A Barley UDP-glucosyltransferase Inactivates Nivalenol and Provides Fusarium Head Blight Resistance in Transgenic Wheat

Overview

Journal J Exp Bot

Publisher Oxford University Press

Specialty Biology

Date 2017 Apr 14

PMID 28407119

Citations 27

Authors

Xin Li

Herbert Michlmayr

Wolfgang Schweiger

Alexandra Malachova

Sanghyun Shin

Yadong Huang

Yanhong Dong

Gerlinde Wiesenberger

Susan McCormick

Marc Lemmens

Philipp Fruhmann

Christian Hametner

Franz Berthiller

Gerhard Adam

Gary J Muehlbauer

Affiliations

Soon will be listed here.

Abstract

Fusarium Head Blight is a disease of cereal crops that causes severe yield losses and mycotoxin contamination of grain. The main causal pathogen, Fusarium graminearum, produces the trichothecene toxins deoxynivalenol or nivalenol as virulence factors. Nivalenol-producing isolates are most prevalent in Asia but co-exist with deoxynivalenol producers in lower frequency in North America and Europe. Previous studies identified a barley UDP-glucosyltransferase, HvUGT13248, that efficiently detoxifies deoxynivalenol, and when expressed in transgenic wheat results in high levels of type II resistance against deoxynivalenol-producing F. graminearum. Here we show that HvUGT13248 is also capable of converting nivalenol into the non-toxic nivalenol-3-O-β-d-glucoside. We describe the enzymatic preparation of a nivalenol-glucoside standard and its use in development of an analytical method to detect the nivalenol-glucoside conjugate. Recombinant Escherichia coli expressing HvUGT13248 glycosylates nivalenol more efficiently than deoxynivalenol. Overexpression in yeast, Arabidopsis thaliana, and wheat leads to increased nivalenol resistance. Increased ability to convert nivalenol to nivalenol-glucoside was observed in transgenic wheat, which also exhibits type II resistance to a nivalenol-producing F. graminearum strain. Our results demonstrate the HvUGT13248 can act to detoxify deoxynivalenol and nivalenol and provide resistance to deoxynivalenol- and nivalenol-producing Fusarium.

Citing Articles

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References

Pasquali M, Beyer M, Logrieco A, Audenaert K, Balmas V, Basler R . A European Database of Fusarium graminearum and F. culmorum Trichothecene Genotypes. Front Microbiol. 2016; 7:406. PMC: 4821861. DOI: 10.3389/fmicb.2016.00406. View

Maul R, Warth B, Schebb N, Krska R, Koch M, Sulyok M . In vitro glucuronidation kinetics of deoxynivalenol by human and animal microsomes and recombinant human UGT enzymes. Arch Toxicol. 2014; 89(6):949-60. DOI: 10.1007/s00204-014-1286-7. View

Cheat S, Gerez J, Cognie J, Alassane-Kpembi I, Bracarense A, Raymond-Letron I . Nivalenol has a greater impact than deoxynivalenol on pig jejunum mucosa in vitro on explants and in vivo on intestinal loops. Toxins (Basel). 2015; 7(6):1945-61. PMC: 4488683. DOI: 10.3390/toxins7061945. View

Poapolathep A, Sugita-Konishi Y, Doi K, Kumagai S . The fates of trichothecene mycotoxins, nivalenol and fusarenon-X, in mice. Toxicon. 2003; 41(8):1047-54. DOI: 10.1016/s0041-0101(03)00089-8. View

Boenisch M, Schafer W . Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol. 2011; 11:110. PMC: 3166921. DOI: 10.1186/1471-2229-11-110. View

Ward T, Clear R, Rooney A, ODonnell K, Gaba D, Patrick S . An adaptive evolutionary shift in Fusarium head blight pathogen populations is driving the rapid spread of more toxigenic Fusarium graminearum in North America. Fungal Genet Biol. 2007; 45(4):473-84. DOI: 10.1016/j.fgb.2007.10.003. View

Maier F, Miedaner T, Hadeler B, Felk A, Salomon S, Lemmens M . Involvement of trichothecenes in fusarioses of wheat, barley and maize evaluated by gene disruption of the trichodiene synthase (Tri5) gene in three field isolates of different chemotype and virulence. Mol Plant Pathol. 2010; 7(6):449-61. DOI: 10.1111/j.1364-3703.2006.00351.x. View

Lim E, Ashford D, Hou B, Jackson R, Bowles D . Arabidopsis glycosyltransferases as biocatalysts in fermentation for regioselective synthesis of diverse quercetin glucosides. Biotechnol Bioeng. 2004; 87(5):623-31. DOI: 10.1002/bit.20154. View

Alexander N, McCormick S, Waalwijk C, van der Lee T, Proctor R . The genetic basis for 3-ADON and 15-ADON trichothecene chemotypes in Fusarium. Fungal Genet Biol. 2011; 48(5):485-95. DOI: 10.1016/j.fgb.2011.01.003. View

10.

Varga E, Wiesenberger G, Hametner C, Ward T, Dong Y, Schofbeck D . New tricks of an old enemy: isolates of Fusarium graminearum produce a type A trichothecene mycotoxin. Environ Microbiol. 2014; 17(8):2588-600. PMC: 4950012. DOI: 10.1111/1462-2920.12718. View

11.

Ryu J, Ohtsubo K, Izumiyama N, Nakamura K, Tanaka T, Yamamura H . The acute and chronic toxicities of nivalenol in mice. Fundam Appl Toxicol. 1988; 11(1):38-47. DOI: 10.1016/0272-0590(88)90268-0. View

12.

Gardiner S, Boddu J, Berthiller F, Hametner C, Stupar R, Adam G . Transcriptome analysis of the barley-deoxynivalenol interaction: evidence for a role of glutathione in deoxynivalenol detoxification. Mol Plant Microbe Interact. 2010; 23(7):962-76. DOI: 10.1094/MPMI-23-7-0962. View

13.

Nagl V, Woechtl B, Schwartz-Zimmermann H, Hennig-Pauka I, Moll W, Adam G . Metabolism of the masked mycotoxin deoxynivalenol-3-glucoside in pigs. Toxicol Lett. 2014; 229(1):190-7. DOI: 10.1016/j.toxlet.2014.06.032. View

14.

Gratz S, Dinesh R, Yoshinari T, Holtrop G, Richardson A, Duncan G . Masked trichothecene and zearalenone mycotoxins withstand digestion and absorption in the upper GI tract but are efficiently hydrolyzed by human gut microbiota in vitro. Mol Nutr Food Res. 2016; 61(4). DOI: 10.1002/mnfr.201600680. View

15.

Jansen C, von Wettstein D, Schafer W, Kogel K, Felk A, Maier F . Infection patterns in barley and wheat spikes inoculated with wild-type and trichodiene synthase gene disrupted Fusarium graminearum. Proc Natl Acad Sci U S A. 2005; 102(46):16892-7. PMC: 1283850. DOI: 10.1073/pnas.0508467102. View

16.

Wetterhorn K, Newmister S, Caniza R, Busman M, McCormick S, Berthiller F . Crystal Structure of Os79 (Os04g0206600) from Oryza sativa: A UDP-glucosyltransferase Involved in the Detoxification of Deoxynivalenol. Biochemistry. 2016; 55(44):6175-6186. DOI: 10.1021/acs.biochem.6b00709. View

17.

Shin S, Torres-Acosta J, Heinen S, McCormick S, Lemmens M, Kovalsky Paris M . Transgenic Arabidopsis thaliana expressing a barley UDP-glucosyltransferase exhibit resistance to the mycotoxin deoxynivalenol. J Exp Bot. 2012; 63(13):4731-40. PMC: 3428005. DOI: 10.1093/jxb/ers141. View

18.

Caputi L, Malnoy M, Goremykin V, Nikiforova S, Martens S . A genome-wide phylogenetic reconstruction of family 1 UDP-glycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J. 2011; 69(6):1030-42. DOI: 10.1111/j.1365-313X.2011.04853.x. View

19.

Sampietro D, Ficoseco M, Jimenez C, Vattuone M, Catalan C . Trichothecene genotypes and chemotypes in Fusarium graminearum complex strains isolated from maize fields of northwest Argentina. Int J Food Microbiol. 2011; 153(1-2):229-33. DOI: 10.1016/j.ijfoodmicro.2011.10.029. View

20.

Rocco C, Dennison K, Klenchin V, Rayment I, Escalante-Semerena J . Construction and use of new cloning vectors for the rapid isolation of recombinant proteins from Escherichia coli. Plasmid. 2008; 59(3):231-7. PMC: 2386272. DOI: 10.1016/j.plasmid.2008.01.001. View