Skip to main content Accessibility help
×
×
Home

Importance of the P106S Target-Site Mutation in Conferring Resistance to Glyphosate in a Goosegrass (Eleusine indica) Population from the Philippines

  • Shiv S. Kaundun (a1), Ian A. Zelaya (a1), Richard P. Dale (a1), Amy J. Lycett (a1), Patrice Carter (a1), Kate R. Sharples (a1) and Eddie McIndoe (a1)...

Abstract

Few studies on herbicide resistance report data to establish unambiguously the correlation between genotype and phenotype. Here we report on the importance of the EPSPS prolyl106 point mutation to serine (P106S) in conferring resistance to glyphosate in a goosegrass population from Davao, Mindanao Island, the Philippines (Davao). Initial rate-response studies showed clear survivors within the Davao population at glyphosate rates that completely controlled the standard sensitive goosegrass population (STD1). Assessment of potential resistance mechanisms identified the presence of P106S mutant individuals in the Davao population. Polymerase chain reaction (PCR) amplification of specific alleles (PASA) analysis established that the mixed-resistant Davao population was comprised of 39.1% homozygous proline wild-type (PP106), 3.3% heterozygous serine mutant (PS106), and 57.6% homozygous serine mutant (SS106) genotypes. Further rate-response studies on plants with a predetermined genotype estimated the Davao SS106 individuals to be approximately 2-fold more resistant to glyphosate compared to Davao PP106 individuals. Extensive analysis at different goosegrass growth stages and glyphosate rates established strong correlation (P < 0.001) between presence of P106S in EPSPS and the resistant phenotype. Importantly, no differences in the pattern of absorbed or translocated 14C–glyphosate were observed between PP106 and SS106 Davao genotypes or Davao and STD1 individuals, suggesting that glyphosate resistance in the Davao population was attributable to an altered target site mechanism. This study demonstrates that whilst P106S in EPSPS confers a moderate resistance level to glyphosate, the mechanism is sufficient to endow glyphosate failure at the recommended field rates.

Copyright

Corresponding author

Corresponding author's E-mail: deepak.kaundun@syngenta.com

References

Hide All
Anderson, K. S., Sikorski, J. A., and Johnson, K. A. 1988. Evaluation of 5-enolpyruvoylshikimate-3-phosphate synthase substrate and inhibitor binding by stopped-flow and equilibrium fluorescence measurements. Biochemistry. 27:16041610.
Baerson, S. R., Rodriguez, D. J., Biest, N. A., Tran, M., You, J., Kreuger, R. W., Dill, G. M., Pratley, J. E., and Gruys, K. J. 2002a. Investigating the mechanism of glyphosate resistance in rigid ryegrass (Lolium rigidum). Weed Sci. 50:721730.
Baerson, S. R., Rodriguez, D. J., Tran, M., Feng, Y., Biest, N. A., and Dill, G. M. 2002b. Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol. 129:12651275.
Bottema, C. D. and Sommer, S. S. 1993. PCR amplification of specific alleles: rapid detection of known mutations and polymorphisms. Mutat. Res. 288:93102.
Bradshaw, L. D., Padgette, S. R., Kimball, S. L., and Wells, B. H. 1997. Perspectives on glyphosate resistance. Weed Technology. 11:189198.
Comai, L., Facciotti, D., Hiatt, W. R., Thompson, G., Rose, R. E., and Stalker, D. M. 1985. Expression in plants of a mutant aroA gene from Salmonella typhimurium confers tolerance to glyphosate. Nature. 317:741745.
Comai, L., Sen, L. C., and Stalker, D. M. 1983. An altered aroA gene product confers resistance to the herbicide glyphosate. Science. 221:370371.
Dinelli, G., Marotti, I., Bonetti, A., Minelli, M., Catizone, P., and Barnes, J. 2006. Physiological and molecular insight on the mechanisms of resistance to glyphosate in Conyza canadensis (L.) Cronq. biotypes. Pestic. Biochem. Physiol. 86:3041.
Duke, S. O. and Powles, S. B. 2008. Glyphosate: a once-in-a-century herbicide. Pest Manag. Sci. 64:319325.
Feng, P. C. C., Tran, M., Chiu, T., Sammons, R. D., Heck, G. R., and CaJacob, C. A. 2004. Investigations into glyphosate-resistant horseweed (Conyza canadensis): retention, uptake, translocation, and metabolism. Weed Sci. 52:498505.
Franz, J. E., Mao, M. K., and Sikorski, J. A. 1997. Glyphosate: A Unique Global Herbicide. Washington, DC American Chemical Society. 678.
He, M., Nie, Y. F., and Xu, P. 2003. A T42M substitution in bacterial 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS) generates enzymes with increased resistance to glyphosate. Biosci. Biotechnol. Biochem. 67:14051409.
Heap, I. 2008. The International Survey of Herbicide Resistant Weeds. http://www.weedscience.com/. Accessed March 4, 2008.
Holländer, H. and Amrhein, N. 1980. The site of the inhibition of the shikimate pathway by glyphosate. I. Inhibition by glyphosate of phenylpropanoid synthesis in buckwheat (Fagopyrum esculentum Moench). Plant Physiol. 66:823829.
Holm, L. G., Plucknett, D. L., Pancho, J. V., and Herberger, J. P. 1977. The World's Worst Weeds—Distribution and Biology. Honolulu, HA The University Press of Hawaii. 609.
Jasieniuk, M. 1985. Constraints on the evolution of glyphosate resistance in weeds. Resistant Pest Manag. Newsl. 7:3132.
Jaworski, E. G. 1972. Mode of action of N-phosphonomethylglycine. Inhibition of aromatic amino acid biosynthesis. J. Agric. Food Chem. 20:11951198.
Kahrizi, D., Salmanian, A. H., Afshari, A., Moieni, A., and Mousavi, A. 2007. Simultaneous substitution of Gly96 to Ala and Ala183 to Thr in 5-enolpyruvylshikimate-3-phosphate synthase gene of E. coli (k12) and transformation of rapeseed (Brassica napus L.) in order to make tolerance to glyphosate. Plant Cell Rep. 26:95104.
Kishore, G. M., Brundage, L., Kolk, K., Padgette, S. R., Rochester, D., Huynh, K., and della-Cioppa, G. 1986. Isolation, purification and characterization of a glyphosate tolerant mutant E. coli EPSP synthase. Proc. Fed. Am. Soc. Exp. Biol. 45:1506–1506.
Kishore, G. M. and Shah, D. M. 1988. Amino acid biosynthesis inhibitors as herbicides. Annu. Rev. Biochem. 57:627663.
Klee, H. J., Muskopf, Y. M., and Gasser, C. S. 1987. Cloning of an Arabidopsis thaliana gene encoding 5-enolpyruvylshikimate-3-phosphate synthase: sequence analysis and manipulation to obtain glyphosate-tolerant plants. Mol. Gen. Genet. 210:437442.
Koger, C. H. and Reddy, K. N. 2005. Role of absorption and translocation in the mechanism of glyphosate resistance in horseweed (Conyza canadensis). Weed Sci. 53:8489.
Krekel, F., Oecking, C., Amrhein, N., and Macheroux, P. 1999. Substrate and inhibitor-induced conformational changes in the structurally related enzymes UDP-N-acetylglucosamine enolpyruvyl transferase (MurA) and 5-enolpyruvylshikimate 3-phosphate synthase (EPSPS). Biochemistry. 38:88648878.
Lee, L. J. and Ngim, J. 2000. A first report of glyphosate-resistant goosegrass (Eleusine indica (L) Gaertn) in Malaysia. Pest Manag. Sci. 56:336339.
Liu, Q., Thorland, E. C., Heit, J. A., and Sommer, S. S. 1997. Overlapping PCR for bidirectional PCR amplification of specific alleles: a rapid one-tube method for simultaneously differentiating homozygotes and heterozygotes. Genome Res. 7:389398.
Lorraine-Colwill, D. F., Powles, S. B., Hawkes, T. R., Hollinshead, P. H., Warner, S. A. J., and Preston, C. 2003. Investigations into the mechanism of glyphosate resistance in Lolium rigidum . Pestic. Biochem. Physiol. 74:6272.
Lorraine-Colwill, D. F., Powles, S. B., Hawkes, T. R., and Preston, C. 2001. Inheritance of evolved glyphosate resistance in Lolium rigidum (Gaud.). Theor. Appl. Genet. 102:545550.
Michitte, P., de Prado, R., Espinosa, N., and Gauvrit, C. 2005. Glyphosate resistance in a Chilean Lolium multiflorum . Commun. Agric. Appl. Biol. Sci. 70:507513.
Nail, E. L., Young, D. L., and Schillinger, W. F. 2007. Diesel and glyphosate price changes benefit the economics of conservation tillage versus traditional tillage. Soil Tillage Res. 94:321327.
Ng, C. H., Ratnam, W., Surif, S., and Ismail, B. S. 2004a. Inheritance of glyphosate resistance in goosegrass (Eleusine indica). Weed Sci. 52:564570.
Ng, C. H., Wickneswari, R., Salmijah, S., Teng, Y. T., and Ismail, B. S. 2003. Gene polymorphisms in glyphosate-resistant and -susceptible biotypes of Eleusine indica from Malaysia. Weed Res. 43:108115.
Ng, C. H., Wickneswary, R., Salmijah, S., Teng, Y. T., and Ismail, B. S. 2004b. Glyphosate resistance in Eleusine indica (L.) Gaertn. from different origins and polymerase chain reaction amplification of specific alleles. Aust. J. Agric. Res. 55:407414.
Norsworthy, J. K., Burgos, N. R., and Oliver, L. R. 2001. Differences in weed tolerance to glyphosate involve different mechanisms. Weed Technol. 15:725731.
Owen, M. D. K. and Zelaya, I. A. 2005. Herbicide-resistant crops and weed resistance to herbicides. Pest Manag. Sci. 61:301311.
Padgette, S. R., Re, D. B., Gasser, C. S., Eichholtz, D. A., Frazier, R. B., Hironaka, C. M., Levine, E. B., Shah, D. M., Fraley, R. T., and Kishore, G. M. 1991. Site-directed mutagenesis of a conserved region of the 5-enolpyruvylshikimate-3-phosphate synthase active site. J. Biol. Chem. 266:22,36422,369.
Perez-Jones, A., Park, K. W., Polge, N., Colquhoun, J., and Mallory-Smith, C. A. 2007. Investigating the mechanisms of glyphosate resistance in Lolium multiflorum . Planta. 226:395404.
Powles, S. B. 2008. Evolved glyphosate-resistant weeds around the world: lessons to be learnt. Pest Manag. Sci. 64:360365.
Preston, C. and Wakelin, A. M. 2008. Resistance to glyphosate from altered herbicide translocation patterns. Pest Manag. Sci. 64:372376.
Sammons, R. D., Heering, D. C., Dinicola, N., Glick, H., and Elmore, G. A. 2007. Sustainability and stewardship of glyphosate and glyphosate-resistant crops. Weed Technol. 21:347354.
Sidhu, R. S., Hammond, B. G., Fuchs, R. L., Mutz, J. N., Holden, L. R., George, B., and Olson, T. 2000. Glyphosate-tolerant corn: the composition and feeding value of grain from glyphosate-tolerant corn is equivalent to that of conventional corn (Zea mays L.). J. Agric. Food Chem. 48:23052312.
Simarmata, M., Bughrara, S., and Penner, D. 2005. Inheritance of glyphosate resistance in rigid ryegrass (Lolium rigidum) from California. Weed Sci. 53:615619.
Simarmata, M. and Penner, D. 2008. The basis for glyphosate resistance in rigid ryegrass (Lolium rigidum) from California. Weed Sci. 56:181188.
Smart, C. C., Johänning, D., Müller, G., and Amrhein, N. 1985. Selective overproduction of 5-enol-pyruvylshikimic acid 3-phosphate synthase in a plant cell culture which tolerates high doses of the herbicide glyphosate. J. Biol. Chem. 260:16,33816,346.
Sost, D. and Amrhein, N. 1990. Substitution of Gly-96 to Ala in the 5-enolpyruvylshikimate-3-phosphate synthase of Klebsiella pneumoniae results in a greatly reduced affinity for the herbicide glyphosate. Arch. Biochem. Biophys. 282:433436.
Stalker, D. M., Hiatt, W. R., and Comai, L. 1985. A single amino acid substitution in the enzyme 5-enolpyruvylshikimate-3-phosphate synthase confers resistance to the herbicide glyphosate. J. Biol. Chem. 260:47244728.
Steinrücken, H. C. and Amrhein, N. 1980. The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase. Biochem. Biophys. Res. Commun. 94:12071212.
Tranel, P. J., Lee, R. M., Bell, M. S., Singh, S., Walter, J. R., and Bradley, K. W. 2006. What we know (and don't know) about glyphosate resistance in waterhemp. Proc. North Cent. Weed Sci. Soc. Abstr. 61:100.
Wakelin, A. M., Lorraine-Colwill, D. F., and Preston, C. 2004. Glyphosate resistance in four different populations of Lolium rigidum is associated with reduced translocation of glyphosate to meristematic zones. Weed Res. 44:453459.
Wakelin, A. M. and Preston, C. 2006. A target-site mutation is present in a glyphosate-resistant Lolium rigidum population. Weed Res. 46:432440.
Westwood, J. H. and Weller, S. C. 1997. Cellular mechanisms influence differential glyphosate sensitivity in field bindweed (Convolvulus arvensis) biotypes. Weed Sci. 45:211.
Yu, Q., Cairns, A., and Powles, S. B. 2007. Glyphosate, paraquat and ACCase multiple herbicide resistance evolved in a Lolium rigidum biotype. Planta. 225:499513.
Yuan, C. I., Hsieh, Y. C., and Chiang, M. Y. 2005. Glyphosate-resistant goosegrass in Taiwan: cloning of target enzyme (EPSPS) and molecular assay of field populations. Plant Prot. Bull. 47:251261.
Zelaya, I. A. and Owen, M. D. K. 2005. Differential response of Amaranthus tuberculatus (Moq ex DC) JD Sauer to glyphosate. Pest Manag. Sci. 61:936950.
Zelaya, I. A., Owen, M. D. K., and VanGessel, M. J. 2004. Inheritance of evolved glyphosate resistance in Conyza canadensis (L.) Cronq. Theor. Appl. Genet. 110:5870.
Zelaya, I. A., Owen, M. D. K., and VanGessel, M. J. 2007. Transfer of glyphosate resistance: evidence of hybridization in Conyza (Asteraceae). Am. J. Bot. 94:660673.
Zhou, M., Xu, H., Wei, X., Ye, Z., Wei, L., Gong, W., Wang, Y., and Zhu, Z. 2006. Identification of a glyphosate-resistant mutant of rice 5-enolpyruvylshikimate 3-phosphate synthase using a directed evolution strategy. Plant Physiol. 140:184195.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Weed Science
  • ISSN: 0043-1745
  • EISSN: 1550-2759
  • URL: /core/journals/weed-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed