Sulfur Containing Compound Database
| AGI ID | UniProt ID | EnsemblPlants | Gene Name | Protein Name | Function | Description |
|---|---|---|---|---|---|---|
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GSTF6 |
Glutathione S-transferase F6 |
GSTF6 overexpression increased and GSTF6-knockout reduced camalexin production. Arabidopsis GSTF6 expressed in yeast cells catalyzed GSH(IAN) formation. GSH(IAN), (IAN)CysGly, and γGluCys(IAN) were determined to be intermediates within the camalexin biosynthetic pathway. The expression of GSTF6, GGT1, GGT2, and PCS1 was coordinately upregulated during camalexin biosynthesis. These results suggest that GSH is the Cys derivative used during camalexin biosynthesis, that the conjugation of GSH with IAN is catalyzed by GSTF6, and that GGTs and PCS are involved in camalexin biosynthesis (Su et al. 2011). |
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AAO4 |
Benzaldehyde dehydrogenase |
A. thaliana siliques produce high levels of benzoic acid (BA) that also include GSL compounds such as 3-benzoyloxypropylGSL (3BZO) and 4-benzoyloxybutylGSL (4BZO). T-DNA insertions that eliminate functional transcripts of At1g04580 (AAO4) cause decreases in the levels of total benzoic acid (BA) and in the levels of benzoylated GSLs in seeds (Ibdah et al. 2009) |
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SDI2 |
Protein SULFUR DEFICIENCY-INDUCED 2 |
Sulfur deficiency induced 1 (SD1) and SD2 are –S marker genes sulfur deficiency that act as major repressors controlling GSL biosynthesis in Arabidopsis under –S condition. SDI1 and SDI2 expression negatively correlated with GSL biosynthesis in both transcript and metabolite levels. Principal components analysis of transcriptome data indicated that SDI1 regulates aliphatic GSL biosynthesis as part of –S response. SDI1 was localized to the nucleus and interacted with MYB28 a major transcription factor that promotes aliphatic GSL biosynthesis in both yeast and plant cells (Aarabi et al. 2016) |
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OBP2 |
Dof zinc finger protein DOF1.1 |
OBP2 is expressed in the vasculature of all Arabidopsis organs; including leaves; roots; flower stalks and petals. OBP2 expression is induced in response to a generalist herbivore; Spodoptera littoralis and by treatment with the plant signalling molecule methyl jasmonate both of which also trigger indolic GSL accumulation (Skirycz et al. 2006) |
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CYP71A18 |
Cytochrome P450 71A18 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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FMOGS-OX6 |
Flavin-containing monooxygenase FMO GS-OX6 |
Two additional FMOGS-OX enzymes; FMOGS-OX6 and FMOGS-OX7 encoded by At1g12130 and At1g12160 respectively. The overexpression of both FMOGS-OX6 and FMOGS-OX7 decreased the ratio of methylthioalkyl GSLs to the sum of methylthioalkyl and methylsulfinylalkyl GSLs suggesting that the introduction of the two genes converted methylthioalkyl GSLs into methylsulfinylalkyl GSLs (Kong et al. 2016) |
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FMOGS-OX5 |
Flavin-containing monooxygenase FMO GS-OX5 |
Four uncharacterized FMOs designated FMOGS-OX2 to FMOGS-OX5 were found to involve in biosynthesis aliphatic GSL. Biochemical characterization of the recombinant protein combined with the analysis of GSL content in knockout mutants and overexpression lines show that FMOGS-OX2; FMOGS-OX3; and FMOGS-OX4 have broad substrate specificity and catalyze the conversion from methylthioalkyl GSL to the corresponding methylsulfinylalkyl GSL independent of chain length. In contrast; FMOGS-OX5 shows substrate specificity toward the long-chain 8-methylthiooctyl GSL. Identification of the FMOGS-OX subclade will generate better understanding of the evolution of biosynthetic activities and specificities in secondary metabolism and provides an important tool for breeding plants with improved cancer prevention characteristics as provided by the methylsulfinylalkyl GSL (Li et al. 2008) |
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FMOGS-OX7 |
Flavin-containing monooxygenase FMO GS-OX7 |
Two additional FMOGS-OX enzymes; FMOGS-OX6 and FMOGS-OX7 encoded by At1g12130 and At1g12160 respectively. The overexpression of both FMOGS-OX6 and FMOGS-OX7 decreased the ratio of methylthioalkyl GSLs to the sum of methylthioalkyl and methylsulfinylalkyl GSLs suggesting that the introduction of the two genes converted methylthioalkyl GSLs into methylsulfinylalkyl GSLs (Kong et al. 2016) |
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FMO |
Flavin-containing monooxygenase FMO GS-OX-like 2 |
FMO convert 4-methylthioalkyl to 4-meth-ylsulfinylalkyl GSLs and is pathogen-induced independent of COI1. Simultaneous induction of methionine, tryptophan,camalexin, and GSL biosynthetic genes provided evidence for coordinated regulation of primary and secondary metabolism (Stotz et al. 2011) |
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CYP71B7 |
Cytochrome P450 71B7 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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CYP79F2 |
Hexahomomethionine N-hydroxylase |
CYP79F1 and CYP79F2 are two important genes whose products catalyse accumulation of long-chain aliphatic GSLs; while the product of CYP79F1 also functions in the biosynthesis of short-chain aliphatic GSLs (Chen et al. 2003) |
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CYP79F1 |
Dihomomethionine N-hydroxylase |
CYP79F1 and CYP79F2 are two important genes whose products catalyse accumulation of long-chain aliphatic GSLs; while the product of CYP79F1 also functions in the biosynthesis of short-chain aliphatic GSLs (Chen et al. 2003) |
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MYB51 |
Transcription factor MYB51 |
MYB34; MYB51 and MYB122 act together to control the biosynthesis of indole-3-ylmethyl-GSL (I3M) in shoots and roots with MYB34 controlling biosynthesis of indolic GSLs (IGs) mainly in the roots. MYB51 regulating biosynthesis in shoots and MYB122 having an accessory role in the biosynthesis of IGs (Frerigmann & Gigolashvili 2014) |
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SOT17 |
Cytosolic sulfotransferase 17 |
The three enzymes were shown to catalyze the final step in the biosynthesis of the GSL core structure; the sulfation of desulfoGSLs (dsGSs). They accept a broad range of desulfoGSLs as substrates. In a competitive situation; AtST5a (SOT16) clearly prefers tryptophan and phenylalanine-derived desulfoGSLs whereas long chain desulfoGSLs derived from methionine are the preferred substrates of SOT17 and SOT18 (Piotrowski et al. 2004) |
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IGMT1 |
Indole glucosinolate O-methyltransferase 1 |
Arabidopsis O-methyl-transferase genes were found to coexpressed with CYP81F genes are fairly specific for the biosynthesis of modified indole GSLs which are IGMT1 and IGMT2. IGMT1 and 2 form a small gene cluster of O-MT genes on Arabidopsis chromosome 1 (Pfalz et al. 2011) |
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IGMT2 |
Indole glucosinolate O-methyltransferase 2 |
Arabidopsis O-methyl-transferase genes were found to coexpressed with CYP81F genes are fairly specific for the biosynthesis of modified indole GSLs which are IGMT1 and IGMT2. IGMT1 and 2 form a small gene cluster of O-MT genes on Arabidopsis chromosome 1 (Pfalz et al. 2011) |
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UGT74B1 |
UDP-glycosyltransferase 74B1 |
Analysis of UGT74B1 promoter activity during plant development reveals expression patterns consistent with GSL metabolism and induction by auxin treatment. The results are discussed in the context of known mutations in GSL pathway genes and their effects on auxin homeostasis. This research provides complementary in vitro and in vivo evidence for a primary role of UGT74B1 in GSL biosynthesis (Grubb et al. 2004) |
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MED25 |
Mediator Subunit 25 |
The expression of PFT1 that encode MED25 affect several GSL biosynthetic and regulatory genes such as MAM1 and MYB28 in the presence of glucose |
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MYC2 |
Transcription factor MYC2 |
The myc2 myc3 myc4 (myc234) triple mutant was almost completely devoid of GSL and was extremely susceptible to the generalist herbivore Spodoptera littoralis. On the contrary the specialist Pieris brassicae was unaffected by the presence of GSL and preferred to feed on wild-type plants. In addition lack of GSL in myc234 drastically modified S. littoralis feeding behavior. Surprisingly the expression of MYB factors known to regulate GS biosynthesis genes was not altered in myc234; suggesting that MYC2/MYC3/MYC4 are necessary for direct transcriptional activation of GS biosynthesis genes. Yeast two-hybrid and pull-down experiments indicated that MYC2/MYC3/MYC4 interact directly with GS-related MYBs. This specific MYC–MYB interaction plays a crucial role in the regulation of defense secondary metabolite production and underlines the importance of GSL in shaping plant interactions with adapted and nonadapted herbivores (Schweizer et al. 2013) |
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TGG4 |
Myrosinase 4 |
Different myrosinases in A. thaliana were compared: cDNAs corresponding to TGG1 from leaves and TGG4 and TGG5 from roots were cloned and overexpressed in Pichia pastoris. The His-tagged recombinant proteins were purified using affinity chromatography and the preparations were homogenous according to SDS–PAGE analysis. Myrosinase activity was confirmed for all forms and compared with respect to catalytic activity towards the allyl-GSL sinigrin (Andersson et al. 2009) |
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BCAT6 |
Branched-chain-amino-acid aminotransferase 6 |
The activity with Met and 4-methylthio-2-oxobutanoate (MTOB) suggests a potential function of BCAT6 in the Met chain elongation pathway (Lachler et al. 2015) |
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TGG5 |
Myrosinase 5 |
Different myrosinases in A. thaliana were compared: cDNAs corresponding to TGG1 from leaves and TGG4 and TGG5 from roots were cloned and overexpressed in Pichia pastoris. The His-tagged recombinant proteins were purified using affinity chromatography and the preparations were homogenous according to SDS–PAGE analysis. Myrosinase activity was confirmed for all forms and compared with respect to catalytic activity towards the allyl-GSL sinigrin (Andersson et al. 2009) |
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ESP |
Epithiospecifier protein |
Myrosinase is not sufficient for indol-3-acetonitrile production from indol-3-ylmethyl GSL and requires the presence of functional epithospecifier protein (ESP) in planta and in vitro to produce significant levels of indol-3-acetonitrile (Burow et al. 2008) |
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CYP79C2 |
Cytochrome P450, putative |
member of CYP79C subfamily of cytochrome p450s. Encodes a putative xylan endohydrolase. similar to some closely linked pseudogenes |
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ARF1 |
auxin response factor 1 |
ARF1 and ARF9 negatively regulate glucosinolate accumulation, and that ARF9 positively regulates camalexin accumulation. The action of miR393 on auxin signalling triggers two complementary responses. First, it prevents suppression of SA levels by auxin. Second, it stabilizes ARF1 and ARF9 in inactive complexes (Robert-Seilaniantz et al. 2011) |
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PEN3 |
ABC transporter G family member 36 |
Two genes; PEN2 and PEN3 are also necessary for resistance to pathogens and are required for both callose deposition and GSL activation suggesting that the pathogen-triggered callose response is required for resistance to microbial pathogens. The study shows that well- studied plant metabolites previously identified as important in avoiding damage by herbivores are also required as a component of the plant defense response against microbial pathogens (Clay et al. 2009) |
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APR2 |
5'-adenylylsulfate reductase 2 chloroplastic |
Using trans-activation assays two isoforms of APK; APK1 and APK2 are regulated by both classes of GSL MYB transcription factors; whereas two ATPS genes; ATPS1 and ATPS3 are differentially regulated by these two groups of MYB factors. The adenosine 5-phosphosulfate reductases APR1; APR2; and APR3 which participate in primary sulfate reduction are also activated by the MYB factors (Yatusevich et al. 2010) |
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FMOGS-OX2 |
Flavin-containing monooxygenase FMO GS-OX2 |
Four uncharacterized FMOs designated FMOGS-OX2 to FMOGS-OX5 were found to involve in biosynthesis aliphatic GSL. Biochemical characterization of the recombinant protein combined with the analysis of GSL content in knockout mutants and overexpression lines show that FMOGS-OX2; FMOGS-OX3; and FMOGS-OX4 have broad substrate specificity and catalyze the conversion from methylthioalkyl GSL to the corresponding methylsulfinylalkyl GSL independent of chain length. In contrast; FMOGS-OX5 shows substrate specificity toward the long-chain 8-methylthiooctyl GSL. Identification of the FMOGS-OX subclade will generate better understanding of the evolution of biosynthetic activities and specificities in secondary metabolism and provides an important tool for breeding plants with improved cancer prevention characteristics as provided by the methylsulfinylalkyl GSL (Li et al. 2008) |
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FMOGS-OX3 |
Flavin-containing monooxygenase FMO GS-OX3 |
Four uncharacterized FMOs. designated FMOGS-OX2 to FMOGS-OX5 were found to involve in biosynthesis aliphatic GSL. Biochemical characterization of the recombinant protein combined with the analysis of GSL content in knockout mutants and overexpression lines show that FMOGS-OX2. FMOGS-OX3. and FMOGS-OX4 have broad substrate specificity and catalyze the conversion from methylthioalkyl GSL to the corresponding methylsulfinylalkyl GSL independent of chain length. In contrast. FMOGS-OX5 shows substrate specificity toward the long-chain 8-methylthiooctyl GSL. Identification of the FMOGS-OX subclade will generate better understanding of the evolution of biosynthetic activities and specificities in secondary metabolism and provides an important tool for breeding plants with improved cancer prevention characteristics as provided by the methylsulfinylalkyl GSL (Li et al. 2008) |
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FMOGS-OX4 |
Flavin-containing monooxygenase FMO GS-OX4 |
Four uncharacterized FMOs. designated FMOGS-OX2 to FMOGS-OX5 were found to involve in biosynthesis aliphatic GSL. Biochemical characterization of the recombinant protein combined with the analysis of GSL content in knockout mutants and overexpression lines show that FMOGS-OX2. FMOGS-OX3. and FMOGS-OX4 have broad substrate specificity and catalyze the conversion from methylthioalkyl GSL to the corresponding methylsulfinylalkyl GSL independent of chain length. In contrast. FMOGS-OX5 shows substrate specificity toward the long-chain 8-methylthiooctyl GSL. Identification of the FMOGS-OX subclade will generate better understanding of the evolution of biosynthetic activities and specificities in secondary metabolism and provides an important tool for breeding plants with improved cancer prevention characteristics as provided by the methylsulfinylalkyl GSL (Li et al. 2008) |
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RLM1A |
Disease resistance protein RML1A |
Analyses of mutants defective in hormone signaling in the camalexin-free rlm1(Ler)pad3 background revealed a significant influence of JA and ET on symptom development and pathogen colonization. The overall results indicate that the defense responses of primary importance induced by RLM1 are all associated with physical barriers, and that responses of secondary importance involve complex cross-talk among SA, JA and ET (Persson et al. 2009) |
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NPR1 |
Regulatory protein NPR1 |
Decreasing camalexin levels by mutation of the camalexin synthetase gene PAD3 or the camalexin synthesis regulator AtWRKY33 compromised the powdery mildew resistance in these mutants (Liu et al. 2016) |
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FMOGS-OX1 |
Flavin-containing monooxygenase FMO GS-OX1 |
Flavin-monooxygenase (FMO) enzyme; FMOGS-OX1 catalyzes the conversion of methylthioalkyl GSLs into methylsulfinylalkyl GSLs. This is evidenced by biochemical characterization of the recombinant protein and analyses of the GSL content in FMOGS-OX1 overexpression lines and an FMOGS-OX1 knock-out mutant of Arabidopsis. The FMOGS-OX1 overexpression lines show almost complete conversion of methylthioalkyl into methylsulfinylalkyl GSLs with an approximately fivefold increase in 4-methylsulfinylbutyl GSL in seeds. Identification of FMOGS-OX1 provides a molecular tool for breeding of Brassica vegetable crops with increased levels of this important GSL which has implications for production of functional foods enriched with the cancer-preventive sulforaphane (Hansen et al. 2007) |
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BZO1 |
Benzoate--CoA ligase peroxisomal |
Genetic mapping and analysis of T-DNA insertions in candidate genes identified BZO1 (At1g65880) which encodes an enzyme with benzoyl-CoA ligase activity as being required for the accumulation of benzoyloxyGSLs. Long-chain aliphatic GSLs are elevated in bzo1 mutants suggesting substrate competition for the common short-chain aliphatic GSL precursors. Whereas bzo1 mutations have seed-specific effects on benzoyloxyGSL accumulation the relative abundance of 3-benzoyloxypropyl- and 4-benzoyloxy-butylGSLs depends on the maternal genotype (Kliebenstein et al. 2007) |
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MKK9 |
Mitogen-activated protein kinase kinase 9 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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SLIM1 |
ETHYLENE INSENSITIVE 3-like 3 protein |
SLIM1 functioned as a central transcriptional regulator which controlled both the activation of sulfate acquisition and degradation of GSLs under –S conditions. Metabolite analysis indicated stable accumulation of GSLs in slim1 mutants; even under –S conditions; particularly in the molecular species with methylsulfinylalkyl side chains beneficial to human health (Maruyama-Nakashita et al. 2006) |
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MYB122 |
Transcription factor MYB122 |
MYB34; MYB51 and MYB122 act together to control the biosynthesis of indole-3-ylmethyl-GSL (I3M) in shoots and roots with MYB34 controlling biosynthesis of indolic GSLs (IGs) mainly in the roots. MYB51 regulating biosynthesis in shoots and MYB122 having an accessory role in the biosynthesis of IGs (Frerigmann & Gigolashvili 2014) |
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SOT18 |
Cytosolic sulfotransferase 18 |
The three enzymes were shown to catalyze the final step in the biosynthesis of the GSL core structure; the sulfation of desulfoGSLs (dsGSs). They accept a broad range of desulfoGSLs as substrates. In a competitive situation; AtST5a (SOT16) clearly prefers tryptophan and phenylalanine-derived desulfoGSLs whereas long chain desulfoGSLs derived from methionine are the preferred substrates of SOT17 and SOT18 (Piotrowski et al. 2004) |
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SOT16 |
Cytosolic sulfotransferase 16 |
The three enzymes were shown to catalyze the final step in the biosynthesis of the GSL core structure; the sulfation of desulfoGSLs (dsGSs). They accept a broad range of desulfoGSLs as substrates. In a competitive situation; AtST5a (SOT16) clearly prefers tryptophan and phenylalanine-derived desulfoGSLs whereas long chain desulfoGSLs derived from methionine are the preferred substrates of SOT17 and SOT18 (Piotrowski et al. 2004) |
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ICS1 |
Isochorismate synthase 1, chloroplastic |
Decreasing camalexin levels by mutation of the camalexin synthetase gene PAD3 or the camalexin synthesis regulator AtWRKY33 compromised the powdery mildew resistance in these mutants (Liu et al. 2016) |
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IGMT5 |
Indole glucosinolate O-methyltransferase 5 |
Biosynthesis of 1-methoxyindol-3-ylmethyl GSL (1MOI3M) from I3M involves the predicted instable intermediate 1-hydroxyindol-3-ylmethyl GSL (1OHI3M) and that IGMT5; a gene with moderate similarity to previously characterized IGMTs encodes the methyltransferase that is responsible for the conversion of 1OHI3M to 1MOI3M. Disruption of IGMT5 function increases resistance against the root-knot nematode Meloidogyne javanica and suggests a potential role for the 1-IG-modification pathway in Arabidopsis below-ground defense (Pfalz et al. 2016) |
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SULTR1;2 |
Sulfate transporter 1.2 |
SLIM1 is required for the –S-responsive induction of the high-affinity sulfate transport system facilitated by SULTR1;2 sulfate transporter in Arabidopsis roots (Maruyama-Nakashita et al. 2006) |
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GSTU20 |
Glutathione S-transferase U20 |
GST-type enzymes may be involved in an enzyme complex formed by CYP83s and C-S lyase. The S-alkylthiohydroximate formed after CYP83-catalyzed aldoxime oxidation and spontaneous conjugation to cysteine is cyclized in vitro to form a dead-end product. Hence metabolic channeling aided by GST-type enzymes is postulated in vivo to avoid this consequence the dead-end product. The two putative GST genes (At3g03190 and At1g78370) could be candidates coding for such an activity (Hirai et al. 2005) |
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CYP79C1 |
Cytochrome P450, family 79, subfamily C, polypeptide 1 |
member of CYP79C |
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UPS1 |
Ureide permease 1 |
Pre-treatment of A. thaliana with UV-C leads to increased camalexin accumulation and substantial resistance to B. cinerea. UV-C-induced resistance was not seen in the camalexin-deficient mutants cyp79B2/B3, cyp71A13, pad3 or pad2, and was strongly reduced in ups1. ABC transporter demonstrates as a virulence factor that increases tolerance of the pathogen towards a phytoalexin, and the complete restoration of virulence on host plants lacking this phytoalexin (Stefanato et al 2009). |
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APK1 |
Adenylyl-sulfate kinase 1 chloroplastic |
The levels of GSLs and the sulfated 12-hydroxyjasmonate were reduced approximately fivefold in apk1 apk2 plants. The reduction in GSLs resulted in increased transcript levels for genes involved in GSL biosynthesis and accumulation of desulfated precursors (Mugford et al. 2009) |
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SUR1 |
S-alkyl-thiohydroximate lyase SUR1 |
SUPERROOT1 (SUR1) was characterized as the C-S lyase in GSL biosynthesis. This is supported by selective metabolite profiling of sur1 which is completely devoid of aliphatic and indolic GSLs (Mikkelsen et al. 2004) |
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CAMTA3 |
Calmodulin-binding transcription activator 3 |
AtSR1/CAMTA3 is an important component of plant resistance to insect herbivory as well as one of the proteins involved in Ca2+/CaM-dependent signaling to function in the regulation of GSL metabolism (Laluk et al. 2012) |
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CYP79B3 |
Tryptophan N-monooxygenase 2 |
Two Arabidopsis cytochrome P450s (CYP79B2 and CYP79B3) are able to convert Trp to indole-3-acetaldoxime (IAOx); a precursor to indole-3-acetic acid (IAA) and indole GSLs (Hull et al. 2000) |
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GSL-OH |
Probable 2-oxoacid dependent dioxygenase |
Arabidopsis thaliana contain three different patterns of 2-hydroxybut-3-enyl GSL accumulation (present in leaves and seeds; seeds only; or absent) corresponding to three different alleles at a single locus GSL-OH. Fine-scale mapping of the GSL-OH locus identified a 2-oxoacid-dependent dioxygenase encoded by At2g25450 required for the formation of both 2R- and 2S-2-hydroxybut-3-enyl GSL from the precursor 3-butenyl GSL precursor. Naturally occurring null mutations and T-DNA insertional mutations in At2g25450 exhibit a complete absence of 2-hydroxybut-3-enyl GSL accumulation. Analysis of herbivory by the generalist lepidopteran Trichoplusia ni showed that production of 2-hydroxybut-3-enyl GSL provides increased resistance. These results show that At2g25450 is necessary for the hydroxylation of but-3-enyl GSL to 2-hydroxybut-3-enyl GSL in planta and that this metabolite increases resistance to generalist herbivory (Hansen et al. 2008) |
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CYP707A2 |
Abscisic acid 8'-hydroxylase 2 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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CYP71A12 |
Cytochrome P450 71A12 |
Camalexin biosynthesis was induced in infected roots of both Col-0 (susceptible) and Bur-0 (partially resistant) accessions during the secondary phase of infection. However, the level of accumulation was four-to-seven times higher in Bur-0 than Col-0. This was associated with the enhanced transcription of a set of camalexin biosynthetic P450 genes in Bur-0: CYP71A13, CYP71A12, and CYP79B2 (Lemarié et al 2015) |
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CYP71A13 |
Indoleacetaldoxime dehydratase |
Camalexin biosynthesis was induced in infected roots of both Col-0 (susceptible) and Bur-0 (partially resistant) accessions during the secondary phase of infection. However, the level of accumulation was four-to-seven times higher in Bur-0 than Col-0. This was associated with the enhanced transcription of a set of camalexin biosynthetic P450 genes in Bur-0: CYP71A13, CYP71A12, and CYP79B2 (Lemarié et al 2015) |
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GSTF9 |
Glutathione S-transferase F9 |
An analysis of candidate genes for QTL-controlling GSL networks of transcripts and metabolites suggested that the controlling factors are a mix of enzymes and regulatory factors that include GSTF9 and GSTF10 (Wentzell et al. 2007) |
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GSTF10 |
Glutathione S-transferase F10 |
An analysis of candidate genes for QTL-controlling GSL networks of transcripts and metabolites suggested that the controlling factors are a mix of enzymes and regulatory factors that include GSTF9 and GSTF10 (Wentzell et al. 2007) |
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UGT74C1 |
UDP-glycosyltransferase 74C1 |
UGT74C1 complement phenotypes and chemotypes of the ugt74b1-2 knockout mutant and was able to express thiohydroximate UGT activity in planta provides conclusive evidence for UGT74C1 being an accessory enzyme in GSL biosynthesis with a potential function during plant adaptation to environmental challenge (Grubb et al. 2014) |
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NSP2 |
Nitrile-specifier protein 2 |
Nitrile formation by NSP2 is evident from GSL hydrolysis product profiles in homogenates of Arabidopsis expressing NSP2 under control of the CaMV35S-promoter (Kissen & Bones 2009) |
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ABCG34 |
ABC transporter G family member 34 |
Mediates the secretion of camalexin from the epidermal cells to the surface of leaves and thereby confers resistance to A. brassicicola infection (Khare et al. 2017) |
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WRKY33 |
Probable WRKY transcription factor 33 |
Decreasing camalexin levels by mutation of the camalexin synthetase gene PAD3 or the camalexin synthesis regulator AtWRKY33 compromised the powdery mildew resistance in these mutants (Liu et al. 2016) |
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COI1 |
Coronatine-insensitive protein 1 |
FMO convert 4-methylthioalkyl to 4-meth-ylsulfinylalkyl GSLs and is pathogen-induced independent of COI1. Simultaneous induction of methionine, tryptophan,camalexin, and GSL biosynthetic genes provided evidence for coordinated regulation of primary and secondary metabolism (Stotz et al. 2011) |
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JUB1 |
Transcription factor JUNGBRUNNEN 1 |
ANAC042, a member of the NAM, ATAF1/2, and CUC2 (NAC) transcription factor family genes, is involved in camalexin biosynthesis induction. ANAC042 as a key transcription factor involved in previously unknown regulatory mechanisms to induce phytoalexin biosynthesis in Arabidopsis (Saga et al. 2012) |
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IPMI2 |
3-isopropylmalate dehydratase small subunit 1 |
Two isopropylmalate isomerases genes; IPMI1 and IPMI2 and the isopropylmalate dehydrogenase gene; IPMDH1 were identified as targets of HAG1/MYB28 and the corresponding proteins localized to plastids suggesting a role in plastidic chain elongation reactions (Gigolashvili et al. 2009) |
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MPK6 |
Mitogen-activated protein kinase 6 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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BGLU28 |
BETA GLUCOSIDASE 28 |
Atypical myrosinases, β-glucosidase 28 (BGLU28), and β-glucosidase 30 (BGLU30) are responsible for GSL catabolism in sulfur deficiency environment by activating primary sulfur metabolism |
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PEN2 |
Beta-glucosidase 26 peroxisomal |
The Arabidopsis CYP81F2 gene encodes a P450 monooxygenase that is essential for the pathogen-induced accumulation of 4-methoxyindol-3-ylmethylGSL which in turn is activated by the atypical PEN2 myrosinase (a type of b-thioglucoside glucohydrolase) for antifungal defense (Bednarek et al. 2009) |
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CYP86A8 |
Cytochrome P450 86A8 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
MPK12 |
Mitogen-activated protein kinase 12 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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|
JAR1 |
Jasmonic acid-amido synthetase JAR1 |
The rate of development of B. cinerea disease symptoms on primary infected leaves was affected by responses mediated by the genes EIN2, JAR1, EDS4, PAD2, and PAD3, but was largely independent of EDS5, SID2/ICS1, and PAD4. a double ein2 npr1 mutant was significantly more susceptible than ein2 plants, and exogenous application of SA decreased B. cinerea lesion size through an NPR1-dependent mechanism that could be mimicked by the cpr1 mutation. These data indicate that local resistance to B. cinerea requires ethylene-, jasmonate-, and SA-mediated signaling, that the SA affecting this resistance does not require ICS1 and is likely synthesized via PAL, and that camalexin limits lesion development (Ferrari et al. 2003) |
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|
CYTB5-C |
Cytochrome B5 isoform C |
The roles of the many CB5 isoforms in plants remain unknown. CB5 proteins was predicted to support the cytochrome P450 enzymes of plant specialized metabolism and found CB5C from Arabidopsis thaliana to co-express with GSL biosynthetic genes. GSL profiles of 2 T-DNA insertion mutants of CB5C were characterized and found that long-chained aliphatic glucosinolates were reduced in one of the mutant lines – a phenotype that was exaggerated upon methyl-jasmonate treatment. These results support the hypothesis that CB5C influences glucosinolate biosynthesis however; the mode of action remains unknown (Vik et al. 2016) |
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|
CCA1 |
CIRCADIAN CLOCK-ASSOCIATED1 |
The aphid feeding in CCA1 overexpression plants (CCA1-OX) showed significant comparisons with those on Col-0 in terms of lower reproduction and reduced body size and weight. Furthermore, basal indolic GSLs were higher in CCA1-OX compared to Col-0, suggesting the importance of CCA1 in the plant defense against aphids |
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|
GSTF11 |
Glutathione S-transferase F11 |
GST-type enzymes may be involved in an enzyme complex formed by CYP83s and C-S lyase. The S-alkylthiohydroximate formed after CYP83-catalyzed aldoxime oxidation and spontaneous conjugation to cysteine is cyclized in vitro to form a dead-end product. Hence metabolic channeling aided by GST-type enzymes is postulated in vivo to avoid this consequence the dead-end product. The two putative GST genes (At3g03190 and At1g78370) could be candidates coding for such an activity (Hirai et al. 2005) |
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|
FRS7 |
Far1 Related Sequence 7 |
Far1 Related Sequence 7 (FRS7) and Far1 Related Sequence 12 (FRS12) are two repressor proteins that regulate GSL biosynthesis in short-day conditions. A combinatorial analysis with transcriptome data revealed FRS7 and FRS12 can trancriptionally affect known GSL genes such as the IPM1, IPMI2, BAT5, and GSTF11 and MAM1, respectively |
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|
BGLU23 |
BETA GLUCOSIDASE 23 |
PYK10 hydrolyzes indole glucosinolates (GSLs) in A. thaliana, co-expressed with GSL biosynthetic genes and tightly linked to the physiological functions of ER bodies |
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|
IQD1 |
Protein IQ-DOMAIN 1 |
Analysis of steady-state messenger RNA levels of GSL pathway genes indicates that IQD1 affects expression of multiple genes with roles in GSL metabolism. Histochemical analysis of tissue-specific IQD1::GUS expression reveals IQD1 promoter activity mainly in vascular tissues of all organs. consistent with the expression patterns of several GSL-related genes. Interestingly overexpression of IQD1 reduces insect herbivory which is demonstrated in dual-choice assays with the generalist phloem-feeding green peach aphid (Myzus persicae) and in weight-gain assays with the cabbage looper (Trichoplusia ni); a generalist-chewing lepidopteran (Levy et al. 2005) |
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|
SCPL17 |
Serine carboxypeptidase-like 17 |
SCPL17 is the acyltransferase involved in transferring the benzoyl moiety from benzoylglucose (BG) to hydroxylated GSLs (OH-GSLs) (Lee et al. 2012) |
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|
ESM1 |
GDSL esterase/lipase ESM1 |
Following tissue disruption; indol-3-acetonitrile (IACN) can be generated from indole GSLs through the action of ESP and myrosinase; and that its production is regulated by ESM1 (Burow et al. 2008) |
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|
NSP3 |
Nitrile-specifier protein 3 |
Besides NSP2; 3-butenylnitrile was also detected upon incubation with NSP1 and NSP3 showing that these proteins also possess nitrile-specifier activity (Kissen & Bones 2009) |
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|
NSP1 |
Nitrile-specifier protein 1 |
Product formation by ESP and NSP1 from different GSLs as substrates for myrosinase has been analyzed using purified proteins expressed in E. coli (Burow et al. 2008) |
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|
NSP4 |
Nitrile-specifier protein 4 |
The seed content of the precursor GSL; 4-methylthiobutylGSL was consistently reduced in nsp3-2; nsp4-1 and nsp5-1 relative to WT (Wittstock et al. 2016) |
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|
BCAT4 |
Methionine aminotransferase BCAT4 |
Recombinant BCAT4 showed high efficiency with Met and its derivatives and the corresponding 2-oxo acids suggesting its participation in the chain elongation pathway of Met-derived GSL biosynthesis. This was substantiated by in vivo analysis of two BCAT4 T-DNA knockout mutants in which Met-derived aliphatic GSL accumulation is reduced by nearly 50% (Schuster et al. 2006) |
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|
CYP705A33 |
At3g20960 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
APS1 |
ATP sulfurylase 1 chloroplastic |
Using trans-activation assays two isoforms of APK; APK1 and APK2 are regulated by both classes of GSL MYB transcription factors; whereas two ATPS genes; ATPS1 and ATPS3 are differentially regulated by these two groups of MYB factors. The adenosine 5-phosphosulfate reductases APR1; APR2; and APR3 which participate in primary sulfate reduction are also activated by the MYB factors (Yatusevich et al. 2010) |
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|
MED5 |
Mediator Subunit 5 |
Mediator Subunit 5 (MED5) involves in the crosstalk between phenylpropanoid and GSL biosynthesis. Expressly, the accumulation of GSL derivatives (aldoximes) would limit phenylpropanoid biosynthesis that requires MED5 |
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|
CYP82G1 |
Cytochrome P450 82G1 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
CYP71B15 |
Bifunctional dihydrocamalexate synthase/camalexin synthase |
Multifunctional enzyme involved in the biosynthesis of the indole-derived phytoalexin camalexin. Catalyzes two reactions, the formation of dihydrocamalexate from indole-3-acetonitrile-cysteine conjugate and the oxidative decarboxylation of dihydrocamalexate which is the final step in camalexin biosynthesis (Ferrari et al. 2003) |
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|
MYB118 |
Myb domain protein 118 |
Two conserved TFs; MYB115 and MYB118 were co-expressed with the key enzyme encoding genes in the newly evolved benzoyloxy GSL (GLS) pathway. These TFs interacted with the promoters of the GLS biosynthetic genes and negatively influenced their expression. Similarly the GLS profiles of these two TFs knockouts showed that they influenced the aliphatic GLS accumulation within seed; leaf and flower while they mainly expressed in seeds (Zhang et al. 2015) |
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|
NIT2 |
Nitrilase 2 |
Enzymes of the NIT1 group have a broad substrate specificity and accept nitriles with structural similarity to GSL-derived nitriles and the predominant isoform NIT1 (At3g44310) is most active on nitriles derived from GSLs (Piotrowski et al. 2008) |
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|
NIT1 |
Nitrilase 1 |
Enzymes of the NIT1 group have a broad substrate specificity and accept nitriles with structural similarity to GSL-derived nitriles and the predominant isoform NIT1 (At3g44310) is most active on nitriles derived from GSLs (Piotrowski et al. 2008) |
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|
NIT3 |
Nitrilase 3 |
Enzymes of the NIT1 group have a broad substrate specificity and accept nitriles with structural similarity to GSL-derived nitriles and the predominant isoform NIT1 (At3g44310) is most active on nitriles derived from GSLs (Piotrowski et al. 2008) |
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|
MPK3 |
Mitogen-activated protein kinase 3 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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|
GTR1 |
Protein NRT1/ PTR FAMILY 2.10 |
Leaf apoplastic fluid analysis and GSL feeding experiments showed two GSL transporters. GTR1 and GTR2 were essential for long-distance transport of GSLs in Arabidopsis and also play key roles in GSL allocation within a mature leaf by effectively importing apoplastically localized GSLs into appropriate cells (Madsen et al. 2014) |
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|
EDS1 |
Protein EDS |
Decreasing camalexin levels by mutation of the camalexin synthetase gene PAD3 or the camalexin synthesis regulator AtWRKY33 compromised the powdery mildew resistance in these mutants (Liu et al. 2016) |
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|
BCAT3 |
Branched-chain-amino-acid aminotransferase 3 chloroplastic |
Metabolite profiling of bcat3-1 single and bcat3-1/bcat4-2 double knockout mutants showed significant alterations in the profiles of both amino acids and GSLs. The changes in GSL proportions suggest that BCAT3 most likely catalyzes the terminal steps in the chain elongation process leading to short-chain GSLs (Knill et al. 2008) |
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|
PAD4 |
Lipase-like PAD4 |
Decreasing camalexin levels by mutation of the camalexin synthetase gene PAD3 or the camalexin synthesis regulator AtWRKY33 compromised the powdery mildew resistance in these mutants (Liu et al. 2016) |
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|
IPMI1 |
3-isopropylmalate dehydratase small subunit 2 |
Two isopropylmalate isomerases genes; IPMI1 and IPMI2 and the isopropylmalate dehydrogenase gene; IPMDH1 were identified as targets of HAG1/MYB28 and the corresponding proteins localized to plastids suggesting a role in plastidic chain elongation reactions (Gigolashvili et al. 2009) |
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|
BGLU30 |
BETA GLUCOSIDASE 30 |
Atypical myrosinases, β-glucosidase 28 (BGLU28), and β-glucosidase 30 (BGLU30) are responsible for GSL catabolism in sulfur deficiency environment by activating primary sulfur metabolism |
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|
RPS27AC |
Ubiquitin-40S ribosomal protein S27a-3 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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|
AOP3 |
2-oxoglutarate-dependent dioxygenase AOP3 |
AOP3 directs the formation of hydroxyalkyl GSLs from methylsulfinylalkyl GSLs. Absence of functional AOP2 and AOP3 leads to the accumulation of the precursor methylsulfinylalkyl GSLs (Kliebenstein et al. 2001) |
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|
AOP2 |
Alkenyl hydroxalkyl producing 2 |
By heterologous expression in Escherichia and the correlation of gene expression patterns to the GSL phenotype. AOP2 catalyzes the conversion of methylsulfinylalkyl GSLs to alkenyl GSLs in Arabidopsis. Absence of functional AOP2 and AOP3 leads to the accumulation of the precursor methylsulfinylalkyl GSLs (Kliebenstein et al. 2001) |
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|
GRH1 |
GRR1-like protein 1 |
ARF1 and ARF9 negatively regulate glucosinolate accumulation, and that ARF9 positively regulates camalexin accumulation. The action of miR393 on auxin signalling triggers two complementary responses. First, it prevents suppression of SA levels by auxin. Second, it stabilizes ARF1 and ARF9 in inactive complexes (Robert-Seilaniantz et al. 2011) |
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|
APR1 |
5'-adenylylsulfate reductase 1 chloroplastic |
Using trans-activation assays two isoforms of APK; APK1 and APK2 are regulated by both classes of GSL MYB transcription factors; whereas two ATPS genes; ATPS1 and ATPS3 are differentially regulated by these two groups of MYB factors. The adenosine 5-phosphosulfate reductases APR1; APR2; and APR3 which participate in primary sulfate reduction are also activated by the MYB factors (Yatusevich et al. 2010) |
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|
SULTR1;1 |
Sulfate transporter 1.1 |
Gene expression studies with promoter-reporter constructs indicated that both SULTR1;1 and SULTR1;2 are regulated under their –S-responsive promoters in response to sulfur nutrition (Maruyama-Nakashita et al. 2006) |
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|
BAT5 |
Probable sodium/metabolite cotransporter BASS5 chloroplastic |
Mechanical stimuli and methyl jasmonate transiently induced BAT5 expression in inflorescences and leaves. BAT5 was identified as the first transporter component of the aliphatic GSL biosynthetic pathway (Gigolashvili et al. 2009) |
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|
CYP706A6 |
At4g12320 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
IIL1 |
3-isopropylmalate dehydratase large subunit |
Knocking out either of the candidate genes; AtleuC1 (IIL1) or AtIMD1 (IMD1) would reduced the level of Met-GSLs indicating that both genes are actually involved in Met-GSL biosynthesis (Sawada & Kuwahara et al. 2009) |
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|
CYP83A1 |
Cytochrome P450 83A1 |
The GSL profiles of transgenic Arabidopsis overexpressing either CYP83A1 or CYP83B1 exhibited wild-type levels of indole GSLs (Naur et al. 2003) |
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|
APS3 |
ATP-sulfurylase 3 chloroplastic |
Using trans-activation assays two isoforms of APK; APK1 and APK2 are regulated by both classes of GSL MYB transcription factors; whereas two ATPS genes; ATPS1 and ATPS3 are differentially regulated by these two groups of MYB factors. The adenosine 5-phosphosulfate reductases APR1; APR2; and APR3 which participate in primary sulfate reduction are also activated by the MYB factors (Yatusevich et al. 2010) |
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|
OASA1 |
Cysteine synthase 1 |
In plants OAS has a similar direct regulatory role as its counterpart N-acetylserine in E. coli is questionable; as no clear cut correlation was found between the Arabidopsis root OAS cellular content and the mRNA levels of either SULTR1;1 and SULTR1;2 (Rouached et al. 2008) |
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|
BARS1 |
Baruol synthase |
The effect of low R : FR increasing Arabidopsis susceptibility to B. cinerea was not present in mutants deficient in the biosynthesis of camalexin (pad3) or metabolism of iGS (pen2). In a mutant deficient in the JASMONATE ZIM DOMAIN-10 (JAZ10) protein, which does not respond to low R : FR with increased susceptibility to B. cinerea, supplemental FR failed to down-regulate iGS production. These results indicate that suppression of Arabidopsis immunity against B. cinerea by low R : FR ratios is mediated by reduced levels of Trp-derived defenses, and provide further evidence for a functional role of JAZ10 in the link between phytochrome and jasmonate signaling (Cargnel et al. 2014) |
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|
CYP705A4 |
Cytochrome P450, family 705, subfamily A, polypeptide 4 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
ERF6 |
Ethylene-responsive transcription factor 6 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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|
MYC4 |
Transcription factor MYC4 |
The myc2 myc3 myc4 (myc234) triple mutant was almost completely devoid of GSL and was extremely susceptible to the generalist herbivore Spodoptera littoralis. On the contrary the specialist Pieris brassicae was unaffected by the presence of GSL and preferred to feed on wild-type plants. In addition lack of GSL in myc234 drastically modified S. littoralis feeding behavior. Surprisingly the expression of MYB factors known to regulate GS biosynthesis genes was not altered in myc234; suggesting that MYC2/MYC3/MYC4 are necessary for direct transcriptional activation of GS biosynthesis genes. Yeast two-hybrid and pull-down experiments indicated that MYC2/MYC3/MYC4 interact directly with GS-related MYBs. This specific MYC–MYB interaction plays a crucial role in the regulation of defense secondary metabolite production and underlines the importance of GSL in shaping plant interactions with adapted and nonadapted herbivores (Schweizer et al. 2013) |
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|
APR3 |
5'-adenylylsulfate reductase 3 chloroplastic |
Using trans-activation assays two isoforms of APK; APK1 and APK2 are regulated by both classes of GSL MYB transcription factors; whereas two ATPS genes; ATPS1 and ATPS3 are differentially regulated by these two groups of MYB factors. The adenosine 5-phosphosulfate reductases APR1; APR2; and APR3 which participate in primary sulfate reduction are also activated by the MYB factors (Yatusevich et al. 2010) |
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|
CYP706A1 |
Cytochrome P450, family 706, subfamily A, polypeptide 1 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
GSH1 |
Glutamate--cysteine ligase chloroplastic |
Both gamma–glutamyl cysteine ligase (GSH1) and glutathione synthetase (GSH2); which catalyse its synthesis were significantly enriched in bundle sheath (BS) cells that can be related with sulfur and GSL metabolism (Aubry et al. 2014) |
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|
ARF9 |
Auxin response factor 9 |
ARF1 and ARF9 negatively regulate glucosinolate accumulation, and that ARF9 positively regulates camalexin accumulation. The action of miR393 on auxin signalling triggers two complementary responses. First, it prevents suppression of SA levels by auxin. Second, it stabilizes ARF1 and ARF9 in inactive complexes (Robert-Seilaniantz et al. 2011) |
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|
WES1 |
Indole-3-acetic acid-amido synthetase |
Arabidopsis GH3.5 protein, a multifunctional acetyl-amido synthetase, is involved in camalexin biosynthesis via conjugating indole-3-carboxylic acid (ICA) and cysteine (Cys) and regulating camalexin biosynthesis genes. Camalexin levels were increased in the activation-tagged mutant gh3.5-1D in both Col-0 and cyp71A13-2 mutant backgrounds after pathogen infection. The recombinant GH3.5 protein catalyzed the conjugation of ICA and Cys to form a possible intermediate indole-3-acyl-cysteinate (ICA(Cys)) in vitro. In support of the in vitro reaction, feeding with ICA and Cys increased camalexin levels in Col-0 and gh3.5-1D. Dihydrocamalexic acid (DHCA), the precursor of camalexin and the substrate for PAD3, was accumulated in gh3.5-1D/pad3-1, suggesting that ICA(Cys) could be an additional precursor of DHCA for camalexin biosynthesis (Wang et al. 2012) |
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|
GGP1 |
Gamma-glutamyl peptidase 1 |
GGP1 is a gamma-glutamyl peptidase that cleaves off the gamma-glutamyl residue from the glutathione conjugate intermediate (S-[(Z)-phenylacetohydroximoyl]-L-glutathione; GS-B) in the benzylGSLs (BGLS) pathway (Geu-Flores et al. 2009) |
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|
GGP3 |
Gamma-glutamyl peptidase 3 |
Arabidopsis thaliana mutant impaired in the production of the γ-glutamyl peptidases GGP1 and GGP3 has altered glucosinolate levels and accumulates up to 10 related GSH conjugates. The double mutant is impaired in the production of camalexin and accumulates high amounts of the camalexin intermediate GS-IAN upon induction. In addition, the cellular and subcellular localization of GGP1 and GGP3 matches that of known glucosinolate and camalexin enzymes. GSH is the sulfur donor in the biosynthesis of glucosinolates and establish an in vivo function for the only known cytosolic plant γ-glutamyl peptidases, namely, the processing of GSH conjugates in the glucosinolate and camalexin pathways (Geu-Flores et al. 2011) |
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|
CYP83B1 |
Cytochrome P450 83B1 |
The GSL profiles of transgenic Arabidopsis overexpressing either CYP83A1 or CYP83B1 exhibited wild-type levels of indole GSLs (Naur et al. 2003) |
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|
CYP81F3 |
Cytochrome P450 81F3 |
All four Arabidopsis CYP81F gene products had the capacity to modify the indole GSL structure. CYP81F1; CYP81F2; and CYP81F3 but not CYP81F4 catalyzed the conversion of indol-3-yl-methyl GSL (I3M) to 4-hydroxy-indol-3-yl-methyl (4OH-I3M) and all four CYP81Fs converted I3M to 1-hydroxy-indol-3-yl-methyl GSL (1OH-I3M) (Pfalz et al. 2011) |
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|
CYP81F4 |
Cytochrome P450 81F4 |
All four Arabidopsis CYP81F gene products had the capacity to modify the indole GSL structure. CYP81F1; CYP81F2; and CYP81F3 but not CYP81F4 catalyzed the conversion of indol-3-yl-methyl GSL (I3M) to 4-hydroxy-indol-3-yl-methyl (4OH-I3M) and all four CYP81Fs converted I3M to 1-hydroxy-indol-3-yl-methyl GSL (1OH-I3M) (Pfalz et al. 2011) |
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|
CYP81F1 |
Cytochrome P450 81F1 |
All four Arabidopsis CYP81F gene products had the capacity to modify the indole GSL structure. CYP81F1; CYP81F2; and CYP81F3 but not CYP81F4 catalyzed the conversion of indol-3-yl-methyl GSL (I3M) to 4-hydroxy-indol-3-yl-methyl (4OH-I3M) and all four CYP81Fs converted I3M to 1-hydroxy-indol-3-yl-methyl GSL (1OH-I3M) (Pfalz et al. 2011) |
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|
DTX47 |
Protein DETOXIFICATION 47, chloroplastic |
Decreasing camalexin levels by mutation of the camalexin synthetase gene PAD3 or the camalexin synthesis regulator AtWRKY33 compromised the powdery mildew resistance in these mutants (Liu et al. 2016) |
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|
GGT2 |
Glutathione hydrolase 2 |
GSTF6 overexpression increased and GSTF6-knockout reduced camalexin production. Arabidopsis GSTF6 expressed in yeast cells catalyzed GSH(IAN) formation. GSH(IAN), (IAN)CysGly, and γGluCys(IAN) were determined to be intermediates within the camalexin biosynthetic pathway. The expression of GSTF6, GGT1, GGT2, and PCS1 was coordinately upregulated during camalexin biosynthesis. These results suggest that GSH is the Cys derivative used during camalexin biosynthesis, that the conjugation of GSH with IAN is catalyzed by GSTF6, and that GGTs and PCS are involved in camalexin biosynthesis (Su et al. 2011). |
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|
APK2 |
Adenylyl-sulfate kinase 2 chloroplastic |
The levels of GSLs and the sulfated 12-hydroxyjasmonate were reduced approximately fivefold in apk1 apk2 plants. The reduction in GSLs resulted in increased transcript levels for genes involved in GSL biosynthesis and accumulation of desulfated precursors (Mugford et al. 2009) |
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|
CYP79B2 |
Tryptophan N-monooxygenase 1 |
Two Arabidopsis cytochrome P450s (CYP79B2 and CYP79B3) are able to convert Trp to indole-3-acetaldoxime (IAOx); a precursor to indole-3-acetic acid (IAA) and indole GSLs (Hull et al. 2000) |
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|
EIN2 |
Ethylene-insensitive protein 2 |
The rate of development of B. cinerea disease symptoms on primary infected leaves was affected by responses mediated by the genes EIN2, JAR1, EDS4, PAD2, and PAD3, but was largely independent of EDS5, SID2/ICS1, and PAD4. a double ein2 npr1 mutant was significantly more susceptible than ein2 plants, and exogenous application of SA decreased B. cinerea lesion size through an NPR1-dependent mechanism that could be mimicked by the cpr1 mutation. These data indicate that local resistance to B. cinerea requires ethylene-, jasmonate-, and SA-mediated signaling, that the SA affecting this resistance does not require ICS1 and is likely synthesized via PAL, and that camalexin limits lesion development (Ferrari et al. 2003) |
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|
CYP77A4 |
Cytochrome P450 77A4 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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|
CYP79A2 |
Phenylalanine N-monooxygenase |
Arabidopsis expressing CYP79D2 from cassava accumulated aliphatic isopropyl and methylpropyl GSL and showed enhanced resistance against the bacterial soft-rot pathogen Erwinia carotovora whereas Arabidopsis expressing the sorghum CYP79A1 or over-expressing the endogenous CYP79A2 accumulated p-hydroxybenzyl or benzyl GSL respectively and showed increased resistance towards the bacterial pathogen Pseudomonas syringae (Brader et al. 2006) |
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|
ASA1 |
Anthranilate synthase alpha subunit 1 chloroplastic |
In RNA gel-blot analysis 35S-ATR1 displayed elevated accumulation of ATR1 and Trp gene transcripts including two Trp synthesis genes; ASA1 and TSB1 and three Trp secondary metabolism genes CYP79B2; CYP79B3; and CYP83B1. ASA1 encodes the catalytic alpha-subunit of anthranilate synthase the first committed enzyme of the Trp pathway and TSB1 encodes the Trp synthase beta-subunit activity that converts indole to Trp (Celenza et al. 2005) |
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|
MYB29 |
Transcription factor MYB29 |
A phylogenetic analysis with the R2R3 motif of MYB28 showed that it and two homologues. MYB29 and MYB76 were members of an clade that included three characterized regulators of indole GSLs. Over-expression of the individual MYB genes showed that they all had the capacity to increase the production of aliphatic GSLs in leaves and seeds and induce gene expression of aliphatic biosynthetic genes within leaves. Analysis of leaves and seeds knockout mutants showed that mutants of MYB29 and MYB76 have reductions in only short-chained aliphatic GSLs whereas a mutant in MYB28 has reductions in both short- and long-chained aliphatic GSLs (Sonderby et al. 2007) |
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|
MYB76 |
Transcription factor MYB76 |
A phylogenetic analysis with the R2R3 motif of MYB28 showed that it and two homologues; MYB29 and MYB76 were members of an clade that included three characterized regulators of indole GSLs. Over-expression of the individual MYB genes showed that they all had the capacity to increase the production of aliphatic GSLs in leaves and seeds and induce gene expression of aliphatic biosynthetic genes within leaves. Analysis of leaves and seeds knockout mutants showed that mutants of MYB29 and MYB76 have reductions in only short-chained aliphatic GSLs whereas a mutant in MYB28 has reductions in both short- and long-chained aliphatic GSLs (Sonderby et al. 2007) |
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HY5 |
LONG HYPOCOTYL5 |
LONG HYPOCOTYL5 (HY5) acts as a transcription regulator leading to increased GSL biosynthesis in light-induced condition via sulfate assimilation and light regulation mechanism |
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TIFY9 |
Protein TIFY 9 |
The effect of low R : FR increasing Arabidopsis susceptibility to B. cinerea was not present in mutants deficient in the biosynthesis of camalexin (pad3) or metabolism of iGS (pen2). In a mutant deficient in the JASMONATE ZIM DOMAIN-10 (JAZ10) protein, which does not respond to low R : FR with increased susceptibility to B. cinerea, supplemental FR failed to down-regulate iGS production. These results indicate that suppression of Arabidopsis immunity against B. cinerea by low R : FR ratios is mediated by reduced levels of Trp-derived defenses, and provide further evidence for a functional role of JAZ10 in the link between phytochrome and jasmonate signaling (Cargnel et al. 2014) |
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IMDH1 |
3-isopropylmalate dehydrogenase 3 chloroplastic |
Knocking out either of the candidate genes; AtleuC1 (IIL1) or AtIMD1 (IMD1) would reduced the level of Met-GSLs indicating that both genes are actually involved in Met-GSL biosynthesis (Sawada & Kuwahara et al. 2009) |
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FRS12 |
Far1 Related Sequence 12 |
Far1 Related Sequence 7 (FRS7) and Far1 Related Sequence 12 (FRS12) are two repressor proteins that regulate GSL biosynthesis in short-day conditions. A combinatorial analysis with transcriptome data revealed FRS7 and FRS12 can trancriptionally affect known GSL genes such as the IPM1, IPMI2, BAT5, and GSTF11 and MAM1, respectively |
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NIT4 |
Bifunctional nitrilase/nitrile hydratase NIT4 |
Comparison of the amino acid sequences of NIT4 and NIT1 homologs has permitted the identification of typical sequence motifs for NIT4 and NIT1. One of these motifs was mutated in Arabidopsis NIT4 and obtained enzymes that could convert 3-phen-ylpropionitrile three to nearly tenfold faster than the wild-type enzyme (Janowitz et al. 2009) |
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MAM1 |
Methylthioalkylmalate synthase 1 chloroplastic |
MAM1 catalyses the condensation step of the first three elongation cycles while MAM3 catalyzes the condensation step of all six elongation cycles in met derived GSL biosynthesis (Redovnikovic et al. 2012) |
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MAM3 |
Methylthioalkylmalate synthase 3 chloroplastic |
Analysis of MAM3 mutants demonstrated that MAM3 catalyzes the formation of all GSL chain lengths in vivo as well as in vitro making this enzyme the major generator of GSL chain length diversity in the plant. The localization of MAM3 in the chloroplast suggests that this organelle is the site of Met chain elongation (Textor et al. 2007) |
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CYP71A14 |
Cytochrome P450 71A14 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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TGG2 |
Myrosinase 2 |
Glucosinolate breakdown in crushed leaves of tgg1 or tgg2 single mutants was comparable to that of wild-type; indicating redundant enzyme function. In contrast; leaf extracts of tgg1 tgg2 double mutants had undetectable myrosinase activity in vitro and damage-induced breakdown of endogenous GSLs was apparently absent for aliphatic and greatly slowed for indole GSLs (Barth & Jander 2006) |
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TGG1 |
Myrosinase 1 |
Glucosinolate breakdown in crushed leaves of tgg1 or tgg2 single mutants was comparable to that of wild-type; indicating redundant enzyme function. In contrast; leaf extracts of tgg1 tgg2 double mutants had undetectable myrosinase activity in vitro and damage-induced breakdown of endogenous GSLs was apparently absent for aliphatic and greatly slowed for indole GSLs (Barth & Jander 2006) |
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GSH2 |
Glutathione synthetase chloroplastic |
Both gamma–glutamyl cysteine ligase (GSH1) and glutathione synthetase (GSH2); which catalyse its synthesis were significantly enriched in bundle sheath (BS) cells that can be related with sulfur and GSL metabolism (Aubry et al. 2014) |
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CYP735A1 |
Cytokinin hydroxylase |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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MYB115 |
Myb domain protein 115 |
Two conserved TFs; MYB115 and MYB118 were co-expressed with the key enzyme encoding genes in the newly evolved benzoyloxy GSL (GLS) pathway. These TFs interacted with the promoters of the GLS biosynthetic genes and negatively influenced their expression. Similarly the GLS profiles of these two TFs knockouts showed that they influenced the aliphatic GLS accumulation within seed; leaf and flower while they mainly expressed in seeds (Zhang et al. 2015) |
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PCS1 |
Glutathione gamma-glutamylcysteinyltransferase 1 |
Microarray data of Flg22-inducible expression profiles identified a phytochelatin synthase gene; PCS1 whose corresponding mutants (pcs1-1; pcs1-2 and cad1-3) were all impaired in the callose response to Flg22. The transcriptional and indolic GSL profiles of the pcs1 mutant resemble those of the pen2 mutant; suggesting that it too is involved in the breakdown of 4-methoxy-indol-3-ylmethylGSL (Clay et al. 2009) |
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MYC3 |
Transcription factor MYC3 |
The myc2 myc3 myc4 (myc234) triple mutant was almost completely devoid of GSL and was extremely susceptible to the generalist herbivore Spodoptera littoralis. On the contrary the specialist Pieris brassicae was unaffected by the presence of GSL and preferred to feed on wild-type plants. In addition lack of GSL in myc234 drastically modified S. littoralis feeding behavior. Surprisingly the expression of MYB factors known to regulate GS biosynthesis genes was not altered in myc234; suggesting that MYC2/MYC3/MYC4 are necessary for direct transcriptional activation of GS biosynthesis genes. Yeast two-hybrid and pull-down experiments indicated that MYC2/MYC3/MYC4 interact directly with GS-related MYBs. This specific MYC–MYB interaction plays a crucial role in the regulation of defense secondary metabolite production and underlines the importance of GSL in shaping plant interactions with adapted and nonadapted herbivores (Schweizer et al. 2013) |
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ERF5 |
Ethylene-responsive transcription factor 5 |
MKK9, an MKK, is an upstream activator of the MPKs MPK3 and MPK6 both in vitro and in planta. Expression of active MKK9 protein in transgenic plants induces the synthesis of ethylene and camalexin through the activation of the endogenous MPK3 and MPK6 kinases. MKK9-MPK3/MPK6 cascade participates in the regulation of the biosynthesis of ethylene and camalexin and may be an important axis in the stress responses of Arabidopsis (Xu et al. 2008). |
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NSP5 |
Nitrile-specifier protein 5 |
The seed content of the precursor GSL; 4-methylthiobutylGSL was consistently reduced in nsp3-2; nsp4-1 and nsp5-1 relative to WT (Wittstock et al. 2016) |
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SDI1 |
Protein SULFUR DEFICIENCY-INDUCED 1 |
Sulfur deficiency induced 1 (SD1) and SD2 are –S marker genes sulfur deficiency that act as major repressors controlling GSL biosynthesis in Arabidopsis under –S condition. SDI1 and SDI2 expression negatively correlated with GSL biosynthesis in both transcript and metabolite levels. Principal components analysis of transcriptome data indicated that SDI1 regulates aliphatic GSL biosynthesis as part of –S response. SDI1 was localized to the nucleus and interacted with MYB28 a major transcription factor that promotes aliphatic GSL biosynthesis in both yeast and plant cells (Aarabi et al. 2016) |
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ILL3 |
IAA-amino acid hydrolase ILR1-like 3 |
Camalexin originates from tryptophan and its biosynthesis involves the cytochrome P450 enzymes CYP79B2 and CYP71B15 (PAD3). Camalexin induction is a complex process, for which triggering by reactive oxygen species (ROS), salicylic acid signalling, and the glutathione status are important. Targets of the signalling cascade are the tryptophan and camalexin biosynthetic genes, which are strongly transcriptionally upregulated at the sites of pathogen infection (Glawischnig et al. 2004) . |
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TSB1 |
Tryptophan synthase beta chain 1 chloroplastic |
In RNA-blot analysis; the atr1-2 mutation suppressed elevated expression of Trp genes caused by the cyp83B1 mutation: The ASA1 and TSB1 Trp synthesis genes were suppressed to wild-type levels by atr1-2 (Celenza et al. 2005) |
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CYP81F2 |
Cytochrome P450 81F2 |
All four Arabidopsis CYP81F gene products had the capacity to modify the indole GSL structure. CYP81F1; CYP81F2; and CYP81F3 but not CYP81F4 catalyzed the conversion of indol-3-yl-methyl GSL (I3M) to 4-hydroxy-indol-3-yl-methyl (4OH-I3M) and all four CYP81Fs converted I3M to 1-hydroxy-indol-3-yl-methyl GSL (1OH-I3M) (Pfalz et al. 2011) |
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MYB34 |
Transcription factor MYB34 |
MYB34; MYB51 and MYB122 act together to control the biosynthesis of indole-3-ylmethyl-GSL (I3M) in shoots and roots with MYB34 controlling biosynthesis of indolic GSLs (IGs) mainly in the roots. MYB51 regulating biosynthesis in shoots and MYB122 having an accessory role in the biosynthesis of IGs (Frerigmann & Gigolashvili 2014) |
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MYB28 |
Transcription factor MYB28 |
In a screen for the trans-activation potential of various transcription factors toward GSL biosynthetic genes; MYB28 was identified as a positive regulator of aliphatic methionine-derived GSLs. The content of aliphatic GSLs as well as transcript levels of aliphatic GSL biosynthetic genes were elevated in gain-of-function mutants and decreased in MYB28 RNAi knock-down mutants (Gigolashvili et al. 2007) |
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GTR2 |
Protein NRT1/ PTR FAMILY 2.11 |
Leaf apoplastic fluid analysis and GSL feeding experiments showed two GSL transporters. GTR1 and GTR2 were essential for long-distance transport of GSLs in Arabidopsis and also play key roles in GSL allocation within a mature leaf by effectively importing apoplastically localized GSLs into appropriate cells (Madsen et al. 2014) |
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CHY1 |
3-hydroxyisobutyryl-CoA hydrolase 1 |
Mutations in the gene At5g65940. previously shown to encode a peroxisomal protein with beta-hy- droxyisobutyryl-CoA hydrolase activity and designated as Chy1; lead to a deficiency of benzoic acid-containing GSLs in the seeds (Ibdah and Pichersky 2009) |