Molecular Hydrogen Confers Resistance to Rice Stripe Virus

Microbiol Spectr. 2023 Feb 22;11(2):e0441722. doi: 10.1128/spectrum.04417-22. Online ahead of print.

Abstract

Although molecular hydrogen (H2) has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. Here, after rice stripe virus (RSV) infection, H2 production was pronouncedly stimulated in Zhendao 88, a resistant rice variety, compared to that in a susceptible variety (Wuyujing No.3). External H2 supply remarkably reduced the disease symptoms and RSV coat protein (CP) levels, especially in Wuyujing No.3. The above responses were abolished by the pharmacological inhibition of H2 production. The transgenic Arabidopsis plants overexpressing a hydrogenase gene from Chlamydomonas reinhardtii also improved plant resistance. In the presence of H2, the transcription levels of salicylic acid (SA) synthetic genes were stimulated, and the activity of SA glucosyltransferases was suppressed, thus facilitating SA accumulation. Genetic evidence revealed that two SA synthetic mutants of Arabidopsis (sid2-2 and pad4) were more susceptible to RSV than the wild type (WT). The treatments with H2 failed to improve the resistance to RSV in two SA synthetic mutants. The above results indicated that H2 enhances rice resistance to RSV infection possibly through the SA-dependent pathway. This study might open a new window for applying the H2-based approach to improve plant disease resistance. IMPORTANCE Although molecular hydrogen has potential therapeutic effects in animals, whether or how this gas functions in plant disease resistance has not yet been elucidated. RSV was considered the most devastating plant virus in rice, since it could cause severe losses in field production. This disease was thus selected as a classical model to explore the interrelationship between molecular hydrogen and plant pathogen resistance. In this study, we discovered that both exogenous and endogenous H2 could enhance plant resistance against Rice stripe virus infection by regulating salicylic acid signaling. Compared with some frequently used agrochemicals, H2 is almost nontoxic. We hope that the findings presented here will serve as an opportunity for the scientific community to push hydrogen-based agriculture forward.

Keywords: Arabidopsis; disease resistance; molecular hydrogen; rice; rice stripe virus; salicylic acid.