Skip to main content
SpringerLink
Log in

Agronomic evaluation and molecular characterisation of the acetolactate synthase gene in imazapyr tolerant sugarcane (Saccharum hybrid) genotypes

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Mutagenesis had no effect on number of stalks/plot, stalk height, fibre and sucrose content of mutants. Imazapyr tolerance is likely due to a S622N mutation in the acetolactate synthase gene.

Abstract

The herbicidal compound imazapyr is effective against weeds such as Cynodon and Rottboellia species that constrain sugarcane production. This study aimed to compare agronomic characteristics of three imazapyr tolerant mutants (Mut 1, Mut 6 and Mut 7) with the non-mutated N12 control after 18 months of growth, and to sequence the acetolactate synthase (ALS) gene to identify any point mutations conferring imazapyr tolerance. There were no significant differences in the number of stalks/plot, stalk height, fibre and sucrose contents of the mutants compared with the N12 control. However, Mut 1 genotype was more susceptible to the Lepidopteran stalk borer, Eldana saccharina when compared with the non-mutated N12 (11.14 ± 1.37 and 3.89 ± 0.52% internodes bored, respectively), making Mut 1 less desirable for commercial cultivation. Molecular characterisation of the ALS gene revealed non-synonymous mutations in Mut 6. An A to G change at nucleotide position 1857 resulted in a N513D mutation, while a G to A change at nucleotide position 2184 imposed a S622N mutation. Molecular dynamics simulations revealed that the S622N mutation renders an asparagine side chain clash with imazapyr, hence this mutation is effective in conferring imazapyr tolerance.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Abraham MJ, Murtola T, Schulz R, Páll S, Smith JC, Hess B, Lindahl E (2015) CROMACS: high performance molecular simulations through multi-level parallelism from laptop to super computers. Software X1:19–25

    Article  Google Scholar 

  • Ali A, Alam S, Iqbal J (2007) In vitro induced mutation for screening of red rot (Colletotrichum falcatum) resistance in sugarcane (Saccharum officinarum). Pak J Bot 39:1979–1994

    Google Scholar 

  • Allen WJ, Balius TE, Mukherjee S, Brozell SR, Moustakas DT, Lang PT, Case DA, Kuntz ID, Rizzo RC (2015) DOCK6: impact of new features and current docking performance. J Comput Chem 36:1132–1156

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Anon (2005) South African Sugarcane Research Institute (SASRI). Guidelines and recommendations for Eldana control in the South African Sugar Industry. pp 1–18

  • Arencibia AD, Carmona ER, Maizeide MT, Castiglione S, O’Relly J, Chinea A, Aramas P, Sala F (1999) Somaclonal variation in insect-resistant transgenic sugarcane (Saccharum hybrid) plants produced by electroporation. Transgenic Res 8:349–360

    Article  CAS  Google Scholar 

  • Brooks CL, Case DA, Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, Roux B, Won Y, Archontis G, Bartels C, Boresch S, Caflisch A, Caves L, Cui Q, Dinner AR, Feig M, Fischer S, Gao J, Hodoscek M, Im W, Kuczera K, Lazaridis T, Ma J, Ovchinnikov V, Paci E, Pastor RW, Post CB, Pu JZ, Schaefer M, Tidor B, Venable RM, Woodcock HL, Wu X, Yang W, York DM, Karplus M (2009) CHARMM: the biomolecular simulation program. J Comput Chem 30(10):1545–1614

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Campbell PL (2008) Efficacy of glyphosate: alternative post-emergence herbicides and tillage for control of Cynodon dactylon. S Afr J Plant Soil 25:220–228

    Article  CAS  Google Scholar 

  • Cane Testing Service, South African Sugar Association (SASA). http://www.sasa.org.za/divisions/CaneTestingService.aspx. Accessed 10 Mar 2017

  • Chaleff RS, Ray TB (1984) Herbicide-resistant mutants from tobacco cell cultures. Science 223(4641):1148–1151

    Article  PubMed  CAS  Google Scholar 

  • Croughan TP (1998) Herbicide resistant rice. US Patent application 5773704

  • De Chaumont F, Dallongeville S, Chenouard N, Hervé N, Pop S, Provoost T, Meas-Yedid V, Pankajakshan P, Lecomte T, Le Montagner Y, Lagache T (2012) Icy: an open bioimage informatics platform for extended reproducible research. Nat Methods 9:690

    Article  PubMed  CAS  Google Scholar 

  • Dehouck Y, Kwasigroch JM, Rooman M, Gilis D (2013) BeAtMuSiC: prediction of changes in protein–protein binding affinity on mutations. Nucl Acids Res 41:W333-W339

    Article  Google Scholar 

  • Dermawan H, Karan R, Jung JH, Zhao Y, Parajuli S, Sanahuja G, Altpeter F (2016) Development of an intragenic gene transfer and selection protocol for sugarcane resulting in resistance to acetolactate synthase-inhibiting herbicide. Plant Cell Tiss Org Cult 26:459–468

    Article  CAS  Google Scholar 

  • Devine MD, Eberlein CV (1997) Physiological, biochemical and molecular aspects of herbicide resistance based on altered target sites. In: Roe RM, Burton JD, Kuhr RJ (eds) Herbicide activity: toxicology, biochemistry and molecular biology. IOS Press, Amsterdam, pp 159–185

    Google Scholar 

  • Dietrich GE (1998) Imidazoline resistant AHAS mutants. US Patent 5767361

  • Dufour A, Thibeaux R, Labruyere E, Guillen N, Olivo-Marin JC (2011) 3-D active meshes: fast discrete deformable models for cell tracking in 3-D time-lapse microscopy. IEEE Trans Image Process 20:1925–1937

    Article  PubMed  Google Scholar 

  • Dundas J, Ouyang Z, Tseng J, Binkowski A, Turpaz Y, Liang J (2006) CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucl Acid Res 34:W116–W118

    Article  CAS  Google Scholar 

  • Falco MC, Neto AT, Ulian EC (2000) Transformation and expression of a gene for herbicide resistance in a Brazilian sugarcane. Plant Cell Rep 19:1188–1194

    Article  CAS  Google Scholar 

  • Gallo-Meagher M, Irvine JE (1996) Herbicide resistant transgenic sugarcane plants containing the bar gene. Crop Sci 36:1367–1374

    Article  CAS  Google Scholar 

  • Gaur RK, Sharma P (2013) Approaches to plant stress and their management. Springer, New Delhi

    Google Scholar 

  • Gilbert RA, Gallo-Meagher M, Comstock JC, Miller JD, Jain M, Abouzid A (2005) Agronomic evaluation of sugarcane lines transformed for resistance to sugarcane mosaic virus Strain E. Crop Sci 45:2060–2067

    Article  Google Scholar 

  • Gilbert RA, Glynn NC, Comstock JC, Davis MJ (2009) Agronomic performance and genetic characterisation of sugarcane transformed for resistance to sugarcane yellow leaf virus. Field Crops Res 111:39–46

    Article  Google Scholar 

  • Hart SE, Saunders JW, Penner D (1992) Chlorsulfuron resistant sugar beet: cross-resistance and physiological basis of resistance. Weed Sci 40:378–383

    CAS  Google Scholar 

  • Haughn GW, Somerville CR (1986) Sulfonylurea-resistant mutants of Arabidopsis thaliana. Mol Genet Genomics 204:430–434

    Article  CAS  Google Scholar 

  • Hoang NV, Furtado A, Botha FC, Simmons BA, Henry RJ (2015) Potential for genetic improvement of sugarcane as a source of biomass for biofuels. Front Bioeng Biotechnol 3:182

    Article  PubMed  PubMed Central  Google Scholar 

  • Kamisetty H, Ovchinnikov S, Baker D (2013) Assessing the utility of coevolution-based residue–residue contact predictions in a sequence-and-structure-rich era. Proc Natl Acad Sci 110:15674–15679

    Article  PubMed  Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Keeping MG (2006) Screening of South African sugarcane cultivars for resistance to the stalk borer Eldana saccharina Walker (Lepidoptera: Pyralidae). Afr Entomol 14:277–288

    Google Scholar 

  • Kenganal M, Hanchinal RR, Nadaf HL (2008) Ethyl methanesulfonate (EMS) induced mutation, selection for salt tolerance in sugarcane in vitro. Indian J Plant Physiol 13:405–410

    CAS  Google Scholar 

  • Kishchenko EM, Komarnitskii IK, Kuchuk N (2011) Transgenic sugar beet tolerant to imidazolinone obtained by agrobacterium-mediated transformation. Cytol Genet 45:148–152

    Article  Google Scholar 

  • Koçar G, Civas N (2013) An overview of biofuels from energy crops: current status and future prospects. Renew Sust Energ Rev 28:900–916

    Article  CAS  Google Scholar 

  • 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 Plant 48:417–427

    Article  CAS  Google Scholar 

  • Leibbrandt NB, Snyman SJ (2003) Stability of gene expression and agronomic performance of a transgenic herbicide-resistant sugarcane line in South Africa. Crop Sci 43: 671–77

    Article  CAS  Google Scholar 

  • Li M, Simonetti FL, Goncearenco A, Panchenko AR (2016) MutaBind estimates and interprets the effects of sequence variants on protein–protein interactions. Nucl Acids Res 44:W494–W501

    Article  PubMed  CAS  Google Scholar 

  • Lloyd Evans D, Joshi SV (2016) Elucidating modes of activation and herbicide resistance by sequence assembly and molecular modelling of the acetolactate synthase complex in sugarcane. J Theor Biol 407:184–197

    Article  PubMed  CAS  Google Scholar 

  • Mahlanza T, Rutherford RS, Snyman SJ, Watt MP (2014) Eldana saccharina (Lepidoptera: Pyralidae) resistance in sugarcane (Saccharum sp.): effects of Fusarium spp., stalk rind, fibre and nitrogen content. Afr Entomol 22:810–822

    Article  Google Scholar 

  • Manabe Y, Tinker N, Colville A, Miki B (2007) CSR1, the sole target of imidazolinone herbicide in Arabidopsis thaliana. Plant Cell Physiol 48:1340–1358

    Article  PubMed  CAS  Google Scholar 

  • Newhouse KE, Singh BK, Shaner D, Stidham MA (1991) Mutations in maize (Zea mays) conferring resistance to imidazolinone herbicides. Theor Appl Genet 83:65–70

    Article  PubMed  CAS  Google Scholar 

  • Parry MAJ, Madgwick PJ, Bayon C, Tearall K, Hernandez-Lopez A, Baudo M, Rakszegi M, Hamada W, Al-Yassin A, Ouabbou H, Labhilili M, Phillips AL (2009) Mutation discovery for crop improvement. J Exp Biol 60:2817–2825

    CAS  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF Chimera—a visualization system for exploratory research and analysis. J Compt Chem 25:1605–1612

    Article  CAS  Google Scholar 

  • Piao Z, Wang W, Wei Y, Zonta F, Wan C, Bai J, Wu S, Wang X, Fang J (2017) Characterization of an acetohydroxy acid synthase mutant conferring tolerance to imidazolinone herbicides in rice (Oriza sativa). Planta: https://doi.org/10.1007/s00425-017-2817-2

  • Ponziak CJ, Huci PJ (2004) Genetic analysis of imidazolinone resistance in mutation-derived lines of common wheat. Crop Sci 44:23–30

    Article  Google Scholar 

  • R Core Team (2013) R: A language and environment for statistical computing. R foundation for statistical computing. Viena, Austria. ISBN 3-900051-07-0. http://www.R-project.org/

  • Rajasekaran K, Grula JW, Anderson DM (1996) Selection and characterisation of mutant cotton (Gossypium hirsutum L.) cell lines resistant to sulfonylurea and imidazolinone herbicides. Plant Sci 199:115–124

    Article  Google Scholar 

  • Rutherford RS (2015) IPM for eldana control: an integrated pest management (IPM) approach for the control of the stalk borer Eldana saccharina Walker (Lepidoptera Pyralidae). South African Sugarcane Research Institute, ISBN:1-874903-41-7

  • Rutherford RS, Meyer JH, Smith GS, Van Staden J (1993) Resistance to Eldana saccharina (Lepidoptera: Pyralidae) in sugarcane and some phytochemical correlations. Proc S Afr Sug Technol Ass 67:82–87

    CAS  Google Scholar 

  • Rutherford RS, Snyman SJ, Watt MP (2014) In vitro studies on somaclonal variation and induced mutagenesis: progress and prospects in sugarcane (Saccharum spp.)—a review. J Hort Sci Biotechnol 89:1–16

    Article  Google Scholar 

  • Rutherford RS, Maphalala KZ, Koch AC, Snyman SJ, Watt MP (2017) Field and laboratory assessments of sugarcane mutants selected in vitro for resistance to the imidazolinone herbicide imazapyr. Crop Breed Appl Biotechnol 17:107–114

    Article  CAS  Google Scholar 

  • Sabastian SA, Fader GM, Ulrich DR, Forney DR, Chaleff RS (1989) Semidominant soybean mutations for resistance to sulfonylurea herbicides. Crop Sci 29:1403–1408

    Article  Google Scholar 

  • Saika H, Horita J, Taguchi-Shiobara F, Nonaka S, Ayako NY, Iwakami S, Hori K, Matsumoto T, Tanaka T, Itoh T, Yano M (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  CAS  Google Scholar 

  • Sala CA, Bulos M (2012) Inheritance and molecular characterisation of broad range tolerance to herbicides targeting acetohydroxyacid synthase in sunflower. Theor Appl Genet 124:355–364

    Article  PubMed  CAS  Google Scholar 

  • Salassi ME, Breaux JB, Naquin CJ (2002) Modelling within-season sugarcane growth for optimal harvest system selection. Agr Syst 73:261–278

    Article  Google Scholar 

  • Sanger F, Coulson AR (1975) A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol 94:441–448

    Article  PubMed  CAS  Google Scholar 

  • Schoonees-Muir BM, Ronaldson MA, Naidoo G, Schorn PM (2009) SASTA Laboratory Manual including the official methods. ISBN:978-0-620-43586-4

  • Schymkowitz J, Borg J, Stricher F, Nys R, Rousseau F, Serrano L (2005) The FoldX webserver: an online force field. Nucl Acids Res 33:W382–W384

    Article  PubMed  CAS  Google Scholar 

  • Shimizu T, Nakayama I, Nakao T, Nezu Y, Abe H (1994) Inhibition of plant acetolactate synthase by herbicides, pyrimidinyl salicylic acids. J Pestic Sci 19:187–196

    Article  CAS  Google Scholar 

  • Shimizu T, Nakayama I, Nagayama K, Miyazawa T, Nezu Y (2012) Acetolactate synthase inhibitors. In: Böger P, Wakabayashi K, Hirai K (eds) Herbicide classes in development: mode of action, targets, genetic engineering, chemistry. Springer, New York, pp 1–42

    Google Scholar 

  • Showler AT (2016) Selected abiotic and biotic stress factors affecting two economically important sugarcane stalk boring pests in the United States. Agronomy 6:1–18

    Article  CAS  Google Scholar 

  • Showler AT, Castro BA (2010) Influence of drought stress on Mexican rice borer (Lepidoptera: Crambidae) oviposition preference and development to adulthood in sugarcane. Crop Prot 29:722–727

    Article  Google Scholar 

  • Snyman SJ, Shezi SN, Ramburan S (2018) Field assessment of in vitro micropropagated NovaCane® sugarcane (Saccharum spp. hybrids). Sugar Tech. https://doi.org/10.1007/s12355-017-0574-y

    Article  Google Scholar 

  • Stidham MA (1991) Herbicides that inhibit acetohydroxyacid synthase. Weed Sci 39:428–434

    CAS  Google Scholar 

  • Swanson EB, Herrgesell MJ, Arnoldo M, Sippell DW, Wong RSC (1989) Microspore mutagenesis and selection: canola plants with field tolerance to the imidazolinones. Theor Appl Genet 78:525–530

    Article  PubMed  CAS  Google Scholar 

  • Thompson C, Tar’an B (2014) Genetic characterisation of the acetohydroxyacid synthase (AHAS) gene responsible for resistance to imidazolinone in chickpea (Cicer arietinum L.). Theor Appl Genet 127:1583–1591

    Article  PubMed  CAS  Google Scholar 

  • To TL, Maheshri N (2010) Noise can induce bimodality in positive transcriptional feedback loops without bistability. Science 327:1142–1145

    Article  PubMed  CAS  Google Scholar 

  • Tranel PJ, Wright TR (2002) Resistance of weeds to AHAS inhibiting herbicides: what have we learned? Weed Sci 50:700–712

    Article  CAS  Google Scholar 

  • Van der Vyver C, Conradie T, Kossmann J, Lloyd J (2013) In vitro selection of transgenic sugarcane callus utilizing a plant gene encoding mutant form of acetolactate synthase. In Vitro Cell Dev Biol Plant 49:198–206

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Wright TR, Penner D (1998a) Cell selection and inheritance of imidazolinone resistance in sugar beet (Beta vulgaris). Theor Appl Genet 96:612–620

    Article  CAS  Google Scholar 

  • Wright TR, Penner D (1998b) Maize (Zea mays) acetolactate synthase sensitivity to four classes of ALS-inhibiting herbicides. Weed Sci 46:8–12

    CAS  Google Scholar 

  • Yu Q, Powles S (2014) 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  CAS  Google Scholar 

Download references

Acknowledgements

The financial support provided by the National Research Foundation of South Africa (grants 85414, 85573, 96178 and 106468), the University of KwaZulu-Natal (UKZN), and the South African Sugarcane Research Institute (SASRI) is highly appreciated. Many thanks to SASRI staff D Sweby, E Albertse and R Jacob for providing technical advice.

Author information

Authors and Affiliations

  1. South African Sugarcane Research Institute, Private Bag X02, Mount Edgecombe, Durban, 4300, South Africa

    Motselisi J. Koetle, Dyfed Lloyd Evans, Varnika Singh, Sandy J. Snyman & R. Stuart Rutherford

  2. School of Life Sciences, University of KwaZulu-Natal, Private Bag X54001, Durban, South Africa

    Motselisi J. Koetle, Dyfed Lloyd Evans, Varnika Singh, Sandy J. Snyman, R. Stuart Rutherford & M. Paula Watt

Authors
  1. Motselisi J. Koetle
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Dyfed Lloyd Evans
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Varnika Singh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sandy J. Snyman
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. R. Stuart Rutherford
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. M. Paula Watt
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Motselisi J. Koetle.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Prakash Lakshmanan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Koetle, M.J., Lloyd Evans, D., Singh, V. et al. Agronomic evaluation and molecular characterisation of the acetolactate synthase gene in imazapyr tolerant sugarcane (Saccharum hybrid) genotypes. Plant Cell Rep 37, 1201–1213 (2018). https://doi.org/10.1007/s00299-018-2306-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-018-2306-5

Keywords

Search

Navigation