The ABC transporter BcatrB from <i>Botrytis cinerea</i> exports camalexin and is a virulence factor on <i>Arabidopsis thaliana</i>

Stefanato, Francesca L.; Abou-Mansour, Eliane; Buchala, Antony; Kretschmer, Matthias; Mosbach, Andreas; Hahn, Matthias; Bochet, Christian G.; Métraux, Jean‐Pierre; Schoonbeek, Henk‐jan

doi:10.1111/j.1365-313x.2009.03794.x

Cited by 174 publications

(177 citation statements)

References 63 publications

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“…3A), and JA-signaling components are involved in the biosynthesis of camalexin (25). Interestingly, a full-size ABCG transporter, BcatrB, in B. cinerea is necessary for the export of camalexin (44). This transporter is a critical virulence factor, as evidenced by the failure of a BcatrB-knockout mutant to infect A. thaliana.…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin

Khare

Choi

Huh

et al. 2017

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

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Plant pathogens cause huge yield losses. Plant defense often depends on toxic secondary metabolites that inhibit pathogen growth. Because most secondary metabolites are also toxic to the plant, specific transporters are needed to deliver them to the pathogens. To identify the transporters that function in plant defense, we screened Arabidopsis thaliana mutants of full-size ABCG transporters for hypersensitivity to sclareol, an antifungal compound. We found that atabcg34 mutants were hypersensitive to sclareol and to the necrotrophic fungi Alternaria brassicicola and Botrytis cinerea. AtABCG34 expression was induced by A. brassicicola inoculation as well as by methyl-jasmonate, a defense-related phytohormone, and AtABCG34 was polarly localized at the external face of the plasma membrane of epidermal cells of leaves and roots. atabcg34 mutants secreted less camalexin, a major phytoalexin in A. thaliana, whereas plants overexpressing AtABCG34 secreted more camalexin to the leaf surface and were more resistant to the pathogen. When treated with exogenous camalexin, atabcg34 mutants exhibited hypersensitivity, whereas BY2 cells expressing AtABCG34 exhibited improved resistance. Analyses of natural Arabidopsis accessions revealed that AtABCG34 contributes to the disease resistance in naturally occurring genetic variants, albeit to a small extent. Together, our data suggest that AtABCG34 mediates camalexin secretion to the leaf surface and thereby prevents A. brassicicola infection.AtABCG34 | ABC transporters | camalexin | A. brassicicola | B. cinerea P lants are exposed to a multitude of pathogens, but they usually resist infection by using their unique defense systems and compounds, including secondary metabolites produced either constitutively (phytoanticipins) or in response to pathogen attack (phytoalexins). Plants produce tens of thousands of secondary metabolites, which are classified as phenolics, terpenoids, alkaloids, glucosinolates, cyanogenic glucosides, and betanins. Secondary metabolites are secreted from the infected cells and their surrounding cells after pathogen attack or are released, hydrolyzed, and become toxic when the cells are destroyed by pathogens (1), thus inhibiting pathogen growth on the plant. Many secondary metabolites are dangerous to the plants because of their toxicity to cellular metabolism. To avoid self-toxicity, plants either secrete these compounds to the leaf surface or sequester them in the vacuole, a compartment with low metabolic activity. In both cases, specific transporters are required either to deliver the secondary metabolites to the site where the pathogens are located or to store them as weapons against pathogen attack.Several full-size ABCG transporters are involved in the transport of secondary metabolites. Nicotiana plumbaginifolia PDR1/ABC1 and Nicotiana tabacum PDR1 are induced by jasmonate, a defense-related hormone highly expressed in the leaf epidermal cells and trichomes, and transport sclareol, a diterpene alcohol secreted by Nicotiana species in response to p...

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Section: Discussionmentioning

confidence: 99%

Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin

Khare

Choi

Huh

et al. 2017

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

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“…Camalexin is a known phytoalexin in Arabidopsis that provides defense against B. cinerea depending upon the ability of the fungus to detoxify camalexin (Zhou et al, 1999;Stefanato et al, 2009;Rowe et al, 2010). Genetic variation in the host and pathogen significantly affected camalexin accumulation (Table 1; Supplemental Figure 1 and for an interactive plot, see Supplemental Data Set 4).…”

Section: Variation In Camalexin Accumulation In Response To B Cinerementioning

confidence: 99%

“…Additionally, B. cinerea is a true haploid ascomycete that infects a wide range of evolutionarily distinct plant hosts, from bryophytes to eudicots. B. cinerea has elevated natural genetic variation that results in multiple major-effect polymorphisms in known virulence mechanisms, including the production of phytotoxic metabolites (Colmenares et al, 2002;Dalmais et al, 2011), enzymes that detoxify plant defense metabolites (Ferrari et al, 2003;Pedras et al, 2005Pedras et al, , 2007Pedras et al, , 2008Pedras et al, , 2009Pedras et al, , 2011Stefanato et al, 2009;Rowe et al, 2010), and the ability to degrade plant cell walls (Rowe and Kliebenstein, 2007;Schumacher et al, 2012Schumacher et al, , 2015Kumari et al, 2014). Because wild B. cinerea isolates have recombination and random mating, a population of isolates is a random intermixed sample of the diverse virulence mechanisms (Rowe and Kliebenstein, 2007;Kretschmer et al, 2009;Rowe et al, 2010;Kumari et al, 2014;Atwell et al, 2015;Corwin et al, 2016aCorwin et al, , 2016bZhang et al, 2016).…”

Section: Introductionmentioning

confidence: 99%

Plastic Transcriptomes Stabilize Immunity to Pathogen Diversity: The Jasmonic Acid and Salicylic Acid Networks within the Arabidopsis/Botrytis Pathosystem

et al. 2017

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To respond to pathogen attack, selection and associated evolution has led to the creation of plant immune system that are a highly effective and inducible defense system. Central to this system are the plant defense hormones jasmonic acid (JA) and salicylic acid (SA) and crosstalk between the two, which may play an important role in defense responses to specific pathogens or even genotypes. Here, we used the Arabidopsis thaliana-Botrytis cinerea pathosystem to test how the host's defense system functions against genetic variation in a pathogen. We measured defense-related phenotypes and transcriptomic responses in Arabidopsis wild-type Col-0 and JA-and SA-signaling mutants, coi1-1 and npr1-1, individually challenged with 96 diverse B. cinerea isolates. Those data showed genetic variation in the pathogen influences on all components within the plant defense system at the transcriptional level. We identified four gene coexpression networks and two vectors of defense variation triggered by genetic variation in B. cinerea. This showed that the JA and SA signaling pathways functioned to constrain/canalize the range of virulence in the pathogen population, but the underlying transcriptomic response was highly plastic. These data showed that plants utilize major defense hormone pathways to buffer disease resistance, but not the metabolic or transcriptional responses to genetic variation within a pathogen.

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“…Camalexin exhibits cytotoxicity (Rogers et al, 1996), particularly against eukaryotic pathogens. Some fungal strains are resistant to camalexin due to efficient degradation or export Stefanato et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

The Multifunctional Enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) Converts Cysteine-Indole-3-Acetonitrile to Camalexin in the Indole-3-Acetonitrile Metabolic Network ofArabidopsis thaliana

et al. 2009

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Accumulation of camalexin, the characteristic phytoalexin of Arabidopsis thaliana, is induced by a great variety of plant pathogens. It is derived from Trp, which is converted to indole-3-acetonitrile (IAN) by successive action of the cytochrome P450 enzymes CYP79B2/B3 and CYP71A13. Extracts from wild-type plants and camalexin biosynthetic mutants, treated with silver nitrate or inoculated with Phytophthora infestans, were comprehensively analyzed by ultra-performance liquid chromatography electrospray ionization quadrupole time-of-flight mass spectrometry. This metabolomics approach was combined with precursor feeding experiments to characterize the IAN metabolic network and to identify novel biosynthetic intermediates and metabolites of camalexin. Indole-3-carbaldehyde and indole-3-carboxylic acid derivatives were shown to originate from IAN. IAN conjugates with glutathione, g-glutamylcysteine, and cysteine [Cys(IAN)] accumulated in challenged phytoalexin deficient3 (pad3) mutants. Cys(IAN) rescued the camalexin-deficient phenotype of cyp79b2 cyp79b3 and was itself converted to dihydrocamalexic acid (DHCA), the known substrate of CYP71B15 (PAD3), by microsomes isolated from silver nitrate-treated Arabidopsis leaves. Surprisingly, yeast-expressed CYP71B15 also catalyzed thiazoline ring closure, DHCA formation, and cyanide release with Cys(IAN) as substrate. In conclusion, in the camalexin biosynthetic pathway, IAN is derivatized to the intermediate Cys (IAN), which serves as substrate of the multifunctional cytochrome P450 enzyme CYP71B15.

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The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana

Cited by 174 publications

References 63 publications

Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin

Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin

Plastic Transcriptomes Stabilize Immunity to Pathogen Diversity: The Jasmonic Acid and Salicylic Acid Networks within the Arabidopsis/Botrytis Pathosystem

The Multifunctional Enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) Converts Cysteine-Indole-3-Acetonitrile to Camalexin in the Indole-3-Acetonitrile Metabolic Network ofArabidopsis thaliana

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