Developmental dynamic transcriptomics reveals multiple effectors and transcription factors critical for Ditylenchus destructor parasitism

Abstract Plant-parasitic nematodes (PPNs) pose a major threat to global agricultural production, yet fundamental research on their biology remains limited. The origin and evolutionary trajectory of PPNs remain elusive, largely due to the scarcity of chromosome-level genomic data. Among them, migratory PPNs are considered a key transitional form between free-living and obligate parasitic lifestyles, as they exhibit both plant parasitism and fungal feeding behaviors. In this study, we assembled a chromosome-level genome of the sweet potato rot nematode Ditylenchus destructor and confirmed the presence of four chromosomes through Hi-C scaffolding and karyotype analysis. Comparative genomic analysis with two other migratory PPNs, Bursaphelenchus xylophilus and Aphelenchoides besseyi, revealed that the Nigon elements in B. xylophilus are largely conserved with those of the model organism Caenorhabditis elegans, while D. destructor and A. besseyi exhibit extensive Nigon element rearrangements. These rearrangements were strongly correlated with patterns of protein sequence collinearity. Moreover, transcriptomic profiling across five developmental stages of D. destructor identified numerous stage-specific effectors and transcription factors. Functional analysis via RNA interference demonstrated that many of these genes play essential roles in embryogenesis and parasitic activity. Together, our results provide valuable genomic and transcriptomic resources for studying PPNs, uncovering critical insights into their genome evolution and parasitism-related gene functions, and laying a crucial foundation for advancing the understanding of PPN biology and their impact on agricultural systems. Competing Interest Statement The authors have declared no competing interest. Footnotes We revised the content of the abstract and partially revised the introduction. In addition, we found that the order of authors in the submission was inconsistent with that in the original manuscript, so we adjusted the order of authors. Finally, we found that the main figure in the composite pdf file was repeated twice, and we removed the repeated figures.