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Molecular and biochemical characterization of an induced mutation conferring imidazolinone resistance in sunflower

  • Carlos A. Sala
  • Mariano Bulos
  • Mariel Echarte
  • Sherry R. Whitt
  • Robert Ascenzi
Original Paper

Abstract

A partially dominant nuclear gene conferring resistance to the imidazolinone herbicides was previously identified in the cultivated sunflower (Helianthus annuus L.) line CLHA-Plus developed by seed mutagenesis. The objective of this study was to characterize this resistant gene at the phenotypic, biochemical and molecular levels. CLHA-Plus showed a complete susceptibility to sulfonylureas (metsulfuron, tribenuron and chlorsulfuron) but, on the other hand, it showed a complete resistance to imidazolinones (imazamox, imazapyr and imazapic) at two rates of herbicide application. This pattern was in close association with the AHAS-inhibition kinetics of protein extracts of CLHA-Plus challenged with different doses of imazamox and chlorsulfuron. Nucleotide and deduced amino acid sequence comparisons between resistant and susceptible lines indicated that the imidazolinone-resistant AHAS of CLHA-Plus has a threonine codon (ACG) at position 122 (relative to the Arabidopsis thaliana AHAS sequence), whereas the herbicide-susceptible enzyme from BTK47 has an alanine residue (GCG) at this position. Since the resistance genes to AHAS-inhibiting herbicides so far characterized in sunflower code for the catalytic (large) subunit of AHAS, we propose to redesignate the wild type allele as ahasl1 and the incomplete dominant resistant alleles as Ahasl1-1 (previously Imr1 or Ar pur ), Ahasl1-2 (previously Ar kan ) and Ahasl1-3 (for the allele present in CLHA-Plus). The higher tolerance level to imidazolinones and the lack of cross-resistance to other AHAS-inhibiting herbicides of Ahasl1-3 indicate that this induced mutation can be used to develop commercial hybrids with superior levels of tolerance and, at the same time, to assist weed management where control of weedy common sunflower is necessary.

Keywords

Sulfonylurea Chlorsulfuron Imazapyr Metsulfuron Methyl Lower Asymptote 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Al-Khatib K, Baumgartner JR, Peterson DE, Currie RS (1998) Imazethapyr resistance in common sunflower (Helianthus annuus). Weed Sci 46:403–407Google Scholar
  2. Al-Khatib K, Miller JF (2002) Registration of four genetic stocks of sunflower resistant to imidazolinone herbicides. Crop Sci 40:869–870Google Scholar
  3. Anderson PC, Georgeson M (1989) Herbicide-tolerant mutants of corn. Genome 34:994–999Google Scholar
  4. Ashburner M (1990) Drosophila: a Laboratory Handbook. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  5. Bently A, Mac Lennan B, Calvo J, Dearolf CR (2000) Targeted recovery of mutations in Drosophila. Genetics 156:1169–1173Google Scholar
  6. Bernasconi P, Woodworth AR, Rosen BA, Subramanian MV, Siehl DL (1995) A naturally occurring point mutation confers broad range tolerance to herbicides that target acetolactate synthase. J Biol Chem 270:17381–17385PubMedCrossRefGoogle Scholar
  7. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Ann Biochem 72:248–254CrossRefGoogle Scholar
  8. Bruniard JM, Miller JF (2001) Inheritance of imidazolinone herbicide resistance in sunflower. Helia 24:11–16Google Scholar
  9. Chong CK, Choi JD (2000) Amino acid residues conferring herbicide tolerance in tobacco acetolactate synthase. Biochem Biophys Res Commun 279:462–467PubMedCrossRefGoogle Scholar
  10. Croughan TP (1996) Herbicide resistant rice. US Patent 5,545,822Google Scholar
  11. D’Halluin KM, Bossut M, Bonne E, Mazur B, Leemans J, Botterman J (1992) Transformation of sugarbeet (Beta vulgaris L.) and evaluation of herbicide resistance in transgenic plants. Biotechnology 10:309–314CrossRefGoogle Scholar
  12. Duggleby RG, Pang SS (2000) Acetohydroxyacid synthase. J Biochem Mol Biol 33:1–36Google Scholar
  13. Duggleby RG, McCourt JA, Guddat L (2008) Structure and mechanism of inhibition of plant acetohydroxiacid synthase. Plant Physiol Biochem 46:309–324PubMedCrossRefGoogle Scholar
  14. Faure N, Serieys H, Bervillé A (2002) Potential gene flow from cultivated sunflower to volunteer, wild Helianthus species in Europe. Agric Ecosyst Environ 89:183–190CrossRefGoogle Scholar
  15. Grula JW, Hudspeth RL, Hobbs SL, Anderson DM (1995) Organization, inheritance and expression of acetohydroxyacid synthase genes in the cotton allotetraploid Gossypium hirsutum. Plant Mol Biol 28:837–846PubMedCrossRefGoogle Scholar
  16. Guttieri MJ, Eberlein CV, Mallory-Smith CA, Thill DC, Hoffman DL (1992) DNA sequence variation in domain A of the acetolactate synthase genes of herbicide-resistant and -susceptible weed biotypes. Weed Sci 40:670–676Google Scholar
  17. Guttieri MJ, Eberlein CV, Thill DC (1995) Diverse mutations in the acetolactate synthase allele confer chlorsulfuron resistance in Kochia scoparia biotypes. Weed Sci 43:175–178Google Scholar
  18. Harms CT, Armour SL, DiMaio JJ, Middlesteadt LA, Murray D, Negrotto DV, Thompson-Tyler H, Weymann K, Montoya AL, Shillito RD, Jen GC (1992) Herbicide resistance due to amplification of a mutant acetohydroxyacid synthase allele. Mol Gen Genet 233:427–435PubMedCrossRefGoogle Scholar
  19. Hart SE, Saunders JW, Penner D (1992) Chlorsulfuron resistant sugar beet: cross-resistance and physiological basis of resistance. Weed Sci 40:378–383Google Scholar
  20. Haughn GW, Smith J, Mazur B, Somerville C (1988) Transformation with a mutant Arabidopsis acetolactate synthase gene renders tobacco resistant to sulfonylureas. Mol Gen Genet 211:266–271CrossRefGoogle Scholar
  21. Inukai T, Sako A, Hirano HY, Sano Y (2000) Analysis of intragenic recombination at wx in rice: correlation between molecular and genetic maps within the locus. Genome 43:589–596PubMedCrossRefGoogle Scholar
  22. Jander G, Baerson SR, Hudak JA, Gonzalez KA, Gruys KJ, Last RL (2003) Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol 131:139–146PubMedCrossRefGoogle Scholar
  23. Kolkman JM, Slabaugh MB, Bruniard JM, Berry S, Bushman BS, Olungu C, Maes N, Abratti G, Zambelli A, Miller JF, Leon A, Knapp SJ (2004) Acetohydroxyacid synthase mutations conferring resistance to imidazolinone or sulfonylurea herbicides in sunflower. Theor Appl Genet 109:1147–1159PubMedCrossRefGoogle Scholar
  24. Kozik A, Michelmore RW, Knapp SJ, Matvienko MS, Rieseberg L, Lin H, van Damme M, Lavelle D, Chevalier P, Ziegle J, Ellison P, Kolkman JM, Slabaugh MB, Livingston K, Zhou LZ, Church S, Edberg S, Jackson L, Kesseli R, Bradford K (2002) Sunflower and lettuce ESTs from the compositae genome project. http://compgenomics.ucdavis.edu
  25. Lee YT, Duggleby RG (2001) Identification of the regulatory subunit of Arabidopsis thaliana acetohydroxyacid synthase and reconstitution with its catalytic subunit. Biochem 40:6836–6844CrossRefGoogle Scholar
  26. Lee YT, Duggleby RG (2002) Regulatory interactions in Arabidopsis thaliana acetohydroxyacid synthase. FEBS Lett 512:180–184PubMedCrossRefGoogle Scholar
  27. Lee KY, Townsend J, Tepperman J, Black M, Chui CF, Mazur B, Dunsmuir P, Bedbrook J (1988) The molecular basis of sulfonylurea resistance in tobacco. EMBO J 7:1241–1248PubMedGoogle Scholar
  28. Mallory-Smith CA, Thill DC, Dial MJ (1990) Identification of sulfonylurea herbicide-resistant prickly lettuce (Lactuca serriola). Weed Technol 4:163–168Google Scholar
  29. Marshall MW, Al-Khatib K, Loughin T (2001) Gene flow, growth, and competitiveness of imazethapyr-resistant common sunflower. Weed Sci 49:14–21CrossRefGoogle Scholar
  30. Massinga RA, Al-Khatib K, Amand PSt, Miller JF (2003) Gene flow from imidazolinone-resistant domesticated sunflower to wild relatives. Weed Sci 51:854–862CrossRefGoogle Scholar
  31. McCourt JA, Duggleby RG (2006) Acetohydroxyacid synthase and its role en the biosynthetic pathway for branched-chain amino acids. Amino Acids 31:173PubMedCrossRefGoogle Scholar
  32. 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 103:569–573PubMedCrossRefGoogle Scholar
  33. McHughen A (1989) Agrobacterium mediated transfer of chlorsulfuron resistance to commercial flax cultivars. Plant Cell Rep 8:445–449CrossRefGoogle Scholar
  34. McNaughton KE, Letarte J, Lee EA, Tardif FJ (2005) Mutations in ALS confer herbicide resistance in redroot pigweed (Amaranthus retroflexus) and powell amaranth (Amaranthus powellii). Weed Sci 53:17–22CrossRefGoogle Scholar
  35. Miller JF, Al-Khatib K (2002) Registration of imidazolinone herbicide-resistant sunflower maintainer (HA425) and fertility restorer (RHA426 and RHA427) germplasms. Crop Sci 42:988–989Google Scholar
  36. Miller JF, Al-Khatib K (2004) Registration of two oilseed sunflower genetic stocks, SURES-1 and SURES-2, resistant to tribenuron herbicide. Crop Sci 44:1037–1038Google Scholar
  37. Milliman LD, Riechers DE, Wax LM, Simmons FW (2003) Characterization of two biotypes of imidazolinone-resistant eastern black nightshade (Solanum ptycanthum). Weed Sci 51:139–144CrossRefGoogle Scholar
  38. Mourad G, King J (1992) Effect of four classes of herbicides on growth and acetolactate synthase activity in several variants of Arabidopsis thaliana. Planta 188:491–497CrossRefGoogle Scholar
  39. Newhouse K, Singh BK, Shaner DL, Stidham M (1991) Mutations in corn (Zea mays L.) conferring resistance to imidazolinones. Theor Appl Genet 83:65–70CrossRefGoogle Scholar
  40. Newhouse K, Smith W, Starrett M, Schaefer T, Singh BK (1992) Tolerance to imidazolinone herbicides in wheat. Plant Physiol 100:882–886PubMedGoogle Scholar
  41. Ouellet T, Rutledge RG, Miki BL (1992) Members of the acetohydroxyacid synthase multigene family of Brassica napus have divergent patterns of expression. Plant J 2:321–330PubMedGoogle Scholar
  42. Powles SB, Holtum JAM (1994) Herbicide resistance in plants: biology and biochemistry. Lewis Publishers, Boca RatónGoogle Scholar
  43. Pozniak CJ, Hucl PJ (2004) Genetic analysis of imidazolinone resistance in mutation-derived lines of common wheat. Crop Sci 44:23–30Google Scholar
  44. Preston C, Mallory-Smith CA (2001) Biochemical mechanisms, inheritance, and molecular genetics of herbicide resistance in weeds. In: Powles SB, Shaner DL (eds) Herbicide resistance and world grains. CRC Press, Boca Raton, pp 23–60Google Scholar
  45. Rajasekaran K, Grula JW, Anderson DM (1996) Selection and characterization of mutant cotton (Gossypium hirsutum L.) cell lines resistant to sulfonylurea and imidazolinone herbicides. Plant Sci 199:115–124CrossRefGoogle Scholar
  46. Ray TB (1984) Site of action of chlorsulfuron. Inhibition of valine and isoleucine biosynthesis in plants. Plant Physiol 75:827–831PubMedCrossRefGoogle Scholar
  47. Saari LL, Cotterman JC, Thill DC (1994) Resistance to acetolactate synthase inhibiting herbicides. In: Powles SB, Holtum JAM (eds) Herbicide resistance in plants: biology and biochemistry. Lewis Publishers, Boca Ratón, pp 83–139Google Scholar
  48. Sala CA, Bulos M, Echarte AM (2008) Genetic analysis of an induced mutation conferring imidazolinone resistance in sunflower. Crop Sci (in press)Google Scholar
  49. Santel HJ, Bowden BA, Sorenson VM, Mueller KH, Reynolds J (1999) Flucarbazone-sodium—a new herbicide for grass control in wheat. Proc West Soc Weed Sci 52:124–125Google Scholar
  50. Schneiter AA, Miller JF (1981) Description of sunflower growth stages. Crop Sci 21:901–903Google Scholar
  51. Sebastian SA, Fader GM, Ulrich JF, Forney DR, Chaleff RS (1989) Semi-dominant soybean mutation for resistance to sulfonylurea herbicides. Crop Sci 29:1403–1408Google Scholar
  52. Seefeldt SS, Jensen JE, Fuerst EP (1995) Log-logistic analysis of herbicide dose response relationships. Weed Technol 9:218–227Google Scholar
  53. Shaner DL (1991) Physiological effects of the imidazolinone herbicides. In: Shaner DL, O’Connor SL (eds) The imidazolinone herbicides. Lewis, Ann Arbor, pp 129–138Google Scholar
  54. Shaner DL, Anderson PC, Stidham MA (1984) Imidazolinones: potent inhibitors of acetohydroxyacid synthase. Plant Physiol 76:545–546PubMedGoogle Scholar
  55. Singh BK (1999) Biosynthesis of valine, leucine and isoleucine. In: Singh BK (ed) Plant amino acids. Marcel Dekker Inc, New York, pp 227–247Google Scholar
  56. Singh BK, Stidham MA, Shaner DL (1988) Assay of acetohydroxyacid synthase. Ann Biochem 171:173–179CrossRefGoogle Scholar
  57. Snow ET, Foote RS, Mitra S (1984) Base-pairing properties of O-6-methylguanine in template DNA during in vitro DNA replication. J Biol Chem 259:8095–8100PubMedGoogle Scholar
  58. Subramanian MV, Gerwick BC (1989) Inhibition of acetolactate synthase by triazolopyrimidines: a review of recent developments. In: Whitaker JR, Sonnet PE (eds) Biocatalysis in agricultural biotechnology. American Chemical Society, Washington, pp 277–288Google Scholar
  59. Subramanian MV, Hung HY, Dias JM, Miner VW, Butler JH, Jachetta JJ (1990) Properties of mutant acetolactate synthases resistant to triazolopyrimidine sulfonanilide. Plant Physiol 94:239–244PubMedGoogle Scholar
  60. Swanson EB, Hergesell MJ, Arnoldo M, Sippell DW, Wong RSC (1989) Microspore mutagenesis and selection: canola plants with field tolerance to imidazolinones. Theor Appl Genet 78:525–530CrossRefGoogle Scholar
  61. Tan S, Evans RR, Dahmer ML, Singh BK, Shaner DL (2005) Imidazolinone-tolerant crops: history, current status and future. Pest Manag Sci 61:246–257PubMedCrossRefGoogle Scholar
  62. Tranel PJ, Wright TR (2002) Resistance of weeds to AHAS inhibiting herbicides: what have we learned? Weed Sci 50:700–712CrossRefGoogle Scholar
  63. Trucco F, Hager AG, Tranel PJ (2006) Acetolactate synthase mutation conferring imidazolinone-specific herbicide resistance in Amaranthus hybridus. J Plant Physiol 163:475–479PubMedCrossRefGoogle Scholar
  64. Umbarger HE (1978) Amino acid biosynthesis and its regulation. Annu Rev Biochem 47:533–606CrossRefGoogle Scholar
  65. White AD, Owen MD, Hartzler RG, Cardina J (2002) Common sunflower resistance to acetolactate-inhibiting herbicides. Weed Sci 50:432–437CrossRefGoogle Scholar
  66. Wright TR, Bascomb NF, Sturner SF, Penner D (1998) Biochemical mechanism and molecular basis for ALS-inhibiting herbicide resistance in sugar beet (Beta vulgaris) somatic cell selections. Weed Sci 46:13–23Google Scholar
  67. Wright TR, Penner D (1998) Cell selection and inheritance of imidazolinone resistance in sugar beet (Beta vulgaris). Theor Appl Genet 96:612–620CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2008

Authors and Affiliations

  • Carlos A. Sala
    • 1
  • Mariano Bulos
    • 1
  • Mariel Echarte
    • 1
  • Sherry R. Whitt
    • 2
  • Robert Ascenzi
    • 2
  1. 1.Biotechnology DepartmentNIDERA S.A.Venado TuertoArgentina
  2. 2.BASF Plant Science LLCResearch Triangle Park, DurhamUSA

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