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A Pro106 to Ala Substitution is Associated with Resistance to Glyphosate in Annual Bluegrass (Poa annua)

Published online by Cambridge University Press:  20 January 2017

Robert B. Cross ,
Lambert B. McCarty ,
Nishanth Tharayil ,
J. Scott McElroy ,
Shu Chen ,
Patrick E. McCullough ,
Brian A. Powell  and
William C. Bridges Jr.
Robert B. Cross
Affiliation:
School of Agriculture, Forestry, and Environmental Sciences, E-143 Poole Agriculture Center, Clemson University, Clemson, SC 29634
Lambert B. McCarty*
Affiliation:
School of Agriculture, Forestry, and Environmental Sciences, E-143 Poole Agriculture Center, Clemson University, Clemson, SC 29634
Nishanth Tharayil
Affiliation:
School of Agriculture, Forestry, and Environmental Sciences, E-143 Poole Agriculture Center, Clemson University, Clemson, SC 29634
J. Scott McElroy
Affiliation:
Department of Agronomy and Soils, 201 Funchess Hall, Auburn University, Auburn, AL 36849
Shu Chen
Affiliation:
Department of Agronomy and Soils, 201 Funchess Hall, Auburn University, Auburn, AL 36849
Patrick E. McCullough
Affiliation:
115 Redding Building, Department of Crop and Soil Sciences, University of Georgia, Griffin, GA 30223
Brian A. Powell
Affiliation:
Department of Environmental Engineering and Earth Sciences, 166 Rich Laboratory, Clemson University, Anderson, SC 29625
William C. Bridges Jr.
Affiliation:
Department of Mathematical Sciences, O-110 Martin Hall, Clemson University, Clemson, SC 29634
*
Corresponding author's E-mail: bmccrty@clemson.edu
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Abstract

Glyphosate is used in the transition zone to control annual bluegrass in fully dormant warm-season grasses. A suspected resistant (R) biotype of annual bluegrass was identified on a golf course in South Carolina after at least 10 consecutive years of glyphosate application. Greenhouse bioassays revealed the R biotype was 4.4-fold resistant to glyphosate compared with a standard susceptible (S) biotype. Further studies were conducted to investigate the mechanism conferring glyphosate resistance in the R biotype. Leaf discs of both biotypes accumulated shikimate in response to increasing glyphosate concentration, but the glyphosate concentration resulting in 50% EPSP synthase inhibition as a result of shikimate accumulation (I50) was 4.2-fold higher in the R biotype compared with the S biotype. At the whole plant level, similar levels of shikimate accumulation were observed between biotypes at 6 and 24 h after treatment (HAT) with glyphosate, but greater shikimate accumulation occurred in the S biotype at 72, 120, and 168 HAT. Shikimate levels decreased in the R biotype after 72 HAT. There were no differences in 14C-glyphosate absorption between biotypes. However, more 14C-glyphosate translocated out of the treated leaf in the R biotype and into root tissues over time compared with the S biotype. Partial sequencing of the EPSP synthase gene revealed a point mutation that resulted in an Ala substitution at Pro106. Although other mechanisms may contribute to glyphosate resistance, these results confirm a Pro106 to Ala substitution is associated with resistance to glyphosate in the R annual bluegrass biotype.

Keywords

GlyphosateEPSP, 5-enolpyruvyl-shikimate-3-phosphateshikimate, (3R,4S,5R)-3,4,5-trihydroxycyclohex-1-ene-1-carboxylic acidannual bluegrass, Poa annua L.EPSP synthasegolf courseshikimate accumulationtarget site resistancetranslocationturfgrass
Type
Physiology, Chemistry, and Biochemistry
Information
Weed Science , Volume 63 , Issue 3 , September 2015 , pp. 613 - 622
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Alarcón-Reverte, R, Garcia, A, Urzua, J, Fischer, AJ (2013) Resistance to glyphosate in junglerice (Echinochloa colona) from California. Weed Sci. 61:48–54 Google Scholar
Baerson, SR, Rodriguez, DJ, Tran, M, Feng, Y, Biest, NA, Dill, GM (2002) Glyphosate-resistant goosegrass. Identification of a mutation in the target enzyme 5-enolpyruvylshikimate-3-phosphate synthase. Plant Physiol. 129:1265–1275 Google Scholar
Binkholder, KM, Fresenburg, BS, Teuton, TC, Xiong, X, Smeda, RJ (2011) Selection of glyphosate-resistant annual bluegrass (Poa annua) on a golf course. Weed Sci. 59:286–289 Google Scholar
Bostamam, Y, Malone, JM, Dolman, FC, Boutsalis, P, 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
Bradshaw, LD, Padgette, SR, Kimball, SL, Wells, BH (1997) Perspectives on glyphosate resistance. Weed Technol. 11:189–198 Google Scholar
Brosnan, JT, Breeden, JK, Mueller, TC (2012) A glyphosate-resistant biotype of annual bluegrass in Tennessee. Weed Sci. 60:97–100 Google Scholar
Collavo, A, Sattin, M (2012) Resistance to glyphosate in Lolium rigidum selected in Italian perennial crops: bioevaluation, management and molecular bases of target-site resistance. Weed Res. 52:16–24 Google Scholar
Coupland, D, Caseley, JC (1979) Presence of 14C activity in root exudates and guttation fluid from Agropyron repens treated with 14C-labeled glyphosate. New Phytol. 83:17–22 Google Scholar
Cromartie, TH, Polge, ND (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 Google Scholar
Darmency, H, Gasquez, J (1983) Esterase polymorphism and growth form differentiation in Poa annua L. New Phytol. 95:289–297 Google Scholar
Ellis, WM (1973) The breeding system and variation in populations of Poa annua L. Evolution. 27:656–662 Google Scholar
Eschenburg, S, Healy, ML, Priestman, MA, Lushington, GH, Schönbrunn, E (2002) How the mutation glycine96 to alanine confers glyphosate insensitivity to 5-enolpyruvyl shikimate-3-phosphate synthase from Escherichia coli . Planta. 216:129–135 Google Scholar
Feng, PCC, Tran, M, Chiu, T, Sammons, RD, Heck, GR, CaJacob, CA (2004) Investigations into glyphosate-resistant horseweed (Conyza canadensis): retention, uptake, translocation, and metabolism. Weed Sci. 52:498–505 Google Scholar
Franz, JE, Mao, JA, Sikorski, JA (1997) Glyphosate: A Unique Global Herbicide. Washington, DC American Chemical Society. 653 pGoogle Scholar
Funke, T, Yang, Y, Han, H, Healy-Fried, M, Olesen, S, Becker, A, Schönbrunn, E (2009) Structural basis of glyphosate resistance resulting from the double mutation Thr197 → Ile and Pro101 → Ser in 5-enolpyruvylshikimate-3-phosphate synthase from Escherichia coli . J Biol Chem. 284:9854–9860 Google Scholar
Gaines, TA, Zhang, W, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS, Grey, TL, Webster, TM, Vencill, WK, Sammons, RD, Jiang, J, Preston, C, Leach, JE, Westra, P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri . Proc Natl Acad Sci USA. 107:1029–1034 Google Scholar
Ge, X, d'Avignon, DA, Ackerman, JJH, Sammons, RD (2010) Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag Sci. 66:345–348 Google Scholar
Geiger, DR, Bestman, HD (1990) Self-limitation of herbicide mobility by phytotoxic action. Weed Sci. 38:324–329 Google Scholar
González-Torralva, F, Gil-Humanes, J, Barro, F, Brants, I, De Prado, R (2012a) Target site mutation and reduced translocation are present in a glyphosate-resistant Lolium rigidum Lam. biotype from Spain. Plant Physiol Biochem. 58:16–22 Google Scholar
González-Torralva, F, Rojano-Delgado, AM, de Castro, MDL, Mülleder, N, De Prado, R (2012b) Two non-target mechanisms are involved in glyphosate-resistant horseweed (Conzya Canadensis L. Cronq.) biotypes. J Plant Physiol. 169:1673–1679 Google Scholar
Healy-Fried, ML, Funke, T, Priestman, MA, Han, H, Schönbrunn, E (2007) Structural basis of glyphosate tolerance resulting from mutations of Pro101 in Escherichia coli 5-enolpyruvylshikimate-3-phosate synthase. J Biol Chem. 282:32,949–32,955 Google Scholar
Heap, I (2014) The International Survey of Herbicide Resistant Weeds. http://www.weedscience.com. Accessed October 7, 2014Google Scholar
Herrmann, KM, Weaver, LM (1999) The shikimate pathway. Ann Rev Plant Physiol Plant Mol Biol. 50:473–503 Google Scholar
Jasieniuk, M, Ahmad, R, Sherwood, AM, Firestone, JL, Perez-Jones, A, Lanini, WT, Mallory-Smith, C, 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 Google Scholar
Kaundun, SS, Zelaya, IA, Dale, RP, Lycett, AJ, Carter, P, Sharples, KR, 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 Google Scholar
Lorraine-Colwill, DF, Powles, SB, Hawkes, TR, Preston, C (2001) Inheritance of evolved glyphosate resistance in Lolium rigidum Gaud. Theor Appl Gen. 102:545–550 Google Scholar
Mao, Q, Huff, DR (2012) The evolutionary origin of Poa annua L. Crop Sci. 52:1910–1922 Google Scholar
McElroy, JS, Flessner, ML, Wang, Z, Dane, F, Walker, RH, Wehtje, GR (2013) A Trp574 to Leu amino acid substitution in the ALS gene of annual bluegrass (Poa annua) is associated with resistance to ALS-inhibiting herbicides. Weed Sci. 61:21–25 Google Scholar
McElroy, JS, Walker, RH, van Santen, E (2002) Patterns of variation in Poa annua populations as revealed by canonical discriminant analysis of life history traits. Crop Sci. 42:513–517 Google Scholar
Michitte, P, De Prado, R, Espinoza, N, Ruiz-Santaella, JP, Gauvrit, C (2007) Mechanisms of resistance to glyphosate in a ryegrass (Lolium multiflorum) biotype from Chile. Weed Sci. 55:435–440 Google Scholar
Norsworthy, JK, Smith, KL, Scott, RC, Gbur, EE (2007) Consultant perspectives on weed management needs in Arkansas cotton. Weed Tech. 21:825–831 Google Scholar
Perez-Jones, A, Park, KW, Polge, N, Colquhoun, J, Mallory-Smith, CA (2007) Investigating the mechanisms of glyphosate resistance in Lolium multiflorum . Planta. 226:395–404 Google Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol. 61:317–347 Google Scholar
Pratley, J, Baines, P, Eberbach, P, Incerti, M, Broster, J (1996) Glyphsoate resistance in annual ryegass. Pages 126p in Virgona, J, Michalk, D, eds. Proceedings of the 11th annual conference of the Grassland Society of New South Wales. Wagga Wagga, Australia Grassland Society of NSW Google Scholar
Rodrigues, JJV, Worsham, AD, Corbin, FT (1982) Exudation of glyphosate from wheat (Triticum aestivum) plants and its effects on interplanted corn (Zea mays) and soybeans (Glycine max). Weed Sci. 30:316–320 Google Scholar
Shaner, DL, Nadler-Hassar, T, Henry, WB, Koger, CH (2005) A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci. 53:769–774 Google Scholar
Steinrücken, HC, Amrhein, N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvyl-shikimic acid-3-phosphate synthase. Biochem Biophys Res Commun. 94:1207–1212 Google Scholar
Wakelin, AM, Lorraine-Colwill, DF, Preston, C (2004) Glyphosate resistance in four different populations of Lolium rigidum is associated with reduced translocation of glyphosate to meristematic zones. Weed Res. 44:453–459 Google Scholar
Wakelin, AM, Preston, C (2006) A target-site mutation is present in a glyphosate-resistant Lolium rigidum population. Weed Res. 46:432–440 Google Scholar
Yu, Q, Cairns, A, Powles, S (2007) Glyphosate, paraquat and ACCase multiple herbicide resistance evolved in a Lolium rigidum biotype. Planta. 225:499–513 Google Scholar