery platform for protein-protein interactions

Affinity capture of polyribosomes followed by RNAseq (ACAPseq), a discovery platform for protein-protein interactions | Host-Microbe Interactions. Plant Biology. | Scoop.it
Affinity capture of polyribosomes followed by RNAseq(ACAPSeq) is a technique that harnesses massively parallel sequencing to identify protein-protein interactions from any source from which polyribosomes can be purified.
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Transcriptional Regulation of the Immune Receptor FLS2 Controls the Ontogeny of Plant Innate Immunity

Transcriptional Regulation of the Immune Receptor FLS2 Controls the Ontogeny of Plant Innate Immunity | Host-Microbe Interactions. Plant Biology. | Scoop.it
Innate immunity plays a vital role in protecting plants and animals from pathogen infections. Immunity varies with age in both animals and plants. However, little is known about the ontogeny of plant innate immunity during seedling development. We report here that the Arabidopsis thaliana microRNA miR172b regulates the transcription of the immune receptor gene FLAGELLIN-SENSING 2 (FLS2) through TARGET OF EAT1 (TOE1) and TOE2, which directly bind to the FLS2 promoter and inhibit its activity. The level of miR172b is very low in the early stage of seedling development, but increases over time, which results in decreased TOE½ protein accumulation and, consequently, increased FLS2 transcription and the ontogeny of FLS2-mediated immunity during seedling development. Our study reveals a role for the miR172b-TOE½ module in regulating plant innate immunity, and elucidates a regulatory mechanism underlying the ontogeny of plant innate immunity.
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Daily humidity oscillation regulates the circadian clock to influence plant physiology

Daily humidity oscillation regulates the circadian clock to influence plant physiology | Host-Microbe Interactions. Plant Biology. | Scoop.it
Humidity has been shown to influence many aspects of plant physiology. Here Mwimba et al. show that oscillating humidity entrains the circadian clock under constant light conditions and enhances clock amplitude in simulated natural environments, while also improving immunity and overall growth.
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Molecular, spatial and functional single-cell profiling of the hypothalamic preoptic region

Molecular, spatial and functional single-cell profiling of the hypothalamic preoptic region | Host-Microbe Interactions. Plant Biology. | Scoop.it
The hypothalamus controls essential social behaviors and homeostatic functions. However, the cellular architecture of hypothalamic nuclei, including the molecular identity, spatial organization, and function of distinct cell types, is poorly understood. Here, we developed an imaging-based in situ cell type identification and mapping method and combined it with single-cell RNA-sequencing to create a molecularly annotated and spatially resolved cell atlas of the mouse hypothalamic preoptic region. We profiled ~1 million cells, identified ~70 neuronal populations characterized by distinct neuromodulatory signatures and spatial organizations, and defined specific neuronal populations activated during social behaviors in male and female mice, providing a high-resolution framework for mechanistic investigation of behavior circuits. The approach described opens a new avenue for the construction of cell atlases in diverse tissues and organisms.
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Experimental evolution of a fungal pathogen into a gut symbiont

Experimental evolution of a fungal pathogen into a gut symbiont | Host-Microbe Interactions. Plant Biology. | Scoop.it
Fungi, such as Candida albicans , are found in the mammalian gut, but we know little about what they are doing there. Tso et al. put C. albicans under evolutionary pressure by serial passage in mice that were treated with antibiotics and were thus lacking gut bacteria (see the Perspective by d'Enfert). Passage accelerated fungal mutation, especially around the FLO8 gene, resulting in low-virulence phenotypes unable to form hyphae. Nevertheless, these phenotypes stimulated proinflammatory cytokines and conferred transient cross-protection against several other gut inhabitants. However, if an intact microbiota was present, only the virulent hyphal forms persisted.

Science , this issue p. [589][1]; see also p. [523][2]

Gut microbes live in symbiosis with their hosts, but how mutualistic animal-microbe interactions emerge is not understood. By adaptively evolving the opportunistic fungal pathogen Candida albicans in the mouse gastrointestinal tract, we selected strains that not only had lost their main virulence program but also protected their new hosts against a variety of systemic infections. This protection was independent of adaptive immunity, arose as early as a single day postpriming, was dependent on increased innate cytokine responses, and was thus reminiscent of “trained immunity.” Because both the microbe and its new host gain some advantages from their interaction, this experimental system might allow direct study of the evolutionary forces that govern the emergence of mutualism between a mammal and a fungus.

[1]: /lookup/doi/10.1126/science.aat0537
[2]: /lookup/doi/10.1126/science.aav3374
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Multi-omics at single-cell resolution: comparison of experimental and data fusion approaches

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Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota

Plant-Derived Exosomal MicroRNAs Shape the Gut Microbiota | Host-Microbe Interactions. Plant Biology. | Scoop.it
Teng et al. show that exosome-like nanoparticles (ELNs) from edible plants such as
ginger are preferentially taken up by gut bacteria in an ELN lipid-dependent manner.
ELN RNAs regulate gut microbiota composition and localization as well as host physiology,
notably enhancing gut barrier function to alleviate colitis.
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The human gut microbiome in early-onset type 1 diabetes from the TEDDY study

The human gut microbiome in early-onset type 1 diabetes from the TEDDY study | Host-Microbe Interactions. Plant Biology. | Scoop.it
An analysis of more than 10,000 metagenomes from the TEDDY study provides a detailed functional profile of the gut microbiome in relation to islet autoimmunity, and supports the protective effects of short-chain fatty acids in early-onset type 1 diabetes.
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Transcriptional regulation of nitrogen-associated metabolism and growth

Transcriptional regulation of nitrogen-associated metabolism and growth | Host-Microbe Interactions. Plant Biology. | Scoop.it
The yeast one-hybrid network for nitrogen-associated metabolism in Arabidopsis reveals the transcription factors that regulate the architecture of root and shoot systems under conditions of changing nitrogen availability.
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Single-molecule DNA-mapping and whole-genome sequencing of individual cells

Single-molecule DNA-mapping and whole-genome sequencing of individual cells | Host-Microbe Interactions. Plant Biology. | Scoop.it
We report optical mapping of DNA from a single cell. Notably, we demonstrate isolation of single cells, DNA extraction, and optical mapping, all within a single integrated micro-/nanofluidic device. Single-cell optical mapping is less complex than sequencing, which we performed after whole-genome amplification of DNA extracted from a single cell isolated on-chip. In some cases, optical mapping was more efficient than sequencing at detecting structural variation. As single-cell analysis can address genomic heterogeneity within a tumor, it may prove useful for the selection of cancer therapies. Thus, optical mapping of the long-range features of single-cell genomes and sequencing of the short-range features may become complementary tools for the analysis of tumors.

To elucidate cellular diversity and clonal evolution in tissues and tumors, one must resolve genomic heterogeneity in single cells. To this end, we have developed low-cost, mass-producible micro-/nanofluidic chips for DNA extraction from individual cells. These chips have modules that collect genomic DNA for sequencing or map genomic structure directly, on-chip, with denaturation–renaturation (D-R) optical mapping [Marie R, et al. (2013) Proc Natl Acad Sci USA 110:4893–4898]. Processing of single cells from the LS174T colorectal cancer cell line showed that D-R mapping of single molecules can reveal structural variation (SV) in the genome of single cells. In one experiment, we processed 17 fragments covering 19.8 Mb of the cell’s genome. One megabase-large fragment aligned well to chromosome 19 with half its length, while the other half showed variable alignment. Paired-end single-cell sequencing supported this finding, revealing a region of complexity and a 50-kb deletion. Sequencing struggled, however, to detect a 20-kb gap that D-R mapping showed clearly in a megabase fragment that otherwise mapped well to the reference at the pericentromeric region of chromosome 4. Pericentromeric regions are complex and show substantial sequence homology between different chromosomes, making mapping of sequence reads ambiguous. Thus, D-R mapping directly, from a single molecule, revealed characteristics of the single-cell genome that were challenging for short-read sequencing.
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JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis

JAZ repressors of metabolic defense promote growth and reproductive fitness in Arabidopsis | Host-Microbe Interactions. Plant Biology. | Scoop.it
The plant hormone jasmonate promotes resistance to plant-eating organisms, ranging from pathogenic microbes to mammals. Jasmonate reprograms metabolism to fuel the production of diverse defense compounds and simultaneously inhibits plant growth. Understanding how growth is influenced across a range of defense levels remains unclear, but has important implications for optimizing crop productivity. Using a genetic approach to “tune” the jasmonate response, we assessed the physiological consequences of discrete levels of defense throughout the plant life cycle. Overactivation of jasmonate response led to carbon starvation, near loss of seed production and, under extreme conditions, lethality. Our findings explain the emergence of diverse strategies to keep jasmonate responses at bay and provide new insights into metabolic processes that underlie growth–defense trade-offs.

Plant immune responses mediated by the hormone jasmonoyl-l-isoleucine (JA-Ile) are metabolically costly and often linked to reduced growth. Although it is known that JA-Ile activates defense responses by triggering the degradation of JASMONATE ZIM DOMAIN (JAZ) transcriptional repressor proteins, expansion of the JAZ gene family in vascular plants has hampered efforts to understand how this hormone impacts growth and other physiological tasks over the course of ontogeny. Here, we combined mutations within the 13-member Arabidopsis JAZ gene family to investigate the effects of chronic JAZ deficiency on growth, defense, and reproductive output. A higher-order mutant ( jaz decuple, jazD ) defective in 10 JAZ genes ( JAZ1 – 7 , -9 , -10 , and -13 ) exhibited robust resistance to insect herbivores and fungal pathogens, which was accompanied by slow vegetative growth and poor reproductive performance. Metabolic phenotypes of jazD discerned from global transcript and protein profiling were indicative of elevated carbon partitioning to amino acid-, protein-, and endoplasmic reticulum body-based defenses controlled by the JA-Ile and ethylene branches of immunity. Resource allocation to a strong defense sink in jazD leaves was associated with increased respiration and hallmarks of carbon starvation but no overt changes in photosynthetic rate. Depletion of the remaining JAZ repressors in jazD further exaggerated growth stunting, nearly abolished seed production and, under extreme conditions, caused spreading necrotic lesions and tissue death. Our results demonstrate that JAZ proteins promote growth and reproductive success at least in part by preventing catastrophic metabolic effects of an unrestrained immune response.
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Chromatin run-on and sequencing maps the transcriptional regulatory landscape of glioblastoma multiforme

Chromatin run-on and sequencing (ChRO-seq) is a new method that maps the location of RNA polymerase using virtually any input sample. Here, ChRO-seq is used to study nascent transcription in human glioblastoma, and to identify regulators of tumor subtype.
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Single-molecule nascent RNA sequencing identifies regulatory domain architecture at promoters and enhancers

Sequencing nascent RNAs at single-molecule resolution with CoPRO unravels the interplay between Pol II initiation, capping and pausing. Transcription start site clusters provide a framework for understanding genome regulatory architecture.
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Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors

Distinct modes of derepression of an Arabidopsis immune receptor complex by two different bacterial effectors | Host-Microbe Interactions. Plant Biology. | Scoop.it
Plants and animals carry intracellular nucleotide-binding leucine-rich repeat (NLR) immune receptors. How NLR receptors activate defense on perceiving pathogen molecules is poorly understood, especially in plants. Some NLRs function in pairs, with one NLR carrying a domain that mimics a pathogen effector target. Effector action on this domain activates the second “helper” NLR. In the Arabidopsis RPS4 and RRS1 pair, RRS1 carries a WRKY transcription factor domain targeted by bacterial effectors AvrRps4 and PopP2. We monitored conformational changes in RPS4–RRS1 during activation and developed a “molecular padlock” to reversibly restrict such changes. This revealed domains within RRS1 required to keep the RRS1–RPS4 complex inactive prior to effector detection, and specific domain–domain interactions whose disruption or modification contributes to defense activation.
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Real-Time Genetic Compensation Defines the Dynamic Demands of Feedback Control

Real-Time Genetic Compensation Defines the Dynamic Demands of Feedback Control | Host-Microbe Interactions. Plant Biology. | Scoop.it
An optogenetics-based method is developed to explore the temporal requirements for
a gene product to produce a dynamic phenotype.
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