Argonaute (AGO) proteins are central components of RNA silencing. While OsAGO18 is a known defense factor in antiviral immunity, its involvement in basal development and its transcriptomic behavior during fungal stress remains to be fully elucidated. In this study, based on its specific dual-localization in chloroplasts and processing bodies (P-bodies), we investigated the pleiotropic effects of OsAGO18 through transcriptomic network analysis of rice responding to the blast fungus Magnaporthe oryzae B.C. Couch. Our analysis revealed that the OsAGO18-mediated co-expression network is highly correlated with ribosome biogenesis and cell wall organization. Notably, the analyzed datasets reveal that this growth-related network is significantly suppressed upon M. oryzae challenge, highlighting a transcriptomic shift in OsAGO18 during the growth-to-defense transition. Phenotypic evaluations demonstrated that OsAGO18 overexpression accelerates early seedling growth and primary root elongation by promoting endogenous indole-3-acetic acid (IAA) accumulation, whereas ago18 mutants maintain basal growth rates without significant IAA fluctuations, reflecting robust genetic compensation within the highly redundant AGO family. Mechanistically, our integrated analysis suggests that OsAGO18 acts as a putative molecular decoy to sequester miR396d, thereby relieving the repression of the Growth-Regulating Factor OsGRF6 and triggering downstream auxin-dependent cascades. Collectively, our findings highlight OsAGO18 as a pivotal regulator of early seedling development and characterize its transcriptomic responsiveness to biotic stress, providing a plausible molecular link between post-transcriptional RNA regulation and rice growth coordination.

Verticillium wilt, caused by Verticillium dahliae, is a devastating disease that severely threatens cotton production worldwide. The long-term survival of the pathogen in soil and the limited availability of resistant cultivars make effective control strategies challenging. Although the fungal cross-kingdom RNA VdsR-1 has been reported to delay floral transition and prolong vegetative growth, the underlying plant regulatory mechanisms remain largely unclear. Here, we show that the transcription factor AtTOE1, a target of ath-miR172b-3p, displays altered expression in response to changes in ath-miR172b-3p levels during V. dahliae inoculation, coinciding with coordinated changes in plant immune-related and developmental responses. Increased AtTOE1 expression is correlated with enhanced disease resistance, reduced pathogen colonization, and delayed floral transition. Furthermore, our results indicate that the VdsR-1/AtSPL13A module is associated with modulation of AtTOE1 expression via ath-miR172b-3p, suggesting the involvement of a cross-kingdom RNA-related regulatory framework linking plant immunity and development. Notably, this regulatory relationship is also observed in cotton, indicating evolutionary conservation across plant species. Together, our findings highlight TOE1 as a potential integrator of defense and growth-related processes during pathogen challenge and provide insights that may inform strategies to improve resistance to V. dahliae in cotton and other crops.