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Background  Verticillium wilt is a widespread and destructive disease, which causes serious loss of cotton yield and quality. Long non-coding RNA (lncRNA) is involved in many biological processes, such as plant disease resistance response, through a variety of regulatory mechanisms, but their possible roles in cotton against  Verticillium dahliae  infection remain largely unclear.    Results  Here, we measured the transcriptome of resistant  G. hirsutum  following infection by  V. dahliae  and 4277 differentially expressed lncRNAs (delncRNAs) were identified. Localization and abundance analysis revealed that delncRNAs were biased distribution on chromosomes. We explored the dynamic characteristics of disease resistance related lncRNAs in chromosome distribution, induced expression profiles, biological function, and these lncRNAs were divided into three categories according to their induced expression profiles. For the delncRNAs, 687  cis -acting pairs and 14,600  trans -acting pairs of lncRNA-mRNA were identified, which indicated that  trans -acting was the main way of Verticillium wilt resistance-associated lncRNAs regulating target mRNAs in cotton. Analyzing the regulation pattern of delncRNAs revealed that  cis -acting and  trans -acting lncRNAs had different ways to influence target genes. Gene Ontology (GO) enrichment analysis revealed that the regulatory function of delncRNAs participated significantly in stimulus response process, kinase activity and plasma membrane components. Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis indicated that delncRNAs participated in some important disease resistance pathways, such as plant-pathogen interaction, alpha-linolenic acid metabolism and plant hormone signal transduction. Additionally, 21 delncRNAs and 10 target genes were identified as being involved in alpha-linolenic acid metabolism associated with the biosynthesis of jasmonic acid (JA). Subsequently, we found that  GhlncLOX3  might regulate resistance to  V. dahliae  through modulating the expression of  GhLOX3  implicated in JA biosynthesis. Further functional analysis showed that  GhlncLOX3 -silenced seedlings displayed a reduced resistance to  V. dahliae , with down-regulated expression of  GhLOX3  and decreased content of JA.    Conclusion  This study shows the dynamic characteristics of delncRNAs in multiaspect, and suggests that  GhlncLOX3 - GhLOX3 -JA network participates in response to  V. dahliae  invasion. Our results provide novel insights for genetic improvement of Verticillium wilt resistance in cotton using lncRNAs.    Supplementary Information  The online version contains supplementary material available at 10.1186/s12870-021-02835-8.

bmc plant biology

Dynamic characteristics and functional analysis provide new insights into long non-coding RNA responsive to Verticillium dahliae infection in Gossypium hirsutum