Integrative sRNA, DNA Methylation, and Transcriptomics Reveals Dynamic Epigenetic Reprogramming of Meloidogyne javanica-Induced Galls in Arabidopsis

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Abstract
Root knot nematodes (RKNs) induce galls, containing multinucleated giant cells (GCs) to nourish them. The differentiation of precursor cells to galls/GCs involves extensive cellular reprogramming with multiple layers of regulation. Epigenetic regulation during the early stages of infection indicates that RNA-directed DNA methylation (RdDM) and microRNA-dependent gene silencing contribute to transcriptional and post-transcriptional reprogramming during gall organogenesis. Although later stages of galls/GC development are crucial for nematode life-cycle maintenance, epigenetic reprogramming events remain largely unexplored. An integrative analysis of sRNAs, DNA methylation, and transcriptomic dynamics in galls induced by Meloidogyne javanica revealed that enrichment of 24 nt sRNAs represents a gall hallmark across early and late developmental stages. Fewer gall-distinctive sRNAs were detected at mid-to-late stages than at early stages, alongside a pronounced spatial reorganization of rasiRNA accumulation. At early stages, gall-distinctive rasiRNAs preferentially accumulated in pericentromeric retrotransposon-rich regions, whereas, at mid-to-late stages, they predominantly localized to chromosome arms, matching DNA transposons, promoters, and gene bodies. A decline in the regulatory influence of miRNAs was observed as infection progressed, possibly reflecting a transition toward specialized regulatory states associated with gall maintenance. Moreover, three regulatory modules, miR2111-5p/HOLT, miR172/AP2, and miR156/SPL10, were tightly but oppositely regulated at 3 and 14 days post-infection. Furthermore, miR156/SPL10 showed crucial functions during gall formation and/or maintenance, possibly influenced by hormonal cues involving ARF8 among other ARFs. Our results highlight stage-specific patterns involving sRNA dynamics, DNA methylation, and transcriptomic changes underlying nematode feeding site development and maintenance.

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