AUTHOR=Leonetti Paola , Dallera Debora , De Marchi Davide , Candito Pamela , Pasotti Lorenzo , Macovei Anca 

TITLE=Exploring the putative microRNAs cross-kingdom transfer in Solanum lycopersicum-Meloidogyne incognita interactions

JOURNAL=Frontiers in Plant Science

VOLUME=15

YEAR=2024

URL=https://www.frontiersin.org/journals/plant-science/articles/10.3389/fpls.2024.1383986

DOI=10.3389/fpls.2024.1383986

ISSN=1664-462X

ABSTRACT=<sec><title>Introduction</title><p>Plant-pathogen interaction is an inexhaustible source of information on how to sustainably control diseases that negatively affect agricultural production. <italic>Meloidogyne incognita</italic> is a root-knot nematode (RKN), representing a pest for many crops, including tomato (<italic>Solanum lycopersicum</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 <italic>S. lycopersicum</italic> and <italic>M. incognita</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.</p></sec><sec><title>Methods</title><p>Here, we propose a bioinformatics pipeline to highlight potential miRNA-dependent cross-kingdom interactions between tomato and <italic>M. incognita</italic>.</p></sec><sec><title>Results</title><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 <italic>M. incognita</italic> biological processes have negative effects on digestion, mobility, and reproduction. To experimentally test this hypothesis, an <italic>in vitro</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 (<italic>Minc11367, Minc00111</italic>), as revealed by a qRT-PCR analysis.</p></sec><sec><title>Discussions</title><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.</p></sec>