Planta

, Volume 247, Issue 3, pp 693–703 | Cite as

Characterization of an acetohydroxy acid synthase mutant conferring tolerance to imidazolinone herbicides in rice (Oryza sativa)

  • Zhongze Piao
  • Wei Wang
  • Yinan Wei
  • Francesco Zonta
  • Changzhao Wan
  • Jianjiang Bai
  • Shujun Wu
  • Xinqi Wang
  • Jun Fang
Original Article

Abstract

Main conclusion

The acetohydroxy acid synthase S627N mutation confers herbicide tolerance in rice, and the rice variety containing this mutation produces good yields. This variety is commercially viable at Shanghai and Jiangsu regions in China.

Weedy rice is a type of rice that produces lower yields and poorer quality grains than cultivated rice. It plagues commercial rice fields in many countries. One strategy to control its proliferation is to develop rice varieties that are tolerant to specific herbicides. Acetohydroxy acid synthase (AHAS) mutations have been found to confer herbicide tolerance to rice. Here, we identified a single mutation (S627N) in AHAS from an indica rice variety that conferred tolerance against imidazolinone herbicides, including imazethapyr and imazamox. A japonica rice variety (JD164) was developed to obtain herbicide tolerance by introducing the mutated indica ahas gene. Imidazolinone application was sufficient to efficiently control weedy rice in the JD164 field. Although the imazethapyr treatment caused dwarfing in the JD164 plants, it did not significantly reduce yields. To determine whether the decrease of the ahas mRNA expression caused the dwarfism of JD164 after imazethapyr application, we detected the ahas mRNA level in plants. The abundance of the ahas mRNA in JD164 increased after imidazolinone application, thus excluding the mRNA expression level as a possible cause of dwarfism. Activity assays showed that the mutated AHAS was tolerant to imidazolinone but the catalytic efficiency of the mutated AHAS decreased in its presence. Moreover, the activity of the mutated AHAS decreased more in the presence of imazethapyr than in the presence of imazamox. We observed no difference in the AHAS secondary structures, but homology modeling suggested that the S627N mutation enabled the substrate to access the active site channel in AHAS, resulting in imidazolinone tolerance. Our work combined herbicides with a rice variety to control weedy rice and showed the mechanism of herbicide tolerance in this rice variety.

Keywords

S627N mutation JD164 Yields Activities Molecular structures 

Notes

Acknowledgements

The research was funded by Grants to Jun Fang from Natural Science Foundation of Shanghai (No. 15ZR1436500), Foundation of Shanghai Agricultural Talents (No. HNQZ2016-1-1), Key Project of Agriculture Science and Technology of Shanghai (No. HNKGZ2015-6-1-3) and SAAS Excellent Research Team (No. NKC2017A05).

References

  1. Akhgari H, Kaviani B (2011) Assessment of direct seeded and transplanting methods of rice cultivars in the northern part of Iran. Afr J Agric Res 6(3):6492–6498Google Scholar
  2. Biasini M, Bienert S, Waterhouse A, Arnold K, Studer G, Schmidt T, Kiefer F, Gallo Cassarino T, Bertoni M, Bordoli L, Schwede T (2014) SWISS-MODEL: modelling protein tertiary and quaternary structure using evolutionary information. Nucl Acids Res 42(Web Server issue):252–258.  https://doi.org/10.1093/nar/gku340 CrossRefGoogle Scholar
  3. Chang AK, Duggleby RG (1997) Expression, purification and characterization of Arabidopsis thaliana acetohydroxyacid synthase. Biochem J 327:161–169CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chauhan BS (2013) Strategies to manage weedy rice in Asia. Crop Prot 48:51–56CrossRefGoogle Scholar
  5. Chen X, Qiang S, Yang J, Zhang B, Zhang Z, Song X, Dai W (2015) Hierarchical clustering and indica-japonica classification: uncover mutual spread and indica-japonica differentiation for weedy rice in Jiangsu province. Chin J Rice Sci 1:82–90Google Scholar
  6. Chong C-K, Choi J-D (2000) Amino acid residues conferring herbicide tolerance in tobacco acetolactate synthase. Biochem Biophys Res Commun 279:462–467CrossRefPubMedGoogle Scholar
  7. Choudhary B, Gheysen G, Buysse J, Pvd Meer, Burssens S (2014) Regulatory options for genetically modified crops in India. Plant Biotechnol J 12(2):135–146CrossRefPubMedGoogle Scholar
  8. Duggleby RG, McCourt JA, Guddat LW (2008) Structure and mechanism of inhibition of plant acetohydroxyacid synthase. Plant Physiol Biochem 46(3):309–324.  https://doi.org/10.1016/j.plaphy.2007.12.004 CrossRefPubMedGoogle Scholar
  9. Farooq M, Siddique KHM, Rehman HU, Aziz T, Lee DL, Wahid A (2011) Rice direct seeding: experiences, challenges and opportunities. Soil Tillage Res 111(2):87–98CrossRefGoogle Scholar
  10. Garcia MD, Nouwens A, Lonhienne TG, Guddat LW (2017) Comprehensive understanding of acetohydroxyacid synthase inhibition by different herbicide families. Proc Natl Acad Sci USA.  https://doi.org/10.1073/pnas.1616142114 Google Scholar
  11. Gutteridge S, Thompson ME, Ort O, Shaner DL, Stidham M, Singh B, Tan S, Johnson TC, Mann RK, Schmitzer PR, Gast RE, deBoer GJ, Yoshimura T, Hanai R (2012) Acetohydroxyacid synthase inhibitors (AHAS/ALS). In: Krämer W, Schirmer U, Jeschke P and Witschel M (eds) Modern Crop Protection Compounds, 2nd edn. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim, Germany, pp 29–162CrossRefGoogle Scholar
  12. Guttieri MJ, Eberlein CV, Mallory-Smith CA, Hoffman DL (1992) DNA-sequence variation in domain a of the acetolactate synthase genes of herbicide-resistant and herbicide-susceptible weed biotypes. Weed Sci 40:670–676Google Scholar
  13. Haughn GW, Somerville CR (1990) A mutation causing imidazolinone resistance maps to the csr1 locus of Arabidopsis thaliana. Plant Physiol 92(4):1081–1085CrossRefPubMedPubMedCentralGoogle Scholar
  14. Huang X, Yang S, Gong J, Zhao Q, Feng Q, Zhan Q, Zhao Y, Li W, Cheng B, Xia J, Chen N, Huang T, Zhang L, Fan D, Chen J, Zhou C, Yiqi L, Weng Q, Han B (2016) Genomic architecture of heterosis for yield traits in rice. Nature 537:329–633Google Scholar
  15. Islam MK, Islam MS, Biswas JK, Siyoung L, Alam I, Mooryong H (2014) Screening of rice varieties for direct seeding method. Aust J Crop Sci 8(4):536–542Google Scholar
  16. Jung SM, Le DT, Yoon SS, Yoon MY, Kim YT, Choi J-D (2004) Amino acid residues conferring herbicide resistance in tobacco acetohydroxy acid synthase. Biochem J 383:53–61CrossRefPubMedPubMedCentralGoogle Scholar
  17. Kanapeckas KL, Vigueira CC, Ortiz A, Gettler KA, Burgos NR, Fischer AJ, Lawton-Rauh AL (2016) Escape to ferality: the endoferal origin of weedy rice from crop rice through de-domestication. PLoS One 11(9):e0162676.  https://doi.org/10.1371/journal.pone.0162676 CrossRefPubMedPubMedCentralGoogle Scholar
  18. Kawai K, Kaku K, Izawa N, Shimizu T, Fukuda A, Tanaka Y (2007) A novel mutant acetolactate synthase gene from rice cells which confers resistance to ALS-inhibiting herbicides. J Pestic Sci 32(2):89–98CrossRefGoogle Scholar
  19. Koch AC, Ramgareeb S, Rutherford RS, Snyman SJ, Watt MP (2012) An in vitro mutagenesis protocol for the production of sugarcane tolerant to the herbicide imazapyr. In Vitro Cell Dev Biol 48:417–427CrossRefGoogle Scholar
  20. Lea DT, Yoon MY, Kimc YT, Choi J-D (2005) Two consecutive aspartic acid residues conferring herbicide resistance in tobacco acetohydroxy acid synthase. Biochim Biophys Acta 1749:103–112CrossRefGoogle Scholar
  21. Lee YT, Duggleby RG (2001) Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochemistry 40(23):6836–6844CrossRefPubMedGoogle Scholar
  22. Lee YT, Chang AK, Duggleby RG (1999) Effect of mutagenesis at serine 653 of Arabidopsis thaliana acetohydroxyacid synthase on the sensitivity to imidazolinone and sulfonylurea herbicides. FEBS Lett 452:341–345CrossRefPubMedGoogle Scholar
  23. Li T, Liu B, Chen CY, Yang B (2016) TALEN-mediated homologous recombination produces site-directed dna base change and herbicide-resistant rice. J Genet Genom 43:291–305Google Scholar
  24. Liang Y, Guo S, Yin L (2014) Comparative study on morphological differences between weedy rice and cultivate rice in Shanghai area. J Shanghai Norm Univ (Nat Sci) 43(1):87–97Google Scholar
  25. Liu Y, Li Y, Wang X (2016) Acetohydroxyacid synthases: evolution, structure, and function. Appl Microbiol Biotechnol 100(20):8633–8649.  https://doi.org/10.1007/s00253-016-7809-9 CrossRefPubMedGoogle Scholar
  26. Mallory-Smith CA, Thill DC, Dial MJ (1990) Identification of sulfonylurea herbicide-resistant prickly lettuce (Lactuca serriola). Weed Technol 4(1):163–168Google Scholar
  27. McCourt JA, Pang SS, King-Scott J, Guddat LW, Duggleby RG (2006) Herbicide-binding sites revealed in the structure of plant acetohydroxyacid synthase. Proc Natl Acad Sci USA 103(3):569–573.  https://doi.org/10.1073/pnas.0508701103 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Muthayya S, Sugimoto JD, Montgomery S, Maberly GF (2014) An overview of global rice production, supply, trade, and consumption. Ann N Y Acad Sci 1324:7–14.  https://doi.org/10.1111/nyas.12540 CrossRefPubMedGoogle Scholar
  29. Nelson KA, Renner KA, Penner D (1998) Weed control in soybean (Glycine max) with imazamox and imazethapyr. Weed Sci 46(5):587–594Google Scholar
  30. Normile D (2014) China pulls plug on genetically modified rice and corn. Science. http://www.sciencemag.org/news/2014/08/china-pulls-plug-genetically-modified-rice-and-corn. Accessed 20 Aug 2014
  31. Oh KJ, Park EJ, Yoon MY, Han TR, Choi JD (2001) Roles of histidine residues in tobacco acetolactate synthase. Biochem Biophys Res Commun 282(5):1237–1243.  https://doi.org/10.1006/bbrc.2001.4714 CrossRefPubMedGoogle Scholar
  32. O’Sullivan J, Thomas RJ, Bouw WJ (1998) Effect of imazethapyr and imazamox soil residues on several vegetable crops grown in Ontario. Can J Plant Sci 78(4):647–651CrossRefGoogle Scholar
  33. Ott KH, Kwagh JG, Stockton GW, Sidorov V, Kakefuda G (1996) Rational molecular design and genetic engineering of herbicide resistant crops by structure modeling and site-directed mutagenesis of acetohydroxyacid synthase. J Mol Biol 263(2):359–368.  https://doi.org/10.1006/jmbi.1996.0580 CrossRefPubMedGoogle Scholar
  34. Owen MD, Beckie HJ, Leeson JY, Norsworthy JK, Steckel LE (2015) Integrated pest management and weed management in the United States and Canada. Pest Manag Sci 71(3):357–376.  https://doi.org/10.1002/ps.3928 CrossRefPubMedGoogle Scholar
  35. Sun Y, Zhang X, Wu C, He Y, Ma Y, Hou H, Guo X, Du W, Zhao Y, Xia L (2016) Engineering herbicide-resistant rice plants through CRISPR/Cas9-mediated homologous recombination of acetolactate synthase. Mol Plant 9(4):628–631CrossRefPubMedGoogle Scholar
  36. Tan S, Evans RR, Dahmer ML, Singh BK, Shaner DL (2005) Imidazolinone-tolerant crops: history, current status and future. Pest Manag Sci 61(3):246–257.  https://doi.org/10.1002/ps.993 CrossRefPubMedGoogle Scholar
  37. Tan S, Evans R, Singh B (2006) Herbicidal inhibitors of amino acid biosynthesis and herbicide-tolerant crops. Amino Acids 30(2):195–204.  https://doi.org/10.1007/s00726-005-0254-1 CrossRefPubMedGoogle Scholar
  38. Wang Z, Rong J, B-r Lu (2015) Occurence and damage of weedy rice and its threats to rice production in China. Weed Sci (China) 33(1):1–9Google Scholar
  39. Yi SY, Cui Y, Zhao Y, Liu ZD, Lin YJ, Zhou F (2016) A novel naturally occurring class I 5-enolpyruvylshikimate-3-phosphate synthase from Janibacter sp. confers high glyphosate tolerance to rice. Sci Rep 6:19104.  https://doi.org/10.1038/srep19104 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Yoon TY, Chung SM, Chang SI, Yoon MY, Hahn TR, Choi JD (2002) Roles of lysine 219 and 255 residues in tobacco acetolactate synthase. Biochem Biophys Res Commun 293(1):433–439.  https://doi.org/10.1016/S0006-291X(02)00249-8 CrossRefPubMedGoogle Scholar
  41. Yu Q, Powles SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70(9):1340–1350.  https://doi.org/10.1002/ps.3710 CrossRefPubMedGoogle Scholar
  42. Zeng D, Tian Z, Rao Y, Dong G, Yang Y, Huang L, Leng Y, Xu J, Sun C, Zhang G, Hu J, Zhu L, Gao Z, Hu X, Guo L, Xiong G, Wang Y, Li J, Qian Q (2017) Rational design of high-yield and superior-quality rice. Nat Plants 3:17031.  https://doi.org/10.1038/nplants.2017.31 CrossRefPubMedGoogle Scholar
  43. Zhang L, Chen H, Li Y, Li Y, Wang S, Su J, Liu X, Chen D, Chen X (2014) Evaluation of the agronomic performance of atrazine-tolerant transgenic japonica rice parental lines for utilization in hybrid seed production. PLoS One 9(9):e108569.  https://doi.org/10.1371/journal.pone.0108569 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2017

Authors and Affiliations

  1. 1.Crop Breeding and Cultivating InstituteShanghai Academy of Agriculture SciencesShanghaiChina
  2. 2.Shanghai Institute for Advanced Immunochemical StudiesShanghaiTech UniversityShanghaiChina
  3. 3.Department of ChemistryUniversity of KentuckyLexingtonUSA
  4. 4.Department of Biomedical Sciences, Institute of Cell Biology and NeurobiologyItalian National Research CouncilMonterotondoItaly

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