Regulatory non-coding RNAs are emerging as key players in host–pathogen interactions. Small RNAs such as microRNAs are implicated in regulating plant transcripts involved in immunity and defence. Surprisingly, RNAs with silencing properties can be translocated from plant hosts to various invading pathogens and pests. Small RNAs are now confirmed virulence factors, with the first report of fungal RNAs that travel to host cells and hijack post-transcriptional regulatory machinery to suppress host defence. Here, we argue that trans-organism movement of RNAs represents a common mechanism of control in diverse interactions between plants and other eukaryotes. We suggest that extracellular vesicles are the key to such RNA movement events. Plant pathosystems serve as excellent experimental models to dissect RNA ‘information warfare’ and other RNA-mediated interactions.
Trends Plant–pathogen interactions have undergone a paradigm shift, with the observation that silencing, non-coding RNAs move between host and pathogen, and vice versa.
So far, only one unequivocal natural example of this phenomenon has been exposed, where RNAs from Botrytis cinerea (grey mould) move into host plants. There, they ‘hijack’ host silencing machinery to downregulate transcripts involved in defence and immunity.
Similar RNA-based phenomena in interactions between animals and their microbial pathogens suggest that this mechanism is a commonality between infections in widely divergent taxa.
As well as a potent tool for developing new crops with increased disease resistance, studies of RNA traffic between plants and their symbionts will serve as models for other disease interactions.
The C4 photosynthetic pathway evolved to allow efficient CO2 capture by plants where effective carbon supply may be limiting as in hot or dry environments, explaining the high growth rates of C4 plants such as maize.
Effectors secreted by the type III secretion system are essential for bacterial pathogenesis. Members of the Yersinia outer-protein J (YopJ) family of effectors found in diverse plant and animal pathogens depend on a protease-like catalytic triad to acetylate host proteins and produce virulence. However, the structural basis for this noncanonical acetyltransferase activity remains unknown. Here, we report the crystal structures of the YopJ effector HopZ1a, produced by the phytopathogen Pseudomonas syringae, in complex with the eukaryote-specific cofactor inositol hexakisphosphate (IP6) and/or coenzyme A (CoA). Structural, computational and functional characterizations reveal a catalytic core with a fold resembling that of ubiquitin-like cysteine proteases and an acetyl-CoA-binding pocket formed after IP6-induced structural rearrangements. Modeling-guided mutagenesis further identified key IP6-interacting residues of Salmonella effector AvrA that are required for acetylating its substrate. Our study reveals the structural basis of a novel class of acetyltransferases and the conserved allosteric regulation of YopJ effectors by IP6.
Cereals form complex root systems composed of different root types. Lateral root formation is a major determinant of root architecture and is instrumental for the efficient uptake of water and nutrients. Positioning and patterning of lateral roots and cell types involved in their formation are unique in monocot cereals. Recent discoveries advanced the molecular understanding of the intrinsic genetic control of initiation and elongation of lateral roots in cereals by distinct, in part root-type-speciﬁc genetic programs. Moreover, molecular networks modulating the plasticity of lateral root formation in response to water and nutrient availability and arbuscular mycorrhizal fungal colonization have been identified. These novel discoveries provide a better mechanistic understanding of postembryonic lateral root development in cereals. Trends
Lateral root formation in cereals is unique with respect to the involved cell types, their position relative to the vascular elements, their stochastic pattern of emergence and their root-type specificity.
Genetic analyses demonstrated that auxin signal transduction, polar auxin transport, auxin transport regulation and cell cycle regulation are key elements of lateral root formation in cereals.
High resolution tissue- and cell-type-specific transcriptome studies identified candidate genes and metabolic pathways associated with lateral root initiation in cereals.
Architectural remodeling of lateral root branching contributes largely to the adaptive plasticity of the root system in response to extrinsic abiotic and biotic factors such as water availability, nutrients status and interaction with arbuscular mycorrhizal fungi.
Leaf rust is one of the most important diseases of wheat and is caused by Puccinia triticina, a highly variable rust pathogen prevalent worldwide. Decoding the genome of this pathogen will help in unraveling the molecular basis of its evolution and in the identification of genes responsible for its various biological functions. We generated high quality draft genome sequences (approximately 100- 106 Mb) of two races of P. triticina; the variable and virulent Race77 and the old, avirulent Race106. The genomes of races 77 and 106 had 33X and 27X coverage, respectively. We predicted 27678 and 26384 genes, with average lengths of 1,129 and 1,086 bases in races 77 and 106, respectively and found that the genomes consisted of 37.49% and 39.99% repetitive sequences. Genome wide comparative analysis revealed that Race77 differs substantially from Race106 with regard to segmental duplication (SD), repeat element, and SNP/InDel characteristics. Comparative analyses showed that Race 77 is a recent, highly variable and adapted Race compared with Race106. Further sequence analyses of 13 additional pathotypes of Race77 clearly differentiated the recent, active and virulent, from the older pathotypes. Average densities of 2.4 SNPs and 0.32 InDels per kb were obtained for all P. triticina pathotypes. Secretome analysis demonstrated that Race77 has more virulence factors than Race 106, which may be responsible for the greater degree of adaptation of this pathogen. We also found that genes under greater selection pressure were conserved in the genomes of both races, and may affect functions crucial for the higher levels of virulence factors in Race77. This study provides insights into the genome structure, genome organization, molecular basis of variation, and pathogenicity of P. triticina. The genome sequence data generated in this study have been submitted to public domain databases and will be an important resource for comparative genomics studies of the more than 4000 existing Puccinia species.
Arabidopsis thaliana serves as a model organism for the study of fundamental physiological, cellular, and molecular processes. It has also greatly advanced our understanding of intraspecific genome variation. We present a detailed map of variation in 1,135 high-quality re-sequenced natural inbred lines representing the native Eurasian and North African range and recently colonized North America. We identify relict populations that continue to inhabit ancestral habitats, primarily in the Iberian Peninsula. They have mixed with a lineage that has spread to northern latitudes from an unknown glacial refugium and is now found in a much broader spectrum of habitats. Insights into the history of the species and the fine-scale distribution of genetic diversity provide the basis for full exploitation of A. thaliana natural variation through integration of genomes and epigenomes with molecular and non-molecular phenotypes.
Magnus Nordborg and colleagues report a genomic analysis of all 27 known species in the genus Arabidopsis. They find evidence for a complex speciation history that is not accurately reflected by a traditional bifurcating species tree and identify widespread shared polymorphisms between species.
Programmed cell death (PCD) is a conserved process among eukaryotes that serves a multitude of functional roles during an organism’s natural life cycle. PCD involves the tightly regulated process of cell death cued by specific spatiotemporal stimuli, which confer survival benefits. In eukaryotes, PCD is an essential process involved in senescence, aging, embryo development, cell differentiation, and immunity. In animal systems, morphologically distinct forms of PCD have been described (Figure 1) [1, 2]. Type I, or apoptotic cell death, is the best understood form of PCD and is defined by cell shrinkage, nuclear condensation and fragmentation, and eventual disintegration of the cell into apoptotic bodies that are digested by phagocytes. Type II cell death is an autophagic process that is induced during nutrient deprivation and chronic stress. Autophagic cell death is characterized by the rupture of the lysosome and subsequent release of toxic chemicals that degrade the cell contents. Unlike type I and type II, type III PCD is distinguished by the swelling of organelles and subsequent rupture of the plasma membrane. A programmed necrosis or necroptosis was initially believed to be an uncontrolled process of necrosis, but has been recently reclassified as type III form of cell death. Finally, pyroptosis is another recently categorized form of cell death that is mediated by caspase-1 activity. Morphologically, pyroptotic cells share characteristics of both apoptosis and necrosis . Noteworthy, necroptosis and pyroptosis are pro-inflammatory forms of PCD activated by microbial infections and diverse environmental stimuli.
In plants, PCD is less rigorously classified (Figure 1). One difficulty in distinguishing the forms of PCD in plants and animals comes as a result of the different cellular morphology in plant cells — most notably the presence of the cell wall and chloroplasts. Unlike the plasma membrane, the degradation of the cell wall is not a universal feature of PCD in plants. Additionally, the formation of apoptotic bodies is not observed in plant cells, as there are no circulating phagocytes to engulf them . Instead, plant cells committed to PCD release autolytic compounds stored in the vacuole that degrade cell contents. In these cases, the cell wall may develop perforations for the absorption and recycling of cellular components by neighboring cells. Although not as well characterized as the mitochondria, the chloroplasts have been shown to induce light-dependent PCD through singlet oxygen species (1O2) that may function in parallel to mitochondrial-mediated PCD at an early step in initiating the rupture of the vacuole .
A specialized form of plant cell death called hypersensitive response (HR) is initiated as a defense response to pathogen infection. HR shares morphological features and molecular mechanisms reminiscent of both pyroptosis and necroptosis . Moreover, HR is unique in that it induces a signaling cascade to propagate immunity in neighboring cells as well as priming distal tissues for potential pathogen challenge, a phenomenon known as systemic acquired resistance . Here we will briefly describe diverse plant disease resistance pathways, early molecular events during pathogen perception, and downstream signaling components. We will thoroughly discuss how pathogens have evolved strategies to circumvent and/or suppress diverse immune responses, in particular plant cell death. While many of these mechanisms involve indirect disabling of upstream immune responses to avoid cell death, direct manipulation of PCD regulators by pathogen effectors has not been extensively explored in the literature, and will be the focal point of this article.
In recent history, mutagenesis, selection, and breeding of crop varieties have significantly improved agricultural traits and increased yields, for example, the renowned Green Revolution work on control of plant stature. Early in the 1990s, transgenic technologies were transformative to commercial crop agriculture by adding foreign DNA to improve plant traits. The transgenic methods traditionally used for crop improvement have many limitations, including random insertions, potential silencing, and varied gene expression. Transgenic methods also do not exploit the full potential of the genetic repertoire of the plant species targeted for improvement. Moreover, there remain dogged public concerns on consuming food from transgenic plants, “GMOs,” especially those with genes from distantly related organisms. Nonetheless, crop improvement and basic research have greatly benefitted from targeted modification of plant genomes. In this special issue (SI), which includes eight reviews, two opinion papers, and four original articles, the development of targeted genome editing approaches in higher plants is discussed from various perspectives, including research, intellectual property, regulatory affairs, and consumer acceptance issues.
We show that the genomes of maize, sorghum, and brachypodium contain genes that, when transformed into rice, confer resistance to rice blast disease. The genes are resistance genes (R genes) that encode proteins with nucleotide-binding site (NBS) and leucine-rich repeat (LRR) domains (NBS–LRR proteins). By using criteria associated with rapid molecular evolution, we identified three rapidly evolving R-gene families in these species as well as in rice, and transformed a randomly chosen subset of these genes into rice strains known to be sensitive to rice blast disease caused by the fungus Magnaporthe oryzae. The transformed strains were then tested for sensitivity or resistance to 12 diverse strains of M. oryzae. A total of 15 functional blast R genes were identified among 60 NBS–LRR genes cloned from maize, sorghum, and brachypodium; and 13 blast R genes were obtained from 20 NBS–LRR paralogs in rice. These results show that abundant blast R genes occur not only within species but also among species, and that the R genes in the same rapidly evolving gene family can exhibit an effector response that confers resistance to rapidly evolving fungal pathogens. Neither conventional evolutionary conservation nor conventional evolutionary convergence supplies a satisfactory explanation of our findings. We suggest a unique mechanism termed “constrained divergence,” in which R genes and pathogen effectors can follow only limited evolutionary pathways to increase fitness. Our results open avenues for R-gene identification that will help to elucidate R-gene vs. effector mechanisms and may yield new sources of durable pathogen resistance.
Sensitivity to variability in resources has been documented in humans, primates, birds, and social insects, but the fit between empirical results and the predictions of risk sensitivity theory (RST), which aims to explain this sensitivity in adaptive terms, is weak [ 1 ]. RST predicts that agents should switch between risk proneness and risk aversion depending on state and circumstances, especially according to the richness of the least variable option [ 2 ]. Unrealistic assumptions about agents’ information processing mechanisms and poor knowledge of the extent to which variability imposes specific selection in nature are strong candidates to explain the gap between theory and data. RST’s rationale also applies to plants, where it has not hitherto been tested. Given the differences between animals’ and plants’ information processing mechanisms, such tests should help unravel the conflicts between theory and data. Measuring root growth allocation by split-root pea plants, we show that they favor variability when mean nutrient levels are low and the opposite when they are high, supporting the most widespread RST prediction. However, the combination of non-linear effects of nitrogen availability at local and systemic levels may explain some of these effects as a consequence of mechanisms not necessarily evolved to cope with variance [ 3, 4 ]. This resembles animal examples in which properties of perception and learning cause risk sensitivity even though they are not risk adaptations [ 5 ].
Jennifer Mach's insight:
This paper has been all over the news-- looking forward to checking it out.
The membranes of eukaryotic cells create hydrophobic barriers that control substance and information exchange between the inside and outside of cells and between cellular compartments. Besides their roles as membrane building blocks, some membrane lipids, such as phosphoinositides (PIs), also exert regulatory effects. Indeed, emerging evidence indicates that PIs play crucial roles in controlling polarity and growth in plants. Here, I highlight the key roles of PIs as important regulatory membrane lipids in plant development and function.
Breeding crops with more biomass produced per drop of water transpired is a key challenge in the context of climate change. However, the tight coupling between transpiration and carbon assimilation during the day makes it challenging to decrease water loss without altering photosynthesis and reducing crop yield. We tested whether reducing transpiration at night when photosynthesis is inactive could substantially reduce water loss without altering growth—a hypothesis that, to our knowledge, has never been genetically addressed in any species. By studying a whole progeny in grapevine, a major crop for drought-prone areas, we identified genomic regions where selection could be operated to reduce transpiration at night and maintain growth. This opens new horizons for breeding crops with higher water-use efficiency.
Highlights •ENODL11–15 are GPI-anchored proteins, each with a plastocyanin-like domain •ENODL11–15 are predominantly expressed in the ovules and the funiculus •Loss of function or overexpression of ENODLs compromises pollen tube reception •ENODL14 has physical interaction with the extracellular domain of FERONIA Summary During the angiosperm (flowering-plant) life cycle, double fertilization represents the hallmark between diploid and haploid generations [ 1 ]. The success of double fertilization largely depends on compatible communication between the male gametophyte (pollen tube) and the maternal tissues of the flower, culminating in precise pollen tube guidance to the female gametophyte (embryo sac) and its rupture to release sperm cells. Several important factors involved in the pollen tube reception have been identified recently [ 2–6 ], but the underlying signaling pathways are far from being understood. Here, we report that a group of female-specific small proteins, early nodulin-like proteins (ENODLs, or ENs), are required for pollen tube reception. ENs are featured with a plastocyanin-like (PCNL) domain, an arabinogalactan (AG) glycomodule, and a predicted glycosylphosphatidylinositol (GPI) anchor motif. We show that ENs are asymmetrically distributed at the plasma membrane of the synergid cells and accumulate at the filiform apparatus, where arriving pollen tubes communicate with the embryo sac. EN14 strongly and specifically interacts with the extracellular domain of the receptor-like kinase FERONIA, localized at the synergid cell surface and known to critically control pollen tube reception [ 6 ]. Wild-type pollen tubes failed to arrest growth and to rupture after entering the ovules of quintuple loss-of-function EN mutants, indicating a central role of ENs in male-female communication and pollen tube reception. Moreover, overexpression of EN15 by the endogenous promoter caused disturbed pollen tube guidance and reduced fertility. These data suggest that female-derived GPI-anchored ENODLs play an essential role in male-female communication and fertilization.
On 21 October 2013, the Italian phytosanitary service notified the European Commission (EC) that the plant pathogen Xylella fastidiosa had been detected in olive trees near Gallipoli, a tourist destination in Italy's southern region of Apulia (1). This xylem-limited bacterium is spread by insect vectors and causes disease in crops such as grapevines, citrus, coffee, and almond; various ornamentals; and trees such as oaks, elms, and sycamores. Because of the risks of X. fastidiosa being introduced, established, and spread throughout Europe, this species is a regulated quarantine pest. Yet, X. fastidiosa has been left unchecked and has marched northward, leaving destruction in its wake (see the photo) (2). The establishment of X. fastidiosa in Italy has been an agricultural, environmental, political, and cultural disaster.
The threat of X. fastidiosa to European and Mediterranean agriculture, forests, and ecosystems goes beyond specific crops such as grapevines or citrus. The current host range of this bacterium includes more than 300 plant species (3). Most of these species support some degree of pathogen multiplication without expressing symptoms. Susceptible hosts infected with X. fastidiosa often show disease symptoms only after months or years, although epidemics can spread fast and be devastating.
A phylogenetic study has shown that the genotype in Italy was likely introduced via contaminated plant material from Costa Rica (3). Several X. fastidiosa-infected coffee plants from Costa Rica have been intercepted at European ports since 2014, supporting this hypothesis (4). As a response, the EC in February 2014 approved European Union (EU) emergency measures aimed at preventing the introduction and spread of X. fastidiosa. Since May 2015, the import of coffee plants from Costa Rica and Honduras into the EU has been forbidden. Limiting the introduction of insect vectors is considered an easier task, but this is not possible for X. fastidiosa because any xylem-sap-sucking insect species can be a potential vector. Europe has few sharpshooter leafhopper species, the most important group of vectors in the Americas. However, various endemic spittlebug species (froghoppers) are also potential vectors of X. fastidiosa (3).
Trade is an important pathway in the introduction of plant pests and pathogens (5), and X. fastidiosa-infected plant material has likely been introduced via European ports on a regular basis. Given that biological and environmental conditions in Europe support X. fastidiosainfection, the question arises why the pathogen has not been reported previously. One possible explanation is that limited surveillance efforts missed previous introductions. Monitoring was one component of the EU emergency measures. After the French authorities started a systematic monitoring program for X. fastidiosa in 2014, they found 250 distinct infected areas in Corsica and several in the French Riviera. However, no disease epidemic has yet been noted in France, and the genotype of X. fastidiosa differs from that found in Italy.
Long distance transport in plants occurs in sieve tubes of the phloem. The pressure flow hypothesis introduced by Ernst Münch in 1930 describes a mechanism of osmotically generated pressure differentials that are supposed to drive the movement of sugars and other solutes in the phloem, but this hypothesis has long faced major challenges. The key issue is whether the conductance of sieve tubes, including sieve plate pores, is sufficient to allow pressure flow. We show that with increasing distance between source and sink, sieve tube conductivity and turgor increases dramatically in Ipomoea nil. Our results provide strong support for the Münch hypothesis, while providing new tools for the investigation of one of the least understood plant tissues.
Many microbes interact with their hosts across a membrane interface, which is often distinct from existing membranes. Understanding how this interface acquires its identity has significant implications. In the symbiosis between legumes and rhizobia, the symbiosome encases the intracellular bacteria and receives host secretory proteins important for bacterial development. We show that the Medicago truncatula SYNTAXIN 132 (SYP132) gene undergoes alternative cleavage and polyadenylation during transcription, giving rise to two target-membrane soluble NSF attachment protein receptor (t-SNARE) isoforms. One of these isoforms, SYP132A, is induced during the symbiosis, is able to localize to the peribacteroid membrane, and is required for the maturation of symbiosomes into functional forms. The second isoform, SYP132C, has important functions unrelated to symbiosis. The SYP132A sequence is broadly found in flowering plants that form arbuscular mycorrhizal symbiosis, an ancestral mutualism between soil fungi and most land plants. SYP132A silencing severely inhibited arbuscule colonization, indicating that SYP132A is an ancient factor specifying plant–microbe interfaces.
Cellulose synthase is a large, multisubunit machine that “swims” along the plant cell membrane as it spins out cellulose fibers. Kumar et al. show that the cellulose synthase complex is heavily modified through S-acylation. Subsets of the acylation sites were required for the complex to integrate into the plasma membrane. A single functional complex could bear as many as 100 modification sites, potentially changing its biophysical characteristics and helping it to associate with the membrane.
Communication has played a key role in organismal evolution. If sender and receiver have a shared interest in propagating reliable information, such as when they are kin relatives, then effective communication can bring large fitness benefits. However, interspecific communication (among different species) is more prone to dishonesty. Over the last decade, plants and their microbial root symbionts have become a model system for studying interspecific molecular crosstalk. However, less is known about the evolutionary stability of plant–microbe communication. What prevents partners from hijacking or manipulating information to their own benefit? Here, we focus on communication between arbuscular mycorrhizal fungi and their host plants. We ask how partners use directed signals to convey specific information, and highlight research on the problem of dishonest signaling.
Angiosperms and gymnosperms are two major groups of extant seed plants. It has been suggested that gymnosperms lack FLOWERING LOCUS T (FT), a key integrator at the core of flowering pathways in angiosperms. Taking advantage of newly released gymnosperm genomes, we revisited the evolutionary history of the plant phosphatidylethanolamine-binding protein (PEBP) gene family through phylogenetic reconstruction. Expression patterns in three gymnosperm taxa and heterologous expression in Arabidopsis were studied to investigate the functions of gymnosperm FT-like and TERMINAL FLOWER 1 (TFL1)-like genes. Phylogenetic reconstruction suggests that an ancient gene duplication predating the divergence of seed plants gave rise to the FT and TFL1 genes. Expression patterns indicate that gymnosperm TFL1-like genes play a role in the reproductive development process, while GymFT1 and GymFT2, the FT-like genes resulting from a duplication event in the common ancestor of gymnosperms, function in both growth rhythm and sexual development pathways. When expressed in Arabidopsis, both spruce FT-like and TFL1-like genes repressed flowering. Our study demonstrates that gymnosperms do have FT-like and TFL1-like genes. Frequent gene and genome duplications contributed significantly to the expansion of the plant PEBP gene family. The expression patterns of gymnosperm PEBP genes provide novel insight into the functional evolution of this gene family.
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