Transcription activator-like effector nuclease-mediated generation and metabolic analysis of camalexin-deficient cyp71a12 cyp71a13 double knockout lines

Plant Physiology

Volumn 168, Issue 3, 2015, Pages 849-858

  Müller, Teresa M ^a   Böttcher, Christoph ^b   Morbitzer, Robert ^c   Götz, Cornelia C ^a   Lehmann, Johannes ^a   Lahaye, Thomas ^c   Glawischnig, Erich ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b INSTITUTE FOR EPIDEMIOLOGY AND PATHOGEN DIAGNOSTICS   (Germany)

^c UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ARABIDOPSIS PROTEIN; CAMALEXIN; CYTOCHROME P-450 71A12, ARABIDOPSIS; CYTOCHROME P-450 71A13 PROTEIN, ARABIDOPSIS; CYTOCHROME P450; DEOXYRIBONUCLEASE; INDOLE DERIVATIVE; INDOLE-3-ACETALDOXIME; INDOLE-3-ACETONITRILE; OXIME; THIAZOLE DERIVATIVE; TRANSACTIVATOR PROTEIN;

ARABIDOPSIS; BIOLOGICAL MODEL; DEFICIENCY; ENZYMOLOGY; GENE INACTIVATION; GENETICS; INHERITANCE; METABOLISM; METABOLOMICS; MOLECULAR GENETICS; MUTAGENESIS; MUTATION; NUCLEOTIDE SEQUENCE; SECONDARY METABOLISM;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BASE SEQUENCE; CYTOCHROME P-450 ENZYME SYSTEM; DEOXYRIBONUCLEASES; GENE KNOCKOUT TECHNIQUES; INDOLES; INHERITANCE PATTERNS; METABOLOMICS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTAGENESIS; MUTATION; OXIMES; SECONDARY METABOLISM; THIAZOLES; TRANS-ACTIVATORS;

EID: 84936139155     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00481     Document Type: Article

References (42)

1. Agerbirk N, De Vos M, Kim JH, Jander G (2008) Indole glucosinolate breakdown and its biological effects. Phytochem Rev 8: 101-120
2. Ahmad A, Eelnurme I, Spenser I (1960) Indolyl-3-acetaldoxime. Can J Chem 38: 2523
3. Bartling D, Seedorf M, Mith6fer A, Weiler E W (1992) Cloning and expression of an Arabidopsis nitrilase which can convert indole-3-acetonitrile to the plant hormone, indole-3-acetic acid. Eur J Biochem 205: 417-424
4. Bednarek P, Pislewska-Bednarek M, Svatos A, Schneider B, Doubsky J, Mansurova M, Humphry M, Consonni C, Panstruga R, Sanchez-Vallet A, et al (2009) A glucosinolate metabolism pathway in living plant cells mediates broad-spectrum antifungal defense. Science 323: 101-106
5. 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
6. Bolle C, Schneider A, Leister D (2011) Perspectives on systematic analyses of gene function in Arabidopsis thaliana: new tools, topics and trends. Curr Genomics 12: 1-14
7. Böttcher 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
8. Böttcher 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
9. Christian M, Cermak T, Doyle E L, Schmidt C, Zhang F, Hummel A, Bogdanove A J, Voytas D F (2010) Targeting DNA double-strand breaks with TAL effector nucleases. Genetics 186: 757-761
10. Christian M, Qi Y, Zhang Y, Voytas D F (2013) Targeted mutagenesis of Arabidopsis thaliana using engineered TAL effector nucleases. G3 (Bethesda) 3: 1697-1705
11. Clay NK, Adio AM, Denoux C, Jander G, Ausubel FM (2009) Glucosi-nolate metabolites required for an Arabidopsis innate immune response. Science 323: 95-101
12. Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16: 735-743
13. deLange O, Wolf C, Dietze J, Elsaesser J, Morbitzer R, Lahaye T (2014) Programmable DNA-binding proteins from Burkholderia provide a fresh perspective on the TALE-like repeat domain. Nucleic Acids Res 42: 7436-7449
14. de Vos M, Kriksunov KL, Jander G (2008) Indole-3-acetonitrile production from indole glucosinolates deters oviposition by Vieris rapae. Plant Physiol 146: 916-926
15. Eisenthal R, Danson MJ, Hough DW (2007) Catalytic efficiency and kcat/ KM: a useful comparator? Trends Biotechnol 25: 247-249
16. Geu-Flores F, Moldrup ME, Böttcher C, Olsen CE, Scheel D, Halkier BA (2011) Cytosolic g-glutamyl peptidases process glutathione conjugates in the biosynthesis of glucosinolates and camalexin in Arabidopsis. Plant Cell 23: 2456-2469
17. 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
18. 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
19. Hagemeier J, Schneider B, Oldham NJ, Hahlbrock K (2001) Accumulation of soluble and wall-bound indolic metabolites in Arabidopsis thaliana leaves infected with virulent or avirulent Pseudomonas syringae path-ovar tomato strains. Proc Natl Acad Sci USA 98: 753-758
20. Hofberger JA, Lyons E, Edger PP, Pires JC, Schranz ME (2013) Whole genome and tandem duplicate retention facilitated glucosinolate pathway diversification in the mustard family. Genome Biol Evol 5: 2155-2173
21. Hoshaw JP, Unger-Wallace E, Zhang F, Voytas DF (2010) A transient assay for monitoring zinc finger nuclease activity at endogenous plant gene targets. Methods Mol Biol 649: 299-313
22. Iven T, König S, Singh S, Braus-Stromeyer SA, Bischoff M, Tietze LF, Braus GH, Lipka V, Feussner I, Dröge-Laser W (2012) Transcriptional activation and production of tryptophan-derived secondary metabolites in Arabidopsis roots contributes to the defense against the fungal vascular pathogen Verticillium longisporum. Mol Plant 5: 1389-1402
23. Joung JK, Sander JD (2013) TALENs: a widely applicable technology for targeted genome editing. Nat Rev Mol Cell Biol 14: 49-55
24. Klein AP, Anarat-Cappillino G, Sattely ES (2013) Minimum set of cyto-chromes P450 for reconstituting the biosynthesis of camalexin, a major Arabidopsis antibiotic. Angew Chem Int Ed Engl 52: 13625-13628
25. Kriechbaumer V, Park WJ, Piotrowski M, Meeley RB, Gierl A, Glawischnig E (2007) Maize nitrilases have a dual role in auxin ho-meostasis and beta-cyanoalanine hydrolysis. J Exp Bot 58: 4225-4233
26. Millet YA, Danna CH, Clay NK, Songnuan W, Simon MD, Werck-Reichhart D, Ausubel FM (2010) Innate immune responses activated in Arabidopsis roots by microbe-associated molecular patterns. Plant Cell 22: 973-990
27. Moldrup ME, Salomonsen B, Geu-Flores F, Olsen CE, Halkier BA (2013) De novo genetic engineering of the camalexin biosynthetic pathway. J Biotechnol 167: 296-301
28. Morbitzer R, Elsaesser J, Hausner J, Lahaye T (2011) Assembly of custom TALE-type DNA binding domains by modular cloning. Nucleic Acids Res 39: 5790-5799
29. Mussolino C, Morbitzer R, Lütge F, Dannemann N, Lahaye T, Cathomen T (2011) A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 39: 9283-9293
30. Nafisi M, Goregaoker S, Botanga CJ, Glawischnig E, Olsen CE, Halkier BA, Glazebrook J (2007) Arabidopsis cytochrome P450 monooxygenase 71A13 catalyzes the conversion of indole-3-acetaldoxime in camalexin synthesis. Plant Cell 19: 2039-2052
31. Normanly J, Grisafi P, Fink GR, Bartel B (1997) Arabidopsis mutants resistant to the auxin effects of indole-3-acetonitrile are defective in the nitrilase encoded by the NIT1 gene. Plant Cell 9: 1781-1790
32. Nour-Eldin HH, Hansen BG, Norholm MH, Jensen JK, Halkier BA (2006) Advancing uracil-excision based cloning towards an ideal technique for cloning PCR fragments. Nucleic Acids Res 34: e122
33. Omura T, Sato R (1964) The carbon monoxide-binding pigment of liver microsomes. I. Evidence for its hemoprotein nature. J Biol Chem 239: 2370-2378
34. Parisy V, Poinssot B, Owsianowski L, Buchala A, Glazebrook J, Mauch F (2007) Identification of PAD2 as a gamma-glutamylcysteine synthetase highlights the importance of glutathione in disease resistance of Arabidopsis. Plant J 49: 159-172
35. Pedras MS, Yaya EE, Glawischnig E (2011) The phytoalexins from cultivated and wild crucifers: chemistry and biology. Nat Prod Rep 28: 1381-1405
36. Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol 272: 51-64
37. Rauhut T, Glawischnig E (2009) Evolution of camalexin and structurally related indolic compounds. Phytochemistry 70: 1638-1644
38. Schuhegger R, Nafisi M, Mansourova M, Petersen BL, Olsen CE, Svatos A, Halkier BA, Glawischnig E (2006) CYP71B15 (PAD3) catalyzes the final step in camalexin biosynthesis. Plant Physiol 141: 1248-1254
39. Su T, Xu J, Li Y, Lei L, Zhao L, Yang H, Feng J, Liu G, Ren D (2011) Glutathione-indole-3-acetonitrile is required for camalexin biosynthesis in Arabidopsis thaliana. Plant Cell 23: 364-380
40. Weber E, Engler C, Gruetzner R, Werner S, Marillonnet S (2011) A modular cloning system for standardized assembly of multigene constructs. PLoS ONE 6: e16765
41. Zhao Y, Hull AK, Gupta NR, Goss KA, Alonso J, Ecker JR, Normanly J, Chory J, Celenza JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16: 3100-3112
42. Zhou N, Tootle TL, Glazebrook J (1999) Arabidopsis PAD3, a gene required for camalexin biosynthesis, encodes a putative cytochrome P450 mono-oxygenase. Plant Cell 11: 2419-2428