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Camalexin contributes to the partial resistance of Arabidopsis thaliana to the biotrophic soilborne protist Plasmodiophora brassicae.

Lemarié S, Robert-Seilaniantz A, Lariagon C, Lemoine J, Marnet N, Levrel A, Jubault M, Manzanares-Dauleux MJ, Gravot A - Front Plant Sci (2015)

Bottom Line: This induction correlated with slower P. brassicae growth in Bur-0 compared to Col-0, thus suggesting a relationship between the levels of camalexin biosynthesis and the different levels of resistance.The Bur/Col allelic substitution in the region of the previously identified clubroot resistance QTL PbAt5.2 (Chromosome 5) was associated with both the enhanced clubroot-triggered induction of camalexin biosynthesis and the reduced P. brassicae development.Altogether, our results suggest that high levels of clubroot-triggered camalexin biosynthesis play a role in the quantitative control of partial resistance of Arabidopsis to clubroot.

View Article: PubMed Central - PubMed

Affiliation: UMR1349 IGEPP, INRA Le Rheu, France.

ABSTRACT
Camalexin has been reported to play defensive functions against several pathogens in Arabidopsis. In this study, we investigated the possible role of camalexin accumulation in two Arabidopsis genotypes with different levels of basal resistance to the compatible eH strain of the clubroot agent Plasmodiophora brassicae. 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. This induction correlated with slower P. brassicae growth in Bur-0 compared to Col-0, thus suggesting a relationship between the levels of camalexin biosynthesis and the different levels of resistance. Clubroot-triggered biosynthesis of camalexin may also participate in basal defense in Col-0, as gall symptoms and pathogen development were enhanced in the pad3 mutant (Col-0 genetic background), which is defective in camalexin biosynthesis. Clubroot and camalexin responses were then studied in Heterogeneous Inbred Families (HIF) lines derived from a cross between Bur-0 and Col-0. The Bur/Col allelic substitution in the region of the previously identified clubroot resistance QTL PbAt5.2 (Chromosome 5) was associated with both the enhanced clubroot-triggered induction of camalexin biosynthesis and the reduced P. brassicae development. Altogether, our results suggest that high levels of clubroot-triggered camalexin biosynthesis play a role in the quantitative control of partial resistance of Arabidopsis to clubroot.

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Camalexin biosynthesis pathway according to Millet et al. (2010) and Geu-Flores et al. (2011). Camalexin is derived from tryptophan which is firstly converted to indole 3 acetaldoxime (IAOx) by the cytochrome P450 enzymes CYP79B2 and CYP79B3. IAOx is then converted to indole 3 acetonitrile (IAN) by the CYP71A12 and CYP71A13 enzymes. Subsequently, IAN is converted to the Cys(IAN) conjugate after intermediate steps (represented in dashed arrows). The final two steps in camalexin biosynthesis are catalyzed by the P450 enzyme CYP71B15/PAD3.
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Figure 1: Camalexin biosynthesis pathway according to Millet et al. (2010) and Geu-Flores et al. (2011). Camalexin is derived from tryptophan which is firstly converted to indole 3 acetaldoxime (IAOx) by the cytochrome P450 enzymes CYP79B2 and CYP79B3. IAOx is then converted to indole 3 acetonitrile (IAN) by the CYP71A12 and CYP71A13 enzymes. Subsequently, IAN is converted to the Cys(IAN) conjugate after intermediate steps (represented in dashed arrows). The final two steps in camalexin biosynthesis are catalyzed by the P450 enzyme CYP71B15/PAD3.

Mentions: Camalexin is a sulfur-containing tryptophan-derived secondary metabolite, and is considered to be the major phytoalexin involved in biotic responses in A. thaliana (Ausubel et al., 1995; Glawischnig, 2007). The camalexin biosynthesis pathway (summarized in Figure 1) first involves the conversion of tryptophan to indole-3-acetaldoxime (IAOx), through the action of two functionally redundant cytochrome P450 enzymes, CYP79B2 and CYP79B3. This step is followed by the dehydration of IAOx to indole 3 acetonitrile (IAN), catalyzed by CYP71A13 (Nafisi et al., 2007) and CYP71A12 (Millet et al., 2010; Saga et al., 2012). IAN is then conjugated to glutathione by the glutathione-S-transferase GSTF6 to synthesize GSH(IAN) (Su et al., 2011) then metabolized to Cys(IAN) by γ-glutamyl peptidases GGP1 and GGP3 (Geu-Flores et al., 2011). Finally, the PAD3/CYP71B15 enzyme catalyzes the last two reactions of the biosynthesis pathway leading to camalexin (Zhou et al., 1999; Schuhegger et al., 2006; Böttcher et al., 2009). Many genetic approaches confirmed that camalexin plays a positive role in resistance. For instance, camalexin accumulation was correlated with resistance to necrotrophic fungi such as Alternaria brassicicola (Thomma et al., 1999; Nafisi et al., 2007), Botrytis cinerea (Ferrari et al., 2003, 2007; Kliebenstein et al., 2005; van Baarlen et al., 2007) and Plectosphaerella cucumerina (Staal et al., 2006; Sanchez-Vallet et al., 2010). Camalexin has also been reported to play a defensive role against the hemibiotrophic fungus Leptosphaeria maculans (Bohman et al., 2004; Staal et al., 2006) and the oomycete Phytophthora brassicae (Schlaeppi et al., 2010). However, Camalexin accumulation was not always correlated with pathogen resistance. For example, camalexin accumulated in response to various strains of Pseudomonas syringae, but the pad3 mutant, in which the last two steps of camalexin biosynthesis are disrupted, did not show any difference in susceptibility to those strains (Glazebrook et al., 1997; Zhou et al., 1999).


Camalexin contributes to the partial resistance of Arabidopsis thaliana to the biotrophic soilborne protist Plasmodiophora brassicae.

Lemarié S, Robert-Seilaniantz A, Lariagon C, Lemoine J, Marnet N, Levrel A, Jubault M, Manzanares-Dauleux MJ, Gravot A - Front Plant Sci (2015)

Camalexin biosynthesis pathway according to Millet et al. (2010) and Geu-Flores et al. (2011). Camalexin is derived from tryptophan which is firstly converted to indole 3 acetaldoxime (IAOx) by the cytochrome P450 enzymes CYP79B2 and CYP79B3. IAOx is then converted to indole 3 acetonitrile (IAN) by the CYP71A12 and CYP71A13 enzymes. Subsequently, IAN is converted to the Cys(IAN) conjugate after intermediate steps (represented in dashed arrows). The final two steps in camalexin biosynthesis are catalyzed by the P450 enzyme CYP71B15/PAD3.
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Related In: Results  -  Collection

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Figure 1: Camalexin biosynthesis pathway according to Millet et al. (2010) and Geu-Flores et al. (2011). Camalexin is derived from tryptophan which is firstly converted to indole 3 acetaldoxime (IAOx) by the cytochrome P450 enzymes CYP79B2 and CYP79B3. IAOx is then converted to indole 3 acetonitrile (IAN) by the CYP71A12 and CYP71A13 enzymes. Subsequently, IAN is converted to the Cys(IAN) conjugate after intermediate steps (represented in dashed arrows). The final two steps in camalexin biosynthesis are catalyzed by the P450 enzyme CYP71B15/PAD3.
Mentions: Camalexin is a sulfur-containing tryptophan-derived secondary metabolite, and is considered to be the major phytoalexin involved in biotic responses in A. thaliana (Ausubel et al., 1995; Glawischnig, 2007). The camalexin biosynthesis pathway (summarized in Figure 1) first involves the conversion of tryptophan to indole-3-acetaldoxime (IAOx), through the action of two functionally redundant cytochrome P450 enzymes, CYP79B2 and CYP79B3. This step is followed by the dehydration of IAOx to indole 3 acetonitrile (IAN), catalyzed by CYP71A13 (Nafisi et al., 2007) and CYP71A12 (Millet et al., 2010; Saga et al., 2012). IAN is then conjugated to glutathione by the glutathione-S-transferase GSTF6 to synthesize GSH(IAN) (Su et al., 2011) then metabolized to Cys(IAN) by γ-glutamyl peptidases GGP1 and GGP3 (Geu-Flores et al., 2011). Finally, the PAD3/CYP71B15 enzyme catalyzes the last two reactions of the biosynthesis pathway leading to camalexin (Zhou et al., 1999; Schuhegger et al., 2006; Böttcher et al., 2009). Many genetic approaches confirmed that camalexin plays a positive role in resistance. For instance, camalexin accumulation was correlated with resistance to necrotrophic fungi such as Alternaria brassicicola (Thomma et al., 1999; Nafisi et al., 2007), Botrytis cinerea (Ferrari et al., 2003, 2007; Kliebenstein et al., 2005; van Baarlen et al., 2007) and Plectosphaerella cucumerina (Staal et al., 2006; Sanchez-Vallet et al., 2010). Camalexin has also been reported to play a defensive role against the hemibiotrophic fungus Leptosphaeria maculans (Bohman et al., 2004; Staal et al., 2006) and the oomycete Phytophthora brassicae (Schlaeppi et al., 2010). However, Camalexin accumulation was not always correlated with pathogen resistance. For example, camalexin accumulated in response to various strains of Pseudomonas syringae, but the pad3 mutant, in which the last two steps of camalexin biosynthesis are disrupted, did not show any difference in susceptibility to those strains (Glazebrook et al., 1997; Zhou et al., 1999).

Bottom Line: This induction correlated with slower P. brassicae growth in Bur-0 compared to Col-0, thus suggesting a relationship between the levels of camalexin biosynthesis and the different levels of resistance.The Bur/Col allelic substitution in the region of the previously identified clubroot resistance QTL PbAt5.2 (Chromosome 5) was associated with both the enhanced clubroot-triggered induction of camalexin biosynthesis and the reduced P. brassicae development.Altogether, our results suggest that high levels of clubroot-triggered camalexin biosynthesis play a role in the quantitative control of partial resistance of Arabidopsis to clubroot.

View Article: PubMed Central - PubMed

Affiliation: UMR1349 IGEPP, INRA Le Rheu, France.

ABSTRACT
Camalexin has been reported to play defensive functions against several pathogens in Arabidopsis. In this study, we investigated the possible role of camalexin accumulation in two Arabidopsis genotypes with different levels of basal resistance to the compatible eH strain of the clubroot agent Plasmodiophora brassicae. 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. This induction correlated with slower P. brassicae growth in Bur-0 compared to Col-0, thus suggesting a relationship between the levels of camalexin biosynthesis and the different levels of resistance. Clubroot-triggered biosynthesis of camalexin may also participate in basal defense in Col-0, as gall symptoms and pathogen development were enhanced in the pad3 mutant (Col-0 genetic background), which is defective in camalexin biosynthesis. Clubroot and camalexin responses were then studied in Heterogeneous Inbred Families (HIF) lines derived from a cross between Bur-0 and Col-0. The Bur/Col allelic substitution in the region of the previously identified clubroot resistance QTL PbAt5.2 (Chromosome 5) was associated with both the enhanced clubroot-triggered induction of camalexin biosynthesis and the reduced P. brassicae development. Altogether, our results suggest that high levels of clubroot-triggered camalexin biosynthesis play a role in the quantitative control of partial resistance of Arabidopsis to clubroot.

No MeSH data available.


Related in: MedlinePlus