{"doi":"10.3389/fpls.2024.1383986","title":"Exploring the putative microRNAs cross-kingdom transfer in Solanum lycopersicum-Meloidogyne incognita interactions","abstract":"<jats:sec><jats:title>Introduction</jats:title><jats:p>Plant-pathogen interaction is an inexhaustible source of information on how to sustainably control diseases that negatively affect agricultural production. <jats:italic>Meloidogyne incognita</jats:italic> is a root-knot nematode (RKN), representing a pest for many crops, including tomato (<jats:italic>Solanum lycopersicum</jats:italic>). RKNs are a global threat to agriculture, especially under climate change, and RNA technologies offer a potential alternative to chemical nematicides. While endogenous microRNAs have been identified in both <jats:italic>S. lycopersicum</jats:italic> and <jats:italic>M. incognita</jats:italic>, and their roles have been related to the regulation of developmental changes, no study has investigated the miRNAs cross-kingdom transfer during this interaction.</jats:p></jats:sec><jats:sec><jats:title>Methods</jats:title><jats:p>Here, we propose a bioinformatics pipeline to highlight potential miRNA-dependent cross-kingdom interactions between tomato and <jats:italic>M. incognita</jats:italic>.</jats:p></jats:sec><jats:sec><jats:title>Results</jats:title><jats:p>The obtained data show that nematode miRNAs putatively targeting tomato genes are mostly related to detrimental effects on plant development and defense. Similarly, tomato miRNAs putatively targeting <jats:italic>M. incognita</jats:italic> biological processes have negative effects on digestion, mobility, and reproduction. To experimentally test this hypothesis, an <jats:italic>in vitro</jats:italic> feeding assay was carried out using sly-miRNAs selected from the bioinformatics approach. The results show that two tomato miRNAs (sly-miRNA156a, sly-miR169f) soaked by juvenile larvae (J2s) affected their ability to infect plant roots and form galls. This was also coupled with a significant downregulation of predicted target genes (<jats:italic>Minc11367, Minc00111</jats:italic>), as revealed by a qRT-PCR analysis.</jats:p></jats:sec><jats:sec><jats:title>Discussions</jats:title><jats:p>Therefore, the current study expands the knowledge related to the cross-kingdom miRNAs involvement in host-parasite interactions and could pave the way for the application of exogenous plant miRNAs as tools to control nematode infection.</jats:p></jats:sec>","journal":"Frontiers in Plant Science","year":2024,"id":650582,"datarank":0.24141568686511508,"base_score":1.6094379124341003,"endowment":1.6094379124341003,"self_citation_contribution":0.24141568686511508,"citation_network_contribution":0.0,"self_endowment_contribution":0.24141568686511508,"citer_contribution":0.0,"corpus_percentile":null,"corpus_rank":null,"citation_count":4,"citer_count":0,"citers_with_citation_signal":0,"citers_with_endowment":0,"datacite_reuse_total":0,"is_dataset":false,"is_dataset_confidence":null,"is_data_producer":false,"deposit_databanks":null,"is_oa":false,"file_count":0,"downloads":0,"has_version_chain":false,"published_date":null,"fair_score":null,"fair_percentile":null,"algorithm_id":"datarank_citation_only_1hop_v6","ranking_scope":"data_only","authors":[{"id":1696369,"name":"Debora Dallera","orcid":null,"position":1,"is_corresponding":false},{"id":1696370,"name":"Davide De Marchi","orcid":null,"position":2,"is_corresponding":false},{"id":1696371,"name":"Pamela Candito","orcid":null,"position":3,"is_corresponding":false},{"id":1696372,"name":"Lorenzo Pasotti","orcid":null,"position":4,"is_corresponding":false},{"id":1696374,"name":"Anca Macovei","orcid":null,"position":5,"is_corresponding":false},{"id":1696368,"name":"Paola Leonetti","orcid":null,"position":0,"is_corresponding":false}],"reference_count":0,"raw_metadata":{"has_enrichment":true,"resolved":true,"title":"Exploring the putative microRNAs cross-kingdom transfer in <i>Solanum lycopersicum-Meloidogyne incognita</i> interactions.","abstract":"<h4>Introduction</h4>Plant-pathogen interaction is an inexhaustible source of information on how to sustainably control diseases that negatively affect agricultural production. <i>Meloidogyne incognita</i> is a root-knot nematode (RKN), representing a pest for many crops, including tomato (<i>Solanum lycopersicum</i>). RKNs are a global threat to agriculture, especially under climate change, and RNA technologies offer a potential alternative to chemical nematicides. While endogenous microRNAs have been identified in both <i>S. lycopersicum</i> and <i>M. incognita</i>, and their roles have been related to the regulation of developmental changes, no study has investigated the miRNAs cross-kingdom transfer during this interaction.<h4>Methods</h4>Here, we propose a bioinformatics pipeline to highlight potential miRNA-dependent cross-kingdom interactions between tomato and <i>M. incognita</i>.<h4>Results</h4>The obtained data show that nematode miRNAs putatively targeting tomato genes are mostly related to detrimental effects on plant development and defense. Similarly, tomato miRNAs putatively targeting <i>M. incognita</i> biological processes have negative effects on digestion, mobility, and reproduction. To experimentally test this hypothesis, an <i>in vitro</i> feeding assay was carried out using sly-miRNAs selected from the bioinformatics approach. The results show that two tomato miRNAs (sly-miRNA156a, sly-miR169f) soaked by juvenile larvae (J2s) affected their ability to infect plant roots and form galls. This was also coupled with a significant downregulation of predicted target genes (<i>Minc11367, Minc00111</i>), as revealed by a qRT-PCR analysis.<h4>Discussions</h4>Therefore, the current study expands the knowledge related to the cross-kingdom miRNAs involvement in host-parasite interactions and could pave the way for the application of exogenous plant miRNAs as tools to control nematode infection.","is_dataset_classified":null,"base_score":0.0,"endowment":0.0,"datacite_reuse_total":0,"file_count":0,"downloads":0,"views":0,"has_version_chain":false,"is_dataset":false,"is_oa":false,"pmid":"38784062","pmcid":"PMC11114104","openalex_id":null,"authors":[],"funders":[],"total_grants":0,"fwci":null,"citation_percentile":null,"influential_citations":0,"citation_trend":[],"oa_status":"gold","license":"cc-by","oa_locations":[{"url":"https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2024.1383986/pdf","host_type":"publisher"},{"url":"https://pmc.ncbi.nlm.nih.gov/articles/PMC11114104/pdf/fpls-15-1383986.pdf","host_type":"repository"},{"url":"https://doaj.org/article/39a09a327ce045adb5d6b4130e2833e7","host_type":"repository"},{"url":"https://europepmc.org/articles/PMC11114104","host_type":"Europe_PMC"},{"url":"https://europepmc.org/articles/PMC11114104?pdf=render","host_type":"Europe_PMC"}],"fields_of_study":[],"mesh_terms":[],"keywords":["Tomato","root-knot nematode","miRNAs","Plant-pathogen Interaction","Bioinformatics Pipeline","Cross-species Target Prediction"],"sdg_mappings":[],"linked_datasets":[],"clinical_trials":[],"software_tools":[],"database_accessions":[{"name":"gen"},{"name":"go"}],"source":"live","citation_network_status":"fetched"},"created_at":"2026-08-10T05:44:13.777875Z","pmid":null,"pmcid":null,"fwci":null,"citation_percentile":null,"influential_citations":0,"oa_status":null,"license":null,"views":0,"total_file_size_bytes":0,"version_count":0,"fair_f":null,"fair_a":null,"fair_i":null,"fair_r":null,"fair_zscore":null,"fair_rationale":null,"fair_model":null,"fair_agent_version":null,"fair_fulltext_source":null,"fair_has_llm":null,"fair_computed_at":null,"clinical_trials":[],"software_tools":[],"db_accessions":[],"linked_datasets":[],"topics":[]}