Regulation and function of specifier proteins in plants

Burow, Meike; Wittstock, Ute

doi:10.1007/s11101-008-9113-5

Cited by 60 publications

(45 citation statements)

References 85 publications

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“…Hydrolysis of the thioglucosidic bond of glucosinolates by myrosinases releases unstable aglucones, which can rapidly decompose to various bioactive compounds, including isothiocyanates, simple nitriles, organic thiocyanates, or epithionitriles depending on the presence of specifier proteins, thiocyanateforming proteins, and certain environmental factors, such as Fe(II) ions, and pH (Wittstock and Burow, 2010;Bednarek, 2012). In Arabidopsis thaliana, the Col-0 ecotype produces predominantly isothiocyanates because of the absence of epithiospecifier protein activity (Lambrix et al, 2001;Burow and Wittstock, 2009). Among all types of the GS hydrolysis products, isothiocyanates have been demonstrated to have the highest chemical reactivity and are toxic to a wide range of organisms including microorganisms, nematodes, and insects (Bednarek, 2012;Fan and Doerner, 2012).…”

Section: Introductionmentioning

confidence: 99%

Pathogen-Responsive MPK3 and MPK6 Reprogram the Biosynthesis of Indole Glucosinolates and Their Derivatives in Arabidopsis Immunity

et al. 2016

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ORCID IDs: 0000-0001-6683-6415 (J.X.); 0000-0002-9910-3119 (J.M.); 0000-0002-4265-7399 (J.L.); 0000-0002-0757-5208 (Q.W.); 0000-0003-2959-6461 (S.Z.)Antimicrobial compounds have critical roles in plant immunity; for example, Arabidopsis thaliana and other crucifers deploy phytoalexins and glucosinolate derivatives in defense against pathogens. The pathogen-responsive MITOGEN-ACTIVATED PROTEIN KINASE3 (MPK3) and MPK6 have essential functions in the induction of camalexin, the major phytoalexin in Arabidopsis. In search of cyanide, a coproduct of ethylene and camalexin biosynthesis, we found that MPK3 and MPK6 also affect the accumulation of extracellular thiocyanate ion derived from the indole glucosinolate (IGS) pathway. Botrytis cinerea infection activates MPK3/MPK6, which promote indole-3-yl-methylglucosinolate (I3G) biosynthesis and its conversion to 4-methoxyindole-3-yl-methylglucosinolate (4MI3G). Gain-and loss-of-function analyses demonstrated that MPK3/MPK6 regulate the expression of MYB51 and MYB122, two key regulators of IGS biosynthesis, as well as CYP81F2 and IGMT1/ IGMT2, which encode enzymes in the conversion of I3G to 4MI3G, through ETHYLENE RESPONSE FACTOR6 (ERF6), a substrate of MPK3/MPK6. Under the action of PENETRATION2 (PEN2), an atypical myrosinase, and PEN3, an ATP binding cassette transporter, 4MI3G is converted to extracellular unstable antimicrobial compounds, possibly isothiocyanates that can react with nucleophiles and release the stable thiocyanate ion. Recent studies demonstrated the importance of PEN2/ PEN3-dependent IGS derivatives in plant immunity. Here, we report that MPK3/MPK6 and their substrate ERF6 promote the biosynthesis of IGSs and the conversion of I3G to 4MI3G, a target of PEN2/PEN3-dependent chemical defenses in plant immunity.

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Section: Introductionmentioning

confidence: 99%

Pathogen-Responsive MPK3 and MPK6 Reprogram the Biosynthesis of Indole Glucosinolates and Their Derivatives in Arabidopsis Immunity

et al. 2016

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“…The spontaneous formation of nitriles is favoured at low pH values, as protons block the Lossen rearrangement18. Further, if an alkenyl GLS and the epithiospecifier protein (ESP) are present, the degradation process of the aglucon can be modified and an EPT can be released1719 (Fig. 1).…”

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confidence: 99%

Optimizing isothiocyanate formation during enzymatic glucosinolate breakdown by adjusting pH value, temperature and dilution in Brassica vegetables and Arabidopsis thaliana

Hanschen

Oliviero

Schreiner

et al. 2017

Sci Rep

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Consumption of glucosinolate-rich Brassicales vegetables is associated with a decreased risk of cancer with enzymatic hydrolysis of glucosinolates playing a key role. However, formation of health-promotingisothiocyanates is inhibited by the epithiospecifier protein in favour of nitriles and epithionitriles. Domestic processing conditions, such as changes in pH value, temperature or dilution, might also affect isothiocyanate formation. Therefore, the influences of these three factors were evaluated in accessions of Brassica rapa, Brassica oleracea, and Arabidopsis thaliana. Mathematical modelling was performed to determine optimal isothiocyanate formation conditions and to obtain knowledge on the kinetics of the reactions. At 22 °C and endogenous plant pH, nearly all investigated plants formed nitriles and epithionitriles instead of health-promoting isothiocyanates. Response surface models, however, clearly demonstrated that upon change in pH to domestic acidic (pH 4) or basic pH values (pH 8), isothiocyanate formation considerably increases. While temperature also affects this process, the pH value has the greatest impact. Further, a kinetic model showed that isothiocyanate formation strongly increases due to dilution. Finally, the results show that isothiocyanate intake can be strongly increased by optimizing the conditions of preparation of Brassicales vegetables.Brassicales plants, including Arabidopsis thaliana, broccoli, cabbage and pak choi contain glucosinolates (GLSs). These sulphur-containing secondary plant metabolites not only play an important role in the plant's defense against biotic stressors, but also affect the taste of these vegetables and contribute to human health 1 . To date, a total of 130 GLSs have been identified that can be subdivided according to the structure of their variable side chain into the group of aliphatic, aromatic or indole GLS 2 . These plant metabolites are stored in the plant vacuole or in specialized S-cells 3 , but upon cell disruption, they encounter the endogenous GLS-hydrolysing enzyme myrosinase, a β-d-thioglucosidase, and the GLSs will be hydrolysed to release isothiocyanates (ITCs), nitriles and epithionitriles (EPTs) 4 . Due to their electrophilicity, GLSs in general and ITCs in particular act as effective deterrents against a multitude of pathogens as these compounds have antifungal, antimicrobial as well as insecticidal properties [5][6][7] . For humans, ITCs, such as the 4-(methylsulphinyl)butyl ITC (4MSOB-ITC), exert a multitude of health beneficial effects, including antimicrobial, antiinflammatory, antithrombotic and chemopreventive effects [8][9][10]

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“…The profile of hydrolysis products then depends on glucosinolate structure, cellular conditions, and the presence of so-called "specifier proteins" leading to the formation of isothiocyanates (ITCs), thiocyanates, nitriles, and epithionitriles (6). Due to their chemical properties, ITCs are the most reactive hydrolysis products of glucosinolates (6,9). Although several generalist lepidopterans detoxify ITCs via conjugation with glutathione (10), the specialists investigated so far circumvent ITC formation (7,11,12).…”

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Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

Beran¹,

Pauchet²,

Kunert

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

109

143

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The ability of a specialized herbivore to overcome the chemical defense of a particular plant taxon not only makes it accessible as a food source but may also provide metabolites to be exploited for communication or chemical defense. Phyllotreta flea beetles are adapted to crucifer plants (Brassicales) that are defended by the glucosinolate-myrosinase system, the so-called "mustard-oil bomb." Tissue damage caused by insect feeding brings glucosinolates into contact with the plant enzyme myrosinase, which hydrolyzes them to form toxic compounds, such as isothiocyanates. However, we previously observed that Phyllotreta striolata beetles themselves produce volatile glucosinolate hydrolysis products. Here, we show that P. striolata adults selectively accumulate glucosinolates from their food plants to up to 1.75% of their body weight and express their own myrosinase. By combining proteomics and transcriptomics, a gene responsible for myrosinase activity in P. striolata was identified. The major substrates of the heterologously expressed myrosinase were aliphatic glucosinolates, which were hydrolyzed with at least fourfold higher efficiency than aromatic and indolic glucosinolates, and β-O-glucosides. The identified beetle myrosinase belongs to the glycoside hydrolase family 1 and has up to 76% sequence similarity to other β-glucosidases. Phylogenetic analyses suggest species-specific diversification of this gene family in insects and an independent evolution of the beetle myrosinase from other insect β-glucosidases. convergent evolution | host plant specialization P hytophagous insects are confronted with an arsenal of constitutive and inducible chemical plant defenses (1). To avoid deleterious effects from plant toxins, herbivores require appropriate biochemical adaptations allowing them to deal with these metabolites, for example, by developing insensitive target sites or by enzymatic detoxification. Many specialized insects are able to sequester plant defense compounds and exploit them for their own protection against natural enemies and/or as semiochemicals in interspecific communication (2, 3).The glucosinolate-myrosinase system characteristic of plants in the order Brassicales is one of the best-studied activated plant defense systems (4-6), and several different strategies for avoiding glucosinolate toxicity have been described in specialized insect herbivores of the orders Lepidoptera, Hemiptera, and Hymenoptera (7). Glucosinolates are a structurally diverse group of β-thioglucoside-N-hydroxysulfates that are classified according to their precursor amino acid as aliphatic, aromatic, or indolic glucosinolates (6,8). Plant myrosinases, ascorbate-dependent β-thioglucosidases (EC 3.2.1.147) belonging to glycoside hydrolase family 1 (GH1), are stored separately from the glucosinolates and only come into contact with their substrate when the spatial compartmentalization is destroyed, for example, by herbivore feeding (6). The profile of hydrolysis products then depends on glucosinolate structure, cellular conditio...

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Regulation and function of specifier proteins in plants

Cited by 60 publications

References 85 publications

Pathogen-Responsive MPK3 and MPK6 Reprogram the Biosynthesis of Indole Glucosinolates and Their Derivatives in Arabidopsis Immunity

Pathogen-Responsive MPK3 and MPK6 Reprogram the Biosynthesis of Indole Glucosinolates and Their Derivatives in Arabidopsis Immunity

Optimizing isothiocyanate formation during enzymatic glucosinolate breakdown by adjusting pH value, temperature and dilution in Brassica vegetables and Arabidopsis thaliana

Phyllotreta striolataflea beetles use host plant defense compounds to create their own glucosinolate-myrosinase system

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