In-depth transcriptome and physiological function analysis reveals the toxicology of sodium fluoride in the fall webworm Hyphantria cunea.

• RNA-seq reveals the toxic mechanism of fluoride exposure in Hyphantria cunea.
• Fluoride damages energy metabolism process and disturbs ferroptosis signaling pathway.
• Fluoride exposure disrupts the iron absorption in the larval body of H. cunea.
• Fluoride activates ROS and causes mortality in H. cunea by inducing Fe²⁺ overload.

Fluoride is an environmental pollutant that severely injures various organisms in ecosystems. Herein, the non-target organism, fall webworm (Hyphantria cunea), was used to determine the toxicological mechanism of NaF exposure. In this study, H. cunea exposed to NaF showed significant declines in growth and reproduction. The authors conducted RNA sequencing on adipose bodies and midgut tissues from NaF-exposed H. cunea larvae to uncover the toxicological mechanisms. The results showed that extracellular matrix-receptor interaction, pentose and glucuronate interconversions, fatty acid biosynthesis, and ferroptosis might contribute to NaF stress. NaF significantly decreased the antioxidant level, nitrous oxide synthase activity, and NO content, while significantly increasing lipid peroxidation. NaF induced significant changes in the expression of energy metabolism genes. However, the triglyceride content was significantly decreased and the lipase enzyme activity was significantly increased. Moreover, the expression levels of light and heavy chains of ferritin were inhibited in NaF-exposed H. cunea. NaF caused ferritin Fe²⁺overload in FerHCH1 and FerLCH knockdown H. cunea larvae, activated reactive oxygen species, and reduced the total iron content, eventually increasing the mortality H. cunea larvae. This study identified the toxicological mechanisms of NaF in lipid synthesis and energy metabolism in H. cunea, providing a basis for understanding the molecular mechanisms of NaF toxicity and developing pollution control strategies.

Graphical abstract

Full text article online at https://www.sciencedirect.com/science/article/pii/S0147651324008182?via%3Dihub

Excerpt:
Conclusions:

In this study, transcriptome analysis was used to understand the stress response of fat body and midgut of H. cunea to sodium fluoride. The results showed that fatty acid biosynthesis, fatty acid elongation, energy metabolism, peroxisome and ferroptosis were involved in the NaF toxicology. Additionally, HcFerHCH1 and HcFerLCH were found to play roles in H. cunea’s tolerance to NaF. In summary, sodium fluoride caused Fe²⁺ overload, activated ROS, and ultimately led to the death of H. cunea larvae. This study underscores the significant implications of our findings for environmental toxicology and pest management, particularly in understanding the mechanisms underlying insect responses to environmental stressors such as sodium fluoride.