Abstract
Deoxynivalenol (DON) is a prominent mycotoxin showing significant accumulation in cereal plants during infection by the phytopathogen Fusarium graminearum. It is a virulence factor that is important in the spread of F. graminearum within cereal heads, and it causes serious yield losses and significant contamination of cereal grains. In recent decades, genetic and genomic studies have facilitated the characterization of the molecular pathways of DON biosynthesis in F. graminearum and the environmental factors that influence DON accumulation. In addition, diverse scab resistance traits related to the repression of DON accumulation in plants have been identified, and experimental studies of wheat–pathogen interactions have contributed to understanding detoxification mechanisms in host plants. The present review illustrates and summarizes the molecular networks of DON mycotoxin production in F. graminearum and the methods of DON detoxification in plants based on the current literature, which provides molecular targets for crop improvement programs. This review also comprehensively discusses recent advances and challenges related to genetic engineering-mediated cultivar improvements to strengthen scab resistance. Furthermore, ongoing advancements in genetic engineering will enable the application of these molecular targets to develop more scab-resistant wheat cultivars with DON detoxification traits.
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References
Ahmed P, Jaleel CA, Azooz MM, Nabi G (2009) Generation of ROS and nonenzymatic antioxidants during abiotic stress in plants. Bot Res Int 2:11–20
Akohoue F, Koch S, Plieske J, Miedaner T (2022) Separation of the effects of two reduced height (Rht) genes and genomic background to select for less Fusarium head blight of short-strawed winter wheat (Triticum aestivum L.) varieties. Theor Appl Genet 135:4303–4326. https://doi.org/10.1007/s00122-022-04219-4
Alexander NJ, Hohn TM, McCormick SP (1998) The tri11 gene of Fusarium sporotrichioides encodes a cytochrome P-450 monooxygenase required for C-15 hydroxylation in trichothecene biosynthesis. Appl Environ Microb 64:221–225. https://doi.org/10.1128/AEM.64.1.221-225.1998
Alexander NJ, McCormick SP, Waalwijk C, van der Lee T, Proctor RH (2011) The genetic basis for 3-ADON and 15-ADON trichothecene chemotypes in Fusarium. Fungal Genet Biol 48:485–495. https://doi.org/10.1016/j.fgb.2011.01.003
Ali M, Cheng Z, Ahmad H, Hayat S (2018) Reactive oxygen species (ROS) as defenses against a broad range of plant fungal infections and case study on ROS employed by crops against Verticillium dahliae wilts. J Plant Interact 13:353–363. https://doi.org/10.1080/17429145.2018.1484188
Arunachalam C, Doohan FM (2013) Trichothecene toxicity in eukaryotes: cellular and molecular mechanisms in plants and animals. J Plant Interact 217:149–158. https://doi.org/10.1016/j.toxlet.2012.12.003
Atanasova-Penichon V, Legoahec L, Bernillon S, Deborde C, Maucourt M, Verdal-Bonnin M, Pinson-Gadais L, Ponts N, Moing A, Richard-Forget F (2018) Mycotoxin biosynthesis and central Metabolism are two interlinked pathways in Fusarium graminearum, as demonstrated by the extensive metabolic changes induced by caffeic acid exposure. Appl Environ Microb 84:e01705-e1717. https://doi.org/10.1128/AEM.01705-17
Audenaert K, Vanheule A, Höfte M, Haesaert G (2014) Deoxynivalenol: a major player in the multifaceted response of Fusarium to its environment. Toxins 6:1–19. https://doi.org/10.3390/toxins6010001
Bai G, Shaner G (2004) Management and resistance in wheat and barley to fusarium head blight. Annu Rev Phytopathol 42:135–161. https://doi.org/10.1146/annurev.phyto.42.040803.140340
Bai GH, Desjardins AE, Plattner RD (2002) Deoxynivalenol-nonproducing Fusarium graminearum causes initial infection, but does not cause disease spread in wheat spikes. Mycopathologia 153:91–98. https://doi.org/10.1023/A:1014419323550
Berthiller F, Crews C, Dall’Asta C, Saeger SD, Haesaert G, Karlovsky P, Oswald IP, Seefelder W, Speijers G, Stroka J (2013) Masked mycotoxins: a review. Mol Nutr Food Res 57:165–186. https://doi.org/10.1002/mnfr.201100764
Boenisch MJ, Schäfer W (2011) Fusarium graminearum forms mycotoxin producing infection structures on wheat. BMC Plant Biol 11:110. https://doi.org/10.1186/1471-2229-11-110
Bönnighausen J, Schauer N, Schäfer W, Bormann J (2019) Metabolic profiling of wheat rachis node infection by Fusarium graminearum-decoding deoxynivalenol-dependent susceptibility. New Phytol 221:459–469. https://doi.org/10.1111/nph.15377
Bosompem MA, Wellington MO, Columbus DA (2021) 200 effect of long-term feeding of deoxynivalenol (DON) contaminated diets on performance of grower-finisher pigs. J Anim Sci 99:67–68. https://doi.org/10.1093/jas/skab054.111
Bottalico A, Perrone G (2002) Toxigenic Fusarium species and mycotoxins associated with head blight in small-grain cereals in Europe. Eur J Plant Pathol 108:611–624. https://doi.org/10.1023/A:1020635214971
Bowles D, Lim E, Poppenberger B, Vaistij FE (2006) Glycosyltransferases of lipophilic small molecules. Annu Rev Plant Biol 57:567–597. https://doi.org/10.1146/annurev.arplant.57.032905.105429
Brar GS, Brûlé-Babel AL, Ruan Y, Henriquez MA, Pozniak CJ, Kutcher HR, Hucl PJ (2019) Genetic factors affecting Fusarium head blight resistance improvement from introgression of exotic Sumai 3 alleles (including Fhb1, Fhb2, and Fhb5) in hard red spring wheat. BMC Plant Biol 19:179. https://doi.org/10.1186/s12870-019-1782-2
Brauer EK, Balcerzak M, Rocheleau H, Leung W, Schernthaner J, Subramaniam R, Ouellet T (2020) Genome editing of a deoxynivalenol-induced transcription factor confers resistance to Fusarium graminearum in wheat. Mol Plant Microbe 33:553–560. https://doi.org/10.1094/MPMI-11-19-0332-R
Brodersen P, Malinovsky FG, Hématy K, Newman M, Mundy J (2005) The role of salicylic acid in the induction of cell death in Arabidopsis acd11. Plant Physiol 138:1037–1045. https://doi.org/10.1104/pp.105.059303
Brown DW, McCormick SP, Alexander NJ, Proctor RH, Desjardins AE (2002) Inactivation of a cytochrome P-450 is a determinant of trichothecene diversity in Fusarium species. Fungal Genet Biol 36:224–233. https://doi.org/10.1016/s1087-1845(02)00021-x
Chen D, Wang Y, Zhou X, Wang Y, Xu JR (2014) The Sch9 kinase regulates conidium size, stress responses, and pathogenesis in Fusarium graminearum. PLoS ONE 9:e105811. https://doi.org/10.1371/journal.pone.0105811
Chen H, Su Z, Tian B, Liu Y, Pang Y, Kavetskyi V, Trick HN, Bai G (2022) Development and optimization of a Barley stripe mosaic virus (BSMV)-mediated gene editing system to improve Fusarium head blight (FHB) resistance in wheat. Plant Biotechnol J 20:1018–1020. https://doi.org/10.1111/PBI.13819
Cheng W, Song X, Li H, Cao L, Sun K, Qiu X, Xu Y, Yang P, Huang T, Zhang J et al (2015) Host-induced gene silencing of an essential chitin synthase gene confers durable resistance to Fusarium head blight and seedling blight in wheat. Plant Biotechnol J 13:1335–1345. https://doi.org/10.1111/pbi.12352
Constabel CP, Barbehenn R (2008) Defensive roles of polyphenol oxidase in plants. In: Schaller A (ed) Induced plant resistance to herbivory. Springer, Dordrecht, pp 253–270. https://doi.org/10.1007/978-1-4020-8182-8_12
Cummins I, Dixon DP, Freitag-Pohl S, Skipsey M, Edwards R (2011) Multiple roles for plant glutathione transferases in xenobiotic detoxification. Drug Metab Rev 43:266–280. https://doi.org/10.3109/03602532.2011.552910
Dänicke S, Valenta H, Döll S (2004) On the toxicokinetics and the metabolism of deoxynivalenol (DON) in the pig. Arch Anim Nutr 58:169–180. https://doi.org/10.1080/00039420410001667548
Das K, Roychoudhury A (2014) Reactive oxygen species (ROS) and response of antioxidants as ROS-scavengers during environmental stress in plants. Front Env Sci 2:1–13. https://doi.org/10.3389/fenvs.2014.00053
Desiardins AE, Proctor RH, Bai GH, Mccormick SP, Hohn TM (1996) Reduced virulence of trichothecene-nonproducing mutants of Gibberella zeae in wheat field tests. Mol Plant Microbe Interact 9:775–781
Desjardins AE, Hohn TM, McCormick SP (1993) Trichothecene biosynthesis in Fusarium species: chemistry, genetics, and significance. Microbiol Rev 57:595–604. https://doi.org/10.1006/mpat.1993.1074
Dhokane D, Karre S, Kushalappa AC, McCartney C (2016) Integrated metabolo-transcriptomics reveals Fusarium head blight candidate resistance genes in wheat QTL-Fhb2. PLoS ONE 11:e0155851. https://doi.org/10.1371/journal.pone.0155851
Fu J, Hao Y, Li H, Reif JC, Chen S, Huang C, Wang G, Li X, Xu Y, Li L (2022) Integration of genomic selection with doubled-haploid evaluation in hybrid breeding: from GS 1.0 to GS 4.0 and beyond. Mol Plant 15:577–580. https://doi.org/10.1016/j.molp.2022.02.005
Gachon CMM, Langlois-Meurinne M, Saindrenan P (2005) Plant secondary metabolism glycosyltransferases: the emerging functional analysis. Trends Plant Sci 10:542–549. https://doi.org/10.1016/j.tplants.2005.09.007
Gaire R, Arruda MP, Mohammadi M, Brown Guedira G, Kolb FL, Rutkoski J (2022) Multi-trait genomic selection can increase selection accuracy for deoxynivalenol accumulation resulting from Fusarium head blight in wheat. Plant Genome 15:1–12. https://doi.org/10.1002/tpg2.20188
Gallé Á, Pelsőczi A, Benyó D, Podmaniczki A, Szabó-Hevér Á, Poór P, Tóth B, Horváth E, Erdei L, Csiszár J (2022) Systemic response to Fusarium graminearum and culmorum inoculations: changes in detoxification of flag leaves in wheat. Cereal Res Commun 2:1–9. https://doi.org/10.1007/s42976-022-00272-3
Gardiner SA, Boddu J, Berthiller F, Hametner C, Stupar RM, Adam G, Muehlbauer GJ (2010) Transcriptome analysis of the barley–deoxynivalenol interaction: evidence for a role of glutathione in deoxynivalenol detoxification. Mol Plant Microbe in 23:962–976. https://doi.org/10.1094/MPMI-23-7-0962
Garvey GS, McCormick SP, Rayment I (2008) Structural and Functional Characterization of the TRI101 Trichothecene 3-O-Acetyltransferase from Fusarium sporotrichioides and Fusarium graminearum: kinetic insights to combating Fusarium head blight. J Biol Chem 283:1660–1669. https://doi.org/10.1074/jbc.M705752200
Gatti M, Cambon F, Tassy C, Macadre C, Guerard F, Langin T, Dufresne M (2019) The Brachypodium distachyon UGT Bradi5gUGT03300 confers type II Fusarium head blight resistance in wheat. Plant Pathol 68:334–343. https://doi.org/10.1111/ppa.12941
Goswami RS, Kistler HC (2004) Heading for disaster: fusarium graminearum on cereal crops. Mol Plant Pathol 5:515–525. https://doi.org/10.1111/j.1364-3703.2004.00252.x
Gunupuru LR, Perochon A, Doohan FM (2017) Deoxynivalenol resistance as a component of FHB resistance. Fitopatol Bras 42:175–183. https://doi.org/10.1007/s40858-017-0147-3
Gunupuru LR, Arunachalam C, Malla KB, Kahla A, Perochon A, Jia J, Thapa G, Doohan FM (2018) A wheat cytochrome P450 enhances both resistance to deoxynivalenol and grain yield. PLoS ONE 13:e0204992. https://doi.org/10.1371/journal.pone.0204992
Hao G, McCormick S, Tiley H, Usgaard T (2021) Detoxification and excretion of trichothecenes in transgenic Arabidopsis thaliana expressing Fusarium graminearum trichothecene 3-O-acetyltransferase. Toxins 13:320. https://doi.org/10.3390/toxins13050320
He W, Zhang L, Yi S, Tang X, Yuan Q, Guo M, Wu A, Qu B, Li H, Liao Y (2017) An aldo-keto reductase is responsible for Fusarium toxin-degrading activity in a soil Sphingomonas strain. Sci Rep 7:9549. https://doi.org/10.1038/s41598-017-08799-w
He W, Shi M, Yang P, Huang T, Zhao Y, Wu A, Dong W, Li H, Zhang J, Liao Y (2020) A quinone-dependent dehydrogenase and two NADPH-dependent aldo/keto reductases detoxify deoxynivalenol in wheat via epimerization in a Devosia strain. Food Chem 321:126703. https://doi.org/10.1016/j.foodchem.2020.126703
Irani Z, Sanjarian F, Azimi MR (2015) Conversion of deoxynivalenol to 3-acetyl deoxynivalenol in wheat and tobacco through the expression of synthetic acetyltransferase gene. Agric Biotechnol J 7:17–28. https://doi.org/10.22103/jab.2015.1349
Ito M, Sato I, Ishizaka M, Yoshida S, Koitabashi M, Yoshida S, Tsushima S (2013) Bacterial cytochrome P450 system catabolizing the Fusarium toxin deoxynivalenol. Appl Environ Microb 79:1619–1628. https://doi.org/10.1128/AEM.03227-12
Jez JM, Penning TM (2001) The aldo-keto reductase (AKR) superfamily: an update. Chem-Biol Interact 130–132:499–525. https://doi.org/10.1016/S0009-2797(00)00295-7
Jiang C, Zhang C, Wu C, Sun P, Hou R, Liu H, Wang C, Xu J (2016) TRI6 andTRI10 play different roles in the regulation of deoxynivalenol (DON) production by cAMP signaling in Fusarium graminearum. Environ Microbiol 18:3689–3701. https://doi.org/10.1111/1462-2920.13279
Jiang X, Zhang W, Fernie AR, Wen W (2022) Combining novel technologies with interdisciplinary basic research to enhance horticultural crops. Plant J 1:35–46. https://doi.org/10.1111/tpj.15553
Jiao J, Peng D (2018) Wheat microRNA1023 suppresses invasion of Fusarium graminearum by targeting and silencing FGSG_03101. J Plant Interact 13:514–521. https://doi.org/10.1080/17429145.2018.1528512
Karlovsky P (2011) Biological detoxification of the mycotoxin deoxynivalenol and its use in genetically engineered crops and feed additives. Appl Microbiol Biot 91:491–504. https://doi.org/10.1007/s00253-011-3401-5
Khaledi N, Taheri P, Falahati-Rastegar M (2016) Reactive oxygen species and antioxidant system responses in wheat cultivars during interaction with Fusarium species. Aust Plant Path 45:653–670. https://doi.org/10.1007/s13313-016-0455-y
Khaledi N, Taheri P, Falahati-Rastegar M (2017) Evaluation of resistance and the role of some defense responses in wheat cultivars to Fusarium head blight. J Plant Protect Res 57:396–408. https://doi.org/10.1515/jppr-2017-0054
Kheiri A, Jorf S, Malihipour A (2018) Infection process and wheat response to Fusarium head blight caused by Fusarium graminearum. Eur J Plant Pathol 153:489–502. https://doi.org/10.1007/s10658-018-1576-7
Kimura M, Kaneko I, Komiyama M, Takatsuki A, Koshino H, Yoneyama K, Yamaguchi I (1998) Trichothecene 3-O-Acetyltransferase protects both the producing organism and transformed yeast from related mycotoxins: Cloning and characterizatIion of Tri101. J Biol Chem 273:1654–1661. https://doi.org/10.1074/jbc.273.3.1654
Kimura M, Kaneko I, Komiyama M, Takatsuki A, Koshino H, Yoneyama K, Kimura M, Tokai T, Takahashi-Ando N, Ohsato S, Fujimura M (2007) Molecular and genetic studies of Fusarium trichothecene biosynthesis: pathways, genes, and evolution. Biosci Biotech Bioch 71:2105–2123. https://doi.org/10.1271/bbb.70183
Koch A, Kumar N, Weber L, Keller H, Imani J, Kogel K (2013) Host-induced gene silencing of cytochrome P450 lanosterol C14α-demethylase–encoding genes confers strong resistance to Fusarium species. Proc Natl Acad Sci USA 110:19324–19329. https://doi.org/10.1073/pnas.1306373110
Krattinger SG, Lagudah ES, Wicker T, Risk JM, Ashton AR, Selter LL, Matsumoto T, Keller B (2011) Lr34 multi-pathogen resistance ABC transporter: Molecular analysis of homoeologous and orthologous genes in hexaploid wheat and other grass species. Plant J 65:392–403. https://doi.org/10.1111/j.1365-313X.2010.04430.x
Laetitia P, Florence R, Pierre F, Christian B, Bernard C, Daniel R, Bénédicte B (2008) Magnesium represses trichothecene biosynthesis and modulates Tri5, Tri6, and Tri12 genes expression in Fusarium graminearum. Mycopathologia 165:51–59. https://doi.org/10.1007/s11046-007-9076-x
Langevin F, Eudes F, Comeau A (2004) Effect of trichothecenes produced by Fusarium graminearum during Fusarium head blight development in six cereal species. Eur J Plant Pathol 110:735–746. https://doi.org/10.1023/B:EJPP.0000041568.31778.ad
Li X, Zhang JB, Song B, Li HP, Xu HQ, Qu B, Dang FJ, Liao YC (2010) Resistance to Fusarium head blight and seedling blight in wheat is associated with activation of a cytochrome P450 gene. Phytopathology 100:183–191. https://doi.org/10.3390/toxins12020121
Li X, Shin S, Heinen S, Dill-Macky R, Berthiller F, Nersesian N, Clemente T, McCormick S, Muehlbauer GJ (2015) Transgenic wheat expressing a barley UDP-glucosyltransferase detoxifies deoxynivalenol and provides high levels of resistance to Fusarium graminearum. Mol Plant Microbe Interact 28:1237–1246. https://doi.org/10.1094/MPMI-03-15-0062-R
Li G, Zhou J, Jia H, Gao Z, Fan M, Luo Y, Zhao P, Xue S, Li N, Yuan Y, Ma S, Kong Z, Jia L, An X, Jiang G, Liu W, Cao W, Zhang R, Fan J, Xu X, Liu Y, Kong Q, Zheng S, Wang Y, Qin B, Cao S, Ding Y, Shi J, Yan H, Wang X, Ran C, Ma Z (2019) Mutation of a histidine-rich calcium-binding-protein gene in wheat confers resistance to Fusarium head blight. Nat Genet 51:1106–1112. https://doi.org/10.1038/s41588-019-0426-7
Li D, Lu X, Zhu Y, Pan J, Zhou S, Zhang X, Zhu G, Shang Y, Huang S, Zhang C (2021) The multiomics basis of potato heterosis. J Integr Plant Biol 64:671–687. https://doi.org/10.1111/jipb.13211
Liang X, Ou Y, Zhao H, Zhou W, Sun C, Lin X (2021) Lipid peroxide-derived short-chain aldehydes are involved in aluminum toxicity of wheat (Triticum aestivum) roots. J Agric Food Chem 69:10496–10505. https://doi.org/10.1021/acs.jafc.1c03975
Liu N, Fan F, Qiu D, Jiang L (2013) The transcription cofactor FgSwi6 plays a role in growth and development, carbendazim sensitivity, cellulose utilization, lithium tolerance, deoxynivalenol production and virulence in the filamentous fungus Fusarium graminearum. Fungal Genet Biol 58–59:42–52. https://doi.org/10.1016/j.fgb.2013.08.010
Liu S, Geng S, Li A, Mao Y, Mao L (2021) RNAi technology for plant protection and its application in wheat. Biotech 2:365–374. https://doi.org/10.1007/s42994-021-00036-3
Luo K, Ouellet T, Zhao H, Wang X, Kang Z (2021) Wheat-Fusarium graminearum interactions under Sitobion avenae influence: From nutrients and hormone signals. Front Nutr 8:1–13. https://doi.org/10.3389/fnut.2021.703293
Ma Y, Zhang A, Shi Z, He C, Ding J, Wang X, Ma J, Zhang H (2012) A mitochondria-mediated apoptotic pathway induced by deoxynivalenol in human colon cancer cells. Toxicol in Vitro 26:414–420. https://doi.org/10.1016/j.tiv.2012.01.010
Ma H, Zhang X, Yao J, Cheng S (2019) Breeding for the resistance to Fusarium head blight of wheat in China. Front Agric Sci Eng 6:251. https://doi.org/10.15302/J-FASE-2019262
Ma Z, Xie Q, Li G, Jia H, Zhou J, Kong Z, Li N, Yuan Y (2020) Germplasms, genetics and genomics for better control of disastrous wheat Fusarium head blight. Theor Appl Genet 133:1541–1568. https://doi.org/10.1007/s00122-019-03525-8
Madadkhah E, Lotfi M, Nabipour A, Rahmanpour S, Banihashemi Z, Shoorooei M (2012) Enzymatic activities in roots of melon genotypes infected with Fusarium oxysporum f. sp. melonis race 1. Sci Hortic 135:171–176. https://doi.org/10.1016/j.scienta.2011.11.020
Manoharan M, Dahleen LS, Hohn TM, Neate SM, Yu X, Alexander NJ, McCormick SP, Bregitzer P, Schwarz PB, Horsley RD (2006) Expression of 3-OH trichothecene acetyltransferase in barley (Hordeum vulgare L.) and effects on deoxynivalenol. Plant Sci 171:699–706. https://doi.org/10.1016/j.plantsci.2006.07.004
Matić M, Vuković R, Vrandečić K, Štolfa Čamagajevac I, Ćosić J, Vuković A, Sabljić K, Sabo N, Dvojković K, Novoselović D (2021) Oxidative status and antioxidative response to Fusarium attack and different nitrogen levels in winter wheat varieties. Plants 10:611. https://doi.org/10.3390/plants10040611
McCormick SP, Alexander NJ, Trapp SE, Hohn TM (1999) Disruption of TRI101, the gene encoding trichothecene 3-O-acetyltransferase, from Fusarium sporotrichioides. Appl Environ Microb 65:5252–5256. https://doi.org/10.1128/AEM.65.12.5252-5256.1999
McLaughlin JE, Darwish NI, Garcia-Sanchez J, Tyagi N, Trick HN, McCormick S, Dill-Macky R, Tumer NE (2020) A lipid transfer protein has antifungal and antioxidant activity and suppresses Fusarium head blight disease and DON accumulation in transgenic wheat. Phytopathology 111:671–683. https://doi.org/10.1094/PHYTO-04-20-0153-R
Mentges M, Glasenapp A, Boenisch M, Malz S, Henrissat B, Frandsen RJN, Güldener U, Münsterkötter M, Bormann J, Lebrun M, Schäfer W, Martinez-Rocha AL (2020) Infection cushions of Fusarium graminearum are fungal arsenals for wheat infection. Mol Plant Pathol 21:1070–1087. https://doi.org/10.1111/mpp.12960
Merhej J, Richard-Forget F, Barreau C (2011) Regulation of trichothecene biosynthesis in Fusarium: Recent advances and new insights. Appl Microbiol Biotechnol 91:519–528. https://doi.org/10.1007/s00253-011-3397-x
Michlmayr H, Malachová A, Varga E, Kleinová J, Lemmens M, Newmister S, Rayment I, Berthiller F, Adam G (2015) Biochemical characterization of a recombinant UDP-glucosyltransferase from rice and enzymatic production of deoxynivalenol-3-O-β-D-glucoside. Toxins 7:2685–2700. https://doi.org/10.3390/toxins7072685
Miedaner T, Wilde F, Steiner B, Buerstmayr H, Korzun V, Ebmeyer E (2006) Stacking quantitative trait loci (QTL) for Fusarium head blight resistance from nonadapted sources in a European elite spring wheat background and assessing their effects on deoxynivalenol (DON) content and disease severity. Theor Appl Genet 112:562–569. https://doi.org/10.1007/s00122-005-0163-4
Mitterbauer R, Adam G (2002) Saccharomyces cerevisae and Arabidopsis thaliana: useful model systems for the identification of molecular mechanisms involved in resistance of plants to toxins. Eur J Plant Pathol 108:699–703. https://doi.org/10.1023/A:1020666627267
Mohammadi M, Karr AL (2002) β-1,3-glucanase and chitinase activities in soybean root nodules. J Plant Physiol 159:245–256. https://doi.org/10.1078/0176-1617-00702
Muhitch MJ, McCormick SP, Alexander NJ, Hohn TM (2000) Transgenic expression of the TRI101 or PDR5 gene increases resistance of tobacco to the phytotoxic effects of the trichothecene 4, 15-diacetoxyscirpenol. Plant Sci 157:201–207. https://doi.org/10.1016/S0168-9452(00)00282-X
Nuruzzaman M, Zhang R, Cao HZ, Luo ZY (2014) Plant pleiotropic drug resistance transporters: transport mechanism, gene expression, and function. J Integr Plant Biol 56:729–740. https://doi.org/10.1111/jipb.12196
Ohsato S, Ochiai-Fukuda T, Nishiuchi T, Takahashi-Ando N, Koizumi S, Hamamoto H, Kudo T, Yamaguchi I, Kimura M (2007) Transgenic rice plants expressing trichothecene 3-O-acetyltransferase show resistance to the Fusarium phytotoxin deoxynivalenol. Plant Cell Rep 26:531–538. https://doi.org/10.1007/s00299-006-0251-1
Okubara P, Blechl A, McCormick S, Alexander N, Dill-Macky R, Hohn T (2002) Engineering deoxynivalenol metabolism in wheat through the expression of a fungal trichothecene acetyltransferase gene. Theor Appl Genet 106:74–83. https://doi.org/10.1007/s00122-002-1066-2
Osborne LE, Stein JM (2007) Epidemiology of Fusarium head blight on small-grain cereals. Int J Food Microbiol 119:103–108. https://doi.org/10.1016/j.ijfoodmicro.2007.07.032
Parry DW, Jenkinson P, Mcleod L (1995) Fusarium ear blight (scab) in small grain cereals-a review. Plant Pathol 44:207–238. https://doi.org/10.1111/j.1365-3059.1995.tb02773.x
Pasquet JJ, Changenet VV, Macadré CC, Boex-Fontvieille EE, Soulhat CC, Bouchabké-Coussa OO, Dalmais MM, Atanasova-Pénichon VV, Bendahmane AA, Saindrenan PP et al (2016) A brachypodium UDP-Glycosyltransferase confers root tolerance to deoxynivalenol and resistance to Fusarium infection1. Plant Physiol 172:559–574. https://doi.org/10.1104/pp.16.00371
Pinton P, Braicu C, Nougayrede J, Laffitte J, Taranu I, Oswald IP (2010) Deoxynivalenol impairs porcine intestinal barrier function and decreases the protein expression of claudin-4 through a mitogen-Activated protein kinase-dependent mechanism. J Nutr 140:1956–1962. https://doi.org/10.3945/jn.110.123919
Poppenberger B, Berthiller F, Lucyshyn D, Sieberer T, Schuhmacher R, Krska R, Kuchler K, Glössl J, Luschnig C, Adam G (2003) Detoxification of the Fusarium Mycotoxin Deoxynivalenol by a UDP-glucosyltransferase from Arabidopsis thaliana. J Biol Chem 278:47905–47914. https://doi.org/10.1074/jbc.M307552200
Proctor RH, Hohn TM, McCormick SP (1995) Reduced virulence of Gibberella zeae caused by disruption of a trichothecene toxin biosynthetic gene. Mol Plant Microbe 8:593–601. https://doi.org/10.1094/MPMI-8-0593
Qu B, Li HP, Zhang JB, Xu YB, Huang T, Wu AB, Zhao CS, Carter J, Nicholson P, Liao YC (2008) Geographic distribution and genetic diversity of Fusarium graminearum and F. asiaticum on wheat spikes throughout China. Plant Pathol 57:15–24. https://doi.org/10.1111/j.1365-3059.2007.01711.x
Rawat N, Pumphrey MO, Liu S, Zhang X, Tiwari VK, Ando K, Trick HN, Bockus WW, Akhunov E, Anderson JA, Gill BS (2016) Wheat Fhb1 encodes a chimeric lectin with agglutinin domains and a pore-forming toxin-like domain conferring resistance to Fusarium head blight. Nat Genet 48:1576–1580. https://doi.org/10.1038/ng.3706
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375. https://doi.org/10.1146/annurev.arplant.57.032905.105406
Reed DJ (1990) Glutathione: toxicological implications. Annu Rev Pharmacol Toxicol 30:603–631. https://doi.org/10.1146/annurev.pa.30.040190.003131
Riechers DE, Vaughn KC, Molin WT (2005) The role of plant glutathione S-transferases in herbicide metabolism. ACS Publ. https://doi.org/10.1021/BK-2005-0899.CH019
Rychlik M, Humpf H, Marko D, Dänicke S, Mally A, Berthiller F, Klaffke H, Lorenz N (2014) Proposal of a comprehensive definition of modified and other forms of mycotoxins including “masked” mycotoxins. Mycotoxin Res 30:197–205. https://doi.org/10.1007/s12550-014-0203-5
Salcedo A, Al-Haddad J, Buell CR, Trail F, Góngora-Castillo E, Quesada-Ocampo L (2021) Comparative transcriptome analysis of two contrasting maize inbred lines provides insights on molecular mechanisms of stalk rot resistance. PhytoFrontiers 1:314–329. https://doi.org/10.1094/PHYTOFR-12-20-0055-R
Sato Y, Masuta Y, Saito K, Murayama S, Ozawa K (2011) Enhanced chilling tolerance at the booting stage in rice by transgenic overexpression of the ascorbate peroxidase gene, OsAPXa. Plant Cell Rep 30:399–406. https://doi.org/10.1007/s00299-010-0985-7
Schmeitzl C, Varga E, Warth B, Kugler K, Malachová A, Michlmayr H, Wiesenberger G, Mayer K, Mewes H, Krska R et al (2016) Identification and characterization of carboxylesterases from Brachypodium distachyon deacetylating trichothecene mycotoxins. Toxins 8:1–17. https://doi.org/10.3390/toxins8010006
Schweiger W, Pasquet J, Nussbaumer T, Paris MPK, Wiesenberger G, Macadré C, Ametz C, Berthiller F, Lemmens M, Saindrenan P, Mewes H, Mayer KFX, Dufresne M, Adam G (2013) Functional characterization of two clusters of Brachypodium distachyon UDP-glycosyltransferases encoding putative deoxynivalenol detoxification genes. Mol Plant Microbe 26:781–792. https://doi.org/10.1094/MPMI-08-12-0205-R
Sengupta D, Naik D, Reddy AR (2015) Plant aldo-keto reductases (AKRs) as multitasking soldiers involved in diverse plant metabolic processes and stress defense: a structure-function update. J Plant Physiol 179:40–55. https://doi.org/10.1016/j.jplph.2015.03.004
Seong K, Pasquali M, Zhou X, Song J, Hilburn K, McCormick S, Dong Y, Xu J, Kistler HC (2009) Global gene regulation by Fusarium transcription factors Tri6 and Tri10 reveals adaptations for toxin biosynthesis. Mol Microbiol 72:354–367. https://doi.org/10.1111/j.1365-2958.2009.06649.x
Sgarbi C, Malbrán I, Saldúa L, Lori GA, Lohwasser U, Arif MAR, Börner A, Yanniccari M, Castro AM (2021) Mapping resistance to Argentinean Fusarium (graminearum) head blight isolates in wheat. Int J Mol Sci 22:13653. https://doi.org/10.3390/ijms222413653
Shostak K, Bonner C, Sproule A, Thapa I, Shields SWJ, Blackwell B, Vierula J, Overy D, Subramaniam R (2020) Activation of biosynthetic gene clusters by the global transcriptional regulator TRI6 in Fusarium graminearum. Mol Microbiol 114:664–680. https://doi.org/10.1111/mmi.14575
Sobhy SE, Abo-Kassem EM, Sewelam NA, Hafez EE, Aseel DG, Saad-Allah KM (2022) Presoaking in weed extracts is a reasonable approach to mitigate Fusarium graminearum infection in wheat. J Plant Growth Regul 41:2261–2278. https://doi.org/10.1007/s00344-021-10442-y
Sorahinobar M, Niknam V, Ebrahimzadeh H, Soltanloo H, Behmanesh M, Enferadi ST (2016) Central role of salicylic acid in resistance of wheat against Fusarium graminearum. J Plant Growth Regul 35:477–491. https://doi.org/10.1007/s00344-015-9554-1
Spanic V, Viljevac Vuletic M, Abicic I, Marcek T (2017) Early response of wheat antioxidant system with special reference to Fusarium head blight stress. Plant Physiol Biochem 115:34–43. https://doi.org/10.1016/j.plaphy.2017.03.010
Su Z, Bernardo A, Tian B, Chen H, Wang S, Ma H, Cai S, Liu D, Zhang D, Li T (2019) A deletion mutation in TaHRC confers Fhb1 resistance to Fusarium head blight in wheat. Nat Genet 51:1099–1105. https://doi.org/10.1038/s41588-019-0425-8
Tada Y, Hata S, Takata Y, Nakayashiki H, Tosa Y, Mayama S (2001) Induction and signaling of an apoptotic response typified by DNA laddering in the defense response of oats to infection and elicitors. Mol Plant Microbe Interact 14:477–486. https://doi.org/10.1094/MPMI.2001.14.4.477
Tag AG, Garifullina GF, Peplow AW, Ake C, Phillips TD, Hohn TM, Beremand MN (2001) A novel regulatory gene, Tri10, controls trichothecene toxin production and gene expression. Appl Environ Microb 67:5294–5302. https://doi.org/10.1128/AEM.67.11.5294-5302.2001
Tommasini R (1998) An ABC-transporter of Arabidopsis thaliana has both glutathione-conjugate and chlorophyll catabolite transport activity. Plant J 13:773–780. https://doi.org/10.1046/j.1365-313X.1998.00076.x
Trail F (2009) For blighted waves of grain: Fusarium graminearum in the postgenomics era. Plant Physiol 149:103–110. https://doi.org/10.1104/pp.108.129684
Venske E, Dos Santos RS, Farias DDR, Rother V, Da Maia LC, Pegoraro C, Costa De Oliveira A (2019) Meta-analysis of the QTLome of Fusarium head blight resistance in bread wheat: Refining the current puzzle. Front Plant Sci 10:1–19. https://doi.org/10.3389/fpls.2019.00727
Villafana RT, Rampersad SN (2020) Signatures of TRI5, TRI8 and TRI11 protein sequences of Fusarium incarnatum-equiseti species complex (FIESC) indicate differential trichothecene analog production. Toxins 12:1–22. https://doi.org/10.3390/toxins12060386
Walter S, Kahla A, Arunachalam C, Perochon A, Khan MR, Scofield SR, Doohan FM (2015) A wheat ABC transporter contributes to both grain formation and mycotoxin tolerance. J Exp Bot 66:2583–2593. https://doi.org/10.1093/jxb/erv048
Wang J, Zhang H, Allen RD (1999) Overexpression of an Arabidopsis peroxisomal ascorbate peroxidase gene in tobacco increases protection against oxidative stress. Plant Cell Physiol 40:725–732. https://doi.org/10.1093/oxfordjournals.pcp.a029599
Wang C, Zhang S, Hou R, Zhao Z, Zheng Q, Xu Q, Zheng D, Wang G, Liu H, Gao X, Ma J, Kistler HC, Kang Z, Xu J (2011) Functional analysis of the kinome of the wheat scab fungus Fusarium graminearum. PLoS Pathog 7:e1002460. https://doi.org/10.1371/journal.ppat.1002460
Wang H, Sun S, Ge W, Zhao L, Hou B, Wang K, Lyu Z, Chen L, Xu S, Guo J et al (2020) Horizontal gene transfer of Fhb7 from fungus underlies Fusarium head blight resistance in wheat. Science 368:5435. https://doi.org/10.1126/science.aba5435
Wang S, Wu K, Xue D, Zhang C, Rajput SA, Qi D (2021) Mechanism of deoxynivalenol mediated gastrointestinal toxicity: Insights from mitochondrial dysfunction. Food Chem Toxicol 153:112214. https://doi.org/10.1016/j.fct.2021.112214
Wang J, Zeng W, Cheng J, Xie J, Fu Y, Jiang D, Lin Y (2022) lncRsp1, a long noncoding RNA, influences Fgsp1 expression and sexual reproduction in Fusarium graminearum. Mol Plant Pathol 23:265–277. https://doi.org/10.1111/mpp.13160
Wellington MO, Bosompem MA, Petracek R, Nagl V, Columbus DA (2021) Effect of long-term feeding of graded levels of deoxynivalenol on performance, nutrient utilization, and organ health of grower-finisher pigs (35 to 120 kg). J Anim Sci 99:378. https://doi.org/10.1093/jas/skab109
Wu J, Zeng Q, Wang Q, Liu S, Yu S, Mu J, Huang S, Sela H, Distelfeld A, Huang L et al (2018) SNP-based pool genotyping and haplotype analysis accelerate fine-mapping of the wheat genomic region containing stripe rust resistance gene Yr26. Theor Appl Genet 131:1481–1496. https://doi.org/10.1007/s00122-018-3092-8
Xu Y, Li H, Zhang J, Song B, Chen F, Duan X, Xu H, Liao Y (2010) Disruption of the chitin synthase gene CHS1 from Fusarium asiaticum results in an altered structure of cell walls and reduced virulence. Fungal Genet Biol 47:205–215. https://doi.org/10.1016/j.fgb.2009.11.003
Yang P, Yi S, Nian J, Yuan Q, He W, Zhang J, Liao Y (2021) Application of double-strand RNAs targeting chitin synthase, glucan synthase, and protein kinase reduces Fusarium graminearum spreading in wheat. Front Microbiol 12:1–12. https://doi.org/10.3389/fmicb.2021.660976
Yao Y, Kan W, Su P, Zhu Y, Zhong W, Xi J, Wang D, Tang C, Wu L (2022) Hydrogen sulphide alleviates Fusarium head blight in wheat seedlings. PeerJ 10:e13078. https://doi.org/10.7717/peerj.13078
Yun Y, Liu Z, Yin Y, Jiang J, Chen Y, Xu JR, Ma Z (2015) Functional analysis of the Fusarium graminearum phosphatome. New Phytol 207:119–134. https://doi.org/10.1111/nph.13374
Zhang J, Sun X (2021) Recent advances in polyphenol oxidase-mediated plant stress responses. Phytochemistry 181:112588. https://doi.org/10.1016/j.phytochem.2020.112588
Zhang Z, Nie D, Fan K, Yang J, Guo W, Meng J, Zhao Z, Han Z (2020) A systematic review of plant-conjugated masked mycotoxins: occurrence, toxicology, and metabolism. Crit Rev Food Sci Nutr 60:1523–1537. https://doi.org/10.1080/10408398.2019.1578944
Zhang Y, Yang Z, Ma H, Huang L, Ding F, Du Y, Jia H, Li G, Kong Z, Ran C, Gu Z, Ma Z (2021) Pyramiding of Fusarium head blight resistance quantitative trait loci, Fhb1, Fhb4, and Fhb5, in modern Chinese wheat cultivars. Front Plant Sci 12:694023. https://doi.org/10.3389/fpls.2021.694023
Zhao X, Guan J (2011) Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv Drug Delivery Rev 63:610–615. https://doi.org/10.1016/j.addr.2010.11.001
Zhu Z, Hao Y, Mergoum M, Bai G, Humphreys G, Cloutier S, Xia X, He Z (2019) Breeding wheat for resistance to Fusarium head blight in the global north: China, USA, and Canada. Crop J 7:730–738. https://doi.org/10.1016/j.cj.2019.06.003
Zhu F, Wen W, Cheng Y, Alseekh S, Fernie AR (2023) Integrating multiomics data accelerates elucidation of plant primary and secondary metabolic pathways. aBIOTECH 3:250–266. https://doi.org/10.1007/s42994-022-00091-4
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We apologize to our colleagues whose work could not be included because of space constraints. We would like to thank the reviewers for their critical comments on earlier versions of this manuscript and American Journal Experts for providing editing services to improve the English language of this manuscript.
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This work was financially supported by the National Natural Science Foundation of China (32260717), Natural Science Foundation of Shaanxi Province, China (2021JQ-619), China Postdoctoral Science Foundation’s funded project (2017M613228), and Research Fund for the Doctoral Start-up Foundation of Yan’an University (YDBK2019-65).
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Luo, K., Guo, J., He, D. et al. Deoxynivalenol accumulation and detoxification in cereals and its potential role in wheat–Fusarium graminearum interactions. aBIOTECH 4, 155–171 (2023). https://doi.org/10.1007/s42994-023-00096-7
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DOI: https://doi.org/10.1007/s42994-023-00096-7