Topsoil drying combined with increased sulfur supply leads to enhanced aliphatic glucosinolates in Brassica juncea leaves and roots

Highlights

• Topsoil drying distinctly increased the predominant aliphatic glucosinolate.

• Abscisic acid concentration was significantly increased by topsoil drying.

• Leaf biomass of Brassica juncea was not affected by topsoil drying.

• Aromatic and indole glucosinolates were less involved in drought stress response.

• High S supply modified glucosinolate formation in response to topsoil drying.

Abstract

The decrease of water availability is leading to an urgent demand to reduce the plants’ water supply. This study evaluates the effect of topsoil drying, combined with varying sulfur (S) supply on glucosinolates in Brassica juncea in order to reveal whether a partial root drying may already lead to a drought-induced glucosinolate increase promoted by an enhanced S supply. Without decreasing biomass, topsoil drying initiated an increase in aliphatic glucosinolates in leaves and in topsoil dried roots supported by increased S supply. Simultaneously, abscisic acid was determined, particularly in dehydrated roots, associated with an increased abscisic acid concentration in leaves under topsoil drying. This indicates that the dehydrated roots were the direct interface for the plants’ stress response and that the drought-induced accumulation of aliphatic glucosinolates is related to abscisic acid formation. Indole and aromatic glucosinolates decreased, suggesting that these glucosinolates are less involved in the plants’ response to drought.

Introduction

Glucosinolates are a group of secondary plant metabolites found almost exclusively in plants of the order Brassicales, which include the important horticultural crops of the Brassicaceae family (Fahey, Zalsmann, & Talalay, 2001). Certain individual glucosinolates are known to confer health-promoting effects due to the anti-carcinogenic properties of their hydrolysis products. Recently, aliphatic isothiocyanates derived from 2-propenyl glucosinolate have been reported to bear strong anti-carcinogenic properties (Verkerk et al., 2009). Additionally, hydrolysis products of indole 3-indolylmethyl glucosinolates and their derivatives, as well as aromatic isothiocyanates derived from 2-phenylethyl glucosinolate, have been reported to be effective against the development of cancer (Plate & Gallaher, 2006).

In addition to genotype, glucosinolate synthesis is strongly regulated by ecophysiological factors, such as nutrition and water availability (Verkerk et al., 2009). Exploitation of these regulatory factors could have pronounced effects on anti-carcinogenic glucosinolate concentrations in foods, and thus strong implications for the production of health-promoting food for human nutrition. Moreover, scenarios of global climate change predict increased water shortages, especially in arid and semi-arid regions where great seasonal and annual irregularity in precipitation already limit access to water.

Vegetable mustard (Brassica juncea) is an important crop in many parts of the world and is extensively cultivated in Asia, especially in China. It is primarily produced as an oilseed but also as a vegetable with relatively high concentrations of the health-promoting 2-propenyl glucosinolate and 3-indolylmethyl glucosinolate (Krumbein, Schonhof, & Schreiner, 2005). A great diversity of types exists, with some showing tolerance to adverse environmental conditions such as drought and low soil fertility (Dixon, 2007). Several previous studies on Brassica species have established a distinct drought-induced increase in glucosinolate concentration. However, this water deficit in most cases also caused a simultaneous reduction in shoot growth (Radovich, Kleinhenz, & Streeter, 2005), even in drought-adapted Brassica species such as Brassica carinata (Schreiner, Beyene, Krumbein, & Stützel, 2009). Thus, nutritional quality improvement in response to drought stress is usually accompanied by a yield decrease. Due to the current and predicted decreases in water resources, there is an urgent need for water-saving strategies that reduce water use but do not significantly affect yield and quality.

Under natural conditions, plants often encounter progressive soil-drying, as upper soil layers dry quickly, the subsoil remains moist and roots with access to these lower layers are able to provide enough water for adequate growth (Neumann & George, 2004). As a variation of topsoil drying, partial root zone drying was established as a water-deficit irrigation technique (dos Santos et al., 2007). Previous studies, using partial root zone drying, have focussed primarily on the plant’s physiological responses to a partially limited water supply and subsequent influences on yield and primary plant compounds, such as total soluble solids, organic acids, lipids and proteins (Campos, Trejo, Pena-Valdivia, Ramirez-Ayala, & Sanchez-Garcia, 2009). The relationships between secondary plant metabolites and a partially limited water supply, however, have scarcely been studied, apart from investigations which have focussed on the concentration of phenolic substances in grapes (Bindon, Dry, & Loveys, 2008). This is surprising, as limited water supply could cause a shift from growth-related primary metabolism to preferential allocation of carbon and nitrogen into secondary metabolism (at least in perennial plants, Gayler, Grams, Heller, Treutter, & Priesack, 2008), thereby promoting the biosynthesis of carbon- and nitrogen-based secondary metabolites, such as glucosinolates. So far, glucosinolate changes in relation to topsoil drying have not been studied.

Therefore, we hypothesised that topsoil drying also leads to a drought-induced increase in glucosinolate concentration but without any biomass loss. With regard to establishing an optimised agro-ecological crop-management strategy for the production of glucosinolate-enriched vegetable mustard plants, our aims were (1) to characterise the B. juncea plant response to drought stress and glucosinolate formation in roots and leaves, and (2) to assess whether topsoil drying can increase leaf glucosinolate concentrations in B. juncea plants without decreasing yield.

In addition to water availability, nutrient status also influences the production of secondary metabolites. High nitrogen (N) supply was found to increase protein concentration in seeds of Brassica napus and, when sulphur (S) was limited, most of the S was incorporated into proteins, resulting in a reduced glucosinolate formation (Asare & Scarisbrick, 1995). Thus, a well-balanced N:S supply ratio is necessary, particularly for supporting glucosinolate biosynthesis in Brassica species (Li et al., 2007), leading to the hypothesis that an increased S supply promotes the drought-induced glucosinolate biosynthesis. Thus, a further aim of our study was (3) to examine the interactive effect of S supply and topsoil drying on glucosinolate concentrations in B. juncea.

To the best of our knowledge, this study is the first to report the effects of topsoil drying on glucosinolate concentration and to provide a detailed profile of glucosinolate composition in B. juncea plants, as influenced by topsoil drying and a glucosinolate-oriented mineral nutrient supply.