ABSTRACT
Aphids transmit viruses and are destructive crop pests1. Plants that have been attacked by aphids release volatile compounds to elicit airborne defence (AD) in neighbouring plants2-5. However, the mechanism underlying AD is unclear. Here we reveal that methyl-salicylate (MeSA), salicylic acid-binding protein-2 (SABP2), the transcription factor NAC2 and salicylic acid-carboxylmethyltransferase-1 (SAMT1) form a signalling circuit to mediate AD against aphids and viruses. Airborne MeSA is perceived and converted into salicylic acid by SABP2 in neighbouring plants. Salicylic acid then causes a signal transduction cascade to activate the NAC2-SAMT1 module for MeSA biosynthesis to induce plant anti-aphid immunity and reduce virus transmission. To counteract this, some aphid-transmitted viruses encode helicase-containing proteins to suppress AD by interacting with NAC2 to subcellularly relocalize and destabilize NAC2. As a consequence, plants become less repellent to aphids, and more suitable for aphid survival, infestation and viral transmission. Our findings uncover the mechanistic basis of AD and an aphid-virus co-evolutionary mutualism, demonstrating AD as a potential bioinspired strategy to control aphids and viruses.
Subject(s)
Air , Aphids , Plant Diseases , Plants , Salicylic Acid , Signal Transduction , Aphids/physiology , Aphids/virology , Host Microbial Interactions , Plant Diseases/immunology , Plant Diseases/parasitology , Plant Diseases/prevention & control , Plant Diseases/virology , Plant Proteins/metabolism , Plants/metabolism , Plants/parasitology , Plants/virology , Salicylic Acid/metabolism , Symbiosis , Nicotiana/immunology , Nicotiana/metabolism , Nicotiana/parasitology , Nicotiana/virology , Viral Proteins/metabolism , AnimalsABSTRACT
Oomycete protists share phenotypic similarities with fungi, including the ability to cause plant diseases, but branch in a distant region of the tree of life. It has been suggested that multiple horizontal gene transfers (HGTs) from fungi-to-oomycetes contributed to the evolution of plant-pathogenic traits. These HGTs are predicted to include secreted proteins that degrade plant cell walls, a barrier to pathogen invasion and a rich source of carbohydrates. Using a combination of phylogenomics and functional assays, we investigate the diversification of a horizontally transferred xyloglucanase gene family in the model oomycete species Phytophthora sojae. Our analyses detect 11 xyloglucanase paralogs retained in P. sojae. Using heterologous expression in yeast, we show consistent evidence that eight of these paralogs have xyloglucanase function, including variants with distinct protein characteristics, such as a long-disordered C-terminal extension that can increase xyloglucanase activity. The functional variants analyzed subtend a phylogenetic node close to the fungi-to-oomycete transfer, suggesting the horizontally transferred gene was a bona fide xyloglucanase. Expression of three xyloglucanase paralogs in Nicotiana benthamiana triggers high-reactive oxygen species (ROS) generation, while others inhibit ROS responses to bacterial immunogens, demonstrating that the paralogs differentially stimulate pattern-triggered immunity. Mass spectrometry of detectable enzymatic products demonstrates that some paralogs catalyze the production of variant breakdown profiles, suggesting that secretion of variant xyloglucanases increases efficiency of xyloglucan breakdown as well as diversifying the damage-associated molecular patterns released. We suggest that this pattern of neofunctionalization and the variant host responses represent an aspect of the Red Queen host-pathogen coevolutionary dynamic.
Subject(s)
Gene Transfer, Horizontal , Glycoside Hydrolases , Phylogeny , Glycoside Hydrolases/metabolism , Glycoside Hydrolases/genetics , Phytophthora/pathogenicity , Phytophthora/genetics , Plant Diseases/microbiology , Plant Diseases/parasitology , Evolution, Molecular , Gene DuplicationABSTRACT
Plant-parasitic nematodes constrain global food security. During parasitism, they secrete effectors into the host plant from two types of pharyngeal gland cells. These effectors elicit profound changes in host biology to suppress immunity and establish a unique feeding organ from which the nematode draws nutrition. Despite the importance of effectors in nematode parasitism, there has been no comprehensive identification and characterisation of the effector repertoire of any plant-parasitic nematode. To address this, we advance techniques for gland cell isolation and transcriptional analysis to define a stringent annotation of putative effectors for the cyst nematode Heterodera schachtii at three key life-stages. We define 717 effector gene loci: 269 "known" high-confidence homologs of plant-parasitic nematode effectors, and 448 "novel" effectors with high gland cell expression. In doing so we define the most comprehensive "effectorome" of a plant-parasitic nematode to date. Using this effector definition, we provide the first systems-level understanding of the origin, deployment and evolution of a plant-parasitic nematode effectorome. The robust identification of the effector repertoire of a plant-parasitic nematode will underpin our understanding of nematode pathology, and hence, inform strategies for crop protection.
Subject(s)
Host-Parasite Interactions , Plant Diseases , Animals , Plant Diseases/parasitology , Tylenchoidea/genetics , Plants/parasitology , Helminth Proteins/genetics , Helminth Proteins/metabolism , Nematoda/geneticsABSTRACT
Cotton is a globally cultivated crop, producing 87% of the natural fiber used in the global textile industry. The pigment glands, unique to cotton and its relatives, serve as a defense structure against pests and pathogens. However, the molecular mechanism underlying gland formation and the specific role of pigment glands in cotton's pest defense are still not well understood. In this study, we cloned a gland-related transcription factor GhHAM and generated the GhHAM knockout mutant using CRISPR/Cas9. Phenotypic observations, transcriptome analysis, and promoter-binding experiments revealed that GhHAM binds to the promoter of GoPGF, regulating pigment gland formation in cotton's multiple organs via the GoPGF-GhJUB1 module. The knockout of GhHAM significantly reduced gossypol production and increased cotton's susceptibility to pests in the field. Feeding assays demonstrated that more than 80% of the cotton bollworm larvae preferred ghham over the wild type. Furthermore, the ghham mutants displayed shorter cell length and decreased gibberellins (GA) production in the stem. Exogenous application of GA3 restored stem cell elongation but not gland formation, thereby indicating that GhHAM controls gland morphogenesis independently of GA. Our study sheds light on the functional differentiation of HAM proteins among plant species, highlights the significant role of pigment glands in influencing pest feeding preference, and provides a theoretical basis for breeding pest-resistant cotton varieties to address the challenges posed by frequent outbreaks of pests.
Subject(s)
Gene Expression Regulation, Plant , Gossypium , Plant Proteins , Gossypium/genetics , Gossypium/parasitology , Gossypium/metabolism , Plant Proteins/metabolism , Plant Proteins/genetics , Animals , Gibberellins/metabolism , Gossypol/metabolism , Transcription Factors/metabolism , Transcription Factors/genetics , Disease Resistance/genetics , Plant Diseases/parasitology , Plant Diseases/immunology , Moths/physiology , Larva/growth & developmentABSTRACT
Cucumber plants are highly susceptible to the hemibiotroph oomycete Phytophthora melonis. However, the mechanism of resistance to cucumber blight remains poorly understood. Here, we demonstrated that cucumber plants with impairment in the biosynthesis of brassinosteroids (BRs) or gibberellins (GAs) were more susceptible to P. melonis. By contrast, increasing levels of endogenous BRs or exogenously application of 24-epibrassinolide enhanced the resistance of cucumber plants against P. melonis. Furthermore, we found that both knockout and overexpression of the BR biosynthesis gene CYP85A1 reduced the endogenous GA3 content compared with that of wild-type plants under the condition of inoculation with P. melonis, and the enhancement of disease resistance conferred by BR was inhibited in plants with silencing of the GA biosynthetic gene GA20ox1 or KAO. Together, these findings suggest that GA homeostasis is an essential factor mediating BRs-induced disease resistance. Moreover, BZR6, a key regulator of BR signaling, was found to physically interact with GA20ox1, thereby suppressing its transcription. Silencing of BZR6 promoted endogenous GA biosynthesis and compromised GA-mediated resistance. These findings reveal multifaceted crosstalk between BR and GA in response to pathogen infection, which can provide a new approach for genetically controlling P. melonis damage in cucumber production.
Subject(s)
Brassinosteroids , Cucumis sativus , Disease Resistance , Gibberellins , Phytophthora , Plant Diseases , Phytophthora/physiology , Brassinosteroids/metabolism , Cucumis sativus/microbiology , Cucumis sativus/genetics , Cucumis sativus/metabolism , Cucumis sativus/parasitology , Disease Resistance/genetics , Plant Diseases/microbiology , Plant Diseases/parasitology , Plant Diseases/immunology , Gibberellins/metabolism , Gene Expression Regulation, Plant , Plant Proteins/metabolism , Plant Proteins/genetics , Plant Growth Regulators/metabolism , Signal TransductionABSTRACT
Tuta absoluta ("leafminer"), is a major pest of tomato crops worldwide. Controlling this insect is difficult due to its efficient infestation, rapid proliferation, and resilience to changing weather conditions. Furthermore, chemical pesticides have only a short-term effect due to rapid development of T. absoluta strains. Here, we show that a variety of tomato cultivars, treated with external phenylalanine solutions exhibit high resistance to T. absoluta, under both greenhouse and open field conditions, at different locations. A large-scale metabolomic study revealed that tomato leaves absorb and metabolize externally given Phe efficiently, resulting in a change in their volatile profile, and repellence of T. absoluta moths. The change in the volatile profile is due to an increase in three phenylalanine-derived benzenoid phenylpropanoid volatiles (BPVs), benzaldehyde, phenylacetaldehyde, and 2-phenylethanol. This treatment had no effect on terpenes and green leaf volatiles, known to contribute to the fight against insects. Phe-treated plants also increased the resistance of neighboring non-treated plants. RNAseq analysis of the neighboring non-treated plants revealed an exclusive upregulation of genes, with enrichment of genes related to the plant immune response system. Exposure of tomato plants to either benzaldehyde, phenylacetaldehyde, or 2-phenylethanol, resulted in induction of genes related to the plant immune system that were also induced due to neighboring Phe-treated plants. We suggest a novel role of phenylalanine-derived BPVs as mediators of plant-insect interactions, acting as inducers of the plant defense mechanisms.
Subject(s)
Phenylalanine , Plant Leaves , Solanum lycopersicum , Volatile Organic Compounds , Solanum lycopersicum/genetics , Solanum lycopersicum/metabolism , Solanum lycopersicum/parasitology , Phenylalanine/metabolism , Volatile Organic Compounds/metabolism , Animals , Plant Leaves/metabolism , Plant Leaves/drug effects , Plant Leaves/parasitology , Benzaldehydes/metabolism , Benzaldehydes/pharmacology , Acetaldehyde/analogs & derivatives , Acetaldehyde/metabolism , Acetaldehyde/pharmacology , Moths/physiology , Moths/drug effects , Plant Diseases/parasitology , Plant Diseases/immunology , Manduca/physiologyABSTRACT
Meloidogyne incognita is one of the most widely distributed plant-parasitic nematodes and causes severe economic losses annually. The parasite produces effector proteins that play essential roles in successful parasitism. Here, we identified one such effector named MiCE108, which is exclusively expressed within the nematode subventral esophageal gland cells and is upregulated in the early parasitic stage of M. incognita. A yeast signal sequence trap assay showed that MiCE108 contains a functional signal peptide for secretion. Virus-induced gene silencing of MiCE108 impaired the parasitism of M. incognita in Nicotiana benthamiana. The ectopic expression of MiCE108 in Arabidopsis suppressed the deposition of callose, the generation of reactive oxygen species, and the expression of marker genes for bacterial flagellin epitope flg22-triggered immunity, resulting in increased susceptibility to M. incognita, Botrytis cinerea, and Pseudomonas syringae pv. tomato (Pst) DC3000. The MiCE108 protein physically associates with the plant defense protease RD21A and promotes its degradation via the endosomal-dependent pathway, or 26S proteasome. Consistent with this, knockout of RD21A compromises the innate immunity of Arabidopsis and increases its susceptibility to a broad range of pathogens, including M. incognita, strongly indicating a role in defense against this nematode. Together, our data suggest that M. incognita deploys the effector MiCE108 to target Arabidopsis cysteine protease RD21A and affect its stability, thereby suppressing plant innate immunity and facilitating parasitism.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Nicotiana , Plant Diseases , Tylenchoidea , Animals , Arabidopsis/genetics , Arabidopsis/immunology , Arabidopsis/parasitology , Tylenchoidea/physiology , Tylenchoidea/pathogenicity , Arabidopsis Proteins/metabolism , Arabidopsis Proteins/genetics , Plant Diseases/parasitology , Plant Diseases/immunology , Plant Diseases/microbiology , Nicotiana/genetics , Nicotiana/parasitology , Nicotiana/immunology , Nicotiana/metabolism , Pseudomonas syringae/physiology , Pseudomonas syringae/pathogenicity , Botrytis/physiology , Botrytis/pathogenicity , Cysteine Proteases/metabolism , Cysteine Proteases/genetics , Plant Immunity , Host-Parasite Interactions , Plant Roots/parasitology , Plant Roots/genetics , Plant Roots/immunology , Plant Roots/metabolism , Reactive Oxygen Species/metabolism , Helminth Proteins/metabolism , Helminth Proteins/geneticsABSTRACT
Plant-parasitic nematodes are one of the most economically important pests of crops. It is widely accepted that horizontal gene transfer-the natural acquisition of foreign genes in parasitic nematodes-contributes to parasitism. However, an apparent paradox has emerged from horizontal gene transfer analyses: On the one hand, distantly related organisms with very dissimilar genetic structures (i.e. bacteria), and only transient interactions with nematodes as far as we know, dominate the list of putative donors, while on the other hand, considerably more closely related organisms (i.e. the host plant), with similar genetic structure (i.e. introns) and documented long-term associations with nematodes, are rare among the list of putative donors. Given that these nematodes ingest cytoplasm from a living plant cell for several weeks, there seems to be a conspicuous absence of plant-derived cases. Here, we used comparative genomic approaches to evaluate possible plant-derived horizontal gene transfer events in plant parasitic nematodes. Our evidence supports a cautionary message for plant-derived horizontal gene transfer cases in the sugar beet cyst nematode, Heterodera schachtii. We propose a 4-step model for horizontal gene transfer from plant to parasite in order to evaluate why the absence of plant-derived horizontal gene transfer cases is observed. We find that the plant genome is mobilized by the nematode during infection, but that uptake of the said "mobilome" is the first major barrier to horizontal gene transfer from host to nematode. These results provide new insight into our understanding of the prevalence/role of nucleic acid exchange in the arms race between plants and plant parasites.
Subject(s)
Plants , Tylenchoidea , Animals , Plants/genetics , DNA , Genomics , Tylenchoidea/genetics , Plant Diseases/parasitologyABSTRACT
Type-IV glandular trichomes, which only occur in the juvenile developmental phase of the cultivated tomato (Solanum lycopersicum), produce acylsugars that broadly protect against arthropod herbivory. Previously, we introgressed the capacity to retain type-IV trichomes in the adult phase from the wild tomato, Solanum galapagense, into the cultivated species cv. Micro-Tom (MT). The resulting MT-Galapagos enhanced trichome (MT-Get) introgression line contained 5 loci associated with enhancing the density of type-IV trichomes in adult plants. We genetically dissected MT-Get and obtained a subline containing only the locus on Chromosome 2 (MT-Get02). This genotype displayed about half the density of type-IV trichomes compared to the wild progenitor. However, when we stacked the gain-of-function allele of WOOLLY, which encodes a homeodomain leucine zipper IV transcription factor, Get02/Wo exhibited double the number of type-IV trichomes compared to S. galapagense. This discovery corroborates previous reports positioning WOOLLY as a master regulator of trichome development. Acylsugar levels in Get02/Wo were comparable to the wild progenitor, although the composition of acylsugar types differed, especially regarding fewer types with medium-length acyl chains. Agronomical parameters of Get02/Wo, including yield, were comparable to MT. Pest resistance assays showed enhanced protection against silverleaf whitefly (Bemisia tabaci), tobacco hornworm (Manduca sexta), and the fungus Septoria lycopersici. However, resistance levels did not reach those of the wild progenitor, suggesting the specificity of acylsugar types in the pest resistance mechanism. Our findings in trichome-mediated resistance advance the development of robust, naturally resistant tomato varieties, harnessing the potential of natural genetic variation. Moreover, by manipulating only 2 loci, we achieved exceptional results for a highly complex, polygenic trait, such as herbivory resistance in tomato.
Subject(s)
Solanum lycopersicum , Trichomes , Trichomes/genetics , Solanum lycopersicum/genetics , Solanum lycopersicum/parasitology , Animals , Plant Proteins/genetics , Plant Proteins/metabolism , Mutation/genetics , Herbivory , Multifactorial Inheritance , Manduca/physiology , Plant Diseases/genetics , Plant Diseases/parasitologyABSTRACT
The transcription factor WUSCHEL-RELATED HOMEOBOX 11 (WOX11) in Arabidopsis (Arabidopsis thaliana) initiates the formation of adventitious lateral roots upon mechanical injury in primary roots. Root-invading nematodes also induce de novo root organogenesis leading to excessive root branching, but it is not known if this symptom of disease involves mediation by WOX11 and if it benefits the plant. Here, we show with targeted transcriptional repression and reporter gene analyses in Arabidopsis that the beet cyst nematode Heterodera schachtii activates WOX11-mediated adventitious lateral rooting from primary roots close to infection sites. The activation of WOX11 in nematode-infected roots occurs downstream of jasmonic acid-dependent damage signaling via ETHYLENE RESPONSE FACTOR109, linking adventitious lateral root formation to nematode damage to host tissues. By measuring different root system components, we found that WOX11-mediated formation of adventitious lateral roots compensates for nematode-induced inhibition of primary root growth. Our observations further demonstrate that WOX11-mediated rooting reduces the impact of nematode infections on aboveground plant development and growth. Altogether, we conclude that the transcriptional regulation by WOX11 modulates root system plasticity under biotic stress, which is one of the key mechanisms underlying the tolerance of Arabidopsis to cyst nematode infections.
Subject(s)
Arabidopsis Proteins , Arabidopsis , Gene Expression Regulation, Plant , Plant Roots , Transcription Factors , Tylenchoidea , Animals , Plant Roots/parasitology , Plant Roots/genetics , Plant Roots/growth & development , Arabidopsis/parasitology , Arabidopsis/genetics , Arabidopsis/growth & development , Arabidopsis Proteins/genetics , Arabidopsis Proteins/metabolism , Tylenchoidea/physiology , Transcription Factors/genetics , Transcription Factors/metabolism , Plant Diseases/parasitology , Plant Diseases/genetics , Oxylipins/metabolism , Cyclopentanes/metabolism , Plants, Genetically ModifiedABSTRACT
Plants are resistant to most microbial species due to nonhost resistance (NHR), providing broad-spectrum and durable immunity. However, the molecular components contributing to NHR are poorly characterised. We address the question of whether failure of pathogen effectors to manipulate nonhost plants plays a critical role in NHR. RxLR (Arg-any amino acid-Leu-Arg) effectors from two oomycete pathogens, Phytophthora infestans and Hyaloperonospora arabidopsidis, enhanced pathogen infection when expressed in host plants (Nicotiana benthamiana and Arabidopsis, respectively) but the same effectors performed poorly in distantly related nonhost pathosystems. Putative target proteins in the host plant potato were identified for 64 P. infestans RxLR effectors using yeast 2-hybrid (Y2H) screens. Candidate orthologues of these target proteins in the distantly related non-host plant Arabidopsis were identified and screened using matrix Y2H for interaction with RxLR effectors from both P. infestans and H. arabidopsidis. Few P. infestans effector-target protein interactions were conserved from potato to candidate Arabidopsis target orthologues (cAtOrths). However, there was an enrichment of H. arabidopsidis RxLR effectors interacting with cAtOrths. We expressed the cAtOrth AtPUB33, which unlike its potato orthologue did not interact with P. infestans effector PiSFI3, in potato and Nicotiana benthamiana. Expression of AtPUB33 significantly reduced P. infestans colonization in both host plants. Our results provide evidence that failure of pathogen effectors to interact with and/or correctly manipulate target proteins in distantly related non-host plants contributes to NHR. Moreover, exploiting this breakdown in effector-nonhost target interaction, transferring effector target orthologues from non-host to host plants is a strategy to reduce disease.
Subject(s)
Arabidopsis , Disease Resistance , Host Specificity , Nicotiana , Plant Diseases , Plant Proteins , Arabidopsis/metabolism , Arabidopsis/parasitology , Oomycetes/metabolism , Phytophthora infestans/metabolism , Plant Diseases/parasitology , Plant Diseases/prevention & control , Plant Proteins/metabolism , Solanum tuberosum/parasitology , Nicotiana/metabolism , Nicotiana/parasitology , Two-Hybrid System TechniquesABSTRACT
BACKGROUND: Plant pathogens secrete effector proteins into host cells to suppress immune responses and manipulate fundamental cellular processes. One of these processes is autophagy, an essential recycling mechanism in eukaryotic cells that coordinates the turnover of cellular components and contributes to the decision on cell death or survival. RESULTS: We report the characterization of AVH195, an effector from the broad-spectrum oomycete plant pathogen, Phytophthora parasitica. We show that P. parasitica expresses AVH195 during the biotrophic phase of plant infection, i.e., the initial phase in which host cells are maintained alive. In tobacco, the effector prevents the initiation of cell death, which is caused by two pathogen-derived effectors and the proapoptotic BAX protein. AVH195 associates with the plant vacuolar membrane system and interacts with Autophagy-related protein 8 (ATG8) isoforms/paralogs. When expressed in cells from the green alga, Chlamydomonas reinhardtii, the effector delays vacuolar fusion and cargo turnover upon stimulation of autophagy, but does not affect algal viability. In Arabidopsis thaliana, AVH195 delays the turnover of ATG8 from endomembranes and promotes plant susceptibility to P. parasitica and the obligate biotrophic oomycete pathogen Hyaloperonospora arabidopsidis. CONCLUSIONS: Taken together, our observations suggest that AVH195 targets ATG8 to attenuate autophagy and prevent associated host cell death, thereby favoring biotrophy during the early stages of the infection process.
Subject(s)
Autophagy , Nicotiana , Phytophthora , Plant Diseases , Phytophthora/physiology , Plant Diseases/microbiology , Plant Diseases/parasitology , Nicotiana/microbiology , Autophagy-Related Protein 8 Family/metabolism , Autophagy-Related Protein 8 Family/genetics , Host-Pathogen InteractionsABSTRACT
Root-knot and cyst nematodes are two groups of plant parasitic nematodes that cause the majority of crop losses in agriculture. As a result, these nematodes are the focus of most nematode effector research. Root-knot and cyst nematode effectors are defined as secreted molecules, typically proteins, with crucial roles in nematode parasitism. There are likely hundreds of secreted effector molecules exuded through the nematode stylet into the plant. The current research has shown that nematode effectors can target a variety of host proteins and have impacts that include the suppression of plant immune responses and the manipulation of host hormone signaling. The discovery of effectors that localize to the nucleus indicates that the nematodes can directly modulate host gene expression for cellular reprogramming during feeding site formation. In addition, plant peptide mimicry by some nematode effectors highlights the sophisticated strategies the nematodes employ to manipulate host processes. Here we describe research on the interactions between nematode effectors and host proteins that will provide insights into the molecular mechanisms underpinning plant-nematode interactions. By identifying the host proteins and pathways that are targeted by root-knot and cyst nematode effectors, scientists can gain a better understanding of how nematodes establish feeding sites and subvert plant immune responses. Such information will be invaluable for future engineering of nematode-resistant crops, ultimately fostering advancements in agricultural practices and crop protection. [Formula: see text] The author(s) have dedicated the work to the public domain under the Creative Commons CC0 "No Rights Reserved" license by waiving all of his or her rights to the work worldwide under copyright law, including all related and neighboring rights, to the extent allowed by law, 2024.
Subject(s)
Cysts , Tylenchida , Tylenchoidea , Animals , Female , Tylenchoidea/genetics , Host-Parasite Interactions/physiology , Signal Transduction , Crops, Agricultural , Plant Diseases/parasitologyABSTRACT
Interactions between various microbial pathogens including viruses, bacteria, fungi, oomycetes, and their plant hosts have traditionally been the focus of phytopathology. In recent years, a significant and growing interest in the study of eukaryotic microorganisms not classified among fungi or oomycetes has emerged. Many of these protists establish complex interactions with photosynthetic hosts, and understanding these interactions is crucial in understanding the dynamics of these parasites within traditional and emerging types of farming, including marine aquaculture. Many phytopathogenic protists are biotrophs with complex polyphasic life cycles, which makes them difficult or impossible to culture, a fact reflected in a wide gap in the availability of comprehensive genomic data when compared to fungal and oomycete plant pathogens. Furthermore, our ability to use available genomic resources for these protists is limited by the broad taxonomic distance that these organisms span, which makes comparisons with other genomic datasets difficult. The current rapid progress in genomics and computational tools for the prediction of protein functions and interactions is revolutionizing the landscape in plant pathology. This is also opening novel possibilities, specifically for a deeper understanding of protist effectors. Tools like AlphaFold2 enable structure-based function prediction of effector candidates with divergent protein sequences. In turn, this allows us to ask better biological questions and, coupled with innovative experimental strategies, will lead into a new era of effector research, especially for protists, to expand our knowledge on these elusive pathogens and their interactions with photosynthetic hosts. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Photosynthesis , Plant Diseases , Plants , Plants/parasitology , Plants/microbiology , Plant Diseases/parasitology , Plant Diseases/microbiology , Host-Pathogen Interactions , Eukaryota/genetics , Genomics , Oomycetes/physiology , Oomycetes/pathogenicity , Oomycetes/geneticsABSTRACT
Mountain pine beetle (MPB; Dendroctonus ponderosae Hopkins) is a devastating forest insect pest that has killed millions of hectares of pines in western North America over the past two decades. Like other bark beetles, MPB vectors ophiostomatoid fungal species, some of which are pathogenic to host pine species. The phytopathogenicity of these fungal symbionts has sparked considerable debate regarding their role in facilitating MPB attack success. We tested the hypothesis that MPB ophiostomatoid fungal associates like Grosmannia clavigera (Robinson-Jeffrey and Davidson) Zipfel, de Beer and Wingfield contribute to overwhelming host defenses during MPB mass attack. We compared responses of mature lodgepole pine (Pinus contorta Dougl. ex Loud. var. latifolia Engelm.) trees growing in natural stands that were mass attacked by MPB with those inoculated with G. clavigera by examining host defense hormones, secondary metabolites, and gene expression profiles. The jasmonate and ethylene signatures of necrotrophic pathogen-triggered response were identified in G. clavigera-inoculated trees, but only the jasmonate signature of a herbivore-triggered response was measured in MPB-attacked trees. Several G. clavigera-induced changes in pine phenolic metabolite profiles and phenolic biosynthesis gene expression patterns were absent in MPB-attacked pines. These findings indicate that ophiostomatoid fungi like G. clavigera are not a major factor in overwhelming host defenses during MPB mass attack. Instead, fungal pathogenicity likely is more important in aiding MPB colonization and development within the host tree. Phenolics appear to play a larger role in the host response to G. clavigera than to MPB, although phenolics may also influence MPB feeding and behavior. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY 4.0 International license.
Subject(s)
Coleoptera , Ophiostomatales , Pinus , Symbiosis , Pinus/parasitology , Pinus/microbiology , Animals , Ophiostomatales/physiology , Coleoptera/microbiology , Coleoptera/physiology , Plant Diseases/microbiology , Plant Diseases/parasitology , Oxylipins/metabolism , Cyclopentanes/metabolism , Plant Growth Regulators/metabolism , Secondary Metabolism , Gene Expression Regulation, PlantABSTRACT
Cyst nematodes co-opt plant developmental programs for the establishment of a permanent feeding site called a syncytium in plant roots. In recent years, the role of plant developmental genes in syncytium formation has gained much attention. One main obstacle in studying the function of development-related genes in syncytium formation is that mutation or ectopic expression of such genes can cause pleiotropic phenotypes, making it difficult to interpret nematode-related phenotypes or, in some cases, impossible to carry out infection assays due to aberrant root development. Here, we tested three commonly used inducible gene expression systems for their application in beet cyst nematode infection assays of the model plant Arabidopsis thaliana. We found that even a low amount of ethanol diminished nematode development, deeming the ethanol-based system unsuitable for use in cyst nematode infection assays, whereas treatment with estradiol or dexamethasone did not negatively affect cyst nematode viability. Dose and time course responses showed that in both systems, a relatively low dose of inducer (1 µM) is sufficient to induce high transgene expression within 24 h of treatment. Transgene expression peaked at 3 to 5 days post-induction and began to decline thereafter, providing a perfect window for inducible transgenes to interfere with syncytium establishment while minimizing any adverse effects on root development. These results indicate that both estradiol- and dexamethasone-based inducible gene expression systems are suitable for cyst nematode infection assays. The employment of such systems provides a powerful tool to investigate the function of essential plant developmental genes in syncytium formation. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Arabidopsis , Beta vulgaris , Gene Expression Regulation, Plant , Plant Diseases , Plant Roots , Arabidopsis/parasitology , Arabidopsis/genetics , Animals , Plant Diseases/parasitology , Beta vulgaris/parasitology , Plant Roots/parasitology , Plant Roots/genetics , Dexamethasone/pharmacology , Plants, Genetically Modified , Ethanol/pharmacology , Giant Cells/parasitology , Estradiol/pharmacology , Tylenchoidea/physiology , Transgenes , NematodaABSTRACT
Bemisia tabaci (whitefly) is a polyphagous agroeconomic pest species complex. Two members of this species complex, Mediterranean (MED) and Middle-East-Asia Minor 1 (MEAM1), have a worldwide distribution and have been shown to manipulate plant defenses through effectors. In this study, we used three different strategies to identify three MEAM1 proteins that can act as effectors. Effector B1 was identified using a bioinformatics-driven effector-mining strategy, whereas effectors S1 and P1 were identified in the saliva of whiteflies collected from artificial diet and in phloem exudate of tomato on which nymphs were feeding, respectively. These three effectors were B. tabaci specific and able to increase whitefly fecundity when transiently expressed in tobacco plants (Nicotiana tabacum). Moreover, they reduced growth of Pseudomonas syringae pv. tabaci in Nicotiana benthamiana. All three effectors changed gene expression in planta, and B1 and S1 also changed phytohormone levels. Gene ontology and KEGG pathway enrichment analysis pinpointed plant-pathogen interaction and photosynthesis as the main enriched pathways for all three effectors. Our data thus show the discovery and validation of three new B. tabaci MEAM1 effectors that increase whitefly fecundity and modulate plant immunity. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Hemiptera , Nicotiana , Animals , Nicotiana/genetics , Nicotiana/microbiology , Insect Proteins/genetics , Insect Proteins/metabolism , Solanum lycopersicum/genetics , Solanum lycopersicum/microbiology , Solanum lycopersicum/parasitology , Pseudomonas syringae/physiology , Plant Diseases/parasitology , Plant Diseases/microbiology , Plant Growth Regulators/metabolism , Fertility/geneticsABSTRACT
Soybean cyst nematode (Heterodera glycines, soybean cyst nematode [SCN]) disease adversely affects the yield of soybean and leads to billions of dollars in losses every year. To control the disease, it is necessary to study the resistance genes of the plant and their mechanisms. Isoflavonoids are secondary metabolites of the phenylalanine pathway, and they are synthesized in soybean. They are essential in plant response to biotic and abiotic stresses. In this study, we reported that phenylalanine ammonia-lyase (PAL) genes GmPALs involved in isoflavonoid biosynthesis, can positively regulate soybean resistance to SCN. Our previous study demonstrated that the expression of GmPAL genes in the resistant cultivar Huipizhi (HPZ) heidou are strongly induced by SCN. PAL is the rate-limiting enzyme that catalyzes the first step of phenylpropanoid metabolism, and it responds to biotic or abiotic stresses. Here, we demonstrate that the resistance of soybeans against SCN is suppressed by PAL inhibitor l-α-(aminooxy)-ß-phenylpropionic acid (L-AOPP) treatment. Overexpression of eight GmPAL genes caused diapause of nematodes in transgenic roots. In a petiole-feeding bioassay, we identified that two isoflavones, daidzein and genistein, could enhance resistance against SCN and suppress nematode development. This study thus reveals GmPAL-mediated resistance against SCN, information that has good application potential. The role of isoflavones in soybean resistance provides new information for the control of SCN. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Disease Resistance , Gene Expression Regulation, Plant , Glycine max , Isoflavones , Phenylalanine Ammonia-Lyase , Plant Diseases , Tylenchoidea , Glycine max/genetics , Glycine max/parasitology , Tylenchoidea/physiology , Plant Diseases/parasitology , Plant Diseases/immunology , Plant Diseases/genetics , Animals , Phenylalanine Ammonia-Lyase/genetics , Phenylalanine Ammonia-Lyase/metabolism , Disease Resistance/genetics , Isoflavones/pharmacology , Isoflavones/metabolism , Plant Proteins/genetics , Plant Proteins/metabolism , Plants, Genetically ModifiedABSTRACT
Small RNAs (sRNAs) are involved in gene silencing in multiple ways, including through cross-kingdom transfers from parasites to their hosts. Little is known about the evolutionary mechanisms enabling eukaryotic microbes to evolve functional mimics of host small regulatory RNAs. Here, we describe the identification and functional characterization of SINE_sRNA1, an sRNA family derived from highly abundant short interspersed nuclear element (SINE) retrotransposons in the genome of the wheat powdery mildew pathogen. SINE_sRNA1 is encoded by a sequence motif that is conserved in multiple SINE families and corresponds to a functional plant microRNA (miRNA) mimic targeting Tae_AP1, a wheat gene encoding an aspartic protease only found in monocots. Tae_AP1 has a novel function enhancing both pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), thereby contributing to the cross activation of plant defenses. We conclude that SINE_sRNA1 and Tae_AP1 are functional innovations, suggesting the contribution of transposons to the evolutionary arms race between a parasite and its host. [Formula: see text] Copyright © 2024 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.
Subject(s)
Ascomycota , Plant Diseases , Plant Immunity , Triticum , Plant Diseases/microbiology , Plant Diseases/immunology , Plant Diseases/genetics , Plant Diseases/parasitology , Triticum/genetics , Triticum/microbiology , Triticum/immunology , Ascomycota/pathogenicity , Ascomycota/genetics , Ascomycota/physiology , Plant Immunity/genetics , Host-Pathogen Interactions/genetics , Gene Expression Regulation, Plant , MicroRNAs/genetics , RNA, Plant/genetics , DNA Transposable Elements/genetics , Short Interspersed Nucleotide Elements/genetics , Conserved Sequence/genetics , Base SequenceABSTRACT
Plant parasitic root-knot nematodes are major agricultural pests worldwide, as they infect plant roots and cause substantial damages to crop plants. Root-knot nematodes induce specialized feeding cells known as giant cells (GCs) in the root vasculature, which serve as nutrient reservoirs for the infecting nematodes. Here, we show that the cell walls of GCs thicken to form pitted patterns that superficially resemble metaxylem cells. Interestingly, VASCULAR-RELATED NAC-DOMAIN1 (VND1) was found to be upregulated, while the xylem-type programmed cell death marker XYLEM CYSTEINE PEPTIDASE 1 was downregulated upon nematode infection. The vnd2 and vnd3 mutants showed reduced secondary cell wall pore size, while the vnd1 vnd2 vnd3 triple mutant produced significantly fewer nematode egg masses when compared with the wild type. These results suggest that the GC development pathway likely shares common signaling modules with the metaxylem differentiation pathway and VND1, VND2, and VND3 redundantly regulate plant-nematode interaction through secondary cell wall formation.