Document Type : Original Article
Authors
1 Binh Duong University, 504 Binh Duong Avenue, Hiep Thanh Ward, Thu Dau Mot City, Binh Duong Province, Vietnam
2 School of Agriculture, Food & Wine, University of Adelaide, PMB 1, Glen Osmond, SA 5064, Australia
10.26655/jrweedsci.2019.4.3
Abstract
Glyphosate resistant Echinochloa colona is widespread in fallow systems of northern Australia from intensive glyphosate use. The inheritance of glyphosate resistance and the potential for gene transfer through pollen from resistant to susceptible individuals were investigated. A glyphosate resistant population A533.1, containing a mutation in EPSPS, was used as the resistant parent and Echi S as the susceptible parent. Gene flow via pollen between adjacent susceptible and resistant individuals was examined by treating progeny from the susceptible individuals at 240 g ha-1 glyphosate with 1.38% gene flow detected. Survivors were selfed and the progeny segregated 3:1 for survival to 240 g ha-1 glyphosate, consistent with single dominant gene inheritance. Hand crosses between resistant and susceptible individuals produced a single F1 seed which carried the mutation in EPSPS. The F2 generation from the hand cross had a response to glyphosate, intermediate between the two parents and similar to that expected for a single largely dominant gene. Sequencing the EPSPS cDNA detected at least two EPSPS genes expressed in E. colona, only one of which carried the mutation. Glyphosate resistance in this population of E. colona is inherited as a single largely dominant allele.
Keywords
Alarcón-Reverte R, Garcia A, Watson S.B, Abdallah I, Sabate S, Hernandez M.J, Dayan F.E, Fischer A.J. 2015. Concerted action of target-site mutations and high EPSPS activity in glyphosate-resistant junglerice (Echinochloa colona) from California. Pest Manag. Sci. 71: 996-1007.
Busi R, Michel S, Powles S.B, Delye C. 2011. Gene flow increases the initial frequency of herbicide resistance alleles in unselected Lolium rigidum populations. Agric. Ecosyst. Environ. 142: 403-409.
Busi R, Powles S.B. 2009. Evolution of glyphosate resistance in a Lolium rigidum population by glyphosate selection at sublethal doses. Heredity 103: 318-325.
Chandi A, Milla-Lewis S.R, Giacomini D, Westra P, Preston C, Jordan D.L, York A.C, Burton J.D, Whitaker J.R. 2012. Inheritance of evolved glyphosate resistance in a North Carolina palmer amaranth (Amaranthus palmeri) biotype. Int. J. Agron. 2012: 7 pages.
Chauhan B.S, Johnson D.E. 2009. Seed germination ecology of junglerice (Echinochloa colona): A major weed of rice. Weed Sci. 57: 235-240.
Christoffers M.J. 1999. Genetic aspects of herbicide-resistant weed management. Weed Technol. 13: 647-652.
Davis V.M, Kruger G.R, Hallett S.G, Tranel P.J, Johnson W.G. 2010. Heritability of glyphosate resistance in Indiana horseweed (Conyza canadensis) populations. Weed Sci. 58: 30-38.
Diggle A.J, Neve P. 2001. The population dynamics and genetics of herbicide resistance - A modeling approach, in: Powles S.B., Shaner D.L. (Eds.), Herbicide Resistance and World Grains. CRC Press-Taylor & Francis Group, 6000 Broken Sound Parkway NW, Ste 300, Boca Raton, FL 33487-2742 USA, Agr Western Australia, Bentley, WA 6983, Australia, pp. 61-99.
Ellstrand N.C. 1992. Gene flow by pollen: implications for plant conservation genetics. Oikos 63: 77-86.
Feng P.C.C, Tran M, Chiu T, Sammons R.D, Heck G.R, CaJacob C.A. 2004. Investigations into glyphosate-resistant horseweed (Conyza canadensis): retention, uptake, translocation, and metabolism. Weed Sci. 52: 498-505.
Gaines T.A, Cripps A, Powles S.B. 2012. Evolved resistance to glyphosate in junglerice (Echinochloa colona) from the tropical Ord River region in Australia. Weed Technol. 26: 480-484.
Gaines T.A, Shaner D.L, Ward S.M, Leach J.E, Preston C, Westra P. 2011. Mechanism of resistance of evolved glyphosate-resistant palmer amaranth (Amaranthus palmeri). J. Agric. Food Chem. 59: 5886-5889.
Gaines T.A, Zhang W.L, Wang D.F, 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.M, Preston C, Leach J.E, Westra P. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri. Proc. Natl. Acad. Sci. USA. 107: 1029-1034.
Ge X, d'Avignon D.A, Ackerman J.J.H, Collavo A, Sattin M, Ostrander E.L, Hall E.L, Sammons R.D, 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.
Ge X, d'Avignon D.A, Ackerman J.J.H, Sammons R.D. 2010. Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag. Sci. 66: 345-348.
Goldsbrough P.B, Hatch E.M, Huang B, Kosinski W.G, Dyer W.E, Herrmann K.M, Weller S.C. 1990. Gene amplification in glyphosate tolerant tobacco cells. Plant Sci. 72: 53-62.
Han H, Yu Q, Widderick M.J, Powles S.B. 2016. Target‐site EPSPS Pro‐106 mutations: sufficient to endow glyphosate resistance in polyploid Echinochloa colona?. Pest Manag. Sci. 72: 264-271.
Haroun S.A, Alotaibi M.K. 2015. Cytogenetic studies on two wild species of genus Echinochloa P. Beauv. from Saudi Arabia. Cytologia 80: 117-123.
Heap I, 2015. The International Survey of Herbicide Resistant Weeds. http://www.weedscience.org (accessed 8 December 2015).
Holm L.G, Plucknett D.L, Pancho J.V, Herberger J.P. 1977. The world's worst weeds: Distribution and biology, The University Press of Hawaii, Honolulu, Hawaii.
Iwakami S, Hashimoto M, Matsushima K, Watanabe H, Hamamura K, Uchino A. 2015. Multiple-herbicide resistance in Echinochloa crus-galli var. formosensis, an allohexaploid weed species, in dry-seeded rice. Pest. Biochem. Physiol. 119: 1-8.
Iwakami S, Uchino A, Watanabe H, Yamasue Y, Inamura T. 2012. Isolation and expression of genes for acetolactate synthase and acetyl-CoA carboxylase in Echinochloa phyllopogon, a polyploid weed species. Pest Manag. Sci. 68: 1098-1106.
Jasieniuk M, Brûlé-Babel A.L, Morrison I.N. 1996. The evolution and genetics of herbicide resistance in weeds. Weed Sci. 44: 176-193.
Jessop J, Dashorst G.R.M, James F.M. 2006. Grasses of South Australia : An illustrated guide to the native and naturalised species, Wakefield Press, Kent Town, Australia.
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, Meintjes 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.
Kremer A, Ronce O, Robledo-Arnuncio J.J, Guillaume F, Bohrer G, Nathan R, Bridle J.R, Gomulkiewicz R, Klein E.K, Ritland K, Kuparinen A, Gerber S, Schueler S. 2012. Long-distance gene flow and adaptation of forest trees to rapid climate change. Ecology Letters 15: 378-392.
Levin D.A. 1984. Immigration in plants: An exercise in the subjunctive, in: Dirzo R., Sarukhan J. (Eds.), Perspectives on Plant Population Ecology. Sinauer Associates Inc., Sunderland, Massachusetts, USA, pp. 242-260.
Lorraine-Colwill D.F, Powles S.B, Hawkes T.R, Hollinshead P.H, Warner S.A.J, Preston C. 2003. Investigations into the mechanism of glyphosate resistance in Lolium rigidum. Pest. Biochem. Physiol. 74: 62-72.
Lorraine-Colwill D.F, Powles S.B, Hawkes T.R, Preston C. 2001. Inheritance of evolved glyphosate resistance in Lolium rigidum (Gaud.). Theor. Appl. Genet. 102: 545-550.
Malone J.M, Morran S, Shirley N, Boutsalis P, Preston C. 2016. EPSPS gene amplification in glyphosate‐resistant Bromus diandrus. Pest Manag. Sci. 72: 81-88.
Marshall M.W, Al-Khatib K, Loughin T. 2001. Gene flow, growth, and competitiveness of imazethapyr-resistant common sunflower. Weed Sci. 49: 14-21.
Messeguer J, Fogher C, Guiderdoni E, Marfa V, Catala M.M, Baldi G, Mele E. 2001. Field assessments of gene flow from transgenic to cultivated rice (Oryza sativa L.) using a herbicide resistance gene as tracer marker. Theor. Appl. Genet. 103: 1151-1159.
Mohseni-Moghadam M, Schroeder J, Ashigh J. 2013. Mechanism of resistance and inheritance in glyphosate resistant palmer amaranth (Amaranthus palmeri) populations from New Mexico, USA. Weed Sci. 61: 517-525.
Motten A.F, Antonovics J. 1992. Determinants of outcrossing rate in a predominantly self-fertilizing weed, Datura stramonium (Solanaceae). Am. J. Bot. 79: 419-427.
Murray B.G, Morrison I.N, Friesen L.F. 2002. Pollen-mediated gene flow in wild oat. Weed Sci. 50: 321-325.
Ng C.H, Ratnam W, Surif S, Ismail B.S. 2004a. Inheritance of glyphosate resistance in goosegrass (Eleusine indica). Weed Sci. 52: 564-570.
Ng C.H, Wickneswary R, Salmijah S, Teng Y.T, 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: 407-414.
Nguyen T.H, Malone J.M, Boutsalis P, Shirley N, Preston C. 2016. Temperature influences the level of glyphosate resistance in barnyardgrass (Echinochloa colona). Pest Manag. Sci. 72: 1031-1039.
Nunez-Farfan J, CabralesVargas R.A, Dirzo R. 1996. Mating system consequences on resistance to herbivory and life history traits in Datura stramonium. Am. J. Bot. 83: 1041-1049.
Okada M, Jasieniuk M. 2014. Inheritance of glyphosate resistance in hairy fleabane (Conyza bonariensis) from California. Weed Sci. 62: 258-266.
Osten V.A, Walker S.R, Storrie A, Widderick M, Moylan P, Robinson G.R, Galea K. 2007. Survey of weed flora and management relative to cropping practices in the north-eastern grain region of Australia. Aust. J. Exp. Agric. 47: 57-70.
Preston C, 2015. The Australian Glyphosate Sustainability Working Group. http://www.glyphosateresistance.org.au/ (accessed 28 October 2015).
Preston C, Malone J.M. 2015. Inheritance of resistance to 2,4-D and chlorsulfuron in a multiple-resistant population of Sisymbrium orientale. Pest Manag. Sci. 71: 1523-1528.
Preston C, Shaner D.L, Westra P, Culpepper A.S, Grey T, Vencill W.K, Wakelin A. 2006. Can a shikimate assay be used to determine the genotype of glyphosate resistant plants for population genetic studies?. In: Proceedings of The 15th Australian Weeds Conference on Managing Weeds in A Changing Climate. Weed Management Society of South Australia, Australia, pp. 511-514.
Preston C, Wakelin A.M, Dolman F.C, Bostamam Y, Boutsalis P. 2009. A decade of glyphosate-resistant Lolium around the world: Mechanisms, genes, fitness, and agronomic management. Weed Sci. 57: 435-441.
Rognli O.A, Nilsson N.O, Nurminiemi M. 2000. Effects of distance and pollen competition on gene flow in the wind-pollinated grass Festuca pratensis Huds. Heredity 85: 550-560.
Sammons R.D, Gaines T.A. 2014. Glyphosate resistance: state of knowledge. Pest Manag. Sci. 70: 1367-1377.
Shaner D.L, Nadler-Hassar T, Henry W.B, Koger C.H. 2005. A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci. 53: 769-774.
Simarmata M, Bughrara S, Penner D. 2005. Inheritance of glyphosate resistance in rigid ryegrass (Lolium rigidum) from California. Weed Sci. 53: 615-619.
Slatkin M. 1987. Gene flow and the geographic structure of natural populations. Science 236: 787-792.
Sokal R.R, Rohlf F.J. 1981. Biometry: The principles and practice of statistics in biological research, second ed., W.H. Freeman and Company, New York, USA.
Stallings G.P, Thill D.C, Mallorysmith C.A, Shafii B. 1995. Pollen-mediated gene flow of sulfonylurea-restant kochia (Kochia scoparia). Weed Sci. 43: 95-102.
Storrie A, Cook T, Boutsalis P, Penberthy D, Moylan P. 2008. Glyphosate resistance in awnless barnyard grass (Echinochloa colona (L.) Link) and its implications for Australian farming systems. In: Proceedings of the 16th Australian Weeds Conference. Queensland Weed Society, Brisbane, Australia, pp. 74-76.
Thompson J.D, Gibson T.J, Plewniak F, Jeanmougin F, Higgins D.G. 1997. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
Volenberg D.S, Stoltenberg D.E. 2002. Giant foxtail (Setaria faberi) outcrossing and inheritance of resistance to acetyl-coenzyme A carboxylase inhibitors. Weed Sci. 50: 622-627.
Wakelin A.M, Lorraine-Colwill D.F, 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.
Wakelin A.M, Preston C. 2006. Inheritance of glyphosate resistance in several populations of rigid ryegrass (Lolium rigidum) from Australia. Weed Sci. 54: 212-219.
Yabuno T. 1983. Biology of Echinochloa species. In: Proceedings of the Conference on Weed Control in Rice. International Rice Research Institute (IRRI), Los Banos, Philippines, pp. 307-318.
Yu Q, Ahmad-Hamdani M.S, Han H, Christoffers M.J, Powles S.B. 2013. Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity 110: 220-231.
Zelaya I.A, Owen M.D.K, VanGessel M.J. 2004. Inheritance of evolved glyphosate resistance in Conyza canadensis (L.) Cronq. Theor. Appl. Genet. 110: 58-70.
)