Epigenetic Regulation of CYP72A385-Mediated Metabolic Resistance to Novel Auxin Herbicide Florpyrauxifen-benzyl in Echinochloa crus-galli (L.) P. Beauv.

Weed's metabolic resistance to herbicides has undermined the sustainability of herbicides and global food security. Notably, we identified an Echinochloa crus-galli (L.) P. Beauv population (R) that evolved resistance to the never-used florpyrauxifen-benzyl, in which florpyrauxifen-benzyl was metabolized faster than the susceptible E. crus-galli population (S). RNA-seq identified potential metabolism-related genes, EcCYP72A385 and EcCYP85A1, whose expression in yeast exhibited the capacity to degrade florpyrauxifen-benzyl. Region-2 in the EcCYP72A385 promoter showed significant demethylation after florpyrauxifen-benzyl treatment in the R population. DNA methyltransferase inhibitors induce EcCYP72A385 overexpression in the S population and endow it with tolerance to florpyrauxifen-benzyl. Moreover, methyltransferase-like 7A (EcMETTL7A) was overexpressed in the S population and specifically bound to the EcCYP72A385 promoter. Transgenic EcCYP72A385 in Arabidopsis and Oryza sativa L. exhibited resistance to florpyrauxifen-benzyl, whereas EcMETTL7A transgenic plants were sensitive. Overall, EcCYP72A385 is the principal functional gene for conferring resistance to florpyrauxifen-benzyl and is regulated by EcMETTL7A in E. crus-galli.

[1]  F. Du,et al.  Transcriptomic characterization revealed that METTL7A inhibits melanoma progression via the p53 signaling pathway and immunomodulatory pathway , 2023, PeerJ.

[2]  L. Bai,et al.  Metabolic resistance to acetolactate synthase-inhibitors in Beckmannia syzigachne: Identification of CYP81Q32 and its transcription regulation. , 2023, The Plant journal : for cell and molecular biology.

[3]  Wei Zhang,et al.  The novel putative methyltransferase METTL7A as one prognostic biomarker potentially associated with immune infiltration in human renal cancer , 2023, Heliyon.

[4]  Xinzhuan Yao,et al.  The Overexpression of Oryza sativa L. CYP85A1 Promotes Growth and Biomass Production in Transgenic Trees , 2023, International journal of molecular sciences.

[5]  Zikai Liu,et al.  Evidence Based on an Integrative Analysis of Multi-Omics Data on METTL7A as a Molecular Marker in Pan-Cancer , 2023, Biomolecules.

[6]  J. Tooley,et al.  METTLing in Stem Cell and Cancer Biology , 2022, Stem Cell Reviews and Reports.

[7]  C. Paweletz,et al.  MPS1 inhibition primes immunogenicity of KRAS-LKB1 mutant lung cancer. , 2022, Cancer cell.

[8]  Takeshi Imamura,et al.  Cell–matrix interface regulates dormancy in human colon cancer stem cells , 2022, Nature.

[9]  C. Nicoletti,et al.  LncRNA EPR-induced METTL7A1 modulates target gene translation , 2022, Nucleic acids research.

[10]  P. Heutink,et al.  Drug screen in iPSC-Neurons identifies nucleoside analogs as inhibitors of (G4C2)n expression in C9orf72 ALS/FTD. , 2022, Cell reports.

[11]  Jinxin Wang,et al.  Cytochrome P450 CYP709C56 metabolizing mesosulfuron-methyl confers herbicide resistance in Alopecurus aequalis , 2022, Cellular and Molecular Life Sciences.

[12]  K. Olsen,et al.  Genomic insights into the evolution of Echinochloa species as weed and orphan crop , 2022, Nature communications.

[13]  P. Lin,et al.  Induction of m6A methylation in adipocyte exosomal LncRNAs mediates myeloma drug resistance , 2022, Journal of Experimental & Clinical Cancer Research.

[14]  X. Yang,et al.  CYP81A68 confers metabolic resistance to ALS and ACCase-inhibiting herbicides and its epigenetic regulation in Echinochloa crus-galli. , 2022, Journal of hazardous materials.

[15]  J. Norsworthy,et al.  Absorption, translocation, and metabolism of florpyrauxifen-benzyl and cyhalofop-butyl in cyhalofop-butyl-resistant barnyardgrass [Echinochloa crus-galli (L.) P. Beauv.]. , 2021, Pesticide biochemistry and physiology.

[16]  Hao Wang,et al.  The phytotoxicity mechanism of florpyrauxifen-benzyl to Echinochloa crus-galli (L.) P. Beauv and weed control effect. , 2021, Pesticide biochemistry and physiology.

[17]  Ju-Young Kim,et al.  Methyltransferase-like protein 7A (METTL7A) promotes cell survival and osteogenic differentiation under metabolic stress , 2021, Cell death discovery.

[18]  Jinxin Wang,et al.  Investigating the Mechanism of Metabolic Resistance to Tribenuron-Methyl in Capsella bursa-pastoris (L.) Medik. by Full-Length Transcriptome Assembly Combined with RNA-Seq. , 2021, Journal of agricultural and food chemistry.

[19]  N. Navrot,et al.  Innate promiscuity of the CYP706 family of P450 enzymes provides a suitable context for the evolution of dinitroaniline resistance in weed. , 2020, The New phytologist.

[20]  Q. Qian,et al.  Functional analysis of auxin receptor OsTIR1/OsAFB family members in rice grain yield, tillering, plant height, root system, germination, and auxinic herbicide resistance. , 2020, The New phytologist.

[21]  S. Powles,et al.  DR HEPING HAN (Orcid ID : 00 Cytochrome P450 CYP81A10v7 in Lolium rigidum confers metabolic resistance to herbicides across at least five modes of action. , 2020, The Plant journal : for cell and molecular biology.

[22]  S. Iwakami,et al.  Cytochrome P450-mediated herbicide metabolism in plants: Current understanding and prospects. , 2020, Pest management science.

[23]  K. Olsen,et al.  The genomes of the allohexaploid Echinochloa crus-galli and its progenitors provide insights into polyploidization-driven adaptation. , 2020, Molecular plant.

[24]  C. Jin,et al.  Inhibition of DNA demethylation enhances plant tolerance to cadmium toxicity by improving iron nutrition. , 2019, Plant, cell & environment.

[25]  N. Zhang,et al.  Uptake of atrazine in a paddy crop activates an epigenetic mechanism for degrading the pesticide in plants and environment. , 2019, Environment international.

[26]  Tingting Liu,et al.  Target-site and metabolic resistance mechanisms to penoxsulam in barnyardgrass (Echinochloa crus-galli (L.) P. Beauv). , 2019, Journal of agricultural and food chemistry.

[27]  Tingting Liu,et al.  Transcriptome profiling to identify cytochrome P450 genes involved in penoxsulam resistance in Echinochloa glabrescens. , 2019, Pesticide biochemistry and physiology.

[28]  Takuya Yamaguchi,et al.  Role of CYP81A cytochrome P450s in clomazone metabolism in Echinochloa phyllopogon. , 2019, Plant science : an international journal of experimental plant biology.

[29]  F. Prósper,et al.  Inhibition of a G9a/DNMT network triggers immune-mediated bladder cancer regression , 2019, Nature Medicine.

[30]  Jeffrey A. Evans,et al.  Considering weed management as a social dilemma bridges individual and collective interests , 2019, Nature Plants.

[31]  She Chen,et al.  A methylated-DNA-binding complex required for plant development mediates transcriptional activation of promoter methylated genes. , 2019, Journal of integrative plant biology.

[32]  M. Ishizaka,et al.  CYP81A P450s are involved in concomitant cross-resistance to acetolactate synthase and acetyl-CoA carboxylase herbicides in Echinochloa phyllopogon. , 2018, The New phytologist.

[33]  Jinxin Wang,et al.  Enhanced Herbicide Metabolism and Metabolic Resistance Genes Identified in Tribenuron-Methyl Resistant Myosoton aquaticum L. , 2018, Journal of agricultural and food chemistry.

[34]  Jun Yu Li,et al.  Quinclorac resistance induced by the suppression of the expression of 1-aminocyclopropane-1-carboxylic acid (ACC) synthase and ACC oxidase genes in Echinochloa crus-galli var. zelayensis. , 2018, Pesticide biochemistry and physiology.

[35]  P. Westra,et al.  Cross-resistance to dicamba, 2,4-D, and fluroxypyr in Kochia scoparia is endowed by a mutation in an AUX/IAA gene , 2018, Proceedings of the National Academy of Sciences.

[36]  E. Bezirtzoglou,et al.  The Role of Cytochromes P450 in Infection , 2018, Front. Immunol..

[37]  Wenwen Song,et al.  Overexpression of SoCYP85A1, a Spinach Cytochrome p450 Gene in Transgenic Tobacco Enhances Root Development and Drought Stress Tolerance , 2017, Front. Plant Sci..

[38]  Qinjie Chu,et al.  Echinochloa crus-galli genome analysis provides insight into its adaptation and invasiveness as a weed , 2017, Nature Communications.

[39]  Wei Li,et al.  Transcriptome Profiling to Identify Genes Involved in Mesosulfuron-Methyl Resistance in Alopecurus aequalis , 2017, Front. Plant Sci..

[40]  Youko Oono,et al.  Variation of DNA methylation patterns associated with gene expression in rice (Oryza sativa) exposed to cadmium. , 2016, Plant, cell & environment.

[41]  L. Bai,et al.  Target-site and non-target-site based resistance to the herbicide tribenuron-methyl in flixweed (Descurainia sophia L.) , 2016, BMC Genomics.

[42]  Sergio Alan Cervantes-Pérez,et al.  Methylome analysis reveals an important role for epigenetic changes in the regulation of the Arabidopsis response to phosphate starvation , 2015, Proceedings of the National Academy of Sciences.

[43]  S. Powles.  Global herbicide resistance challenge. , 2014, Pest management science.

[44]  S. Powles,et al.  Metabolism-Based Herbicide Resistance and Cross-Resistance in Crop Weeds: A Threat to Herbicide Sustainability and Global Crop Production1 , 2014, Plant Physiology.

[45]  J. Okuno,et al.  Cytochrome P450 CYP81A12 and CYP81A21 Are Associated with Resistance to Two Acetolactate Synthase Inhibitors in Echinochloa phyllopogon1[W] , 2014, Plant Physiology.

[46]  F. Taguchi-Shiobara,et al.  A Novel Rice Cytochrome P450 Gene, CYP72A31, Confers Tolerance to Acetolactate Synthase-Inhibiting Herbicides in Rice and Arabidopsis1[C][W][OPEN] , 2014, Plant Physiology.

[47]  Jun Yu Li,et al.  A resistance mechanism dependent upon the inhibition of ethylene biosynthesis. , 2013, Pest management science.

[48]  C. Délye.  Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: a major challenge for weed science in the forthcoming decade. , 2013, Pest management science.

[49]  François J. Tardif,et al.  Herbicide cross resistance in weeds , 2012 .

[50]  H. Imaishi,et al.  Isolation and functional characterization in yeast of CYP72A18, a rice cytochrome P450 that catalyzes (ω-1)-hydroxylation of the herbicide pelargonic acid , 2007 .

[51]  Xiangjing Wang,et al.  Expression of a wheat cytochrome P450 monooxygenase cDNA in yeast catalyzes the metabolism of sulfonylurea herbicides , 2006 .

[52]  Y. Sunohara,et al.  Oxidative injury induced by the herbicide quinclorac on Echinochloa oryzicola Vasing. and the involvement of antioxidative ability in its highly selective action in grass species , 2004 .

[53]  J. Holtum,et al.  Cross-Resistance to Herbicides in Annual Ryegrass (Lolium rigidum) : II. Chlorsulfuron Resistance Involves a Wheat-Like Detoxification System. , 1991, Plant physiology.

[54]  M. S. Bhullar,et al.  Seed bank dynamics and emergence pattern of weeds as affected by tillage systems in dry direct-seeded rice , 2015 .