Topsoil drying combined with increased sulfur supply leads to enhanced aliphatic glucosinolates in Brassica juncea leaves and roots
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.
Section snippets
Experimental setup
The study involved a pot-based experiment, carried out at the Leibniz Institute of Vegetable and Ornamental Crops Grossbeeren/Erfurt e.V., in Grossbeeren (Germany), from the 30th of August until the 12th of December. Each treatment was replicated four times and the experimental set-up was completely random. Plants were grown in a greenhouse with a day/night cycle of 16 h/8 h and average air temperatures of 22 °C (day) and 18 °C (night). Relative humidity was in the range 60–70%, with a daily mean
Glucosinolate composition in different parts of the plant
As the predominant glucosinolate, aliphatic 2-propenyl glucosinolate was quantitatively determined in the leaves, as well as in the roots, in upper and lower compartments (Table 1, Table 2). Lower levels of the less prevalent, aliphatic 3-butenyl and 2-hydroxy-3-butenyl glucosinolates, were assessed in the leaves and in roots, respectively (Table 1, Table 2). In addition, 3-indolylmethyl and 4-methoxy-3-indolylmethyl glucosinolates were measured in the entire plant (Table 1, Table 3). Only in
Acknowledgements
This work was supported by the China Scholarship Council. We appreciate Andrea Jankowsky and Kerstin Bieleŕs technical assistance in laboratory work, as well as Nysha Munrós grammar correction of the manuscript.
References (30)
- et al.
Rate of nitrogen and sulphur fertilizers on yield, yield components and seed quality of oilseed rape (Brassica napus L.)
Field Crops Research
(1995) - et al.
Variation of glucosinolate accumulation among different organs and developmental stages of Arabidopsis thaliana
Phytochemistry
(2003) - et al.
Effect of partial rootzone drying on growth, gas exchange, and yield of tomato (Solanum lycopersicum L.)
Scientia Horticulturae
(2009) - et al.
Proteomics and metabolomics of Arabidopsis responses to perturbation of glucosinolate biosynthesis
Molecular Plant
(2012) - et al.
Effects of deficit irrigation strategies on cluster microclimate for improving fruit composition of Moscatel field-grown grapevines
Scientia Horticulturae
(2007) - et al.
The chemical diversity and distribution of glucosinolates and isothiocyanates among plants
Phytochemistry
(2001) - et al.
Nutritive values of Brassica campestris L. oil as affected by growth regulator treatments
Journal of the Chemical Society of Pakistan
(2009) - et al.
Influence of partial rootzone drying on the composition and accumulation of anthocyanins in grape berries (Vitis vinifera cv. Cabernet Sauvignon)
Australian Journal of Grape and Wine Research
(2008) Vegetable Brassicas and related crucifers. Crop production science in horticulture (Series number 14)
(2007)- et al.
Phytochemical changes induced by different nitrogen supply forms and radiation levels in two leafy Brassica species
Journal of Agricultural and Food Chemistry
(2011)
A dynamic model of environmental effects on allocation to carbon based secondary compounds in juvenile trees
Annals of Botany
Specific and coordinated control of indolic and aliphatic glucosinolate biosynthesis by R2R3-MYB transcription factors in Arabidopsis thaliana
Phytochemistry Reviews
HAG2/MYB76 and HAG3/MYB29 exert a specific and coordinated control on the regulation of aliphatic glucosinolate biosynthesis in Arabidopsis thaliana
New Phytologist
Sharing waters: Post-Rio international water management
Natural Resources Forum
Composition and contents of phytochemicals (glucosinolates, carotenoids and chlorophylls) and ascorbic acid in selected Brassica species (B. juncea, B. rapa subsp. nipposincia var. chinoleifera, B. rapa subsp. chinensis and B. rapa subsp. rapa)
Journal of Applied Botany and Food Quality
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