Genome-wide identification and expression analysis of long noncoding RNAs in <i>MdHYL1</i>-mediated regulation of leaf development and water transport in apple

HYL1 serves as a central component of the miRNA processing machinery, playing a vital role in coordinating plant development and adaptation to environmental stresses. In apple, MdHYL1 knockdown impairs leaf development and water transport, though whether this regulation involves miRNA/lncRNA networks remains unclear. To elucidate the regulatory mechanisms underlying leaf development and water transport mediated by MdHYL1 in apple, transcriptome-wide profiling of lncRNAs, miRNAs, and mRNAs in wild-type GL-3 vs MdHYL1 RNAi transgenic plants were conducted. In total, 28 lncRNAs and 813 mRNAs were detected as exhibiting significant differential expression, with lncRNAs predicted to regulate target mRNAs through cis- or trans-acting mechanisms. Functional annotation revealed these target genes to be enriched in flavonoid biosynthesis (MdMYB12, MdCHS), lignin metabolism (MdCYP98A3, MdMYB85), cell wall biogenesis/modification (MdNAC042, MdIRX1, MdIRX6), and water transport pathways (MdSIP1;1, MdTIP1;3, MdPIP2;5). RT-qPCR analysis further confirmed the co-expression networks between the identified mRNAs and lncRNAs. How MdHYL1 influences the regulatory functions of lncRNAs within the miRNA–mRNA–lncRNA network was subsequently examined. Members of the miR482, miR398, miR858, and miR2118 families were identifed as endogenous target mimics (eTMs) for specific lncRNAs. Notably, MSTRG.32670.1 may act as an eTM of miR166 to regulate MdCYP98A3, linking non-coding RNA regulation with lignin deposition and water transport. The present results uncover new mechanistic perspectives on how lncRNAs participate in MdHYL1-mediated regulation of leaf development and water transport in apple, while establishing a conceptual framework for future investigations of lncRNA functions in woody perennial crops.