Skip to main content
SpringerLink
Log in

Camalexin accumulation as a component of plant immunity during interactions with pathogens and beneficial microbes

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main Conclusion

This review provides an overview on the role of camalexin in plant immunity taking into account various plant-pathogen and beneficial microbe interactions, regulation mechanisms and the contribution in basal and induced plant resistance.

Abstract

In a hostile environment, plants evolve complex and sophisticated defense mechanisms to counteract invading pathogens and herbivores. Several lines of evidence support the assumption that secondary metabolites like phytoalexins which are synthesized de novo, play an important role in plant defenses and contribute to pathogens’ resistance in a wide variety of plant species. Phytoalexins are synthesized and accumulated in plants upon pathogen challenge, root colonization by beneficial microbes, following treatment with chemical elicitors or in response to abiotic stresses. Their protective properties against pathogens have been reported in various plant species as well as their contribution to human health. Phytoalexins are synthesized through activation of particular sets of genes encoding specific pathways. Camalexin (3’-thiazol-2’-yl-indole) is the primary phytoalexin produced by Arabidopsis thaliana after microbial infection or abiotic elicitation and an iconic representative of the indole phytoalexin family. The synthesis of camalexin is an integral part of cruciferous plant defense mechanisms. Although the pathway leading to camalexin has been largely elucidated, the regulatory networks that control the induction of its biosynthetic steps by pathogens with different lifestyles or by beneficial microbes remain mostly unknown. This review thus presents current knowledge regarding camalexin biosynthesis induction during plant-pathogen and beneficial microbe interactions as well as in response to microbial compounds and provides an overview on its regulation and interplay with signaling pathways. The contribution of camalexin to basal and induced plant resistance and its detoxification by some pathogens to overcome host resistance are also discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

Data availability

Data sharing not applicable to this article as no datasets were generated or analysed during the current study. All data generated or analysed during this study are included in this published article (and its supplementary information files).

References

  • Adikaram NKB, Brown AE, Swinburne TR (1988) Phytoalexin induction as a factor in the protection of Capsicum annuum L. Fruits against infection by Botrytis cinerea Pers. J Phytopathol 122:267–273

    Article  CAS  Google Scholar 

  • Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17:73–90

    Article  CAS  PubMed  Google Scholar 

  • Antico CJ, Colon C, Banks T, Ramonell KM (2012) Insights into the role of jasmonic acid-mediated defenses against necrotrophic and biotrophic fungal pathogens. Front Biol 7:48–56

    Article  CAS  Google Scholar 

  • Arthur JSC, Ley SC (2013) Mitogen-activated protein kinases in innate immunity. Nat Rev Immunol 13:679–692

    Article  CAS  PubMed  Google Scholar 

  • Aziz A, Verhagen B, Magnin-Robert M, Couderchet M, Clément C, Jeandet P et al (2016) Effectiveness of beneficial bacteria to promote systemic resistance of grapevine to gray mold as related to phytoalexin production in vineyards. Plant Soil 405:141–153

    Article  CAS  Google Scholar 

  • Badri DV, Chaparro JM, Manter DK, Martinoia E, Vivanco JM (2012) Influence of ATP-binding cassette transporters in root exudation of phytoalexins, signals, and in disease resistance. Front Plant Sci 3:149. https://doi.org/10.3389/fpls.2012.00149

    Article  PubMed  PubMed Central  Google Scholar 

  • Bailey J, Rowell PM, Arnold GM (1980) The temporal relationship between host cell death, phytoalexin accumulation and fungal inhibition during hypersensitive reactions of Phaseolus vulgaris to Colletotrichum lindemuthianum. Physiol Plant Pathol 17:329–339

    Article  CAS  Google Scholar 

  • Balmer A, Pastor V, Glauser G, Mauch-Mani B (2018) Tricarboxylates induce defense priming against bacteria in Arabidopsis thaliana. Front Plant Sci 9:1221. https://doi.org/10.3389/fpls.2018.01221

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartels S, Anderson JC, Gonzalez Besteiro MA, Carreri A, Hirt H, Buchala A et al (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21:2884–2897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bednarek P (2012) Sulfur-containing secondary metabolites from Arabidopsis thaliana and other Brassicaceae with function in plant immunity. ChemBioChem 13:1846–1859

    Article  CAS  PubMed  Google Scholar 

  • Bednarek P, Schneider B, Svatos A, Oldham NJ, Hahlbrock K (2005) Structural complexity, differential response to infection, and tissue specificity of indolic and phenylpropanoid secondary metabolism in Arabidopsis roots. Plant Physiol 138:1058–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323:101–106

    Article  CAS  PubMed  Google Scholar 

  • Beets CA, Huang JC, Madala NE, Dubery I (2012) Activation of camalexin biosynthesis in Arabidopsis thaliana in response to perception of bacterial lipopolysaccharides: A gene-to-metabolite study. Planta 236:261–272

    Article  CAS  PubMed  Google Scholar 

  • Bigeard J, Colcombet J, Hirt H (2015) Signaling mechanisms in pattern-triggered immunity (PTI). Mol Plant 8:521–539

    Article  CAS  PubMed  Google Scholar 

  • Birkenbihl RP, Diezel C, Somssich IE (2012) Arabidopsis WRKY33 is a key transcriptional regulator of hormonal and metabolic responses toward Botrytis cinerea infection. Plant Physiol 159:266–285

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Birkenbihl RP, Kracher B, Roccaro M, Somssich IE (2017) Induced genome-wide binding of three Arabidopsis WRKY transcription factors during early MAMP-triggered immunity. Plant Cell 29:20–38

    Article  CAS  PubMed  Google Scholar 

  • Bohman S, Staal J, Thomma BPHJ, Wang M, Dixelius C et al (2004) Characterisation of an Arabidopsis-Leptosphaeria maculans pathosystem: resistance partially requires camalexin biosynthesis and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 37:9–20

    Article  CAS  PubMed  Google Scholar 

  • Bottcher C, Westphal L, Schmotz C, Prade E, Scheel D, Glawischnig E (2009) The multifunctional enzyme CYP71B15 (PHYTOALEXIN DEFICIENT3) converts cysteine-indole-3-acetonitrile to camalexin in the indole-3-acetonitrile metabolic network of Arabidopsis thaliana. Plant Cell 21:1830–1845

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Bottcher C, Chapman A, Fellermeier F, Choudhary M, Scheel D, Glawischnig E (2014) The biosynthetic pathway of indole-3-carbaldehyde and indole-3-carboxylic acid derivatives in Arabidopsis. Plant Physiol 165:841–853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boutrot F, Segonzac C, Chang KN, Qiao H, Ecker JR, Zipfel C, Rathjen JP (2020) Direct transcriptional control of the Arabidopsis immune receptor FLS2 by the ethylene-dependent transcription factors EIN3 and EIL1. Proc Natl Acad Sci USA 107:14502–14507

    Article  Google Scholar 

  • Bozsoki Z, Cheng J, Feng F, Gysel K, Vinther M, Andersen KR, Oldroyd G, Blaise M, Radutoiu S, Stougaard J (2017) Receptor-mediated chitin perception in legume roots is functionally separable from Nod factor perception. Proc Natl Acad Sci USA 114:E8118–E8127

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cargnel MD, Demkura PV, Ballaré CL (2014) Linking phytochrome to plant immunity: low red : far-red ratios increase Arabidopsis susceptibility to Botrytis cinerea by reducing the biosynthesis of indolic glucosinolates and camalexin. New Phytol 204:342–354

    Article  CAS  PubMed  Google Scholar 

  • Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosinolate metabolites required for an Arabidopsis innate immune response. Science 323:95–101

    Article  CAS  PubMed  Google Scholar 

  • Contreras-Cornejo HA, Macías-Rodríguez L, Beltrán-Peña E, Herrera-Estrella A, López-Bucio J (2011) Trichoderma-induced plant immunity likely involves both hormonal- and camalexin-dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungi Botrytis cinerea. Plant Signal Behav 6:1554–1563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cruickshank IA, Perrin DR (1960) Isolation of a phytoalexin from Pisum sativum L. Nature 187:799–800

    Article  CAS  PubMed  Google Scholar 

  • Ferrari S, Plotnikova JM, De Lorenzo G, Ausubel FM (2003) Arabidopsis local resistance to Botrytis cinerea involves salicylic acid and camalexin and requires EDS4 and PAD2, but not SID2, EDS5 or PAD4. Plant J 35:193–205

    Article  CAS  PubMed  Google Scholar 

  • Ferrari S, Galletti R, Denoux C, De Lorenzo G, Ausubel FM, Dewdney J (2007) Resistance to Botrytis cinerea induced in Arabidopsis by elicitors is independent of salicylic acid, ethylene, or jasmonate signaling but requires PHYTOALEXIN DEFICIENT3. Plant Physiol 144:367–379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frerigmann H, Gigolashvili T (2014) MYB34, MYB51, and MYB122 distinctly regulate indolic glucosinolate biosynthesis in Arabidopsis thaliana. Mol Plant 7:814–828

    Article  CAS  PubMed  Google Scholar 

  • Frerigmann H, Glawischnig E, Gigolashvili T (2015) The role of MYB34, MYB51 and MYB122 in the regulation of camalexin biosynthesis in Arabidopsis thaliana. Front Plant Sci 6:654. https://doi.org/10.3389/fpls.2015.00654

    Article  PubMed  PubMed Central  Google Scholar 

  • Frerigmann H, Piślewska-Bednarek M, Sánchez-Vallet A, Molina A, Glawischnig E, Gigolashvili T et al (2016) Regulation of pathogen-triggered tryptophan metabolism in Arabidopsis thaliana by MYB transcription factors and indole glucosinolate conversion products. Mol Plant 9:682–695

    Article  CAS  PubMed  Google Scholar 

  • Galletti R, Ferrari S, De Lorenzo G (2011) Arabidopsis MPK3 and MPK6 play different roles in basal and oligogalacturonide- or flagellin-induced resistance against Botrytis cinerea. Plant Physiol 157:804–814

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geu-Flores F, Møldrup ME, Böttcher C, Olsen CE, Scheel D, Halkier BA (2011) Cytosolic γ-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell 23:2456–2469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glawischnig E (2006) The role of cytochrome P450 enzymes in the biosynthesis of camalexin. Biochem Soc Trans 34:1206–1208

    Article  CAS  PubMed  Google Scholar 

  • Glawischnig E (2007) Camalexin. Phytochemistry 68:401–406

    Article  CAS  PubMed  Google Scholar 

  • Glawischnig E, Hansen BG, Olsen CE, Halkier BA (2004) Camalexin is synthesized from indole-3-acetaldoxime, a key branching point between primary and secondary metabolism in Arabidopsis. Proc Natl Acad Sci USA 101:8245–8250

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227

    Article  CAS  PubMed  Google Scholar 

  • Glazebrook J, Ausubel FM (1994) Isolation of phytoalexin-deficient mutants of Arabidopsis thaliana and characterization of their interactions with bacterial pathogens. Proc Natl Acad Sci USA 91:8955–8959

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J, Rogers EE, Ausubel FM (1996) Isolation of Arabidopsis mutants with enhanced disease susceptibility by direct screening. Genetics 143:973–982

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glazebrook J, Zook M, Mert F, Kagan I, Rogers EE, Crute IR et al (1997) Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics 146:381–392

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gruau C, Trotel-Aziz P, Villaume S, Rabenoelina F, Clément C, Baillieul F, Aziz A (2015) Pseudomonas fluorescens PTA-CT2 triggers local and systemic immune response against Botrytis cinerea in grapevine. Mol Plant-Microbe Interact 28:1117–1129

    Article  CAS  PubMed  Google Scholar 

  • He Y, Xu J, Wang X, He X, Wang Y, Zhou J et al (2019) The Arabidopsis pleiotropic drug resistance transporters PEN3 and PDR12 mediate camalexin secretion for resistance to Botrytis cinerea. Plant Cell 31:2206–2222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heck S, Grau T, Buchala A, Métraux JP, Nawrath C (2003) Genetic evidence that expression of NahG modifies defence pathways independent of salicylic acid biosynthesis in the Arabidopsis-Pseudomonas syringae pv. tomato interaction. Plant J 36:342–352

    Article  CAS  PubMed  Google Scholar 

  • Hiruma K, Fukunaga S, Bednarek P, Piślewska-Bednarek M, Watanabe S, Narusaka Y et al (2013) Glutathione and tryptophan metabolism are required for Arabidopsis immunity during the hypersensitive response to hemibiotrophs. Proc Natl Acad Sci USA 110:9589–9594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hiruma K, Gerlach N, Sacristan S, Nakano RT, Hacquard S et al (2016) Root endophyte Colletotrichum tofieldiae confers plant fitness benefits that are phosphate status dependent. Cell 165:464–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iriti M, Faoro F, Iriti M, Faoro F (2009) Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution. Int J Mol Sci 10:3371–3399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jacoby RP, Koprivova A, Kopriva S (2021) Pinpointing secondary metabolites that shape the composition and function of the plant microbiome. J Exp Bot 72:57–69

    Article  CAS  PubMed  Google Scholar 

  • Jagodzik P, Tajdel-Zielinska M, Ciesla A, Marczak M, Ludwikow A (2018) Mitogen-activated protein kinase cascades in plant hormone signaling. Front Plant Sci 9:1387. https://doi.org/10.3389/fpls.2018.01387

    Article  PubMed  PubMed Central  Google Scholar 

  • Jeandet P (2018) Structure, chemical analysis, biosynthesis, metabolism, molecular engineering, and biological functions of phytoalexins. Molecules 23:61. https://doi.org/10.3390/molecules23010061

    Article  CAS  Google Scholar 

  • Jeandet P, Douillet-Breuil AC, Bessis R, Debord S, Sbaghi M, Adrian M (2002) Phytoalexins from the Vitaceae: biosynthesis, phytoalexin gene expression in transgenic plants, antifungal activity, and metabolism. J Agric Food Chem 50:2731–2741

    Article  CAS  PubMed  Google Scholar 

  • Jeandet P, Clément C, Courot E, Cordelier S (2013) Modulation of phytoalexin biosynthesis in engineered plants for disease resistance. Int J Mol Sci 14:14136–14170

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jeandet P, Hébrard C, Deville MA, Cordelier S, Dorey S, Aziz A et al (2014) Deciphering the role of phytoalexins in plant-microorganism interactions and human health. Molecules 19:18033–18056

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Jeandet P, Vannozzi A, Sobarzo-Sanchez E, Uddin MS, Bru R, Martinez-Marquez A et al (2021) Phytostilbenes as agrochemicals: biosynthesis, bioactivity, metabolic engineering and biotechnology. Nat Prod Rep 28:1282–1329

    Article  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Joubert A, Bataillé-Simoneau N, Campion C, Guillemette T, Hudhomme P, Lacomi-Vasilescu P et al (2011a) Cell wall integrity and high osmolarrity glycerol pathways are required for adaptation of Alternaria brassicicola to cell wall stress caused by brassicaceous indolic phytoalexins. Cell Microbiol 13:62–80

    Article  CAS  PubMed  Google Scholar 

  • Joubert A, Simoneau N, Campion C, Bataillé N, Lacomi-Vasilescu P, Poupard P et al (2011b) Impact of the unfolded protein response on the pathogenicity of the necrotrophic fungus Alternaria brassicicola. Mol Microbiol 79:1305–1324

    Article  CAS  PubMed  Google Scholar 

  • Katagiri F, Tsuda K (2010) Understanding the plant immune system. Mol Plant-Microbe Interact 23:1531–1536

    Article  CAS  PubMed  Google Scholar 

  • Khare D, Choi H, Huh SU, Bassin B, Kim J, Martinoia E et al (2017) Arabidopsis ABCG34 contributes to defense against necrotrophic pathogens by mediating the secretion of camalexin. Proc Natl Acad Sci USA 114:E5712–E5720

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kliebenstein DJ, Rowe HC, Denby KJ (2005) Secondary metabolites influence Arabidopsis/Botrytis interactions: variation in host production and pathogen sensitivity. Plant J 44:25–36

    Article  CAS  PubMed  Google Scholar 

  • Koornneef A, Leon-Reyes A, Ritsema T, Verhage A, Den Otter FC, Van Loon LC et al (2008) Kinetics of salicylate-mediated suppression of jasmonate signaling reveal a role for redox modulation. Plant Physiol 147:1358–1368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprivova A, Schuck S, Jacoby RP, Klinkhammer I, Welter B, Leson L, Martyn A, Nauen J, Grabenhorst N, Mandelkow JF, Zuccaro A, Zeier J, Kopriva S (2019) Root-specific camalexin biosynthesis controls the plant growth-promoting effects of multiple bacterial strains. Proc Natl Acad Sci USA 116:15735–15744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koprivova A, Volz V, Kopriva S (2020) Shoot-root interaction in control of camalexin exudation in Arabidopsis. bioRxiv. https://doi.org/10.1101/2020.12.15.422875

    Article  Google Scholar 

  • Kusch S, Larrouy J, Ibrahim HMM et al (2022) Transcriptional response to host chemical cues underpins the expansion of host range in a fungal plant pathogen lineage. ISME J 16:138–148

    Article  CAS  PubMed  Google Scholar 

  • Kwon YS, Lee DY, Rakwal R, Baek SB, Lee JH, Kwak YS et al (2016) Proteomic analyses of the interaction between the plant-growth promoting rhizobacterium Paenibacillus polymyxa E681 and Arabidopsis thaliana. Proteomics 16:122–135. https://doi.org/10.1002/pmic.201500196

    Article  CAS  PubMed  Google Scholar 

  • Lakkis S, Trotel-Aziz P, Rabenoelina F, Schwarzenberg A, Nguema-Ona E, Clément C, Aziz A (2019) Strengthening grapevine resistance by Pseudomonas fluorescens PTA-CT2 relies on distinct defense pathways in susceptible and partially resistant genotypes to downy mildew and gray mold diseases. Front Plant Sci 10:1112. https://doi.org/10.3389/fpls.2019.01112

    Article  PubMed  PubMed Central  Google Scholar 

  • Langcake P, Pryce RJ (1976) The production of resveratrol by Vitis vinifera and other members of the Vitaceae as a response to infection or injury. Physiol Plant Pathol 9:77–86

    Article  CAS  Google Scholar 

  • Lemarié S, Robert-Seilaniantz A, Lariagon C, Lemoine J, Marnet N, Levrel A et al (2015) Camalexin contributes to the partial resistance of Arabidopsis thaliana to the biotrophic soilborne protist Plasmodiophora brassicae. Front Plant Sci 6:539. https://doi.org/10.3389/fpls.2015.00539

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu S, Ziegler J, Zeier J, Birkenbihl RP, Somssich IE (2017) Botrytis cinerea B05.10 promotes disease development in Arabidopsis by suppressing WRKY33-mediated host immunity. Plant Cell Environ 40:2189–2206

    Article  CAS  PubMed  Google Scholar 

  • López MA, Bannenberg G, Castresana C (2008) Controlling hormone signaling is a plant and pathogen challenge for growth and survival. Curr Opin Plant Biol 11:420–427

    Article  PubMed  CAS  Google Scholar 

  • Luczak S, Forlani F, Papenbrock J (2013) Desulfo-glucosinolate sulfotransferases isolated from several Arabidopsis thaliana ecotypes differ in their sequence and enzyme kinetics. Plant Physiol Biochem 63:15–23

    Article  CAS  PubMed  Google Scholar 

  • Mao G, Meng X, Liu Y, Zheng Z, Chen Z, Zhang S (2011) Phosphorylation of a WRKY transcription factor by two pathogen-responsive MAPKs drives phytoalexin biosynthesis in Arabidopsis. Plant Cell 23:1639–1653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mersmann S, Bourdais G, Rietz S, Robatzek S (2010) Ethylene signaling regulates accumulation of the FLS2 receptor and is required for the oxidative burst contributing to plant immunity. Plant Physiol 154:391–400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mert-Türk F, Bennett MH, Mansfield JW, Holub EB (2003) Camalexin accumulation in Arabidopsis thaliana following abiotic elicitation or inoculation with virulent or avirulent Hyaloperonospora parasitica. Physiol Mol Plant Pathol 62:137–145

    Article  CAS  Google Scholar 

  • Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D et al (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22:973–990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mine A, Seyfferth C, Kracher B, Berens ML, Becker D, Tsuda K (2018) The defense phytohormone signaling network enables rapid, high-amplitude transcriptional reprogramming during effector-triggered immunity. Plant Cell 30:1199–1219

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moldrup ME, Geu-Flores F, Halkier BA (2013) Assigning gene function in biosynthetic pathways: camalexin and beyond. Plant Cell 25:360–367

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mucha S, Heinzlmeir S, Kriechbaumer V, Strickland B, Kirchhelle C, Choudhary M et al (2019) The formation of a camalexin-biosynthetic metabolon. Plant Cell 31:2697–2710

    CAS  PubMed  PubMed Central  Google Scholar 

  • Müller KO, Borger H (1940) Experimentelle untersuchungen über die Phytophtora-resistenz der kartoffel zugleich ein beitrag zum problem der «erworbenen resistenz» in pflanzenreich. Arb Aus Der Biol Reichsanstalt Land-Und Forst-Wirtschaft 23:189–231

    Google Scholar 

  • Müller TM, Böttcher C, Morbitzer R, Götz CC, Lehmann J, Lahaye T et al (2015) Transcription activator-like effector nuclease-mediated generation and metabolic analysis of camalexin-deficient cyp71a12 cyp71a13 double knockout lines. Plant Physiol 168:849–858

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, Halkier BA et al (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19:2039–2052

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narusaka Y, Narusaka M, Park P, Kubo Y, Hirayama T, Seki M et al (2004) RCH1, a locus in Arabidopsis that confers resistance to the hemibiotrophic fungal pathogen Colletotrichum higginsianum. Mol Plant-Microbe Interact 17:749–762

    Article  CAS  PubMed  Google Scholar 

  • Nguyen NH, Trotel-Aziz P, Villaume S, Rabenoelina F, Clement C, Baillieul F, Aziz A (2022) Priming of camalexin accumulation in induced systemic resistance by beneficial bacteria against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000. J Exp Bot. https://doi.org/10.1093/jxb/erac070

    Article  PubMed  Google Scholar 

  • Pandey SP, Roccaro M, Schön M, Logemann E, Somssich IE (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64:912–923

    Article  CAS  PubMed  Google Scholar 

  • Pangesti N, Reichelt M, van de Mortel JE, Kapsomenou E, Gershenzon J, van Loon JJA et al (2016) Jasmonic acid and ethylene signaling pathways regulate glucosinolate levels in plants during rhizobacteria-induced systemic resistance against a leaf-chewing herbivore. J Chem Ecol 42:1212–1225

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patra B, Schluttenhofer C, Wu Y, Pattanaik S, Yuan L (2013) Transcriptional regulation of secondary metabolite biosynthesis in plants. Biochim Biophys Acta 1829:1236–1247

    Article  CAS  PubMed  Google Scholar 

  • Pedras MSC, Abdoli A (2013) Metabolism of the phytoalexins camalexins, their bioisosteres and analogues in the plant pathogenic fungus Alternaria brassicicola. Bioorg Med Chem 21:4541–4549

    Article  CAS  PubMed  Google Scholar 

  • Pedras MSC, Ahiahonu PWK (2005) Metabolism and detoxification of phytoalexins and analogs by phytopathogenic fungi. Phytochemistry 66:391–411

    Article  CAS  PubMed  Google Scholar 

  • Pedras MS, Khan AQ (2000) Biotransformation of the phytoalexin camalexin by the phytopathogen Rhizoctonia solani. Phytochemistry 53:59–69

    Article  CAS  PubMed  Google Scholar 

  • Pedras MSC, Chumala PB, Jin W, Islam MS, Hauck DW (2009) The phytopathogenic fungus Alternaria brassicicola: phytotoxin production and phytoalexin elicitation. Phytochemistry 70:394–402

    Article  CAS  PubMed  Google Scholar 

  • Pedras MSC, Hossain S, Snitynsky RB (2011) Detoxification of cruciferous phytoalexins in Botrytis cinerea: spontaneous dimerization of a camalexin metabolite. Phytochemistry 72:199–206

    Article  CAS  PubMed  Google Scholar 

  • Pedras MS, Minic Z, Abdoli A (2014) The phytoalexin camalexin induces fundamental changes in the proteome of Alternaria brassicicola different from those caused by brassinin. Phytochemistry 53:59–69

    Article  Google Scholar 

  • Peskan-Berghöfer T, Vilches-Barro A, Müller TM, Glawischnig E, Reichelt M, Gershenzon J et al (2015) Sustained exposure to abscisic acid enhances the colonization potential of the mutualist fungus Piriformospora indica on Arabidopsis thaliana roots. New Phytol 208:873–886

    Article  PubMed  CAS  Google Scholar 

  • Piasecka A, Jedrzejczak-Rey N, Bednarek P (2015) Secondary metabolites in plant innate immunity: conserved function of divergent chemicals. New Phytol 206:948–964

    Article  PubMed  Google Scholar 

  • Pieterse CMJ, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SCM (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

    Article  CAS  PubMed  Google Scholar 

  • Pieterse CMJ, Zamioudis C, Berendsen RL, Weller DM, Van Wees SCM, Bakker PAHM (2014) Induced systemic resistance by beneficial microbes. Annu Rev Phytopathol 52:347–375

    Article  CAS  PubMed  Google Scholar 

  • Qiu JL, Fiil BK, Petersen K, Nielsen HB, Botanga CJ, Thorgrimsen S et al (2008) Arabidopsis MAP kinase 4 regulates gene expression through transcription factor release in the nucleus. EMBO J 27:2214–2221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ren D, Liu Y, Yang K, Han L, Mao G, Glazebrook J et al (2008) A fungal-responsive MAPK cascade regulates phytoalexin biosynthesis in Arabidopsis. Proc Natl Acad Sci USA 105:5638–5643

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reuber TL, Plotnikova JM, Dewdney J, Rogers EE, Wood W, Ausubel FM (1998) Correlation of defense gene induction defects with powdery mildew susceptibility in Arabidopsis enhanced disease susceptibility mutants. Plant J 16:473–485

    Article  CAS  PubMed  Google Scholar 

  • Robert-Seilaniantz A, MacLean D, Jikumaru Y, Hill L, Yamaguchi S, Kamiya Y et al (2011) The microRNA miR393 re-directs secondary metabolite biosynthesis away from camalexin and towards glucosinolates. Plant J 67:218–231

    Article  CAS  PubMed  Google Scholar 

  • Roetschi A, Si-Ammour A, Belbahri L, Mauch F, Mauch-Mani B (2001) Characterization of an Arabidopsis-Phytophthora pathosystem: resistance requires a functional pad2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. Plant J 28:293–305

    Article  CAS  PubMed  Google Scholar 

  • Rogers EE, Glazebrook J, Ausubel FM (1996) Mode of action of the Arabidopsis thaliana phytoalexin camalexin and its role in Arabidopsis-pathogen interactions. Mol Plant Microbe Interact 9:748–757

    Article  CAS  PubMed  Google Scholar 

  • Rosslenbroich HJ, Stuebler D (2000) Botrytis cinerea - history of chemical control and novel fungicides for its management. Crop Prot 19:557–561

    Article  CAS  Google Scholar 

  • Rowe HC, Walley JW, Corwin J, Chan EKF, Dehesh K, Kliebenstein DJ (2010) Deficiencies in Jasmonate-mediated plant defense reveal quantitative variation in Botrytis cinerea pathogenesis. PLoS Pathog 6:e1000861. https://doi.org/10.1371/journal.ppat.1000861

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saga H, Ogawa T, Kai K, Suzuki H, Ogata Y, Sakurai N et al (2012) Identification and characterization of ANAC042, a transcription factor family gene involved in the regulation of camalexin biosynthesis in Arabidopsis. Mol Plant-Microbe Interact 25:684–696

    Article  CAS  PubMed  Google Scholar 

  • Salas-Marina MA, Silva-Flores MA, Uresti-Rivera EE, Castro-Longoria E, Herrera-Estrella A, Casas-Flores S (2011) Colonization of Arabidopsis roots by Trichoderma atroviride promotes growth and enhances systemic disease resistance through jasmonic acid/ethylene and salicylic acid pathways. Eur J Plant Pathol 131:15–26

    Article  CAS  Google Scholar 

  • Sanchez-Vallet A, Ramos B, Bednarek P, López G, Piślewska-Bednarek M, Schulze-Lefert P et al (2010) Tryptophan-derived secondary metabolites in Arabidopsis thaliana confer non-host resistance to necrotrophic Plectosphaerella cucumerina fungi. Plant J 63:115–127

    CAS  PubMed  Google Scholar 

  • Saunders JA, O’neill NR, NR (2004) The characterization of defense responses to fungal infection in alfalfa. Biocontrol 6:715–728

    Article  Google Scholar 

  • Schlaeppi K, Abou-Mansour E, Buchala A, Mauch F (2010) Disease resistance of Arabidopsis to Phytophthora brassicae is established by the sequential action of indole glucosinolates and camalexin. Plant J 62:840–851

    Article  CAS  PubMed  Google Scholar 

  • Schmelz EA, Huffaker A, Sims JW, Christensen SA, Lu X, Okada K et al (2014) Biosynthesis, elicitation and roles of monocot terpenoid phytoalexins. Plant J 79:659–678

    Article  CAS  PubMed  Google Scholar 

  • Schuhegger R, Nafisi M, Mansourova M, Petersen BL, Olsen CE, Halkier BA et al (2006) CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol 141:1248–1254

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schuhegger R, Rauhut T, Glawischnig E (2007) Regulatory variability of camalexin biosynthesis. J Plant Physiol 164:636–644

    Article  CAS  PubMed  Google Scholar 

  • Sellam A, Dongo A, Guillemette T, Hudhomme P, Simoneau P (2007) Transcriptional responses to exposure to the brassicaceous defence metabolites camalexin and allyl-isothiocyanate in the necrotrophic fungus Alternaria brassicicola. Mol Plant Pathol 8:195–208

    Article  CAS  PubMed  Google Scholar 

  • Shlezinger N, Minz A, Gur Y, Hatam I, Dagdas YF, Talbot NJ (2011) Anti-apoptotic machinery protects the necrotrophic fungus Botrytis cinerea from host-induced apoptotic-like cell death during plant infection. PLoS Pathog 7:e1002185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith DA, Ingham JL (1980) Legumes, fungal pathogens, and phytoalexins. In: Sumrnerfield RJ, Bunting AH (eds) Advances in legume science. Royal Botanic Gardens, Kew, MAFF, London, pp 207–223

    Google Scholar 

  • Staal J, Kaliff M, Bohman S, Dixelius C (2006) Transgressive segregation reveals two Arabidopsis TIR-NB-LRR resistance genes effective against Leptosphaeria maculans, causal agent of blackleg disease. Plant J 46:218–230

    Article  CAS  PubMed  Google Scholar 

  • Stefanato FL, Abou-Mansour E, Buchala A, Kretschmer M, Mosbach A, Hahn M et al (2009) The ABC transporter BcatrB from Botrytis cinerea exports camalexin and is a virulence factor on Arabidopsis thaliana. Plant J 58:499–510

    Article  CAS  PubMed  Google Scholar 

  • Stotz HU, Sawada Y, Shimada Y, Hirai MY, Sasaki E, Krischke M et al (2011) Role of camalexin, indole glucosinolates, and side chain modification of glucosinolate-derived isothiocyanates in defense of Arabidopsis against Sclerotinia sclerotiorum. Plant J 67:81–93

    Article  CAS  PubMed  Google Scholar 

  • Stringlis IA, Proietti S, Hickman R, Van Verk MC, Zamioudis C, Pieterse CMJ (2018) Root transcriptional dynamics induced by beneficial rhizobacteria and microbial immune elicitors reveal signatures of adaptation to mutualists. Plant J 93:166–180

    Article  CAS  PubMed  Google Scholar 

  • Su T, Xu J, Li Y, Lei L, Zhao L, Yang H et al (2011) Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23:364–380

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Su T, Li Y, Yang H, Ren D (2013) Reply: complexity in camalexin biosynthesis. Plant Cell 25:367–370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thomma B, Nelissen I, Eggermont K, Broekaert W (1999) Deficiency in phytoalexin production causes enhanced susceptibility of Arabidopsis thaliana to the fungus Alternaria brassicicola. Plant J 19:163–171

    Article  CAS  PubMed  Google Scholar 

  • van de Mortel JE, de Vos RCH, Dekkers E, Pineda A, Guillod L, Bouwmeester K et al (2012) Metabolic and transcriptomic changes induced in Arabidopsis by the rhizobacterium Pseudomonas fluorescens SS101. Plant Physiol 160:2173–2188

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Van Wees SCM, Chang HS, Zhu T, Glazebrook J, VanWees SCM, Chang HS et al (2003) Characterization of the early response of Arabidopsis to Alternaria brassicicola infection using expression profiling. Plant Physiol 132:606–617

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Verhagen BWM, Glazebrook J, Zhu T, Chang HS, van Loon LC, Pieterse CMJ (2004) The transcriptome of rhizobacteria-induced systemic resistance in Arabidopsis. Mol Plant-Microbe Interact 17:895–908

    Article  CAS  PubMed  Google Scholar 

  • Verhagen BWM, Trotel-Aziz P, Couderchet M, Höfte M, Aziz A (2010) Pseudomonas spp.-induced systemic resistance to Botrytis cinerea is associated with induction and priming of defence responses in grapevine. J Exp Bot 61:249–260

    Article  CAS  PubMed  Google Scholar 

  • Verhagen B, Trotel-Aziz P, Jeandet P, Baillieul F, Aziz A (2011) Improved resistance against Botrytis cinerea by grapevine-associated bacteria that induce a prime oxidative burst and phytoalexin production. Phytopathology 101:768–777

    Article  CAS  PubMed  Google Scholar 

  • Wang MY, Liu XT, Chen Y, Xu XJ, Yu B, Zhang SQ et al (2012) Arabidopsis acetyl-amido synthetase GH3.5 involvement in camalexin biosynthesis through conjugation of indole-3-carboxylic acid and cysteine and upregulation of camalexin biosynthesis genes. J Integr Plant Biol 54:471–485

    Article  CAS  PubMed  Google Scholar 

  • Wink M (2013) Evolution of secondary metabolites in legumes (Fabaceae). South African J Bot 89:164–175

    Article  CAS  Google Scholar 

  • Xu G, Greene GH, Yoo H, Liu L, Marqués J, Motley J, Dong X (2017) Global translational reprogramming is a fundamental layer of immune regulation in plants. Nature 545:487–490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang Y, Wang G, Wu W, Yao S, Han X, He D et al (2018) Camalexin induces apoptosis via the ROS-ER stress-mitochondrial apoptosis pathway in AML cells. Oxid Med Cell Longev 2018:7426950

    PubMed  PubMed Central  Google Scholar 

  • Yoo H, Greene GH, Yuan M, Xu G, Burton D, Liu L, Marqués J, Dong X (2020) Translational regulation of metabolic dynamics during effector-triggered immunity. Mol Plant 13:88–98

    Article  CAS  PubMed  Google Scholar 

  • Zhai X, Chen L, Jia M, Zheng CJ, Rahman K, Han T et al (2017) The regulatory mechanism of fungal elicitor-induced secondary metabolite biosynthesis in medical plants. Crit Rev Microbiol 43:238–261

    Article  CAS  PubMed  Google Scholar 

  • Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 monooxygenase. Plant Cell 11:2419–2428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou J, Wang X, He Y, Sang T, Wang P, Dai S, Zhang S, Meng X (2020) Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. Plant Cell 32:2621–2638

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zook M, Hammerschmidt R (1997) Origin of the thiazole ring of camalexin, a phytoalexin from Arabidopsis thaliana. Plant Physiol 113:463–468

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank the Grand Est region and European Regional Development Fund (FEDER) for supporting this work. The grant to N-H.N. was supported by a research fellowship from Campus France through Vietnamese Government and Tay Nguyen University. We apologize to researchers whose studies were not included in this review owing to word and reference limits.

Funding

European Regional Development Fund.

Author information

Authors and Affiliations

  1. Induced Resistance and Plant Bioprotection, USC INRAE 1488, University of Reims, UFR Sciences, Campus Moulin de la Housse, 51687 Cedex 02, Reims, France

    Ngoc Huu Nguyen, Patricia Trotel-Aziz, Christophe Clément, Philippe Jeandet, Fabienne Baillieul & Aziz Aziz

  2. Department of Plant Biology, Faculty of Agriculture and Forestry, Tay Nguyen University, 567 Le Duan, Buon Ma Thuot, Daklak, Vietnam

    Ngoc Huu Nguyen

Authors
  1. Ngoc Huu Nguyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Patricia Trotel-Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christophe Clément
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Philippe Jeandet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fabienne Baillieul
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Aziz Aziz
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

NHN wrote the first draft of the manuscript with support from PTA, FB and AA. AA, PJ critically edited the manuscript. All authors contributed to the revisions, read and approved final version of manuscript.

Corresponding author

Correspondence to Aziz Aziz.

Additional information

Communicated by Gerhard Leubner.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Nguyen, N.H., Trotel-Aziz, P., Clément, C. et al. Camalexin accumulation as a component of plant immunity during interactions with pathogens and beneficial microbes. Planta 255, 116 (2022). https://doi.org/10.1007/s00425-022-03907-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s00425-022-03907-1

Keywords

Search

Navigation