Self-DNA Early Exposure in Cultivated and Weedy Setaria Triggers ROS Degradation Signaling Pathways and Root Growth Inhibition

Abstract

The accumulation of fragmented extracellular DNA reduces conspecific seed germination and plantlet growth in a concentration-dependent manner. This self-DNA inhibition was repeatedly reported, but the underlying mechanisms are not fully clarified. We investigated the species-specificity of self-DNA inhibition in cultivated vs. weed congeneric species (respectively, Setaria italica and S. pumila) and carried out a targeted real-time qPCR analysis under the hypothesis that self-DNA elicits molecular pathways that are responsive to abiotic stressors. The results of a cross-factorial experiment on root elongation of seedlings exposed to self-DNA, congeneric DNA, and heterospecific DNA from Brassica napus and Salmon salar confirmed a significantly higher inhibition by self-DNA as compared to non-self-treatments, with the latter showing a magnitude of the effect consistent with the phylogenetic distance between the DNA source and the target species. Targeted gene expression analysis highlighted an early activation of genes involved in ROS degradation and management (FSD2, ALDH22A1, CSD3, MPK17), as well as deactivation of scaffolding molecules acting as negative regulators of stress signaling pathways (WD40-155). While being the first exploration of early response to self-DNA inhibition at molecular level on C4 model plants, our study highlights the need for further investigation of the relationships between DNA exposure and stress signaling pathways by discussing potential applications for species-specific weed control in agriculture.

Self-DNA Inhibition in Drosophila melanogaster Development: Metabolomic Evidence of the Molecular Determinants

“…Self-DNA administration had adverse effects on Drosophila developmental progression and strongly reduced the fly offspring. Similar effects were previously reported in different organisms, either uni-or multi-cellular, which responded to conspecific fragmented genomic DNA present in the culture medium by reducing their growth and performance [1][2][3][4][5][7][8][9][10]. Therefore, the inhibitory phenotypes we described in Drosophila further support the notion that environmental DNA molecules play evolutionarily conserved regulatory roles that have been largely overlooked thus far [2].…”

“…In plants, the molecular mechanisms of the inhibitory process by self-DNA exposure have been investigated by transcriptomic [4,7], physiological [8][9][10], and metabolomic [11] approaches, showing a generalized significant reduction in metabolic activities with molecular responses typical of stress conditions, specifically including ROS production [9,10] and accumulation in the exposed cells of RNA constituents and precursors [11]. In animals, the only previous study on C. elegans highlighted the setting of larval developmental defects and increased mortality with magnification of the effects progressively increasing in subsequent generations [5].…”