Regulation and Functions of Long Noncoding RNAs During <i>Meloidogyne incognita</i> Parasitism of Tomato

Long noncoding RNAs (lncRNAs) are emerging as important regulators of various aspects of immune response and plant-pathogen interactions. However, the regulatory function of lncRNAs during plant-nematode interaction remains largely elusive. In this study, we investigated the differential regulation and function of lncRNAs during two different stages of tomato infection by the root-knot nematode <i>Meloidogyne incognita</i>. At the early stage of infection, 2,218 and 2,827 lncRNAs were regulated locally in the <i>M. incognita</i>-induced galls and systemically in the neighboring root cells, respectively. However, at the later stage of infection, the number of <i>M. incognita</i>-regulated lncRNAs was dramatically reduced, with only 49 lncRNAs being identified as differentially expressed. Differentially expressed lncRNAs were predicted to encode peptides with functionally annotated domains, providing insights into the potential roles of these peptides in regulating gene expression, RNA stability and splicing, and protein-protein-interactions. Among the differentially expressed lncRNAs, 55 were found to contain putative binding sites for 56 microRNAs (miRNAs). Overexpressing five of these lncRNAs significantly increased tomato resistance to <i>M. incognita</i>, supporting the functional importance of lncRNAs for establishing tomato-<i>M. incognita</i> interaction. Functional analysis of the target mimicry of lncRNAs towards miRNAs resulted in the identification of two novel regulatory modules involving miR47 and miR156e-5p and their targeted genes that regulate tomato responses to <i>M. incognita</i> parasitism. Taken together, our data provide novel insights into the transcriptional and posttranscriptional regulatory functions of lncRNA and open a new avenue to engineer crop plants with enhanced nematode resistance by leveraging the regulatory potential of lncRNAs. [Formula: see text] Copyright © 2025 The Author(s). This is an open access article distributed under the CC BY-NC-ND 4.0 International license.