Milestones in plant sulfur research on sulfur-induced-resistance (SIR) in Europe

Abstract

Until the 1970's of the last century sulfur (S) was mainly regarded as a pollutant being the main contributor of acid rain, causing forest dieback in central Europe. When Clean Air Acts came into force at the start of the 1980's SO2 contaminations in the air were consequently reduced within the next years. S changed from an unwanted pollutant into a lacking plant nutrient in agriculture since agricultural fields were no longer "fertilized" indirectly by industrial pollution. S deficiency was first noticed in Brassica crops that display an especially high S demand because of its content of S-containing secondary metabolites, the glucosinolates. In Scotland, where S depositions decreased even faster than in continental Europe, an increasing disease incidence with Pyrenopeziza brassicae was observed in oilseed rape in the beginning 1990's and the concept of sulfur-induced-resistance (SIR) was developed after a relationship between the S status and the disease incidence was uncovered. Since then a lot of research was carried out to unravel the background of SIR in the metabolism of agricultural crops and to identify metabolites, enzymes and reactions, which are potentially activated by the S metabolism to combat fungal pathogens. The S status of the crop is affecting many different plant features such as color and scent of flowers, pigments in leaves, metabolite concentrations and the release of gaseous S compounds which are directly influencing the desirability of a crop for a variety of different organisms from microorganisms, over insects and slugs to the point of grazing animals. The present paper is an attempt to sum up the knowledge about the effect of the S nutritional status of agricultural crops on parameters that are directly related to their health status and by this to SIR. Milestones in SIR research are compiled, open questions are addressed and future projections were developed.

Keywords: S fertilization; biotrophic and necrotrophic pathogens; fungal diseases; nutrient induced resistance; plant S metabolism.

Figure 1

Sulfur metabolites and pathways involved in the defense against fungal pathogens in Brassica species. Metabolites in yellow boxes were found to increase after fungal attack (Williams and Cooper, ; Glazebrook, ; Jost et al., ; Kruse et al., ; Bloem et al., 2012).

Figure 2

Model of the response of plants to biotrophic and necrotrophic plant pathogens (adapted from Glazebrook (2005): displayed are the interactions of Arabidopsis with the biotrophs Peronospora parasitica and Erysiphe ssp. and with the necrotrophs Alternaria brassicicola and Botrytis cinerea; SA, salicylic acid, JA, jasmonic acid, ET, ethylene; broken line arrows indicate to a possible interaction but which was not found in the chosen experiments while the solid line arrows indicate to the observed plant-pathogen-response). The defense reaction of Arabidopsis against biotrophic pathogens start with gene-for-gene recognition of the pathogen followed by rapid activation of defense and the production of reactive oxygen species (ROS), the so-called “oxidative burst,” which is by self a signal for defense activation. ROS production is connected with the hypersensitive response (HR), also called “programmed cell death,” which limits the access of biotrophs that feed on living tissue to water and nutrients. HR is associated with the activation of the salicylic acid (SA) dependent signaling pathway that is connected with systemic acquired resistance (SAR) and the expression of pathogenesis-related proteins. For necrotrophic pathogens a different defense line takes place as they feed on dead plant tissue and host cell death is not predicted to limit their growth. Defense against necrotrophic pathogens is mainly mediated by JA and ET controlled defense as well as production of phytoalexins such as camalexin. The broken line arrows indicate that also mixed defense lines are possible for other biotrophic or nectrotrophic pathogens.