A parasitism gene from a plant‐parasitic nematode with function similar to CLAVATA3/ESR (CLE) of Arabidopsis thaliana
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PROVIDER: S-EPMC6640389 | biostudies-literature | 2009 Jan
REPOSITORIES: biostudies-literature
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Project description:In this article, we present the cloning of two CLAVATA3/ESR (CLE)-like genes, HsCLE1 and HsCLE2, from the beet cyst nematode Heterodera schachtii, a plant-parasitic cyst nematode with a relatively broad host range that includes the model plant Arabidopsis. CLEs are small secreted peptide ligands that play important roles in plant growth and development. By secreting peptide mimics of plant CLEs, the nematode can developmentally reprogramme root cells for the formation of unique feeding sites within host roots for its own benefit. Both HsCLE1 and HsCLE2 encode small secreted polypeptides with a conserved C-terminal CLE domain sharing highest similarity to Arabidopsis CLEs 1-7. Moreover, HsCLE2 contains a 12-amino-acid CLE motif that is identical to AtCLE5 and AtCLE6. Like all other plant and nematode CLEs identified to date, HsCLEs caused wuschel-like phenotypes when overexpressed in Arabidopsis, and this activity was abolished when the proteins were expressed without the CLE motif. HsCLEs could also function in planta without a signal peptide, highlighting the unique, yet conserved function of nematode CLE variable domains in trafficking CLE peptides for secretion. In a direct comparison of HsCLE2 overexpression phenotypes with those of AtCLE5 and AtCLE6, similar shoot and root phenotypes were observed. Exogenous application of 12-amino-acid synthetic peptides corresponding to the CLE motifs of HsCLEs and AtCLE5/6 suggests that the function of this class of CLEs may be subject to complex endogenous regulation. When seedlings were grown on high concentrations of peptide (10 µm), root growth was suppressed; however, when seedlings were grown on low concentrations of peptide (0.1 µm), root growth was stimulated. Together, these findings indicate that AtCLEs1-7 may be the target peptides mimicked by HsCLEs to promote parasitism.
| S-EPMC6640238 | biostudies-literature
Project description:The potato rot nematode, Ditylenchus destructor, is a very destructive nematode pest on many agriculturally important crops worldwide, but the molecular characterization of its parasitism of plant has been limited. The effectors involved in nematode parasitism of plant for several sedentary endo-parasitic nematodes such as Heterodera glycines, Globodera rostochiensis and Meloidogyne incognita have been identified and extensively studied over the past two decades. Ditylenchus destructor, as a migratory plant parasitic nematode, has different feeding behavior, life cycle and host response. Comparing the transcriptome and parasitome among different types of plant-parasitic nematodes is the way to understand more fully the parasitic mechanism of plant nematodes. We undertook the approach of sequencing expressed sequence tags (ESTs) derived from a mixed stage cDNA library of D. destructor. This is the first study of D. destructor ESTs. A total of 9800 ESTs were grouped into 5008 clusters including 3606 singletons and 1402 multi-member contigs, representing a catalog of D. destructor genes. Implementing a bioinformatics' workflow, we found 1391 clusters have no match in the available gene database; 31 clusters only have similarities to genes identified from D. africanus, the most closely related species to D. destructor; 1991 clusters were annotated using Gene Ontology (GO); 1550 clusters were assigned enzyme commission (EC) numbers; and 1211 clusters were mapped to 181 KEGG biochemical pathways. 22 ESTs had similarities to reported nematode effectors. Interestedly, most of the effectors identified in this study are involved in host cell wall degradation or modification, such as 1,4-beta-glucanse, 1,3-beta-glucanse, pectate lyase, chitinases and expansin, or host defense suppression such as calreticulin, annexin and venom allergen-like protein. This result implies that the migratory plant-parasitic nematode D. destructor secrets similar effectors to those of sedentary plant nematodes. Finally we further characterized the two D. destructor expansin proteins.
| S-EPMC3726699 | biostudies-literature
Project description:CLE peptides are key regulators of cell proliferation and differentiation in plant shoots, roots, vasculature, and legume nodules. They are C-terminally encoded peptides that are post-translationally cleaved and modified from their corresponding pre-propeptides to produce a final ligand that is 12-13 amino acids in length. In this study, an array of bionformatic and comparative genomic approaches was used to identify and characterize the complete family of CLE peptide-encoding genes in two of the world's most important crop species, soybean and common bean. In total, there are 84 CLE peptide-encoding genes in soybean (considerably more than the 32 present in Arabidopsis), including three pseudogenes and two multi-CLE domain genes having six putative CLE domains each. In addition, 44 CLE peptide-encoding genes were identified in common bean. In silico characterization was used to establish all soybean homeologous pairs, and to identify corresponding gene orthologues present in common bean and Arabidopsis. The soybean CLE pre-propeptide family was further analysed and separated into seven distinct groups based on structure, with groupings strongly associated with the CLE domain sequence and function. These groups provide evolutionary insight into the CLE peptide families of soybean, common bean, and Arabidopsis, and represent a novel tool that can aid in the functional characterization of the peptides. Transcriptional evidence was also used to provide further insight into the location and function of all CLE peptide-encoding members currently available in gene atlases for the three species. Taken together, this in-depth analysis helped to identify and categorize the complete CLE peptide families of soybean and common bean, established gene orthologues within the two legume species, and Arabidopsis, and provided a platform to help compare, contrast, and identify the function of critical CLE peptide hormones in plant development.
| S-EPMC4526924 | biostudies-literature
Project description:The plant-parasitic nematodes are considered as one of the most destructive pests, from which the migratory and sedentary endoparasitic plant parasitic nematodes infect more than 4000 plant species and cause over $100 billion crop losses annually worldwide. These nematodes use multiple strategies to infect their host and to establish a successful parasitism inside the host such as cell-wall degradation enzymes, inhibition of host defense proteins, and molecular mimicry. In the present study, the main parasitism-associated gene families were identified and compared between the migratory and sedentary endoparasitic nematodes. The results showed that the migratory and sedentary endoparasitic nematodes share a core conserved parasitism mechanism established throughout the evolution of parasitism. However, genes involved in pectin degradation and hydrolase activity are rapidly evolving in the migratory endoparasitic nematodes. Additionally, cell-wall degrading enzymes such as GH45 cellulases and pectate lyase and peptidase and peptidase inhibitors were expanded in the migratory endoparasitic nematodes. The molecular mimicry mechanism was another key finding that differs between the endoparasitic and sedentary parasitic nematodes. The PL22 gene family, which is believed to play a significant role in the molecular mechanisms of nematode parasitism, has been found to be present exclusively in migratory endoparasitic nematodes. Phylogenetic analysis has suggested that it was de novo born in these nematodes. This discovery sheds new light on the molecular evolution of these parasites and has significant implications for our understanding of their biology and pathogenicity. This study contributes to our understanding of core parasitism mechanisms conserved throughout the nematodes and provides unique clues on the evolution of parasitism and the direction shaped by the host.
| S-EPMC10866927 | biostudies-literature
Project description:CLAVATA3/ESR-related (CLE) peptides perform a variety of important functions in plant development and historically have been targeted during the domestication of existing crops. Pennycress (Thlaspi arvense) is an emerging biofuel crop currently undergoing domestication that offers novel monetary and environmental incentives as a winter cover crop during an otherwise fallow period of the corn/soybean farming rotation. Here we report the characterization of the CLE gene family in pennycress through homology comparison of the CLE motif with other dicot species by conducting a homology comparison and maximum likelihood phylogenetic analysis supplemented with manual annotation. Twenty-seven pennycress CLE genes were identified, and their expression analyzed through transcriptome profiling and RT-qPCR. Our study provides a genome-wide analysis of the CLE gene family in pennycress and carries significant value for accelerating the domestication of this crop through identification of potential key developmental regulatory genes.
| S-EPMC10436580 | biostudies-literature
Project description:Coprinopsis cinerea lectin 2 (CCL2) is a fucoside-binding lectin from the basidiomycete C. cinerea that is toxic to the bacterivorous nematode Caenorhabditis elegans as well as animal-parasitic and fungivorous nematodes. We expressed CCL2 in Arabidopsis to assess its protective potential toward plant-parasitic nematodes. Our results demonstrate that expression of CCL2 enhances host resistance against the cyst nematode Heterodera schachtii. Surprisingly, CCL2-expressing plants were also more resistant to fungal pathogens including Botrytis cinerea, and the phytopathogenic bacterium Pseudomonas syringae. In addition, CCL2 expression positively affected plant growth indicating that CCL2 has the potential to improve two important agricultural parameters namely biomass production and general disease resistance. The mechanism of the CCL2-mediated enhancement of plant disease resistance depended on fucoside-binding by CCL2 as transgenic plants expressing a mutant version of CCL2 (Y92A), compromised in fucoside-binding, exhibited wild type (WT) disease susceptibility. The protective effect of CCL2 did not seem to be direct as the lectin showed no growth-inhibition toward B. cinerea in in vitro assays. We detected, however, a significantly enhanced transcriptional induction of plant defense genes in CCL2- but not CCL2-Y92A-expressing lines in response to infection with B. cinerea compared to WT plants. This study demonstrates a potential of fungal defense lectins in plant protection beyond their use as toxins.
| S-EPMC8063123 | biostudies-literature
Project description:BackgroundThere is a rapidly growing awareness that plant peptide signalling molecules are numerous and varied and they are known to play fundamental roles in angiosperm plant growth and development. Two closely related peptide signalling molecule families are the CLAVATA3-EMBRYO-SURROUNDING REGION (CLE) and CLE-LIKE (CLEL) genes, which encode precursors of secreted peptide ligands that have roles in meristem maintenance and root gravitropism. Progress in peptide signalling molecule research in gymnosperms has lagged behind that of angiosperms. We therefore sought to identify CLE and CLEL genes in gymnosperms and conduct a comparative analysis of these gene families with angiosperms.ResultsWe undertook a meta-analysis of the GenBank/EMBL/DDBJ gymnosperm EST database and the Picea abies and P. glauca genomes and identified 93 putative CLE genes and 11 CLEL genes among eight Pinophyta species, in the genera Cryptomeria, Pinus and Picea. The predicted conifer CLE and CLEL protein sequences had close phylogenetic relationships with their homologues in Arabidopsis. Notably, perfect conservation of the active CLE dodecapeptide in presumed orthologues of the Arabidopsis CLE41/44-TRACHEARY ELEMENT DIFFERENTIATION (TDIF) protein, an inhibitor of tracheary element (xylem) differentiation, was seen in all eight conifer species. We cloned the Pinus radiata CLE41/44-TDIF orthologues. These genes were preferentially expressed in phloem in planta as expected, but unexpectedly, also in differentiating tracheary element (TE) cultures. Surprisingly, transcript abundances of these TE differentiation-inhibitors sharply increased during early TE differentiation, suggesting that some cells differentiate into phloem cells in addition to TEs in these cultures. Applied CLE13 and CLE41/44 peptides inhibited root elongation in Pinus radiata seedlings. We show evidence that two CLEL genes are alternatively spliced via 3'-terminal acceptor exons encoding separate CLEL peptides.ConclusionsThe CLE and CLEL genes are found in conifers and they exhibit at least as much sequence diversity in these species as they do in other plant species. Only one CLE peptide sequence has been 100% conserved between gymnosperms and angiosperms over 300 million years of evolutionary history, the CLE41/44-TDIF peptide and its likely conifer orthologues. The preferential expression of these vascular development-regulating genes in phloem in conifers, as they are in dicot species, suggests close parallels in the regulation of secondary growth and wood formation in gymnosperm and dicot plants. Based on our bioinformatic analysis, we predict a novel mechanism of regulation of the expression of several conifer CLEL peptides, via alternative splicing resulting in the selection of alternative C-terminal exons encoding separate CLEL peptides.
| S-EPMC4016512 | biostudies-literature
Project description:Nematode migration, feeding site formation, withdrawal of plant assimilates, and activation of plant defence responses have a significant impact on plant growth and development. Plants display intraspecific variation in tolerance limits for root-feeding nematodes. Although disease tolerance has been recognized as a distinct trait in biotic interactions of mainly crops, we lack mechanistic insights. Progress is hampered by difficulties in quantification and laborious screening methods. We turned to the model plant Arabidopsis thaliana, since it offers extensive resources to study the molecular and cellular mechanisms underlying nematode-plant interactions. Through imaging of tolerance-related parameters, the green canopy area was identified as an accessible and robust measure for assessing damage due to cyst nematode infection. Subsequently, a high-throughput phenotyping platform simultaneously measuring the green canopy area growth of 960 A. thaliana plants was developed. This platform can accurately measure cyst nematode and root-knot nematode tolerance limits in A. thaliana through classical modelling approaches. Furthermore, real-time monitoring provided data for a novel view of tolerance, identifying a compensatory growth response. These findings show that our phenotyping platform will enable a new mechanistic understanding of tolerance to below-ground biotic stress.
| S-EPMC10540735 | biostudies-literature
Project description:Root-knot nematodes (RKNs) are obligate biotrophic parasites that invade plant roots and engage in prolonged and intimate relationships with their hosts. Nematode secretions, some of which have immunosuppressing activity, play essential roles in successful parasitism; however, their mechanisms of action remain largely unknown. Here, we show that the RKN-specific gene MiMsp40, cloned from Meloidogyne incognita, is expressed exclusively in subventral oesophageal gland cells and is strongly upregulated during early parasitic stages. Arabidopsis plants overexpressing MiMsp40 were more susceptible to nematode infection than were wild type plants. Conversely, the host-derived MiMsp40 RNAi suppressed nematode parasitism and/or reproduction. Moreover, overexpression of MiMsp40 in plants suppressed the deposition of callose and the expression of marker genes for bacterial elicitor elf18-triggered immunity. Transient expression of MiMsp40 prevented Bax-triggered defence-related programmed cell death. Co-agroinfiltration assays indicated that MiMsp40 also suppressed macroscopic cell death triggered by MAPK cascades or by the ETI cognate elicitors R3a/Avr3a. Together, these results demonstrate that MiMsp40 is a novel Meloidogyne-specific effector that is injected into plant cells by early parasitic stages of the nematode and that plays a role in suppressing PTI and/or ETI signals to facilitate RKN parasitism.
| S-EPMC4726423 | biostudies-literature
Project description: Not available
| S-EPMC10873892 | biostudies-literature