Elsevier

Phytochemistry

Volume 72, Issue 7, May 2011, Pages 538-556
Phytochemistry

Review
Phytochemicals of Brassicaceae in plant protection and human health – Influences of climate, environment and agronomic practice

https://doi.org/10.1016/j.phytochem.2011.01.014Get rights and content

Abstract

In this review, we provide an overview of the role of glucosinolates and other phytochemical compounds present in the Brassicaceae in relation to plant protection and human health. Current knowledge of the factors that influence phytochemical content and profile in the Brassicaceae is also summarized and multi-factorial approaches are briefly discussed. Variation in agronomic conditions (plant species, cultivar, developmental stage, plant organ, plant competition, fertilization, pH), season, climatic factors, water availability, light (intensity, quality, duration) and CO2 are known to significantly affect content and profile of phytochemicals. Phytochemicals such as the glucosinolates and leaf surface waxes play an important role in interactions with pests and pathogens. Factors that affect production of phytochemicals are important when designing plant protection strategies that exploit these compounds to minimize crop damage caused by plant pests and pathogens. Brassicaceous plants are consumed increasingly for possible health benefits, for example, glucosinolate-derived effects on degenerative diseases such as cancer, cardiovascular and neurodegenerative diseases. Thus, factors influencing phytochemical content and profile in the production of brassicaceous plants are worth considering both for plant and human health. Even though it is known that factors that influence phytochemical content and profile may interact, studies of plant compounds were, until recently, restricted by methods allowing only a reductionistic approach. It is now possible to design multi-factorial experiments that simulate their combined effects. This will provide important information to ecologists, plant breeders and agronomists.

Graphical abstract

This review summarizes and discusses the current knowledge on (1) phytochemicals of brassicaceous plants important for plant protection and human health, (2) factors that influence the content of these compounds, (3) plant protection strategies that exploit secondary metabolites of Brassicaceae to minimize crop damage.

  1. Download : Download full-size image

Research highlights

► We reviewed phytochemicals of Brassicaceae in plant protection and human health. ► We summarize the biotic and abiotic factors influencing Brassicaceae phytochemicals. ► Multi-factorial approaches that simulate effects on phytochemicals are promising. ► Plant protection strategies exploiting phytochemicals of Brassicaceae are promising.

Introduction

Over the last two decades crops in the Brassicaceae (formerly Cruciferae) have been the focus of intense research based on their human health benefits (Traka and Mithen, 2009, Verkerk et al., 2009). Although horticultural brassicaceous plants are excellent sources of fiber, vitamins and minerals, the majority of the research has concentrated on the content of secondary metabolites, primarily glucosinolates. Health benefits, such as reduced risk for degenerative diseases, are largely attributed to the plant content of secondary substances (Forte et al., 2008, van Horn et al., 2008, Virgili and Marino, 2008). In addition to human health aspects, secondary metabolites such as glucosinolates and leaf surface waxes are important for plant defence. As the use of synthetic insecticides is increasingly restricted, there is an increased interest in alternative methods for pest control, such as the use of resistant plants or integrated cropping strategies in which plant secondary metabolites may enhance crop protection. Both climatic conditions and agronomic practices influence the plant content of phytochemicals (Ahuja et al., 2010b). Thus a better understanding of the effects of climatic and agronomic factors is needed to increase the predictability of the content of desired compounds, from a human health or pest control perspective.

In this review, we summarize current knowledge of the role of glucosinolates and other compounds present in Brassicaceae in relation to both plant protection and human health. Furthermore, we discuss factors that influence phytochemical content and profile during production of brassicaceous crops and give examples of cropping strategies in which phytochemicals are important for the control of pests and pathogens. We also discuss plant breeding in relation to both plant resistance and human health. Fig. 1 gives a schematic overview of the factors influencing content and profile of phytochemicals and consequential effects on taste, human health and plant defence. Since glucosinolates are the best studied compounds in the Brassicaceae, this review focuses on these secondary metabolites, but other compounds in the Brassicaceae are also included.

Section snippets

The cultivation and use of brassicaceous crops

Ten thousand year old traces of cultivation give evidence that plants in the family Brassicaceae are among the oldest cultivated plants known (Snowdon et al., 2007). Plants in the Brassicaceae are grown around the world for biofuel, edible oil, biofumigants, human food and animal feed. A long history of plant breeding has resulted in this group of crops being highly variable in appearance, phytochemistry and use. Brassica oleracea is a good example with broccoli (Botrytis group), cauliflower

Glucosinolates, other secondary metabolites and compounds in brassicaceous crops

In Fraenkel (1959) postulated that the overwhelming array of chemicals found in plants were more than simply by-products of primary metabolism. Because there are costs associated with the production of all metabolites, although these may be minor, it is generally assumed that genes for secondary metabolites are inherited due to the evolutionary advantages they impart to the plant, especially for defence from abiotic stress, plant pathogens, parasites and herbivores (Dong and Kahmann, 2009,

Brassica secondary metabolites and other compounds for human health

Secondary plant metabolites, as components of herbal remedies, have been important in human medicine many centuries before the active compounds were identified (Theis and Lerdau, 2003). In the last two decades, the general view of plants as merely sources of food and nutrition has been supplemented with studies on medical and/or bioactive properties of plants used for human consumption. These health properties are largely attributed to the content of secondary substances and are linked to a

Brassica secondary metabolites for healthy plants

Secondary metabolites in plants may have evolved as adaptations to a wide range of selective pressures, of which evolved defences against pests and diseases is the most commonly suggested benefit. Secondary metabolites have been used in the battle against insect herbivores and plant pathogens for the production of healthy food and feed plants for centuries. This has been achieved by plant breeders selecting plants with resistance properties or by including plants with desired chemical

Influence of agro-ecosystem, climate and light on compounds in the Brassicaceae

Levels and profiles of compounds in the Brassicaceae, such as glucosinolates and carotenoids, depend on cultivar, species, plant age and organ, climate, soil type, cultivation and agronomic practices (Bradshaw et al., 1984, Brown et al., 2002, Carlson et al., 1987, Clossais-Besnard and Larher, 1991, Farnham et al., 2004, Heaney et al., 1983, Hill et al., 1987, Jongen, 1996, Kushad et al., 1999, Lewis and Fenwick, 1987, Milford and Evans, 1991, Rangkadilok et al., 2002b, Rodriguez-Amaya et al.,

From theory to practice: Brassica metabolites in pest and disease control

In this section we will focus on different aspects of control of pests and diseases in Brassicaceae based on exploitation of plant metabolites and give some practical examples on the way forward. Several direct methods have been tested to combat pests and diseases in brassicaceous crops, and some have been successful, but most are still in an early stage of development. Methods that involve Brassicaceae metabolites include pest and disease resistant plants, soil biofumigation and to some extent

From theory to practice: understanding the biosynthesis to enhance plant and human health compounds

Understanding the key steps in biosynthesis and degradation opens up possibilities for targeted modifications of glucosinolate profiles and corresponding degradation products. Recent findings suggest that QTLs are associated to glucosinolate metabolism in plants and opens for targeted breeding in Brassicaceae crop plants (Lou et al., 2008, Nagaoka et al., 2010, Schranz et al., 2009, Wentzell et al., 2007). One should, however, bear in mind that a large part of the biochemistry has been

Future perspectives for compounds in plant and human health in the Brassicaceae: Towards a global model strategy?

In this review, we have discussed both abiotic and biotic factors that influence the content and profile of secondary metabolites in the Brassicaceae, as well as described different production systems in which secondary metabolites may contribute to an optimized control of pests and pathogens. Unraveling the mechanisms behind the production of plant compounds under specific agricultural and climatic conditions is of great scientific and economic interest as it is one necessary step towards

Role of the funding source

The Norwegian Research Council (Project Nos. 186903 and 10322600) and the Scottish Government Rural and Environment Research and Analysis Directorate (UK) supported the work financially by funding man-hours used in preparation of this paper.

Acknowledgements

Dr. Ishita Ahuja and Ms. Inger Halvorsen are acknowledged for corrections in the reference list. The authors also thank two anonymous referees for their valuable comments and suggestions that have improved this review.

Ingeborg Klingen is head of the research group Pests in field crops and vegetables at the Norwegian Institute for Agricultural and Environmental Research (Bioforsk), Plant Health and Plant Protection Division. Her research focuses on the use of pathogens of invertebrates in biological and integrated pest management systems including push–pull strategies where invertebrate pathogens are kill elements in the pull part of the strategy. She also studies tritrophic interactions (plant, insect/mite,

References (337)

  • M.E. Daxenbichler et al.

    Glucosinolate composition of seeds from 297 species of wild plants

    Phytochemistry

    (1991)
  • S. De Pascale et al.

    Sulphur fertilization may improve the nutritional value of Brassica rapa L. subsp. sylvestris

    Eur. J. Agron.

    (2007)
  • X. Dong et al.

    Battle for survival: plants and their allies and enemies

    Curr. Opin. Plant Biol.

    (2009)
  • A.B. Durkeet et al.

    Flavonol glycosides in Brassica and Sinapis

    Phytochemistry

    (1973)
  • S.D. Eigenbrode

    The effects of plant epicuticular waxy blooms on attachment and effectiveness of predatory insects

    Arthropod Struct. Dev.

    (2004)
  • J.W. Fahey et al.

    The chemical diversity and distribution of glucosinolates and isothiocyanates among plants

    Phytochemistry

    (2001)
  • M. Francisco et al.

    Simultaneous identification of glucosinolates and phenolic compounds in a representative collection of vegetable Brassica rapa

    J. Chromatogr. A

    (2009)
  • I. Ahuja et al.

    Defence mechanisms of Brassicaceae: implications for plant–insect interactions and potential for integrated pest management. A review

    Agron. Sustain. Dev.

    (2010)
  • A.A. Agrawal et al.

    A role for isothiocyanates in plant resistance against the specialist herbivore Pieris rapae

    J. Chem. Ecol.

    (2003)
  • I. Åhman

    Toxicities of host secondary compounds to eggs of the Brassica specialist Dasineura brassicae

    J. Chem. Ecol.

    (1985)
  • A.M. Arany et al.

    Glucosinolates and other metabolites in the leaves of Arabidopsis thaliana from natural populations and their effects on a generalist and a specialist herbivore

    Chemoecology

    (2008)
  • O. Azarenko et al.

    Suppression of microtubule dynamic instability and turnover in MCF7 breast cancer cells by sulforaphane

    Carcinogenesis

    (2008)
  • I. Badawy et al.

    Biochemical and toxicological studies on the effect of high and low erucic acid rapeseed oil on rats

    Nahrung

    (1994)
  • Badenes-Pérez, F.R., Reichelt, M., Gershenzon, J., Heckel, D.G., 2010. Phylloplane location of glucosinolates in...
  • F.R. Badenes-Pérez et al.

    Evaluating trap crops for diamondback moth (L.) Plutella xylostella (Lepidoptera: Plutellidae)

    J. Econ. Entomol.

    (2004)
  • E.A. Baker

    The influence of environment on leaf wax development in Brassica oleracea var. gemmifera

    New Phytol.

    (1974)
  • J.E. Banks

    The scale of landscape fragmentation affects herbivore response to vegetation heterogeneity

    Oecologia

    (1998)
  • E. Bartlet et al.

    Wound-induced increases in the glucosinolate content of oilseed rape and their effect on subsequent herbivory by a crucifer specialist

    Entomol. Exp. Appl.

    (1999)
  • E. Bartlet et al.

    The influence of glucosinolates and sugars on feeding by the cabbage stem flea beetle, Psylliodes chrysocephala

    Entomol. Exp. Appl.

    (1994)
  • R. Baur et al.

    Oviposition and chemosensory stimulation of the root flies Delia radicum and D. floralis in response to plants and leaf surface extracts from resistant and susceptible Brassica genotypes

    Entomol. Exp. Appl.

    (1996)
  • P. Bednarek et al.

    A glucosinolate metabolism pathway in living plant cells mediates broadspectrum antifungal defense

    Science

    (2009)
  • C.W.W. Beecher

    Cancer preventive properties of varieties of Brassica oleracea: a review

    Am. J. Clin. Nutr.

    (1994)
  • E.A. Bernays

    When host choice is a problem for a generalist herbivore, experiments with the whitefly, Bemisia tabaci

    Ecol. Entomol.

    (1999)
  • S. Bhamre et al.

    Temporal changes in Gene expression induced by sulforaphane in human prostate cancer cells

    Prostate

    (2009)
  • A. Bhattacharya et al.

    Inhibition of bladder cancer development by allyl isothiocyanate

    Carcinogenesis

    (2010)
  • A.N.E. Birch et al.

    A time-course study of chemical and physiological responses in Brassicas induced by turnip root fly (Delia floralis) larval feeding

    Entomol. Exp. Appl.

    (1996)
  • A.N.E. Birch et al.

    Glucosinolate responses of swede, kale, forage and oilseed rape to root damage by turnip root fly (Delia floralis) larvae

    J. Sci. Food Agric.

    (1992)
  • Björkman, M., 2007. Effects of intercropping on the life cycle of the turnip root fly (Delia floralis). Behaviour,...
  • M. Björkman et al.

    Neighbouring monocultures enhance the effect of intercropping on the turnip root fly (Delia floralis)

    Entomol. Exp. Appl.

    (2007)
  • M. Björkman et al.

    Combined effect of intercropping and turniproot fly (Delia floralis) larval feeding on the glucosinolate concentrations in cabbage roots and foliage

    J. Chem. Ecol.

    (2008)
  • M.M. Blight et al.

    Antennal perception of oilseed rape, Brassica napus (Brassicaceae), volatiles by the cabbage seed weevil Ceutorhynchus assimilis (Coleoptera: Curculionidae)

    J. Chem. Ecol.

    (1995)
  • A. Bones et al.

    Sulphate can induce differential expression of thioglucoside glucohydrolases (myrosinases)

    Planta

    (1994)
  • A.M. Bones et al.

    The myrosinase–glucosinolate system, its organisation and biochemistry

    Physiol. Plant.

    (1996)
  • V. Borek et al.

    Allelochemicals produced during sinigrin decomposition in soil

    J. Agric. Food Chem.

    (1994)
  • B.H. Borgen et al.

    Removing the mustard oil bomb from seeds – transgenic ablation of myrosin cells in oilseed rape (Brassicanapus) produces MINELESS seeds

    J. Exp. Bot.

    (2010)
  • R.P. Bradburne et al.

    Glucosinolate genetics and the attraction of the aphid parasitoid Diaeretiella rapae to Brassica

    Proc. R. Soc. Lond. Sci. Ser. B

    (2000)
  • G. Brader et al.

    Altering glucosinolate profiles modulates disease resistance in plants

    Plant J.

    (2006)
  • J.E. Bradshaw et al.

    The glucosinolate content of some fodder brassicas

    J. Sci. Food Agric.

    (1984)
  • K. Brandt et al.

    A systematic approach for identifying plant components with impact on human health

    Acta Hort.

    (2007)
  • M. Bridges et al.

    Spatial organization of the glucosinolate–myrosinase system in Brassica specialist aphids is similar to that of the host plant

    Proc. R. Soc. B

    (2002)
  • Cited by (308)

    View all citing articles on Scopus

    Ingeborg Klingen is head of the research group Pests in field crops and vegetables at the Norwegian Institute for Agricultural and Environmental Research (Bioforsk), Plant Health and Plant Protection Division. Her research focuses on the use of pathogens of invertebrates in biological and integrated pest management systems including push–pull strategies where invertebrate pathogens are kill elements in the pull part of the strategy. She also studies tritrophic interactions (plant, insect/mite, pathogen) that may enhance or disturb these systems and she has been working specifically with Brassicaceae pests and how brassicaceous crops may affect the efficacy of insect pathogenic fungi. She obtained her M.Sc. in Applied Entomology in 1992 at the Norwegian University of Life Sciences (UMB) and earned her Ph.D. in 2000 on microbial control of vegetable pests by insect pathogenic fungi. She is the sectretary of the Fungal Division of Society of Invertebrate Pathology and a member of Food and Feed Panel of the Norwegian Scientific Committee for Food Safety, Panel 2 Pesticides.

    1

    Björkman and Klingen contributed equally.

    View full text