Glucosinolate-Derived Isothiocyanates Inhibit Arabidopsis Growth and the Potency Depends on Their Side Chain Structure

Abstract

Isothiocyanates (ITCs), the biologically important glucosinolate breakdown products, can present health-promoting effects, play an important role in plant defense and affect plant cellular mechanisms. Here, we evaluated the biological effects of ITCs on Arabidopsis thaliana by assessing growth parameters after long-term exposure to low concentrations of aliphatic and aromatic ITCs, ranging from 1 to 1000 µM. Treatment with the aliphatic allylisothiocyanate (allyl-ITC) led to a significant reduction of root length and fresh weight in a dose-dependent manner and affected the formation of lateral roots. To assess the importance of a hormonal crosstalk in the allyl-ITC-mediated growth reduction, the response of auxin and ethylene mutants was investigated, but our results did not allow us to confirm a role for these hormones. Aromatic ITCs generally led to a more severe growth inhibition than the aliphatic allyl-ITC. Interestingly, we observed a correlation between the length of their side chain and the effect these aromatic ITCs caused on Arabidopsis thaliana, with the greatest inhibitory effect seen for 2-phenylethyl-ITC. Root growth recovered when seedlings were removed from exposure to ITCs.

Arabidopsis mutants impaired in glutathione biosynthesis exhibit higher sensitivity towards the glucosinolate hydrolysis product allyl-isothiocyanate

“…The assay revealed however also a higher potency for SFN than for AITC, which might be due to differences in physicochemical properties such as their ability to cross the cell membrane, compound stability or differences in reactivity. This is also consistent with our recent work showing that different ITCs lead to various degree of growth inhibition depending on their side chain structure 74 . That SFN injected directly into Arabidopsis leaves has been reported to lead to a rapid decrease of the cellular glutathione pool 75 further strengthens the involvement of glutathione in ITC-triggered growth inhibition.…”

Diverse Allyl Glucosinolate Catabolites Independently Influence Root Growth and Development

“…This leads to allyl-isothiocyanate, the precursor of acrylic acid and raphanusamic acid, being the prevalent form in Arabidopsis Col-0 leaves when feeding exogenous allyl-GSL. In contrast, Arabidopsis Col-0 roots expressing the nitrile-specifier protein and hence allyl-nitrile, the precursor of butenoic acid, are more common in Col-0 roots (Kissen & Bones 2009, Urbancsok et al 2017. Further, growing plants in crowded or uncrowded conditions can plastically alter the production of nitriles versus isothiocyanates in older plants .…”

“…In roots of Arabidopsis catabolism of allyl-GSL by myrosinase and nitrile specifier proteins results in formation of allyl-nitrile and allyl-isothiocyanate (Burow et al 2008(Burow et al , 2009Urbancsok et al 2017 (Fig. 2A).…”

The Role of a Glucosinolate-Derived Nitrile in Plant Immune Responses

“…Not only they are toxic to susceptible pests and diseases, they are also found to be toxic to Arabidopsis at high dosage (Hara et al, 2010). Isothiocyanates also cause other negative effects on plants, such as triggering stomatal closure (Khokon et al, 2011), inducing cell death (Andersson et al, 2015), disrupting microtubules (Øverby et al, 2015a), depleting glutathione (Øverby et al, 2015b), and inhibiting root growth (Urbancsok et al, 2017).…”

“…However, to date, there is no study that elucidates the function of 3BN in enhancing the disease tolerance of Brassicaceae plants against pathogens. Therefore, in the present study we chose to investigate the effects of 3BN which is the nitrile-counterpart of the much studied sinigrin-derived allyl-isothiocyanate (Hara et al, 2010;Urbancsok et al, 2017). Among the different Brassicaceae species, A. thaliana was used in this study because it is the dicotyledonous model plant.…”