SuCComBase

Sulfur Containing Compound Database

Known SCC Genes

AGI ID UniProt ID EnsemblPlants Gene Name Protein Name Function Description

AT1G02930

P42760

Link

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).

AT1G04580

Q7G191

Link

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)

AT1G04770

Q8L730

Link

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)

AT1G07640

Q8L9V6

Link

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)

AT1G11610

Q9SAB6

Link

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) .

AT1G12130

Q9FWW3

Link

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)

AT1G12140

A8MRX0

Link

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)

AT1G12160

Q9FWW6

Link

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)

AT1G12200

Q9FWW9

Link

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)

AT1G13110

Q96514

Link

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) .

AT1G16400

Q9FUY7

Link

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)

AT1G16410

Q949U1

Link

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)

AT1G18570

O49782

Link

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)

AT1G18590

Q9FZ80

Link

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)

AT1G21100

Q9LPU5

Link

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)

AT1G21120

Q9LPU7

Link

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)

AT1G24100

O48676

Link

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)

AT1G32640

Q39204

Link

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)

AT1G47600

Q8GRX1

Link

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)

AT1G50110

Q9LPM9

Link

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)

AT1G51470

Q3ECS3

Link

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)

AT1G54040

Q8RY71

Link

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)

AT1G59750

Q8L7G0

Link

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)

AT1G59870

Q9XIE2

Link

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)

AT1G62180

P92981

Link

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)

AT1G62540

Q94K43

Link

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)

AT1G62560

Q9SXE1

Link

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)

AT1G62570

Q93Y23

Link

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)

AT1G64070

F4I594

Link

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)

AT1G64280

P93002

Link

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)

AT1G65860

Q9SS04

Link

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)

AT1G65880

Q9SS01

Link

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)

AT1G73500

Q9FX43

Link

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).

AT1G73730

O23116

Link

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)

AT1G74080

Q9C9C8

Link

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)

AT1G74090

Q9C9C9

Link

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)

AT1G74100

Q9C9D0

Link

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)

AT1G74710

Q9S7H8

Link

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)

AT1G76790

Q9SRD4

Link

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)

AT1G78000

Q9MAX3

Link

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)

AT1G78370

Q8L7C9

Link

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)

AT2G03590

Q9ZPR7

Link

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).

AT2G14750

Q43295

Link

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)

AT2G20610

Q9SIV0

Link

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)

AT2G22300

Q8GSA7

Link

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)

AT2G22330

Q501D8

Link

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)

AT2G25450

Q9SKK4

Link

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)

AT2G29090

O81077

Link

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) .

AT2G30750

O49340

Link

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)

AT2G30770

O49342

Link

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)

AT2G30860

O80852

Link

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)

AT2G30870

P42761

Link

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)

AT2G31790

Q9SKC1

Link

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)

AT2G33070

O49326

Link

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)

AT2G36380 

Q7PC87

Link

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)

AT2G38470

Q8S8P5

Link

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)

AT2G39940

O04197

Link

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)

AT2G43000

Q9SK55

Link

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)

AT2G43100

Q9ZW84

Link

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)

AT2G43790

Q39026

Link

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).

AT2G44490

O64883

Link

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)

AT2G45970

O80823

Link

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) .

AT2G46070

Q8GYQ5

Link

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).

AT2G46370

Q9SKE2

Link

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)

AT2G46650

Q9ZNV4

Link

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)

AT3G03190

Q96324

Link

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)

AT3G09710

Q9SF32

Link

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)

AT3G12203

Q9C7D6

Link

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)

AT3G14210

Q9LJG3

Link

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)

AT3G16390

O04318

Link

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)

AT3G16400

Q9SDM9

Link

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)

AT3G16410

O04316

Link

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)

AT3G19710

Q9LE06

Link

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)

AT3G20960

Q8GYY9

Link

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) .

AT3G22890

Q9LIK9

Link

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)

AT3G25180

Q9LSF8

Link

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) .

AT3G26830

Q9LW27

Link

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)

AT3G27785

Q9LVW4

Link

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)

AT3G44300

P32962

Link

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)

AT3G44310

P32961

Link

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)

AT3G44320

P46010

Link

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)

AT3G45640

Q39023

Link

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).

AT3G47960

Q944G5

Link

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)

AT3G48090

Q9SU72

Link

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)

AT3G49680

Q9M401

Link

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)

AT3G52430

Q9S745

Link

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)

AT3G58990

Q9LYT7

Link

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)

AT3G62250

P59233

Link

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).

AT4G03050

Q9ZTA1

Link

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)

AT4G03060

Q9ZTA2

Link

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)

AT4G03190

Q9ZR12

Link

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)

AT4G04610

P92979

Link

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)

AT4G08620

Q9SAY1

Link

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)

AT4G12030

F4JPW1

Link

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)

AT4G12320

Q66GJ1

Link

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) .

AT4G13430

Q94AR8

Link

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)

AT4G13770

P48421

Link

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)

AT4G14680

O23324

Link

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)

AT4G14880

P47998

Link

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)

AT4G15370

O23390

Link

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)

AT4G15380

Q8L7H7

Link

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) .

AT4G17490

Q8VZ91

Link

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).

AT4G17880

O49687

Link

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)

AT4G21990

P92980

Link

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)

AT4G22690

F4JLY4

Link

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) .

AT4G23100

P46309

Link

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)

AT4G23980

Q9XED8

Link

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)

AT4G27260

O81829

Link

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)

AT4G30530

Q9M0A7

Link

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)

AT4G30550

Q9M0A5

Link

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)

AT4G31500

O65782

Link

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)

AT4G37400

Q0WTF4

Link

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)

AT4G37410

Q9SZU1

Link

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)

AT4G37430

O65790

Link

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)

AT4G39030

Q945F0

Link

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)

AT4G39650

Q680I5

Link

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).

AT4G39940

O49196

Link

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)

AT4G39950

O81346

Link

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)

AT5G03280

Q9S814

Link

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)

AT5G04660

Q9LZ31

Link

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) .

AT5G05260

Q9FLC8

Link

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)

AT5G05730

P32068

Link

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)

AT5G07690

Q9FLR1

Link

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)

AT5G07700

Q9SPG5

Link

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)

AT5G13220

Q93ZM9

Link

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)

AT5G14200

Q9FMT1

Link

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)

AT5G22300

P46011

Link

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)

AT5G23010

Q9FG67

Link

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)

AT5G23020

Q9FN52

Link

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)

AT5G24960

P58045

Link

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) .

AT5G25980

Q9C5C2

Link

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)

AT5G26000

P37702

Link

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)

AT5G27380

P46416

Link

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)

AT5G38450

Q9FF18

Link

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) .

AT5G40360

Q1PDP9

Link

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)

AT5G44070

Q9S7Z3

Link

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)

AT5G46760

Q9FIP9

Link

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)

AT5G47230

O80341

Link

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).

AT5G48180

Q93XW5

Link

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)

AT5G48850

Q8GXU5

Link

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)

AT5G54140

O81641

Link

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) .

AT5G54810

P14671

Link

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)

AT5G57220

Q9LVD6

Link

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)

AT5G60890

O64399

Link

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)

AT5G61420

Q9SPG2

Link

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)

AT5G62680

Q9LV10

Link

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)

AT5G65940

Q9LKJ1

Link

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)