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Phytoalexins in Defense Against Pathogens

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Phytoalexins in Defense Against Pathogens Review Feature Review Phytoalexins in defense against pathogens * * Ishita Ahuja , Ralph Kissen and Atle M. Bones Department of Biology, Norwegian University of Science and Technology, Realfagbygget, NO-7491 Trondheim, Norway Plants use an intricate defense system against pests and phytoalexins contribute to the antioxidant, anticarcinogenic pathogens, including the production of low molecular and cardiovascular protective activities of Brassica vegeta- mass secondary metabolites with antimicrobial activity, bles [2,12]. Peanut (Arachis hypogea) phytoalexins have which are synthesized de novo after stress and are antidiabetic, anticancer and vasodilator effects [11]. The collectively known as phytoalexins. In this review, we biological activities of glyceollin, a soybean (Glycine max) focus on the biosynthesis and regulation of camalexin, phytoalexin, include antiproliferative and antitumor and its role in plant defense. In addition, we detail some actions [9]. The sorghum (Sorghum bicolor) phytoalexins, of the phytoalexins produced by a range of crop plants 3-deoxyanthocyanins, might be useful in helping to reduce from Brassicaceae, Fabaceae, Solanaceae, Vitaceae and incidence of gastrointestinal cancer [13]. The phytoalexin Poaceae. This includes the very recently identified kaur- resveratrol from grapevine (Vitis vinifera) has anti-aging, alexins and zealexins produced by maize, and the bio- anticarcinogenic, anti-inflammatory and antioxidant prop- synthesis and regulation of phytoalexins produced by erties that might be relevant to chronic diseases and/or rice. Molecular approaches are helping to unravel some longevity in humans [10]. of the mechanisms and reveal the complexity of these However, the biosynthesis of most phytoalexins, the bioactive compounds, including phytoalexin action and regulatory networks involved in their induction by biotic metabolism. and abiotic stress, and the molecular mechanisms behind their cytotoxicity are largely unknown. In this review, we Phytoalexins: part of the plant response repertoire detail some of the recent advances in this field, focusing on Crop loss due to pest and pathogen attack is a serious the model plant Arabidopsis (Arabidopsis thaliana) and problem worldwide. Plants are constantly attacked by crop plants from Brassicaceae, Fabaceae, Solanaceae, many potential pathogens and respond by the activation Vitaceae and Poaceae. The substantial progress that has of defense genes, the formation of reactive oxygen species recently been made in identifying the biosynthetic steps of (ROS), the synthesis of pathogenesis-related (PR) proteins, camalexin, a phytoalexin produced by Arabidopsis, and the localized cell-wall reinforcement and the production of attempts to decipher its regulation and to understand its antimicrobial compounds. Low molecular mass secondary role in resistance to pathogens will be covered first. Arabi- metabolites with antimicrobial activity that are induced by dopsis mutants affected in their capacity to produce cama- stress are collectively named phytoalexins, and are an lexin upon challenge with pathogens (see Table S1 in the important part of the plant defense repertoire [1,2]. Phy- supplementary material online), their biochemical charac- toalexins are a heterogeneous group of compounds terization and their use in pathogenicity tests have been of (Figure 1) [3–5] that show biological activity towards a great importance in this respect. To develop disease pro- variety of pathogens and are considered as molecular tection strategies, plant pathogen research in the field of markers of disease resistance. phytoalexins has also focused on interpreting their biosyn- The concept of phytoalexins was introduced over 70 years thesis pathways and regulation in different crop plants by ago [6] based on the finding that potato (Solanum tubero- using different cultivars, transgenic plants and mutants, sum) tuber tissue that had previously been infected with an and by applying -omics, molecular biology and biochemical incompatible race of Phytophthora infestans induced resis- approaches. Most of the reviews in this direction so far tance to a compatible race of P. infestans. It was hypothe- have been written on phytoalexins belonging to a particu- sized that the tuber tissue, in response to the incompatible lar plant or family or focused on a particular group of interaction, produced substances (phytoalexins) that inhib- phytoalexins. However, in this review, we provide a ited the pathogen and protected the tissue against later broader perspective on the research on phytoalexins by infection by other compatible races of the pathogen [2,6,7]. covering their diversity, biosynthesis and regulation, and Since then, the field has evolved extensively, not only with their accumulation or enhancement after pathogen infec- respect to studying the roles of phytoalexins in defense tion or elicitor treatment in some major crop plants. against pathogens and pests, but also with respect to their health-promoting effects [2,8–13]. For example, indole Camalexin: the major phytoalexin in Arabidopsis 0 Camalexin (3-thiazol-2 -yl-indole), a phytoalexin that was Corresponding author: Bones, A.M. ([email protected]) * These authors contributed equally. first isolated from a plant in the Brassicaceae family, 1360-1385/$ – see front matter ß 2011 Elsevier Ltd. All rights reserved. doi:10.1016/j.tplants.2011.11.002 Trends in Plant Science, February 2012, Vol. 17, No. 2 73 Review Trends in Plant Science February 2012, Vol. 17, No. 2 Brassicaceae Fabaceae Vitaceae HO S N HO O HO O O OH H O OH O HO N H O H C OH O H O 3 H C H O OH 3 Resveratrol Camalexin CH3 H OH O OCH3 O Medicarpin Wighteone (+)-Pisatin HO HN N CH3 H CH3 S CH3 CH3 S OH CH3 OH CH3 HO OH CH3 Spirobrassinin OH H N OH OH ε S OH -viniferin OH HO O HO HO N OH O CH3 Arachidin 1 Arachidin 2 Arachidin 3 Rutalexin H HO H3C N H C S 3 O O O O H H OH N OH OH HO Brassilexin CH2 O O OH OH Resveratrol Glyceollin I Glyceollin III Poaceae Solanaceae O O O H OH O OCH OCH3 OCH 3 OCH3 3 HO CH3 H CH3 H HO O H CH3 CH2 Capsidiol N Kauralexin A1 Kauralexin B1 Zealexin A1 Zealexin B1 H O H3C O OH OH OH O Avenanthramide A HO O O CH 2 CH CH3 H CH 2 3 CH3 H O O HO Scopoletin H3C OH CH3 H O O HO O H H C H OH O OH 3 O H C 3 CH3 O Momilactone A Phytocassane A Sakuranetin OH O Luteolin TRENDS in Plant Science Figure 1. Structures of selected phytoalexins produced by members of the Brassicaceae, Fabaceae, Solanaceae, Vitaceae and Poaceae. camelina (Camelina sativa), after which it was named [14], supplementary material online. Camalexin can be induced has also been detected in Arabidopsis and a few related in Arabidopsis by the recognition of a range of different Brassicaceae species [15]. Although camalexin biosynthe- pathogen-derived substances known as microbe-associated sis in Arabidopsis has not yet been fully elucidated, sev- molecular patterns (MAMPs), such as the oomycete necro- eral of the steps in the pathway have been characterized sis and ethylene-inducing peptide1 (Nep1)-like proteins over recent years (Box 1). Camalexin was long thought and bacteria-derived peptidoglycan [17,18]. Although oth- to be the only phytoalexin produced by Arabidopsis, er pathogen-mimicking stimuli, such as plant cell wall- but another, rapalexin A, has also been detected in this derived oligogalacturonides, chitosan and the bacterial species [16]. flagellin peptide Flg22, induced the expression of cama- lexin biosynthetic genes [19–21], triggering of camalexin Camalexin-inducing conditions and its natural variation biosynthesis has not been observed in all instances [18,22– in Arabidopsis 24]. Treatment of Arabidopsis with autoclaved baker’s The production of camalexin can be induced in Arabidopsis yeast (Saccharomyces cerevisiae) suspension and fungal leaves by a range of biotrophic and necrotrophic plant toxins (victorin produced by Cochliobolus victoriae or fusa- pathogens (bacteria, oomycetes, fungi and viruses). Some ric acid produced by Fusarium spp.) also induced the examples are listed in Figure 2 and Table S1 in the production of camalexin [25–27]. 74 Review Trends in Plant Science February 2012, Vol. 17, No. 2 Abiotic stresses, such as UV-B, UV-C, chemicals (e.g. challenge with Pseudomonas syringae or Alternaria bras- acifluorfen, paraquat, chlorsulfuron and a-amino butyric sicicola than did the wild type [41,46]. By contrast, cama- acid) and heavy metal ions (e.g. silver nitrate), can also lexin induction after mitogen-activated protein kinase induce camalexin in Arabidopsis leaves [28,29]. Treatment (MAPK) MPK3/MPK6 activation (see below) is considered with C6-aldehydes, which are plant volatiles typically to be independent of ethylene [47]. It has recently been released upon wounding, has been reported to elevate suggested that miR393, a plant miRNA induced by Flg22, levels of camalexin [30]. However, another study showed is able to regulate camalexin production by affecting auxin that wounding alone did not enhance the production of signaling. miR393 targets the auxin receptors and thereby camalexin, although wounding primed the plant for prevents activation of the auxin response factor 9 (ARF9) quicker camalexin production upon subsequent Botrytis transcription factor, a positive regulator of camalexin bio- cinerea inoculation, and hence contributed to enhanced synthesis. This allows Arabidopsis to redirect its metabolic resistance [31]. flow from camalexin to glucosinolates, which are more Although most camalexin measurements reported in effective in biotroph resistance. In addition, repression the literature are performed on whole leaves or seedlings, of auxin signaling prevents auxin from antagonizing SA it has been shown that the increase in camalexin levels is signaling, enabling the plant to mount an SA response [48]. largely limited to the area surrounding the lesion [32,33]. ROS are also generally associated with camalexin produc- There is little information about the induction of camalexin tion, as shown by the induction of camalexin by oxidative production in organs other than rosette leaves in Arabi- stress-inducing chemicals such as paraquat and acifluorfen dopsis.
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