Nickel oxide nanoparticles induce cell wall modifications, root anatomical changes, and nitrosative signaling in ecotypes of Ni hyperaccumulator Odontarrhena lesbiaca

Abstract

The industrial application and environmental release of nickel oxide NPs (NiO NPs) is increasing, but the details of their relationship with plants are largely unknown. In this work, the cellular, tissue, organ, and molecular level responses of three ecotypes of Ni hyperaccumulator Odontarrhena lesbiaca grown in the presence of high doses of NiO NP (250 mg/L and 500 mg/L) were studied. All three ecotypes showed a similar accumulation of Ni in the presence of nano Ni, and in the case of NiO NPs, the root-to-shoot Ni translocation was slighter compared to the bulk Ni. In all three ecotypes, the walls of the root cells effectively prevented internalization of NiO NPs, providing cellular defense against Ni overload. Exposure to NiO NP led to an increase in cortex thickness and the deposition of lignin-suberin and pectin in roots, serving as a tissue-level defense mechanism against excessive Ni. Exposure to NiO NP did not modify or cause a reduction in some biomass parameters of the Ampeliko and Loutra ecotypes, while it increased all parameters in Olympos. The free salt form of Ni exerted more negative effects on biomass production than the nanoform, and the observed effects of NiO NPs can be attributed to the release of Ni ions. Nitric oxide and peroxynitrite levels were modified by NiO NPs in an ecotype-dependent manner. The changes in the abundance and activity of S-nitrosoglutathione reductase protein triggered by NiO NPs suggest that the enzyme is regulated by NiO NPs at the post-translational level. The NiO NPs slightly intensified protein tyrosine nitration, and the slight differences between the ecotypes were correlated with their biomass production in the presence of NiO NPs. Overall, the Odontarrhena lesbiaca ecotypes exhibited tolerance to NiO NPs at the cellular, tissue, organ/organism and molecular levels, demonstrating various defense mechanisms and changes in the metabolism of reactive nitrogen species metabolism and nitrosative protein modification.

Keywords: Alyssum lesbiacum; Ampeliko; Ecotypes; Loutra; Nanoparticles; Nickel oxide; Nitrosative signaling; Olympos.