Skip to main content
Log in

Assessment of ACC and P450 Genes Expression in Wild Oat (Avena ludoviciana) in Different Tissues Under Herbicide Application

  • Original Article
  • Published:
Biochemical Genetics Aims and scope Submit manuscript

A Correction to this article was published on 10 June 2023

This article has been updated

Abstract

Target-site resistance (TSR) and non-target-site resistance (NTSR) to herbicides in arable weeds are increasing rapidly all over the world and threatening universal food safety. Resistance to herbicides that inhibit ACCase activity has been identified in wild oat. In this study, expression of ACC1, ACC2, CYP71R4 and CYP81B1 genes under herbicide stress conditions were studied in two TSR (resistant in the residue Ile1781-Leu and Ile2041-Asn of ACCase) biotypes, two NTSR biotypes and one susceptible biotype of A. ludoviciana for the first time. Treated and untreated biotypes with ACCase-inhibitor clodinafop propargyl herbicide were sampled from the stem and leaf tissues at 24 h after treatment. Our results showed an increase in gene expression levels in different tissues of both types of resistance biotypes that occurred under herbicide treatment compared with non-herbicide treatment. In all samples, the expression levels of leaf tissue in all studied genes were higher than in stem tissue. The results of ACC gene expression showed that the expression level of ACC1 was significantly higher than that of ACC2. Also, expression levels of TSR biotypes were higher than NTSR biotypes for the ACC1 gene. For both CYP71R4 and CYP81B1 genes, the expression ratio increased significantly in TSR and NTSR biotypes in different tissues after herbicide treatment. In contrast, the expression levels of CYP genes in NTSR biotypes were higher than in TSR biotypes. Our results support the hypothesis that the reaction of plants to herbicide is carried out through a different regulation of genes, which can be the result of the interaction of resistance type in the target or non-target-site.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Change history

Abbreviations

ACCase:

Acetyl-CoA carboxylase

GTs:

Glucosyltransferases

GSTs:

Glutathione S-transferases

TSR:

Target-site resistance

NTSR:

Non-target-site resistance

CYP:

Cytochrome P450 monooxygenase

qPCR:

Quantitative polymerase chain reaction

References

  • Akbarabadi A, Ismaili A, Kahrizi D, Nazarian FF (2018) Validation of expression stability of reference genes in response to herbicide stress in wild oat (Avena ludoviciana). Cell Mol Biol 64:113–118

    Article  PubMed  Google Scholar 

  • Apte A, Singh S (2007) AlleleID. In: Yuryev, A. (eds) PCR Primer Design. Methods in Molecular Biology™, vol 402. Humana Press.

  • Awasthi M, Singh S, Pandey VP, Dwivedi UN (2015) Molecular docking and 3D-QSAR-based virtual screening of flavonoids as potential aromatase inhibitors against estrogen-dependent breast cancer. J Biomol Struct Dyn 33:804–819

    Article  CAS  PubMed  Google Scholar 

  • Azeez S, Jafar S, Aziziaram Z, Fang L, Mawlood A, Ercisli M (2021) Insulin-producing cells from bone marrow stem cells versus injectable insulin for the treatment of rats with type I diabetes. Cell Mol Biomed Rep 1(1):42–51

    Article  Google Scholar 

  • Aziziaram Z, Bilal I, Zhong Y, Mahmod A, Roshandel M (2021) Protective effects of curcumin against naproxen-induced mitochondrial dysfunction in rat kidney tissue. Cell Mol Biomed Rep 1(1):23–32

    Article  Google Scholar 

  • Beckie HJ, Tardif FJ (2012) Herbicide cross resistance in weeds. Crop Protect 35:15–28

    Article  CAS  Google Scholar 

  • Beckie HJ, Warwick SI, Sauder CA (2012) Basis for herbicide resistance in Canadian populations of wild oat (Avena fatua). Weed Sci 60:10–18

    Article  CAS  Google Scholar 

  • Bilal I, Xie S, Elburki M, Aziziaram Z, Ahmed S, Jalal Balaky S (2021) Cytotoxic effect of diferuloylmethane, a derivative of turmeric on different human glioblastoma cell lines. Cell Mol Biomed Rep 1(1):14–22

    Article  Google Scholar 

  • Busi R, Vila-Aiub M, Powles S (2011) Genetic control of a cytochrome P450 metabolism-based herbicide resistance mechanism in Lolium rigidum. Heredity 106:817–824

    Article  CAS  PubMed  Google Scholar 

  • Carey VF, Hoagland RE, Talbert RE (1997) Resistance mechanism of propanil-resistant barnyardgrass: II. In-vivo metabolism of the propanil molecule. Pest Manag Sci 49:333–338

    Article  CAS  Google Scholar 

  • Chao WS (2008) Real-time PCR as a tool to study weed biology. Weed Sci 56:290–296

    Article  CAS  Google Scholar 

  • Christopher JT, Powles SB, Liljegren DR, Holtum JA (1991) Cross-resistance to herbicides in annual ryegrass (Lolium rigidum) II. chlorsulfuron resistance involves a wheat-like detoxification system. Plant Physiol 95:1036–1043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Christopher JT, Preston C, Powles SB (1994) Malathion antagonizes metabolism-based chlorsulfuron resistance in Lolium rigidum. Pestic Biochem Physiol 49:172–182

    Article  CAS  Google Scholar 

  • Delye C (2013) Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: a major challenge for weed science in the forthcoming decade. Pest Manag Sci 69:176–187

    Article  CAS  PubMed  Google Scholar 

  • Duhoux A, Délye C (2013) Reference genes to study herbicide stress response in Lolium sp.: up-regulation of P450 genes in plants resistant to acetolactate-synthase inhibitors. PLoS ONE 8:e63576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Duhoux A, Carrère S, Gouzy J, Bonin L, Délye C (2015) RNA-Seq analysis of rye-grass transcriptomic response to an herbicide inhibiting acetolactate-synthase identifies transcripts linked to non-target-site-based resistance. Plant Mol Biol 87:473–487

    Article  CAS  PubMed  Google Scholar 

  • Ercisli M, Lechun G, Azeez S, Hamasalih R, Song S, Aziziaram Z (2021) Relevance of genetic polymorphisms of the human cytochrome P450 3A4 in rivaroxaban-treated patients. Cell Mol Biomed Rep 1(1):33–41

    Article  Google Scholar 

  • Faramarzi S, Hutabarat O (2021) Zinc sulfate and bordeaux mixture treatment towards witches’ broom disease of Mexican Lime in South of Iran. Agrotech Ind Crops 1(2):85–90. https://doi.org/10.22126/atic.2021.6526.1016

    Article  Google Scholar 

  • Fathi A, Barak M, Damandan M, Amani F, Moradpour R, Khalilova I, Valizadeh M (2021) Neonatal screening for glucose-6-phosphate dehydrogenase deficiency in Ardabil Province, Iran, 2018–2019. Cell Mol Biomed Rep 1(1):1–6

    Article  Google Scholar 

  • Fodor SP, Read JL, Pirrung MC, Stryer L, Lu AT, Solas D (1991) Light-directed, spatially addressable parallel chemical synthesis. Science. https://doi.org/10.1126/science.1990438

    Article  PubMed  Google Scholar 

  • Gaines TA, Zhang W, Wang D, Bukun B, Chisholm ST, Shaner DL, Nissen SJ, Patzoldt WL, Tranel PJ, Culpepper AS (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc Nati Acad Sci 107:1029–1034

    Article  CAS  Google Scholar 

  • Gaines TA, Lorentz L, Figge A, Herrmann J, Maiwald F, Ott MC, Han H, Busi R, Yu Q, Powles SB (2014) RNA-Seq transcriptome analysis to identify genes involved in metabolism based diclofop resistance in Lolium rigidum. Plant J 78:865–876

    Article  CAS  PubMed  Google Scholar 

  • Gion K, Inui H, Takakuma K, Yamada T, Kambara Y, Nakai S, Fujiwara H, Miyamura T, Imaishi H, Ohkawa H (2014) Molecular mechanisms of herbicide-inducible gene expression of tobacco CYP71AH11 metabolizing the herbicide chlorotoluron. Pestic Biochem Physiol 108:49–57

    Article  CAS  PubMed  Google Scholar 

  • Glund S, Schoelch C, Thomas L, Niessen H, Stiller D, Roth G, Neubauer H (2012) Inhibition of acetyl-CoA carboxylase 2 enhances skeletal muscle fatty acid oxidation and improves whole-body glucose homeostasis in db/db mice. Diabetologia 55:2044–2053

    Article  CAS  PubMed  Google Scholar 

  • Hamberger B, Bak S (2013) Plant P450s as versatile drivers for evolution of species-specific chemical diversity. Philos Trans R Soc Lond B Biol Sci 368:20120426

    Article  PubMed  PubMed Central  Google Scholar 

  • Han H, Yu Q, Owen MJ, Cawthray GR, Powles SB (2016) Widespread occurrence of both metabolic and target-site herbicide resistance mechanisms in Lolium rigidum populations. Pest Manag Sci 72:255–263

    Article  CAS  PubMed  Google Scholar 

  • Harvey SE, Cheng C (2016) Methods for characterization of alternative RNA splicing. Long Non-Coding RNAs: methods and protoc. pp. 229–241.

  • Harwood HJ (2005) Treating the metabolic syndrome: acetyl-CoA carboxylase inhibition. Expert Opin Ther Targets 9:267–281

    Article  CAS  PubMed  Google Scholar 

  • Harwood HJ, Petras SF, Shelly LD, Zaccaro LM, Perry DA, Makowski MR, Hargrove DM, Martin KA, Tracey WR, Chapman JG (2003) Isozyme-nonselective N-substituted bipiperidylcarboxamide acetyl-CoA carboxylase inhibitors reduce tissue malonyl-CoA concentrations, inhibit fatty acid synthesis, and increase fatty acid oxidation in cultured cells and in experimental animals. J Biol Chem 278:37099–37111

    Article  CAS  PubMed  Google Scholar 

  • Heap I (2021) The international survey of herbicide resistant weeds. Online. Internet. Available www.weedscience.org. Accessed 17 June 2017

  • Higuchi R, Fockler C, Dollinger G, Watson R (1993) Kinetic PCR analysis: real-time monitoring of DNA amplification reactions. Nat Biotechnol 11:1026–1030

    Article  CAS  Google Scholar 

  • Iwakami S, Endo M, Saika H, Okuno J, Nakamura N, Yokoyama M, Watanabe H, Toki S, Uchino A, Inamura T (2014) Cytochrome P450 CYP81A12 and CYP81A21 are associated with resistance to two acetolactate synthase inhibitors in Echinochloa phyllopogon. Plant Physiol 165:618–629

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laforest M, Soufiane B, Simard MJ, Obeid K, Page E, Nurse RE (2017) Acetyl-CoA carboxylase overexpression in herbicide resistant large crabgrass (Digitaria sanguinalis). Pest Manag Sci 73:2227–2235

    Article  CAS  PubMed  Google Scholar 

  • Lv MZ, Chao DY, Shan JX, Zhu MZ, Shi M, Gao JP, Lin HX (2012) Rice carotenoid β-ring hydroxylase CYP97A4 is involved in lutein biosynthesis. Plant Cell Physiol 53:987–1002

    Article  CAS  PubMed  Google Scholar 

  • Matzrafi M, Peleg Z, Lati R (2021) Herbicide Resistance in Weed Management. Agronomy 11:280

    Article  Google Scholar 

  • McKenzie-Gopsill A, Graham G, Laforest M, Ibarra S, Hann S, Wagg C (2020) Occurrence and management of PSII-inhibitor-resistant Chenopodium album L. In Atlantic Canadian Potato Prod Agron 10:1396

    Google Scholar 

  • Mendes RR, Oliveira JRS, Takano HK, Adegas FS, Gaines TA, Dayan FE (2020) A Trp574Leu target-site mutation confers imazamox resistance in multiple herbicide-resistant wild poinsettia populations from Brazil. Agronomy 10:1057

    Article  CAS  Google Scholar 

  • Moreland DE, Corbin FT, McFarland JE (1993) Effects of safeners on the oxidation of multiple substrates by grain sorghum microsomes. Pestic Biochem Physiol 45:43–53

    Article  CAS  Google Scholar 

  • Nandula VK, Reddy KN, Rimando AM, Duke SO, Poston DH (2007) Glyphosate-resistant and-susceptible soybean (Glycine max) and canola (Brassica napus) dose response and metabolism relationships with glyphosate. J Agric Food Chem 55:3540–3545

    Article  PubMed  Google Scholar 

  • Neve P, Vila-Aiub M, Roux F (2009) Evolutionary-thinking in agricultural weed management. New Phytol 184:783–793

    Article  PubMed  Google Scholar 

  • Pan L, Wang Z, Cai J, Gao H, Zhao H, Dong L (2016) High-throughput sequencing reveals differential regulation of miRNAs in fenoxaprop-P-ethyl-resistant Beckmannia syzigachne. Sci Rep 6:28725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandian BA, Friesen A, Laforest M, Peterson DE, Vara Prasad PV, Jugulam M (2020) Confirmation and characterization of the first case of acetolactate synthase (ALS)-inhibitor-resistant wild buckwheat (Polygonum convolvulus) in the United States. Agronomy 10:1496

    Article  CAS  Google Scholar 

  • Preston C, Powles SB (1998) Amitrole inhibits diclofop metabolism and synergises diclofop-methyl in a diclofop-methyl-resistant biotype of Lolium rigidum. Pestic Biochem Physiol 62:179–189

    Article  CAS  Google Scholar 

  • Preston C, Tardif FJ, Christopher JT, Powles SB (1996) Multiple resistance to dissimilar herbicide chemistries in a biotype of Lolium rigidum due to enhanced activity of several herbicide degrading enzymes. Pestic Biochem Physiol 54:123–134

    Article  CAS  Google Scholar 

  • Saika H, Horita J, Taguchi-Shiobara F, Nonaka S, Nishizawa-Yokoi A, Iwakami S, Hori K, Matsumoto T, Tanaka T, Itoh T (2014) A novel rice cytochrome P450 gene, CYP72A31, confers tolerance to acetolactate synthase-inhibiting herbicides in rice and Arabidopsis. Plant Physiol 166:1232–1240

    Article  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Fritsch E, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Schena M, Shalon D, Davis RW, Brown PO (1995) Quantitative monitoring of gene expression patterns with a complementary DNA microarray. Science 270:467–470

    Article  CAS  PubMed  Google Scholar 

  • Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3:1101

    Article  CAS  PubMed  Google Scholar 

  • Shaner DL, Lindenmeyer RB, Ostlie MH (2012) What have the mechanisms of resistance to glyphosate taught us? Pest Manag Sci 68:3–9

    Article  CAS  PubMed  Google Scholar 

  • Siminszky B (2006) Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:445–458

    Article  CAS  Google Scholar 

  • Tourang M, Fang L, Zhong Y, Suthar R (2021) Association between human endogenous retrovirus K gene expression and breast cancer. Cell Mol Biomed Rep 1(1):7–13

    Article  Google Scholar 

  • Travlos I, Kanatas P, Tsekoura A, Gazoulis I, Papastylianou P, Kakabouki I, Antonopoulos N (2020) Efficacy of different herbicides on Echinochloa colona (L.) link control and the first case of its glyphosate resistance in Greece. Agronomy 10:1056

    Article  CAS  Google Scholar 

  • Tsujii H, Dillon N, Ohkawa H (2004) Molecular functions of cytochrome P450 species involved in herbicide resistance in Lolium rigidum biotype WLR2, Int. Symp. Cytochrome P450: Biodiversity and Biotechnology, 7th, Hyogo, Japan. pp. 69.

  • Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484

    Article  CAS  PubMed  Google Scholar 

  • Yang J, Wang Y, Zhang Y (2016a) ResQ: an approach to unified estimation of B-factor and residue-specific error in protein structure prediction. J Mol Biol 428:693–701

    Article  CAS  PubMed  Google Scholar 

  • Yang Q, Deng W, Li X, Yu Q, Bai L, Zheng M (2016b) Target-site and non-target-site based resistance to the herbicide tribenuron-methyl in flixweed (Descurainia sophia L). BMC Genom 17:551

    Article  Google Scholar 

  • Yu Q, Powles S (2014a) Metabolism-based herbicide resistance and cross-resistance in crop weeds: a threat to herbicide sustainability and global crop production. Plant Physiol 166:1106–1118

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Powles SB (2014b) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:1340–1350

    Article  CAS  PubMed  Google Scholar 

  • Yuan JS, Tranel PJ, Stewart CN (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci 12:6–13

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Lorestan University, Khorramabad, Iran, supports this project.

Funding

Lorestan University, Khorramabad, Iran.

Author information

Authors and Affiliations

Authors

Contributions

Software, AA; Supervision, AI and DK; Writing, review and editing, FNF and SE; Research, AA; All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Danial Kahrizi.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical Approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Informed Consent

This article does not contain any studies with human participants.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

The original online version of this article was revised: The authors “Ali Akbarabadi and Ahmad Ismaili” affiliations have been mentioned correctly now.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Akbarabadi, A., Ismaili, A., Nazarian Firouzabadi, F. et al. Assessment of ACC and P450 Genes Expression in Wild Oat (Avena ludoviciana) in Different Tissues Under Herbicide Application. Biochem Genet 61, 1867–1879 (2023). https://doi.org/10.1007/s10528-023-10357-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10528-023-10357-1

Keywords

Navigation