Something smells bad to plant pathogens: Production of hydrogen sulfide in plants and its role in plant defence responses

Abstract

Background: Sulfur and diverse sulfur-containing compounds constitute important components of plant defences against a wide array of microbial pathogens. Among them, hydrogen sulfide (H₂S) occupies a prominent position as a gaseous signalling molecule that plays multiple roles in regulation of plant growth, development and plant responses to stress conditions. Although the production of H₂S in plant cells has been discovered several decades ago, the underlying pathways of H₂S biosynthesis, metabolism and signalling were only recently uncovered.

Aim of the review: Here we review the current knowledge on the biosynthesis of H₂S in plant cells, with special attention to L-cysteine desulfhydrase (DES) as the key enzyme controlling H₂S levels biosynthesis in the cytosol of plant cells during plant growth, development and diverse abiotic and biotic stress conditions.

Key scientific concepts of review: Recent advances have revealed molecular mechanisms of DES properties, functions and regulation involved in modulations of H₂S production during plant responses to abiotic and biotic stress stimuli. Studies on des mutants of the model plant Arabidopsis thaliana uncovered molecular mechanisms of H₂S action as a signalling and defence molecule in plant-pathogen interactions. Signalling pathways of H₂S include S-persulfidation of protein cysteines, a redox-based post-translational modification leading to activation of downstream components of H₂S signalling. Accumulated evidence shows DES and H2S implementation into salicylic acid signalling and activation of pathogenesis-related proteins and autophagy within plant immunity. Obtained knowledge on molecular mechanisms of H₂S action in plant defence responses opens new prospects in the search for crop varieties with increased resistance to bacterial and fungal pathogens.

Keywords: Hydrogen sulfide; L-cysteine; L-cysteine desulfhydrase; Plant defence; Plant signalling; Sulfur metabolism.

Graphical abstract

Fig. 1

Overview of H₂S production in plant cells. APS, adenosine phosphosulfate; CAS-C1, β-cyanoalanine synthase (EC 4.4.1.9); Cyano-Ala, cyanoalanine; DCD, D-cysteine desulfhydrase (EC 4.4.1.15.); DES1, L-cysteine desulfhydrase (EC 4.4.1.2.); DSF, L-cysteine desulfurase (EC 2.8.1.7); Fd, ferredoxin; OAS, O-acetylserine; OAS-A1, cytosolic O-acetylserine (thiol)lyase; OAS-B, plastidial O-acetylserine (thiol)lyase; OAS-C, mitochondrial O-acetylserine (thiol)lyase; Pyr, pyruvate; SiR, sulfite reductase (EC 1.8.7.1.).

Fig. 2

Schematic overview of known molecular mechanisms of H₂S involvement in increased plant resistance to microbial pathogens. DES1, L-cysteine desulfurase; PR, pathogenesis-related; RNS, reactive nitrogen species; ROS, reactive oxygen species; RSS, reactive sulfur species; SA, salicylic acid; SNO-, thionitrite; SSNO^-, perthionitrite; HS_n^-, polysulfides.