Detoxification of α-tomatine by Cladosporium fulvum is required for full virulence on tomato

New Phytologist

Volumn 198, Issue 4, 2013, Pages 1203-1214

  ̈kmen, Bilal ^a   Etalo, Desalegn W ^a,b,c   Joosten, Matthieu H A J ^a,b   Bouwmeester, Harro J ^a,b   de Vos, Ric C H ^a,b,c   Collemare, Jérôme ^a,b   De Wit, Pierre J G M ^a,b  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b CENTRE FOR BIOSYSTEMS GENOMICS   (Netherlands)

^c Netherlands Metabolomics Centre   (Netherlands)

Author keywords

Basal defense; Glycoalkaloids; Glycosyl hydrolase family 10 (GH10); Saponin; Tomatidine; Tomatinase

Indexed keywords

ALPHA-TOMATINE; DRUG DERIVATIVE; FUNGAL PROTEIN; GLYCOSIDASE; TOMATIDINE; TOMATINASE; TOMATINE;

ALKALOID; ANTIMICROBIAL ACTIVITY; BIOCHEMISTRY; BIODEGRADATION; DETOXIFICATION; ENZYME; FUNCTIONAL ROLE; FUNGUS; MOLECULAR ANALYSIS; PLANT DEFENSE; SECRETION; VEGETABLE; VIRULENCE;

ARTICLE; CHEMISTRY; CLADOSPORIUM; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYLOGENY; PLANT LEAF; TOMATO; VIRULENCE;

CLADOSPORIUM; FUNGAL PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, FUNGAL; GLYCOSIDE HYDROLASES; LYCOPERSICON ESCULENTUM; MUTATION; PHYLOGENY; PLANT LEAVES; TOMATINE; VIRULENCE;

CLADOSPORIUM; CLADOSPORIUM FULVUM; FUNGI; LYCOPERSICON ESCULENTUM;

EID: 84877623067     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12208     Document Type: Article

References (44)

1. Arneson PA, Durbin RD. 1967. Hydrolysis of tomatine by Septoria lycopersici - a detoxification mechanism. Phytopathology 57: 1358-1360.
2. Bouarab K, Melton R, Peart J, Baulcombe D, Osbourn A. 2002. A saponin-detoxifying enzyme mediates suppression of plant defences. Nature 418: 889-892.
3. Bowyer P, Clarke BR, Lunness P, Daniels MJ, Osbourn AE. 1995. Host-range of a plant-pathogenic fungus determined by a saponin detoxifying enzyme. Science 267: 371-374.
4. De Vos RCH, Moco S, Lommen A, Keurentjes JJB, Bino RJ, Hall RD. 2007. Untargeted large-scale plant metabolomics using liquid chromatography coupled to mass spectrometry. Nature Protocols 2: 778-791.
5. Dow JM, Callow JA. 1978. A possible role for α-tomatine in the varietal-specific resistance of tomato to Cladosporium fulvum. Phytopatholgische Zeitschrift 92: 211-216.
6. van Esse HP, van't Klooster JW, Bolton MD, Yadeta KA, van Baarlen P, Boeren S, Vervoort J, de Wit PJGM, Thomma BPHJ. 2008. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. Plant Cell 20: 1948-1963.
7. Ford JE, McCance DJ, Drysdale RB. 1977. The detoxification of α-tomatine by Fusarium oxysporum f. sp. lycopersici. Phytochemistry 16: 545-546.
8. Hammerschmidt R, Lamport DTA, Muldoon EP. 1984. Cell-wall hydroxyproline enhancement and lignin deposition as an early event in the resistance of cucumber to Cladosporium cucumerinum. Physiological Plant Pathology 24: 43-47.
9. Hammond-Kosack KE, Staskawicz BJ, Jones JDG, Baulcombe DC. 1995. Functional expression of a fungal avirulence gene from a modified potato-virus-x genome. Molecular Plant-Microbe Interactions 8: 181-185.
10. van der Hooft JJJ, Vervoort J, Bino RJ, Beekwilder J, de Vos RCH. 2011. Polyphenol identification based on systematic and robust high-resolution accurate mass spectrometry fragmentation. Analytical Chemistry 83: 409-416.
11. Iijima Y, Nakamura Y, Ogata Y, Tanaka K, Sakurai N, Suda K, Suzuki T, Suzuki H, Okazaki K, Kitayama M et al. 2008. Metabolite annotations based on the integration of mass spectral information. Plant Journal 54: 949-962.
12. Itkin M, Rogachev I, Alkan N, Rosenberg T, Malitsky S, Masini L, Meir S, Iijima Y, Aoki K, de Vos R et al. 2011. Glycoalkaloid metabolism1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23: 4507-4525.
13. Ito S, Eto T, Tanaka S, Yamauchi N, Takahara H, Ikeda T. 2004. Tomatidine and lycotetraose, hydrolysis products of alpha-tomatine by Fusarium oxysporum tomatinase, suppress induced defense responses in tomato cells. FEBS Letters 571: 31-34.
14. Kaup O, Grafen I, Zellermann EM, Eichenlaub R, Gartemann KH. 2005. Identification of a tomatinase in the tomato-pathogenic actinomycete Clavibacter michiganensis subsp michiganensis NCPPB382. Molecular Plant-Microbe Interactions 18: 1090-1098.
15. Keukens EAJ, de Vrije T, van den Boom C, de Waard P, Plasman HH, Thiel F, Chupin V, Jongen WMF, de Kruijff B. 1995. Molecular basis of glycoalkaloid induced membrane disruption. Biochimica et Biophysica Acta (BBA) - Biomembranes 1240: 216-228.
16. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R et al. 2007. Clustal W and clustal X version 2.0. Bioinformatics 23: 2947-2948.
17. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method. Methods 25: 402-408.
18. Lommen A. 2009. MetAlign: interface-driven, versatile metabolomics tool for hyphenated full-scan mass spectrometry data preprocessing. Analytical Chemistry 81: 3079-3086.
19. Markham KR, Gould KS, Ryan KG. 2001. Cytoplasmic accumulation of flavonoids in flower petals and its relevance to yellow flower colouration. Phytochemistry 58: 403-413.
20. Marrs KA, Alfenito MR, Lloyd AM, Walbot V. 1995. A glutathione-S-transferase involved in vacuolar transfer encoded by the maize gene Bronze-2. Nature 375: 397-400.
21. Martin-Hernandez AM, Dufresne M, Hugouvieux V, Melton R, Osbourn A. 2000. Effects of targeted replacement of the tomatinase gene on the interaction of Septoria lycopersici with tomato plants. Molecular Plant-Microbe Interactions 13: 1301-1311.
22. Melton RE, Flegg LM, Brown JKM, Oliver RP, Daniels MJ, Osbourn AE. 1998. Heterologous expression of Septoria lycopersici tomatinase in Cladosporium fulvum: effects on compatible and incompatible interactions with tomato seedlings. Molecular Plant-Microbe Interactions 11: 228-236.
23. Moco S, Bino RJ, Vorst O, Verhoeven HA, de Groot J, van Beek TA, Vervoort J, de Vos CHR. 2006. A liquid chromatography-mass spectrometry-based metabolome database for tomato. Plant Physiology 141: 1205-1218.
24. Nicholas KB, Nicholas HB, Deerfield DW. 1997. GeneDoc: analysis and visualization of genetic variation. Embnew.news 4: 14.
25. Osbourn A. 1996. Saponins and plant defence - a soap story. Trends in Plant Science 1: 4-9.
26. Osbourn A, Bowyer P, Lunness P, Clarke B, Daniels M. 1995. Fungal pathogens of oat roots and tomato leaves employ closely related enzymes to detoxify different host plant saponins. Molecular Plant-Microbe Interactions 8: 971-978.
27. Pareja-Jaime Y, Roncero MIG, Ruiz-Roldan MC. 2008. Tomatinase from Fusarium oxysporum f. sp lycopersici is required for full virulence on tomato plants. Molecular Plant-Microbe Interactions 21: 728-736.
28. Quidde T, Osbourn AE, Tudzynski P. 1998. Detoxification of α-tomatine by Botrytis cinerea. Physiological and Molecular Plant Pathology 52: 151-165.
29. Roddick JG. 1977. Subcellular localization of steroidal glycoalkaloids in vegetative organs of Lycopersicon esculentum and Solanum tuberosum. Phytochemistry 16: 805-807.
30. Roddick JG, Drysdale RB. 1984. Destabilization of liposome membranes by the steroidal glycoalkaloid alpha-tomatine. Phytochemistry 23: 543-547.
31. Roldan-Arjona T, Perez-Espinosa A, Ruiz-Rubio M. 1999. Tomatinase from Fusarium oxysporum f. sp lycopersici defines a new class of saponinases. Molecular Plant-Microbe Interactions 12: 852-861.
32. Sandrock RW, Vanetten HD. 2001. The relevance of tomatinase activity in pathogens of tomato: disruption of the beta(2)-tomatinase gene in Colletotrichum coccodes and Septoria lycopersici and heterologous expression of the Septoria lycopersici beta(2)-tomatinase in Nectria haematococca, a pathogen of tomato fruit. Physiological and Molecular Plant Pathology 58: 159-171.
33. Seipke RF, Loria R. 2008. Streptomyces scabies 87-22 possesses a functional tomatinase. Journal of Bacteriology 190: 7684-7692.
34. Steel CC, Drysdale RB. 1988. Electrolyte leakage from plant and fungal tissues and disruption of liposome membranes by α-tomatine. Phytochemistry 27: 1025-1030.
35. Stergiopoulos I, de Wit PJGM. 2009. Fungal effector proteins. Annual Review of Phytopathology 47: 233-263.
36. Stergiopoulos I, van den Burg HA, Ökmen B, Beenen HG, van Liere S, Kema GHJ, de Wit PJGM. 2010. Tomato Cf resistance proteins mediate recognition of cognate homologous effectors from fungi pathogenic on dicots and monocots. Proceedings of the National Academy of Sciences, USA 107: 7610-7615.
37. Takken FLW, Lu R. 2001. A functional cloning strategy, based on a binary PVX-expression vector, to isolate HR-inducing cDNAs of plant pathogens (vol 24, pg 275, 2000). Plant Journal 26: 363.
38. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 28: 2731-2739.
39. Tikunov YM, de Vos RCH, González Paramás AM, Hall RD, Bovy AG. 2010. A role for differential glycoconjugation in the emission of phenylpropanoid volatiles from tomato fruit discovered using a metabolic data fusion approach. Plant Physiology 152: 55-70.
40. Untergasser A, Nijveen H, Rao X, Bisseling T, Geurts R, Leunissen JAM. 2007. Primer3Plus, an enhanced web interface to Primer3. Nucleic Acids Research 35: W71-W74.
41. de Wit PJGM, Mehrabi R, van den Burg HA, Stergiopoulos I. 2009. Fungal effector proteins: past, present and future. Molecular Plant Pathology 10: 735-747.
42. de Wit PJGM, Spikman G. 1982. Evidence for the occurrence of race and cultivar-specific elicitors of necrosis in intercellular fluids of compatible interactions of Cladosporium fulvum and tomato. Physiological Plant Pathology 21: 1-11.
43. de Wit PJGM, van der Burgt A, Ökmen B, Stergiopoulos I, Abd-Elsalam K, Aerts AL, Bahkali AHA, Beenen H, Chettri P, Cox MP et al. 2012. The genomes of the fungal plant pathogens Cladosporium fulvum and Dothistroma septosporum reveal adaptation to different hosts and lifestyles but also signatures of common ancestry. PLoS Genetics 8: e1003088.
44. Zwiers LH, De Waard MA. 2001. Efficient Agrobacterium tumefaciens-mediated gene disruption in the phytopathogen Mycosphaerella graminicola. Current Genetics 39: 388-393.