Plants are continuously threatened by pathogen attack and, as such, they have evolved mechanisms to evade, escape and defend themselves against pathogens. However, it is not known what types of defense mechanisms a plant would already possess to defend against a potential pathogen that has not co-evolved with the plant. We addressed this important question in a comprehensive manner by studying the responses of 1041 accessions of Arabidopsis thaliana to the foliar pathogen Pseudomonas syringae pv. tomato (Pst) DC3000. We characterized the interaction using a variety of established methods, including different inoculation techniques, bacterial mutant strains, and assays for the hypersensitive response, salicylic acid (SA) accumulation and reactive oxygen species production . Fourteen accessions showed resistance to infection by Pst DC3000. Of these, two accessions had a surface-based mechanism of resistance, six showed a hypersensitive-like response while three had elevated SA levels. Interestingly, A. thaliana was discovered to have a recognition system for the effector AvrPto, and HopAM1 was found to modulate Pst DC3000 resistance in two accessions. Our comprehensive study has significant implications for the understanding of natural disease resistance mechanisms at the species level and for the ecology and evolution of plant–pathogen interactions.
Mainly due to their economic importance, genomes of 10 legumes, including soybean, wild peanuts, barrel medic, etc, have been sequenced. However, a family-level comparative genomics analysis has been unavailable. With grape and selected legume genomes as outgroups, we managed to perform a hierarchical and event-related alignment of these genomes and deconvoluted layers of homologous regions produced by ancestral polyploidizations or speciations. Consequently, we illustrated genomic fractionation characterized by wide-spread gene losses after the polyploidizations. Notably, high similarity in gene retention between recently duplicated chromosomes in soybean supported a likely autopolypoidy nature of its tetraploid ancestor. Moreover, though mostly gene losses were nearly random, largely but not fully described by geometric distribution, we showed that polyploidization contributed divergently to copy number variation of important gene families. Besides, we showed significantly divergent evolutionary levels among legumes, and by performing Ks correction, re-dated major evolutionary events during their expansion. The present effort laid a solid foundation further genomics exploration in the legume research community and beyond. We described only a tiny fraction of legume comparative genomics analysis that we performed, and more information was stored in the newly constructed Legume Comparative Genomics Research Platform (www.legumegrp.org).
Bacterial wilt of potatoes—also called brown rot—is a devastating disease caused by the vascular pathogen Ralstonia solanacearum that leads to significant yield loss. As in other plant-pathogen interactions, the first contacts established between the bacterium and the plant largely condition the disease outcome. Here, we studied the transcriptome of R. solanacearum UY031 early after infection in two accessions of the wild potato Solanum commersonii showing contrasting resistance to bacterial wilt. Total RNAs obtained from asymptomatic infected roots were deep sequenced and for 4,609 out of the 4,778 annotated genes in strain UY031 were recovered. Only 2 genes were differentially-expressed between the resistant and the susceptible plant accessions, suggesting that the bacterial component plays a minor role in the establishment of disease. On the contrary, 422 genes were differentially expressed (DE) in planta compared to growth on a synthetic rich medium. Only 73 of these genes had been previously identified as DE in a transcriptome of R. solanacearum extracted from infected tomato xylem vessels. Virulence determinants such as the Type Three Secretion System (T3SS) and its effector proteins, motility structures, and reactive oxygen species (ROS) detoxifying enzymes were induced during infection of S. commersonii. On the contrary, metabolic activities were mostly repressed during early root colonization, with the notable exception of nitrogen metabolism, sulfate reduction and phosphate uptake. Several of the R. solanacearum genes identified as significantly up-regulated during infection had not been previously described as virulence factors. This is the first report describing the R. solanacearum transcriptome directly obtained from infected tissue and also the first to analyze bacterial gene expression in the roots, where plant infection takes place. We also demonstrate that the bacterial transcriptome in planta can be studied when pathogen numbers are low by sequencing transcripts from infected tissue avoiding prokaryotic RNA enrichment.
Crop production needs to increase to secure future food supplies, while reducing its impact on ecosystems. Detailed characterization of plant genomes and genetic diversity is crucial for meeting these challenges. Advances in genome sequencing and assembly are being used to access the large and complex genomes of crops and their wild relatives. These have helped to identify a wide spectrum of genetic variation and permitted the association of genetic diversity with diverse agronomic phenotypes. In combination with improved and automated phenotyping assays and functional genomic studies, genomics is providing new foundations for crop-breeding systems.
We describe here the reconstruction of the genome of the most recent common ancestor (MRCA) of modern monocots and eudicots, accounting for 95% of extant angiosperms, with its potential repertoire of 22,899 ancestral genes conserved in present-day crops. The MRCA provides a starting point for deciphering the reticulated evolutionary plasticity between species (rapidly versus slowly evolving lineages), subgenomes (pre- versus post-duplication blocks), genomic compartments (stable versus labile loci), genes (ancestral versus species-specific genes) and functions (gained versus lost ontologies), the key mutational forces driving the success of polyploidy in crops. The estimation of the timing of angiosperm evolution, based on MRCA genes, suggested that this group emerged 214 million years ago during the late Triassic era, before the oldest recorded fossil. Finally, the MRCA constitutes a unique resource for scientists to dissect major agronomic traits in translational genomics studies extending from model species to crops.
The range of hosts that parasites can infect is a key determinant of the emergence and spread of disease. Yet, the impact of host range variation on the evolution of parasite genomes remains unknown. Here, we show that codon optimization underlies genome adaptation in broad host range parasites. We found that the longer proteins encoded by broad host range fungi likely increase natural selection on codon optimization in these species. Accordingly, codon optimization correlates with host range across the fungal kingdom. At the species level, biased patterns of synonymous substitutions underpin increased codon optimization in a generalist but not a specialist fungal pathogen. Virulence genes were consistently enriched in highly codon-optimized genes of generalist but not specialist species. We conclude that codon optimization is related to the capacity of parasites to colonize multiple hosts. Our results link genome evolution and translational regulation to the long-term persistence of generalist parasitism.
Gene conversion, non-reciprocal transfer from one homologous sequence to another, is a major force in evolutionary dynamics, promoting co-evolution in gene families, and maintaining similarities between repeated genes. However, the properties of the transfer – where it initiates, how far it proceeds, and how the resulting conversion tracts are affected by mismatch repair – are not well understood. Here we use the duplicate tuf genes in Salmonella as a quantitatively tractable model system for gene conversion. We selected for conversion in multiple different positions of tuf, and examined the resulting distributions of conversion tracts in mismatch repair-deficient and mismatch repair-proficient strains. A simple stochastic model accounting for the essential steps of conversion showed excellent agreement with the data for all selection points using the same value of the conversion processivity, which is the only kinetic parameter of the model. The analysis suggests that gene conversion effectively initiates uniformly at any position within a tuf gene, and proceeds with an effectively uniform conversion processivity in either direction limited by the bounds of the gene.
Ground-breaking research over recent decades has established that secreted proteins and small molecules, termed effectors, serve important functions to support the interactions of diverse organisms with their plant hosts. Studies focused on effectors have revealed key virulence and avirulence mechanisms, and have provided new insights into the functions of plant regulatory networks, and have informed long-standing questions about host-microbe co-evolution. This fundamental understanding also holds clear implications for management of disease in crops. However, much remains to be learned, and effector biology is one of the most vibrant areas of research in the molecular plant-microbe field.
We invite research and perspective articles that explore all aspects of effector structure, function, and evolution, encompassing the full breadth of plant-associated organisms. Articles highlighting translational research as well as fundamental understanding are welcome. We look forward to assembling an issue that highlights some of the best current research in this rapidly advancing area!
Hydathodes are water pores found on leaves of a wide range of vascular plants and are the sites of guttation. We report here on the detailed anatomy of cauliflower and Arabidopsis hydathodes. Hydathode surface presents pores resembling stomata giving access to large cavities. Beneath, the epithem is composed of a lacunar and highly vascularized parenchyma offering a direct connection between leaf surface and xylem vessels. Arabidopsis hydathode pores were responsive to ABA and light similar to stomata. The flg22 flagellin peptide, a well-characterized elicitor of plant basal immunity, did not induce closure of hydathode pores in contrast to stomata. Because hydathodes are natural infection routes for several pathogens, we investigated hydathode infection by the adapted vascular phytopathogenic bacterium Xanthomonas campestris pv. campestris (Xcc), the causal agent of black rot disease of Brassicaceae. Microscopic observations of hydathodes six days post inoculation indicated a digestion of the epithem cells and a high bacterial multiplication. Post-invasive immunity was shown to limit pathogen growth in the epithem and is actively suppressed by the type III secretion system and its effector proteins. Altogether, these results give a detailed anatomic description of Brassicaceae hydathodes and highlight the efficient use of this tissue as an initial niche for subsequent vascular systemic dissemination of Xcc in distant plant tissues.
... 10% de ces espèces sont endémiques, soit 16 773 espèces pour lesquelles la France est seule garante de leur conservation. A l'inverse, la France recense 76 des 100 espèces envahissantes parmi les plus nuisibles du monde. Chaque année, 600 espèces nouvelles pour la science sont décrites sur le territoire national.
Growing demographic trends require sustainable technologies to improve quality and yield of future food productions. However, there is uncertainty about plant protection strategies in many agro-ecosystems. Pests, diseases, and weeds are overwhelmingly controlled by chemicals which pose health risks and cause other undesirable effects. Therefore, an increasing concern on control measures emerged in recent years. Many chemicals became questioned with regard to their sustainability and are (or will be) banned. Alternative management tools are studied, relying on biological, and low impact solutions.
This Research Topic concerns microbial biocontrol agents, root-associated microbiomes, and rhizosphere networks. Understanding how they interact or respond to (a) biotic environmental cues is instrumental for an effective and sustainable impact. The rhizosphere is in this regard a fundamental object of study, because of its role in plant productivity.
Although interest in animal pathogenic oomycetes is increasing, the molecular basis mediating oomycete-animal relationships remains virtually unknown. Crinkler (CRN) genes, which have been traditionally associated with the cytotoxic activity displayed by plant pathogenic oomycetes, were recently detected in transcriptome sequences from the entomopathogenic oomycete Lagenidium giganteum, suggesting that these genes may represent virulence factors conserved in both animal and plant pathogenic oomycetes. In order to further characterize the L. giganteum pathogenome, an on-going genomic survey was mined to reveal novel putative virulence factors, including canonical oomycete effectors Crinkler 13 (CRN13) orthologs. These novel sequences provided a basis to initiate gene expression analyses and determine if the proposed L. giganteum virulence factors are differentially expressed in the presence of mosquito larvae (Aedes aegypti). Sequence analyses revealed that L. giganteum express CRN13 transcripts. The predicted proteins, like other L. giganteum CRNs, contained a conserved LYLA motif at the N terminal, but did not display signal peptides. In contrast, other potential virulence factors, such as Glycoside Hydrolases family 20 (hexosaminidase) and 37 (trehalase) proteins (GH20 and GH37), contained identifiable signal peptides. Genome mining demonstrated that GH20 genes are absent from phytopathogenic oomycete genomes, and that the L. giganteum GH20 sequence is the only reported peronosporalean GH20 gene. All other oomycete GH20 homologs were retrieved from animal pathogenic, saprolegnialean genomes. Furthermore, phylogenetic analyses demonstrated that saprolegnialean and peronosporalean GH20 protein sequences clustered in unrelated clades. The saprolegnialean GH20 sequences appeared as a strongly supported, monophyletic group nested within an arthropod-specific clade, suggesting that this gene was acquired via a lateral gene transfer event from an insect or crustacean genome. In contrast, the L. giganteum GH20 protein sequence appeared as a sister taxon to a plant-specific clade that included exochitinases with demonstrated insecticidal activities. Finally, gene expression analyses demonstrated that the L. giganteum GH20 gene expression level is significantly modulated in the presence of mosquito larvae. In agreement with the protein secretion predictions, CRN transcripts did not show any differential expression. These results identified GH20 enzymes, and not CRNs, as potential pathogenicity factors shared by all animal pathogenic oomycetes.
Plants encounter a myriad of microorganisms, particularly at the root–soil interface, that can invade with detrimental or beneficial outcomes. Prevalent beneficial associations between plants and microorganisms include those that promote plant growth by facilitating the acquisition of limiting nutrients such as nitrogen and phosphorus. But while promoting such symbiotic relationships, plants must restrict the formation of pathogenic associations. Achieving this balance requires the perception of potential invading microorganisms through the signals that they produce, followed by the activation of either symbiotic responses that promote microbial colonization or immune responses that limit it.
Plant-pathogenic Xanthomonas bacteria inject transcription activator-like effector proteins (TALEs) into host cells to specifically induce transcription of plant genes and enhance susceptibility. Although the DNA-binding mode is well-understood it is still ambiguous how TALEs initiate transcription and whether additional promoter elements are needed to support this. To systematically dissect prerequisites for transcriptional initiation the activity of one TALE was compared on different synthetic Bs4 promoter fragments. In addition, a large collection of artificial TALEs spanning the OsSWEET14 promoter was compared. We show that the presence of a TALE alone is not sufficient to initiate transcription suggesting the requirement of additional supporting promoter elements. At the OsSWEET14 promoter TALEs can initiate transcription from various positions, in a synergistic manner of multiple TALEs binding in parallel to the promoter, and even by binding in reverse orientation. TALEs are known to shift the transcriptional start site, but our data show that this shift depends on the individual position of a TALE within a promoter context. Our results implicate that TALEs function like classical enhancer-binding proteins and initiate transcription in both orientations which has consequences for in planta target gene prediction and design of artificial activators.
Maize is the highest yielding cereal crop grown worldwide. Here Sunet al. show that maize growth can be further enhanced by prolonging the duration of leaf elongation by targeted ectopic expression of the PLASTOCHRON1gene and show that this leads to increased yield in field trials.
Nucleotide-binding domain and leucine-rich repeat domain-containing (NLR) proteins are sentinels of plant immunity that monitor host proteins for perturbations induced by pathogenic effector proteins. Here we show that the Arabidopsis ZAR1 NLR protein requires the ZRK3 kinase to recognize the Pseudomonas syringae type III effector (T3E) HopF2a. These results support the hypothesis that ZAR1 associates with an expanded ZRK protein family to broaden its effector recognition spectrum.
The domestication of new crops would promote agricultural diversity and could provide a solution to many of the problems associated with intensive agriculture. We suggest here that genome editing can be used as a new tool by breeders to accelerate the domestication of semi-domesticated or even wild plants, building a more varied foundation for the sustainable provision of food and fodder in the future. We examine the feasibility of such plants from biological, social, ethical, economic, and legal perspectives.
A second wave of the green revolution is underway that focuses on environmental sustainability, low input, and increased nutritional value. Of the more than 300 000 plant species that exist, less than 200 are commercially important, and three species – rice, wheat, and maize – account for the major part of the plant-derived nutrients that humans consume. Plants with desirable traits, such as perennials with extensive root systems and nitrogen-fixing plants, are currently being domesticated as new crops. Recent years have given rise to the use of CRISPR/Cas9 for genome editing in plants. The method allows mutations to be generated at precise locations in genes that can lead to knockout or knockdown of protein activity. Several traits in crops that were crucial for their domestication are caused by mutations that can be reproduced by genome-editing techniques such as CRISPR/Cas9, offering the potential for accelerated domestication of new crops.
One of the most fundamental questions in plant pathology is what determines whether a pathogen grows within a plant? This question is frequently studied in terms of the role of elicitors and pathogenicity factors in the triggering or overcoming of host defences. However, this focus fails to address the basic question of how the environment in host tissues acts to support or restrict pathogen growth. Efforts to understand this aspect of host–pathogen interactions are commonly confounded by several issues, including the complexity of the plant environment, the artificial nature of many experimental infection systems and the fact that the physiological properties of a pathogen growing in association with a plant can be very different from the properties of the pathogen in culture. It is also important to recognize that the phenotype and evolution of pathogen and host are inextricably linked through their interactions, such that the environment experienced by a pathogen within a host, and its phenotype within the host, is a product of both its interaction with its host and its evolutionary history, including its co-evolution with host plants. As the phenotypic properties of a pathogen within a host cannot be defined in isolation from the host, it may be appropriate to think of pathogens as having an ‘extended phenotype’ that is the product of their genotype, host interactions and population structure within the host environment. This article reflects on the challenge of defining and studying this extended phenotype, in relation to the questions posed below, and considers how knowledge of the phenotype of pathogens in the host environment could be used to improve disease control.
What determines whether a pathogen grows within a plant?
What aspects of pathogen biology should be considered in describing the extended phenotype of a pathogen within a host?
How can we study the extended phenotype in ways that provide insights into the phenotypic properties of pathogens during natural infections?
In 2007, we reported that a phytopathogen effector directly inhibits a MAP kinase cascade. In the decade since, many more effectors have been found to inhibit MAP kinase cascades, providing not only a mechanistic understanding of pathogenesis and immunity in plants, but also the identification of previously unknown enzymes.
L’Inra annonce avoir découvert un gène impliqué dans le processus d’obtention des lignées pures de maïs. Un pas important dans la connaissance de la fécondation des plantes.
Depuis des décennies, les sélectionneurs de maïs exploitent un phénomène unique dans le monde végétal : le pollen d’une plante « mâle » déposé sur l’épi « femelle » déclenche une descendance qui ne porte que les caractères de la mère. Des chercheurs de l’Inra, en collaboration avec le CNRS, l’ENS de Lyon, l’Université Claude Bernard Lyon 1 et Limagrain, ont découvert le gène responsable de ce phénomène chez le maïs et l’ont baptisé « Not Like Dad » (en français « pas comme papa »), puisque l’information génétique du père ne se retrouve pas dans la descendance, explique l’Inra dans un communiqué du 22 février 2017. Moyen de sélection des hybrides
Les sélectionneurs obtiennent ainsi des lignées « pures » en une seule génération, alors que ce processus nécessite normalement plusieurs années. Chez le maïs, ces lignées « pures » servent comme parents des hybrides, c’est-à-dire de plantes possédant des caractères d’intérêt agronomique sélectionnés, et de performance supérieure aux deux plantes parents.
Initially found to be critically involved in inflammation and apoptosis, caspases have since then been implicated in the regulation of various signaling pathways in animals. How caspases and caspase-mediated processes evolved is a topic of great interest and hot debate. In fact, caspases are just the tip of the iceberg, representing a relatively small group of mostly animal-specific enzymes within a broad family of structurally related cysteine proteases (family C14 of CD clan) found in all kingdoms of life. Apart from caspases, this family encompasses para- and metacaspases, and all three groups of proteases exhibit significant variation in biochemistry and function in vivo. Notably, metacaspases are present in all eukaryotic lineages with a remarkable absence in animals. Thus, metacaspases and caspases must have adapted to operate under distinct cellular and physiological settings. Here we discuss biochemical properties and biological functions of metacaspases in comparison to caspases, with a major focus on the regulation of developmental aspects in plants versus animals.
Multicellular eukaryotes coevolve with microbial pathogens, which exert strong selective pressure on the immune systems of their hosts. Plants and animals use intracellular proteins of the nucleotide-binding domain, leucine-rich repeat (NLR) superfamily to detect many types of microbial pathogens. The NLR domain architecture likely evolved independently and convergently in each kingdom, and the molecular mechanisms of pathogen detection by plant and animal NLRs have long been considered to be distinct. However, microbial recognition mechanisms overlap, and it is now possible to discern important key trans-kingdom principles of NLR-dependent immune function. Here, we attempt to articulate these principles. We propose that the NLR architecture has evolved for pathogen-sensing in diverse organisms because of its utility as a tightly folded “hair trigger” device into which a virtually limitless number of microbial detection platforms can be integrated. Recent findings suggest means to rationally design novel recognition capabilities to counter disease.
Stomatal opening and closure depends on changes in turgor pressure acting within guard cells to alter cell shape . The extent of these shape changes is limited by the mechanical properties of the cells, which will be largely dependent on the structure of the cell walls. Although it has long been observed that guard cells are anisotropic due to differential thickening and the orientation of cellulose microfibrils , our understanding of the composition of the cell wall that allows them to undergo repeated swelling and deflation remains surprisingly poor. Here, we show that the walls of guard cells are rich in un-esterified pectins. We identify a pectin methylesterase gene, PME6, which is highly expressed in guard cells and required for stomatal function. pme6-1 mutant guard cells have walls enriched in methyl-esterified pectin and show a decreased dynamic range in response to triggers of stomatal opening/closure, including elevated osmoticum, suggesting that abrogation of stomatal function reflects a mechanical change in the guard cell wall. Altered stomatal function leads to increased conductance and evaporative cooling, as well as decreased plant growth. The growth defect of the pme6-1 mutant is rescued by maintaining the plants in elevated CO2, substantiating gas exchange analyses, indicating that the mutant stomata can bestow an improved assimilation rate. Restoration of PME6 rescues guard cell wall pectin methyl-esterification status, stomatal function, and plant growth. Our results establish a link between gene expression in guard cells and their cell wall properties, with a corresponding effect on stomatal function and plant physiology.
Ralstonia solanacearum, a species complex of bacterial plant pathogens divided into four monophyletic phylotypes, causes plant diseases in tropical climates around the world. Some strains exhibit a broad host range on solanaceous hosts, while others are highly host-specific as for example some banana-pathogenic strains. Previous studies showed that transcription activator-like (TAL) effectors from Ralstonia, termed RipTALs, are capable of activating reporter genes in planta, if these are preceded by a matching effector binding element (EBE). RipTALs target DNA via their central repeat domain (CRD), where one repeat pairs with one DNA-base of the given EBE. The repeat variable diresidue dictates base repeat specificity in a predictable fashion, known as the TALE code. In this work, we analyze RipTALs across all phylotypes of the Ralstonia solanacearum species complex. We find that RipTALs are prevalent in phylotypes I and IV but absent from most phylotype III and II strains (10/12, 8/14, 1/24, and 1/5 strains contained a RipTAL, respectively). RipTALs originating from strains of the same phylotype show high levels of sequence similarity (>98%) in the N-terminal and C-terminal regions, while RipTALs isolated from different phylotypes show 47–91% sequence similarity in those regions, giving rise to four RipTAL classes. We show that, despite sequence divergence, the base preference for guanine, mediated by the N-terminal region, is conserved across RipTALs of all classes. Using the number and order of repeats found in the CRD, we functionally sub-classify RipTALs, introduce a new simple nomenclature, and predict matching EBEs for all seven distinct RipTALs identified. We experimentally study RipTAL EBEs and uncover that some RipTALs are able to target the EBEs of other RipTALs, referred to as cross-reactivity. In particular, RipTALs from strains with a broad host range on solanaceous hosts cross-react on each other’s EBEs. Investigation of sequence divergence between RipTAL repeats allows for a reconstruction of repeat array biogenesis, for example through slipped strand mispairing or gene conversion. Using these studies we show how RipTALs of broad host range strains evolved convergently toward a shared target sequence. Finally, we discuss the differences between TALE-likes of plant pathogens in the context of disease ecology.
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