Research Article: Glucosinolate variability between turnip organs during development

Date Published: June 6, 2019

Publisher: Public Library of Science

Author(s): Guusje Bonnema, Jun Gu Lee, Wang Shuhang, David Lagarrigue, Johan Bucher, Ron Wehrens, Ric de Vos, Jules Beekwilder, Yong Pyo Lim.

http://doi.org/10.1371/journal.pone.0217862

Abstract

Turnip (Brassica rapa spp. rapa) is an important vegetable species, with a unique physiology. Several plant parts, including both the turnip tubers and leaves, are important for human consumption. During the development of turnip plants, the leaves function as metabolic source tissues, while the tuber first functions as a sink, while later the tuber turns into a source for development of flowers and seeds. In the present study, chemical changes were determined for two genotypes with different genetic background, and included seedling, young leaves, mature leaves, tuber surface, tuber core, stalk, flower and seed tissues, at seven different time points during plant development. As a basis for understanding changes in glucosinolates during plant development, the profile of glucosinolates was analysed using liquid chromatography (LC) coupled to mass spectrometry (MS). This analysis was complemented by a gene expression analysis, focussed on GLS biosynthesis, which could explain part of the observed variation, pointing to important roles of specific gene orthologues for defining the chemical differences. Substantial differences in glucosinolate profiles were observed between above-ground tissues and turnip tuber, reflecting the differences in physiological role. In addition, differences between the two genotypes and between tissues that were harvested early or late during the plant lifecycle. The importance of the observed differences in glucosinolate profile for the ecophysiology of the turnip and for breeding turnips with optimal chemical profiles is discussed.

Partial Text

Turnip (Brassica rapa subsp. rapa) forms a large and edible tuber, that is composed of both hypocotyl and root tissue [1]. From turnips, both the tubers and green parts are consumed, in particular in temperate regions in Asia, Europe and North America. In addition to its role in human nutrition it is also important as a fodder crop. Turnips are a source of vitamins and nutrients, but also contain significant amounts of glucosinolates (GLS), a group of secondary plant metabolites almost exclusively found in the order Brassicales [2,3,4]. GLS are water-soluble compounds that derive from glucose and amino-acids such as methionine, tryptophan or phenylalanine. The core structure of all GLS consists of thioglucose and sulphate groups, which are conjugated to an amino-acid derived side chain. Side chains can be aliphatic or indolic or aromatic, vary in chain length and can undergo several modifications (Fig 1) [5]. In plants, GLS have a role to protect the plant from insect damage, both in leaves and in underground tissues [6,7,8,9]. In vegetables, GLS provide a variety of tastes like bitterness and pungency. Upon damage to plants, e.g. by chewing, GLS are enzymatically converted into a range of volatile compounds, like nitriles and isothiocyanates (ITCs). In addition to taste formation GLS have been reported to be implicated in both antinutritional and health-promoting effects [10]. Progoitrin, a GLS known from several brassica species, has anti-thyroid activity and promotes goitre disease [11]. On the other hand, a high consumption of Brassica vegetables correlates negatively with the incidence of degenerative diseases in numerous epidemiological studies [11]. Protective effects are often accredited to GLS breakdown products such as ITCs, nitriles and indoles [12,13]. There is increasing evidence that ITCs are involved in cancer prevention and have anti-inflammatory effects (reviewed in [14]).

During the life cycle of a plant, metabolites are needed at different times and for different purposes. For example, the tuber tissue of a turnip plant initially functions as a sink to store nutrients for the plant, while it will function as a source to supply these nutrients when the plant goes into the reproductive stage and starts bolting, flowering and setting seed. Leaves provide photosynthetic capacity, and are replaced continuously by young fresh leaves during the life cycle of the plant; therefore they likely have different requirements for their functioning than turnip tubers. These requirements are at least partly met by their chemical composition. In recent years, changes in chemistry and nutritional status during sink-source transitions have been addressed on the level of sucrose transport (e.g. [48]), but much less on the level of secondary metabolites. However, in addition to differences in physiological roles of leaves and tubers, their chemistry is also under selection pressure to defend the plant to different biotic stresses, such as insects, snails, vertebrate herbivores, fungi and bacteria. Hence, differences in secondary metabolites such as GLS can be expected between the different tissues of turnip plants. Two recent reviews address these issues. Jørgensen et al. [20] present what is known about transport of defence compounds from source to sink, and use GLS as a case study. They discuss especially the roles of GLS transporters in establishing dynamic GLS patterns in Arabidopsis source and sink tissues. Burow and Halkier [19] also use GLS as case study and discuss how Arabidopsis orchestrates synthesis, storage and mobilization to target tissues.

In this paper, a GLS analysis is presented which aims to provide insight in the chemical changes which accompany development of turnip tissues that function as sinks and sources for the plant. It differs from earlier studies, which focus on single tissues (either leaves or turnip tubers) and or single timepoints. It becomes clear that there are large chemical differences between tissues, between developmental-stages and between genotypes. Clearly these differences will play a role in the eco-physiology of the turnip, given the reported involvement of GLS in plant defence.

 

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http://doi.org/10.1371/journal.pone.0217862

 

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