Involvement of the Electrophilic Isothiocyanate Sulforaphane in Arabidopsis Local Defense Responses

Abstract

Plants defend themselves against microbial pathogens through a range of highly sophisticated and integrated molecular systems. Recognition of pathogen-secreted effector proteins often triggers the hypersensitive response (HR), a complex multicellular defense reaction where programmed cell death of cells surrounding the primary site of infection is a prominent feature. Even though the HR was described almost a century ago, cell-to-cell factors acting at the local level generating the full defense reaction have remained obscure. In this study, we sought to identify diffusible molecules produced during the HR that could induce cell death in naive tissue. We found that 4-methylsulfinylbutyl isothiocyanate (sulforaphane) is released by Arabidopsis (Arabidopsis thaliana) leaf tissue undergoing the HR and that this compound induces cell death as well as primes defense in naive tissue. Two different mutants impaired in the pathogen-induced accumulation of sulforaphane displayed attenuated programmed cell death upon bacterial and oomycete effector recognition as well as decreased resistance to several isolates of the plant pathogen Hyaloperonospora arabidopsidis. Treatment with sulforaphane provided protection against a virulent H. arabidopsidis isolate. Glucosinolate breakdown products are recognized as antifeeding compounds toward insects and recently also as intracellular signaling and bacteriostatic molecules in Arabidopsis. The data presented here indicate that these compounds also trigger local defense responses in Arabidopsis tissue.

Pseudomonas syringae enhances herbivory by suppressing the reactive oxygen burst in Arabidopsis

“…The rbohD and rbohF mutants have less control over limiting the spread of PCD, which we have previously observed around S. flava feeding sites (Whiteman et al, 2011). The release of ROS and other defensive compounds, such as ITCs in the case of Arabidopsis (Andersson et al, 2014) from cells undergoing PCD around feeding sites could exert physiological costs on the herbivore (Agrawal and Kurashige, 2003; Summers and Felton, 1998; Whiteman et al, 2012). However, in this case these costs may fall within the limits of what the larvae can tolerate, so that larval feeding rates do not change.…”

“…Compatible biotrophic microbes tend to enhance feeding by chewing herbivores by suppressing the plant immune system with effectors or phytotoxins they deliver into plant cells (Cui et al, 2002; Groen et al, 2013; Lazebnik et al, 2014), whereas necrotrophic fungi and incompatible biotrophic microbes tend to reduce feeding (Cui et al, 2002; Lazebnik et al, 2014). In necrotrophic and incompatible biotrophic interactions, fungal phytotoxins or the recognition of effectors by the plant immune system trigger programmed cell death (PCD) in the plant, which is associated with a hypersensitive response (HR) and the release of ROS and plant defensive chemicals (Cui et al, 2002; Torres et al, 2006; Andersson et al, 2014). Such chemicals have broad-acting toxicity against microbes and animals in addition to their role as signaling molecules.…”

“…On the other hand, larval feeding was decreased on mutants with a lowered threshold to initiate (PCD). Cell death is an inevitable consequence when ROS levels reach a certain threshold and cause the release of additional ROS and ITCs (Andersson et al, 2014; Torres et al, 2006). …”

Progress and prospects of glucosinolate pathogen resistance in some brassica plants

“…No doubt, this would provide insights on the development of a new range of potent fungicides and fungal-based drugs (Shlezinger et al, 2011). The GSL biosynthesis product, 4methylsulfinylbutyl isothiocyanate (sulforaphane) does not only activate defense in naïve tissues but provide protection against virulent isolates (Andersson et al, 2015). This suggests that GSL byproducts products are involved in cell-to-cell signaling and are prime bacteriostatic molecules albeit their applications warrant more in-depth studies.…”

“…Nonetheless, the turnover of associated secondary metabolite such as glucosinolates (GSLs) is a suggestion of their roles in key interactions (Bednarek et al, 2009). For instance, the effector-triggered hypersensitive response (ET-HR) mechanism, which depends on indole and aliphatic glucosinolates, or their byproducts have been implicated in delayed programmed cell death upon Pseudomonas syringae and Hyaloperonospora arabidopsidis inoculation in aliphatic glucosinolate-deficient myb28 and myb29 plants (Johansson et al, 2014;Andersson et al, 2015). These findings confirm that glucosinolates are associated with the ET-HR and ROS pathways.…”