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Glyphosate Resistance in Tall Waterhemp (Amaranthus tuberculatus) from Mississippi is due to both Altered Target-Site and Nontarget-Site Mechanisms

Published online by Cambridge University Press:  20 January 2017

Vijay K. Nandula ,
Jeffery D. Ray ,
Daniela N. Ribeiro ,
Z. Pan  and
Krishna N. Reddy
Vijay K. Nandula*
Affiliation:
Crop Production Systems Research Unit, USDA–ARS, Stoneville, MS 38776
Jeffery D. Ray
Affiliation:
Crop Genetics Research Unit, USDA–ARS, Stoneville, MS 38776
Daniela N. Ribeiro
Affiliation:
Department of Crop and Soil Sciences, Mississippi State University, Mississippi State, MS 39762
Z. Pan
Affiliation:
Natural Products Utilization Research Unit, USDA–ARS, University, MS 38677
Krishna N. Reddy
Affiliation:
Crop Production Systems Research Unit, USDA–ARS, Stoneville, MS 38776
*
Corresponding author's E-mail: [email protected]
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Abstract

A tall waterhemp population from Missisippi was suspected to be resistant to glyphosate. Glyphosate dose response experiments resulted in GR50 (dose required to reduce plant growth by 50%) values of 1.28 and 0.28 kg ae ha−1 glyphosate for the glyphosate-resistant (GR) and -susceptible (GS) populations, respectively, indicating a five-fold resistance. The absorption pattern of 14C-glyphosate between the GR and GS populations was similar up to 24 h after treatment (HAT). Thereafter, the susceptible population absorbed more glyphosate (55 and 49% of applied) compared to the resistant population (41 and 40% of applied) by 48 and 72 HAT, respectively. Treatment of a single leaf in individual plants with glyphosate at 0.84 kg ha−1, in the form of 10 1-µl droplets, provided greater control (85 vs. 29%) and shoot fresh weight reduction (73 vs. 34% of nontreated control) of the GS plants compared to the GR plants, possibly indicating a reduced movement of glyphosate in the GR plants. The amount of 14C-glyphosate that translocated out of the treated leaves of GR plants (20% of absorbed at 24 HAT and 23% of absorbed at 48 HAT) was significantly lower than the GS plants (31% of absorbed at 24 HAT and 32% of absorbed at 48 HAT). A potential difference in shikimate accumulation between GR and GS populations at different concentrations of glyphosate was also studied in vitro. The IC50 (glyphosate concentration required to cause shikimate accumulation at 50% of peak levels measured) values for the GR and GS populations were 480 and 140 µM of glyphosate, respectively, resulting in more shikimate accumulation in the GS than the GR population. Sequence analysis of 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), the target site of glyphosate, from GR and GS plants identified a consistent single nucleotide polymorphism (T/C, thymine/cytosine) between GR/GS plants, resulting in a proline to serine amino acid substitution at position 106 in the GR population. The GR and GS plants contained equal genomic copy number of EPSPS, which was positively correlated with EPSPS gene expression. Thus, glyphosate resistance in the tall waterhemp population from Mississippi is due to both altered target site and nontarget site mechanisms. This is the first report of an altered EPSPS-based resistance in a dicot weed species that has evolved resistance to glyphosate.

Keywords

Glyphosatetall waterhemp, Amaranthus tuberculatus (Moq.) SauerAbsorptionautoradiographyEPSPSgene amplificationmutationphosphorimagingshikimatetranslocation
Type
Physiology, Chemistry, and Biochemistry
Information
Weed Science , Volume 61 , Issue 3 , September 2013 , pp. 374 - 383
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Alarcón-Reverte, R., García, A., Urzúa, J., and Fischer, A. J. 2013. Resistance to glyphosate in junglerice (Echinochloa colona) from California. Weed Sci. 61:48–54.CrossRefGoogle Scholar
Baerson, S. R., Rodriguez, D. J., Tran, M., Feng, Y., Biest, N. A., and Dill, G. M. 2002. Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol. 129:1265–1275.Google Scholar
Bostamam, Y., Malone, J. M., Dolman, F. C., Boutsalis, P., and Preston, C. 2012. Rigid ryegrass (Lolium rigidum) populations containing a target site mutation in EPSPS and reduced glyphosate translocation are more resistant to glyphosate. Weed Sci. 60:474–479.Google Scholar
Bryson, C. T., and DeFelice, M. S., editors. 2009. Weeds of the South. Athens, GA The University of Georgia Press. 468 p.Google Scholar
Bustin, S. A., Benes, V., Garson, J. A., Hellemans, J., Huggett, J., Kubista, M., Mueller, R., Nolan, T., Pfaffl, M. W., Shipley, G. L., Vandesompele, J., and Wittwer, C. T. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chem. 55:611–622.Google Scholar
Chatham, L. A., Riggins, C., Owen, M. D. K., and Tranel, P. 2010. Association of epsps gene amplification with glyphosate resistance in waterhemp. Proc. North Cent. Weed Sci. Soc. 65:60 [Abstract].Google Scholar
Cromartie, T. H. and Polge, N. D. 2000. An improved assay for shikimic acid and its use as a monitor for the activity of sulfosate. Proc. Weed Sci. Soc. Am. 40:291 [Abstract].Google Scholar
Dinelli, G., Marotti, I., Bonetti, A., Catizone, P., Urbano, J. M., and Barnes, J. 2008. Physiological and molecular bases of glyphosate resistance in Conyza bonariensis biotypes from Spain. Weed Res. 48:257–265.Google Scholar
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. 86:30–41.Google Scholar
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. 52:498–505.Google Scholar
Franssen, A. S., Skinner, D. Z., Al-Khatib, K., Horak, M. J., and Kulakow, P. A. 2001. Interspecific hybridization and gene flow of ALS resistance in Amaranthus species. Weed Sci. 49:598–606.Google Scholar
Gaines, T. A., Ward, S. M., Bukun, B., Preston, C., Leach, J. E., and Westra, P. 2011. Interspecific hybridization transfers a previously unknown glyphosate resistance mechanism in Amaranthus species. Evol. Appl. 5:29–38.Google Scholar
Gaines, T. A., Zhang, W., Wang, D., Bukun, B., Chisholm, S. T., Shaner, D. L., Nissen, S. J., Patzoldt, W. L., Tranel, P. J., Culpepper, A. S., Grey, T. L., Webster, T. M., Vencill, W. K., Sammons, R. D., Jiang, J., Preston, C., Leach, J. E., and Westra, P. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri . Proc. Natl. Acad. Sci. U. S. A. 107:1029–1034.CrossRefGoogle ScholarPubMed
Ge, X., André d' Avignon, D., Ackerman, J.J.H., Collavo, A., Sattin, M., Ostrander, E. L., Hall, E. L., Sammons, R. D., and Preston, C. 2012. Vacuolar glyphosate-sequestration correlates with glyphosate resistance in ryegrass (Lolium spp.) from Australia, South America, and Europe: a 31P NMR investigation. J. Agric. Food Chem. 60:1243–1250.CrossRefGoogle ScholarPubMed
Ge, X., André d' Avignon, D., Ackerman, J.J.H., and Sammons, R. D. 2010. Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag. Sci. 66:345–348.Google Scholar
Heap, I. M. 2012. International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed August 29, 2012.Google Scholar
Jasieniuk, M., Ahmad, R., Sherwood, A. M., Firestone, J. L., Perez-Jones, A., Lanini, W. T., Mallory-Smith, C., and Stednick, Z. 2008. Glyphosate-resistant Italian ryegrass (Lolium multiflorum) in California: distribution, response to glyphosate, and molecular evidence for an altered target enzyme. Weed Sci. 56:496–502.CrossRefGoogle Scholar
Kaundun, S. S., Zelaya, I. A., Dale, R. P., Lycett, A. J., Carter, P., Sharples, K. R., and McIndoe, E. 2008. Importance of the P106S target-site mutation in conferring resistance to glyphosate in a goosegrass (Eleusine indica) population from the Philippines. Weed Sci. 56:637–646.CrossRefGoogle Scholar
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. 53:84–89.CrossRefGoogle Scholar
Legleiter, T. R. and Bradley, K. W. 2008. Glyphosate and multiple herbicide resistance in common waterhemp (Amaranthus rudis) populations from Missouri. Weed Sci. 56:582–587.Google Scholar
Li, J., Smeda, R. J., Sellers, B. A., and Johnson, W. G. 2005. Influence of formulation and glyphosate salt on absorption and translocation in three annual weeds. Weed Sci. 53:153–159.Google Scholar
Light, G. G., Mohammed, M. Y., Dotray, P. A., Chandler, J. M., and Wright, R. J. 2011. Glyphosate-resistant common waterhemp (Amaranthus rudis) confirmed in Texas. Weed Technol. 25:480–485.Google Scholar
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. 74:62–72.Google Scholar
Nandula, V. K., Reddy, K. N., Koger, C. H., Poston, D. H., Rimando, A. M., Duke, S. O., Bond, J. A., and Ribeiro, D. N. 2012. Multiple resistance to glyphosate and pyrithiobac in Palmer amaranth (Amaranthus palmeri) from Mississippi and response to flumiclorac. Weed Sci. 60:179–188.Google Scholar
Nandula, V. K., Reddy, K. N., Poston, D. H., Rimando, A. M., and Duke, S. O. 2008. Glyphosate tolerance mechanism in Italian ryegrass (Lolium multiflorum) from Mississippi. Weed Sci. 56:344–349.Google Scholar
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. 43:108–115.CrossRefGoogle Scholar
Ng, C. H., Wickneswary, R., Salmijah, S., Teng, Y. T., and Ismail, B. S. 2004. Glyphosate resistance in Eleusine indica (L.) Gaertn. from different origins and polymerase chain reaction amplification of specific alleles. Aust. J. Agric. Res. 55:407–414.Google Scholar
Pedersen, B. P., Neve, P., Andreasen, C., and Powles, S. B. 2007. Ecological fitness of a glyphosate-resistant Lolium rigidum population: growth and seed production along a competition gradient. Basic Appl. Ecol 8:258–268.Google Scholar
Perez-Jones, A., Park, K. W., Colquhoun, J., Mallory-Smith, C., and Shaner, D. L. 2005. Identification of glyphosate-resistant Italian ryegrass (Lolium multiflorum) in Oregon. Weed Sci. 53:775–779.Google Scholar
Perez-Jones, A., Park, K. W., Polge, N., Colquhoun, J., and Mallory-Smith, C. 2007. Investigating the mechanisms of glyphosate resistance in Lolium multiflorum . Planta 226:395–404.Google Scholar
Preston, C., Wakelin, A. M., Dolman, F. C., Bostamam, Y., and Boutsalis, P. 2009. A decade of glyphosate-resistant Lolium around the world: mechanisms, genes, fitness and agronomic management. Weed Sci. 57:435–441.Google Scholar
Ribeiro, D. N., Dayan, F. E., Pan, Z., Duke, S. O., Shaw, D. R., Nandula, V. K., and Baldwin, B. S. 2011. EPSPS gene amplification inheritance in glyphosate resistant Amaranthus palmeri from Mississippi. Proc. South. Weed Sci. Soc. 64:137 [Abstract].Google Scholar
Salas, R. A., Dayan, F. E., Pan, Z., Watson, S. B., Dickson, J. W., Scott, R. C., and Burgos, N. R. 2012. EPSPS gene amplification in glyphosate-resistant Italian ryegrass (Lolium perenne ssp. multiflorum) from Arkansas. Pest Manag. Sci. 68:1223–1230.CrossRefGoogle ScholarPubMed
Shaner, D. L. 2009. Role of translocation as a mechanism of resistance to glyphosate. Weed Sci. 57:118–123.CrossRefGoogle Scholar
Shaner, D. L. 2010. Testing methods for glyphosate resistance. Pp. 93–118 in Nandula, V. K., ed. Glyphosate Resistance in Crops and Weeds: History, Development, and Management. Hoboken, NJ John Wiley & Sons.CrossRefGoogle Scholar
Shaner, D. L., Lindenmeyer, R. B., and Ostlie, M. H. 2012. What have the mechanisms of resistance to glyphosate taught us? Pest Manag. Sci. 68:3–9.Google Scholar
Shaner, D. L., Nadler-Hassar, T., Henry, W. B., and Koger, C. H. 2005. A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci. 53:769–774.Google Scholar
Simarmata, M. and Penner, D. 2008. The basis for glyphosate resistance in rigid ryegrass (Lolium rigidum) from California. Weed Sci. 56:181–182.Google Scholar
Thai, H. N., Malone, J., Boutsalis, P., and Preston, C. 2012. Glyphosate resistance in barnyard grass (Echinochloa colona). Pp. 237–240 in Eldershaw, L., ed. Proceedings of the 18th Australasian Weeds Conference. Melbourne, Victoria, Australia Weed Society of Victoria.Google Scholar
Trucco, F., Jeschke, M. R., Rayburn, A. L., and Tranel, P. J. 2005a. Promiscuity in weedy amaranths: high frequency of female tall waterhemp (Amaranthus tuberculatus) × smooth pigweed (A. hybridus) hybridization under field conditions. Weed Sci. 53:46–54.Google Scholar
Trucco, F., Rayburn, A. L., and Tranel, P. J. 2005b. Amaranthus hybridus can be pollinated frequently by A. tuberculatus under field conditions. Heredity 94:64–70.Google Scholar
Trucco, F., Tatum, T., Rayburn, A. L., and Tranel, P. J. 2009. Out of the swamp: unidirectional hybridization with weedy species may explain the prevalence of Amaranthus tuberculatus as a weed. New Phytol. 184:819–827.CrossRefGoogle ScholarPubMed
Wakelin, A. M., Lorraine-Colwill, D. F., and Preston, C. 2004. Glyphosate resistance in four different population of Lolium rigidum is associated with reduced translocation of glyphosate to meristematic zones. Weed Res. 44:453–459.Google Scholar
Wakelin, A. M. and Preston, C. 2006a. A target-site mutation is present in a glyphosate-resistant Lolium rigidum population. Weed Res. 46:432–440.Google Scholar
Wakelin, A. M. and Preston, C. 2006b. The cost of glyphosate resistance: is there a fitness penalty associated with glyphosate resistance in annual ryegrass? Pp. 515–518 in Preston, C., Watts, J. H., and Crossman, N. D., eds. Proceedings of the 15th Australian Weeds Conference. Adelaide, South Australia Weed Management Society of South Australia.Google Scholar
Westra, P., Wiersma, A., Leach, J., and Reddy, A. 2013. Regional whole plant and molecular response of kochia to glyphosate. Proc. Weed Sci. Soc. Am. 53:316 [Abstract].Google Scholar
Wetzel, D. K., Horak, M. J., Skinner, D. Z., and Kulakow, P. A. 1999. Transferal of herbicide resistance traits from Amaranthus palmeri to Amaranthus rudis . Weed Sci. 47:538–543.Google Scholar
Yu, Q., Cairns, A., and Powles, S. 2007. Glyphosate, paraquat and ACCase multiple herbicide resistance evolved in a Lolium rigidum biotype. Planta 225:499–513.Google Scholar