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Evolution of Resistance to Auxinic Herbicides: Historical Perspectives, Mechanisms of Resistance, and Implications for Broadleaf Weed Management in Agronomic Crops

Published online by Cambridge University Press:  20 January 2017

J. Mithila ,
J. Christopher Hall ,
William G. Johnson ,
Kevin B. Kelley  and
Dean E. Riechers
J. Mithila
Affiliation:
School of Environmental Sciences, University of Guelph, Ontario, Canada N1G 2W1
J. Christopher Hall
Affiliation:
School of Environmental Sciences, University of Guelph, Ontario, Canada N1G 2W1
William G. Johnson
Affiliation:
Department of Botany and Plant Pathology, Purdue University, West Lafayette, IN 47907
Kevin B. Kelley
Affiliation:
AgraServ, Inc., American Falls, ID 83211
Dean E. Riechers*
Affiliation:
Department of Crop Sciences, University of Illinois, Urbana, IL 61801
*
Corresponding author's E-mail: [email protected]
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Abstract

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Auxinic herbicides are widely used for control of broadleaf weeds in cereal crops and turfgrass. These herbicides are structurally similar to the natural plant hormone auxin, and induce several of the same physiological and biochemical responses at low concentrations. After several decades of research to understand the auxin signal transduction pathway, the receptors for auxin binding and resultant biochemical and physiological responses have recently been discovered in plants. However, the precise mode of action for the auxinic herbicides is not completely understood despite their extensive use in agriculture for over six decades. Auxinic herbicide-resistant weed biotypes offer excellent model species for uncovering the mode of action as well as resistance to these compounds. Compared with other herbicide families, the incidence of resistance to auxinic herbicides is relatively low, with only 29 auxinic herbicide-resistant weed species discovered to date. The relatively low incidence of resistance to auxinic herbicides has been attributed to the presence of rare alleles imparting resistance in natural weed populations, the potential for fitness penalties due to mutations conferring resistance in weeds, and the complex mode of action of auxinic herbicides in sensitive dicot plants. This review discusses recent advances in the auxin signal transduction pathway and its relation to auxinic herbicide mode of action. Furthermore, comprehensive information about the genetics and inheritance of auxinic herbicide resistance and case studies examining mechanisms of resistance in auxinic herbicide-resistant broadleaf weed biotypes are provided. Within the context of recent findings pertaining to auxin biology and mechanisms of resistance to auxinic herbicides, agronomic implications of the evolution of resistance to these herbicides are discussed in light of new auxinic herbicide-resistant crops that will be commercialized in the near future.

Keywords

Auxinic herbicidesdominant traitevolution of resistancefitness costherbicide-resistant cropsmode of actionmechanism of resistanceplant growth regulatorrecessive trait
Type
Review
Information
Weed Science , Volume 59 , Issue 4 , December 2011 , pp. 445 - 457
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
Copyright
Copyright © Weed Science Society of America

References

Literature Cited

Abdullah, I., Fischer, A. J., Elmore, C. L., Saltveit, M. E., and Zaki, M. 2006. Mechanism of resistance to quinclorac in smooth crabgrass (Digitaria ischaemum L). Pestic. Biochem. Physiol. 84:38–48.Google Scholar
Ashton, F. M. and Crafts, A. S. 1981. Phenoxys. Pages 272–302 in Ashton, F. M. and Crafts, A. S., eds. Mode of Action of Herbicides. Toronto John Wiley and Sons.Google Scholar
Bajguz, A. and Piotrowska, A. 2009. Conjugates of auxin and cytokinin. Phytochemistry. 70:957–969.Google Scholar
Baysinger, J. A. and Sims, B. D. 1991. Giant ragweed (Ambrosia trifida) interference in soybeans (Glycine max). Weed Sci. 39:358–362.Google Scholar
Beckie, H. J. and Reboud, X. 2009. Selecting for weed resistance: herbicide rotation and mixture. Weed Technol. 23:363–370.Google Scholar
Beversdorf, W. D., Hume, D. J., and Donnelly-Vanderloo, M. J. 1988. Agronomic performance of triazine-resistant and susceptible reciprocal spring canola hybrids. Crop Sci. 28:932–934.Google Scholar
Bourdot, G. W., Saville, D. J., and Hurrell, G. A. 1996. Ecological fitness and the decline of resistance to the herbicide MCPA in a population of Ranunculus acris . J. Appl. Ecol. 33:151–160.Google Scholar
Bradshaw, L. D., Padgette, S. R., Kimball, S. L., and Wells, B. H. 1997. Perspectives on glyphosate resistance. Weed Technol. 11:189–198.Google Scholar
Burke, I. C., Yenish, J. P., Pittmann, D., and Gallagher, R. S. 2009. Resistance of a prickly lettuce (Lactuca serriola) biotype to 2,4-D. Weed Technol. 23:586–591.Google Scholar
Calderon-Villalobos, L. I., Tan, X., Zheng, N., and Estelle, M. 2010. Auxin perception–structural insights. Cold Spring Harb. Perspect. Biol. 2:a005546.Google Scholar
Chapman, E. J. and Estelle, M. 2009. Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 43:265–285.Google Scholar
Childs, D. J., Jordan, T. N., and Blackwell, R. L. 1997. Survey of problem weeds in Indiana: 1996. W. Lafayette, IN: Purdue University Cooperative Extension Service, WS–10.Google Scholar
Coupland, D. 1994. Resistance to auxin analog herbicides. Pages 171–214 in Powles, S.B. and Holtum, J.A.M., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL Lewis Publishers, CRC Press.Google Scholar
Cranston, H. J., Kern, A. J., Hackett, J. L., Miller, E. K., Maxwell, B. D., and Dyer, W. E. 2001. Dicamba resistance in kochia. Weed Sci. 49:164–170.Google Scholar
Culpepper, S. A. 2006. Glyphosate-induced weed shifts. Weed Technol. 20:277–281.Google Scholar
Culpepper, S. A., Grey, T. L., Vencill, W. K., Kichler, J. M., Webster, T. M., Brown, S. M., York, A. C., Davis, J. W., and Hanna, W. W. 2006. Glyphosate-resistant Palmer amaranth (Amaranthus palmeri) confirmed in Georgia. Weed Sci. 54:620–626.Google Scholar
Culpepper, S. A. and York, A. C. 2008. Glyphosate-resistant Palmer amaranth impacts Southeastern agriculture. Proc. IL. Crop Protect. Technol. Conf. 60:61–63.Google Scholar
Darmency, H. 1994. Genetics of herbicide resistance in weeds and crops. Pages 263–297 in Powles, S.B. and Holtum, J.A.M., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL Lewis Publishers, CRC Press.Google Scholar
Dauer, J. T., Mortensen, D. A., and Humston, R. 2006. Controlled experiments to predict horseweed (Conyza canadensis) dispersal distances. Weed Sci. 54:484–489.Google Scholar
Davis, V. M., Gibson, K. D., Bauman, T. T., Weller, S. C., and Johnson, W. G. 2007. Influence of weed management practices and crop rotation on glyphosate-resistant horseweed population dynamics and crop yield. Weed Sci. 55:508–516.Google Scholar
Davis, V. M., Gibson, K. D., and Johnson, W. G. 2008. A field survey to determine distribution and frequency of glyphosate-resistant horseweed (Conyza canadensis) in Indiana. Weed Technol. 22:331–338.Google Scholar
Debreuil, D. J., Friesen, L. F., and Morrison, I. N. 1996. Growth and seed return of auxin-type herbicide resistant wild mustard (Brassica kaber) in wheat. Weed Sci. 44:872–878.Google Scholar
DeGennaro, F. P. and Weller, S. C. 1984. Differential susceptibility of field bindweed (Convolvulus arvensis) biotypes to glyphosate. Weed Sci. 32:472–476.Google Scholar
Devine, M. D., Duke, S. O., and Fedtke, C. 1993. Herbicides with auxin activity. Pages 295–309 in Physiology of Herbicide Action. Englewood Cliffs, NJ Prentice Hall PTR.Google Scholar
Devine, M. D. and Shukla, A. 2000. Altered target site as a mechanism of herbicide resistance. Crop Prot. 19:881–889.Google Scholar
Dharmasiri, N., Dharmasiri, S., and Estelle, M. 2005. The F-box protein TIR1 is an auxin receptor. Nature. 435:441–445.Google Scholar
Diggle, A. J., Neve, P. B., and Smith, F. P. 2003. Herbicides used in combination can reduce the probability of herbicide resistance in finite weed populations. Weed Res. 43:371–382.Google Scholar
Duke, S. O. 1996. Herbicide-resistant crops: background and perspectives. Pages 1–10 in Duke, S. O., ed. Herbicide-Resistant Crops: Agricultural, Environmental, Economic, Regulatory, and Technical Aspects. Boca Raton, FL CRC Press.Google Scholar
Dyer, W. E., Goss, G. A., and Buck, P. 2002. Gravitropic responses of auxinic herbicide-resistant Kochia scoparia . Annu. Meet. Weed Sci. Soc. Amer. Abstr. 171. Pg. 49.Google Scholar
Firbank, L. G., Rothery, P., May, M. J., et al. 2006. Effects of genetically modified herbicide-tolerant cropping systems on weed seedbanks in two years of following crops. Biol. Lett. 2:140–143.Google Scholar
Fuerst, E. P., Sterling, T. M., Norman, M. A., Prather, T. S., Irzyk, G. P., Wu, Y., Lownds, N. K., and Callihan, R. H. 1996. Physiological characterization of picloram resistance in yellow starthistle. Pestic. Biochem. Physiol. 56:149–161.Google Scholar
Ge, X., d'Avignon, D. A., 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
Goss, G. A. and Dyer, W. E. 2003. Physiological characterization of auxinic herbicide-resistant biotypes of kochia (Kochia scoparia). Weed Sci. 51:839–844.Google Scholar
Gressel, J. and Ben-Sinai, G. 1989. Low intraspecific competitive fitness in a triazine resistant, nearly isogenic line of Brassica napus . Pages 489–504 in van Vloten-Doting, L., Groot, G.S.P., and Hall, T. C., eds. Molecular Form and Function of Plant Genome. New York Plenum Press.Google Scholar
Gressel, J. and Segel, L. A. 1982. Interrelating factors controlling the rate of appearance of resistance: the outlook for the future. Pages 325–447 in LeBaron, H. M., and Gressel, J., eds. Herbicide Resistance in Plants. New York John Wiley and Sons.Google Scholar
Gressel, J. and Segel, L. A. 1990. Modelling the effectiveness of herbicide rotations and mixtures as strategies to delay or preclude resistance. Weed Technol. 4:186–198.Google Scholar
Grossman, K. 2000. The mode of action of auxin herbicides: a new ending to a long, drawn out story. Trends Plant Sci. 5:506–508.Google Scholar
Grossman, K. 2010. Auxin herbicides: current status of mechanism and mode of action. Pest Manag. Sci. 66:113–120.Google Scholar
Grossmann, K. and Hansen, H. 2001. Ethylene-triggered abscisic acid: a principle in plant growth regulation? Physiol. Plant. 113:9–14.Google Scholar
Grossmann, K., Scheltrup, F., Kwiatkowski, J., and Caspar, G. 1996. Induction of abscisic acid is a common effect of auxin herbicides in susceptible plants. J. Plant Physiol. 149:475–478.Google Scholar
Guilfoyle, T. 2007. Sticking with auxin. Nature. 446:621–622.Google Scholar
Gustafson, D. I. 2008. Sustainable use of glyphosate in North American cropping systems. Pest Manag. Sci. 64:409–416.Google Scholar
Hall, J. C., Alam, S. M. M., and Murr, D. P. 1993. Ethylene biosynthesis following foliar application of picloram to biotypes of wild mustard (Sinapis arvensis L.) susceptible or resistant to auxinic herbicides. Pestic. Biochem. Physiol. 47:36–43.Google Scholar
Hall, J. C. and Romano, M. L. 1995. Morphological and physiological differences between the auxinic herbicide susceptible (S) and resistant (R) wild mustard (Sinapis arvensis) biotypes. Pestic. Biochem. Physiol. 52:149–155.Google Scholar
Hall, J. C., Webb, S. R., and Deshpande, S. 1996. An overview of auxinic herbicide resistance: wild mustard as a case study. Pages 28–43 in Brown, T. M., ed. Molecular Genetics and Evolution of Pesticide Resistance. Washington, DC American Chemical Society.Google Scholar
Hanson, N. S. 1962. Weed control practices and research for sugar cane in Hawaii. Weeds. 10:192–200.Google Scholar
Harper, J. L. 1956. The evolution of weeds in relation to resistance to herbicides. Proc. 3rd Bright. Weed Control Conf. 3:179–188.Google Scholar
Harrison, S. K., Regnier, E. E., Schmoll, J. T., and Webb, J. E. 2001. Competition and fecundity of giant ragweed in corn. Weed Sci. 49:224–229.Google Scholar
Heap, I. 2011. International Survey of Herbicide-Resistant Weeds. http://www.weedscience.org/in.asp. Accessed: April 14, 2011.Google Scholar
Heap, I. M. and Morrison, I. N. 1992. Resistance to auxin-type herbicides in wild mustard (Sinapis arvensis L.) populations in western Canada. Annu. Meet. Weed Sci. Soc. Amer. Abstr. 32:164.Google Scholar
Hilgenfeld, K. L., Martin, A. R., Mortensen, D. A., and Mason, S. C. 2004. Weed management in a glyphosate resistant soybean system: weed species shifts. Weed Technol. 18:284–291.Google Scholar
Industry Task Force II on 2,4-D Research Data. 2005. Issue Backgrounder. http://www.24d.org/background/24D-Backgrounder-Benefits.pdf. Accessed: October 31, 2010.Google Scholar
Jacob, B. F., Duesing, J. H., Antonovics, J., and Patterson, D. T. 1988. Growth performance of triazine-resistant and -susceptible biotypes of Solanum nigrum over a range of temperatures. Can. J. Bot. 66:847–850.Google Scholar
Jasieniuk, M., Brule-Babel, A. L., and Morrison, I. N. 1996. The evolution and genetics of hericide resistance in weeds. Weed Sci. 44:176–193.Google Scholar
Jasieniuk, M., Morrison, I. N., and Brule-Babel, A. L. 1995. Inheritance of dicamba resistance in wild mustard (Brassica kaber). Weed Sci. 43:192–195.Google Scholar
Jeschke, M. R. and Stoltenberg, D. E. 2006. Weed community composition after eight years of continuous glyphosate use in a corn-soybean annual rotation. Proc. N. Cent. Weed Sci. Soc. 58:59.Google Scholar
Johnson, B., Young, B., Matthews, J., et al. 2010. Weed control in dicamba resistant soybeans. Crop Manag. [Online: DOI:10.1094/CM-2010-0920-01-RS].Google Scholar
Johnson, W. G., Ott, E. J., Gibson, K. D., Nielsen, R. L., and Bauman, T. T. 2007. Influence of nitrogen application timing on low-density giant ragweed (Ambrosia trifida) interference in corn. Weed Technol. 21:763–767.Google Scholar
Jugulam, M., McLean, M. D., and Hall, J. C. 2005. Inheritance of picloram and 2,4-D resistance in wild mustard (Brassica kaber). Weed Sci. 53:417–423.Google Scholar
Kelley, K. B., Lambert, K. N., Hager, A. G., and Riechers, D. E. 2004. Quantitative expression analysis of GH3, a gene induced by plant growth regulator herbicides in soybean. J. Agric. Food Chem. 52:474–478.Google Scholar
Kelley, K. B. and Riechers, D. E. 2007. Recent developments in auxin biology and new opportunities for auxinic herbicide research. Pestic. Biochem. Physiol. 89:1–11.Google Scholar
Kepinski, S. and Leyser, O. 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 435:446–451.Google Scholar
Kern, A. J., Chaverra, M. E., Cranston, H. J., and Dyer, W. E. 2005. Dicamba-responsive genes in herbicide-resistant and susceptible biotypes of kochia (Kochia scoparia). Weed Sci. 53:139–145.Google Scholar
Kirby, C. 1980. The Hormone Weedkillers: A Short History of Their Discovery and Development. London Road, Croydon, UK British Crop Protection Council. 55 p.Google Scholar
Kruger, G. R., Johnson, W. G., Weller, S. C., Owen, M. D. K., Shaw, D. R., Wilcut, J. W., Jordan, D. L., Wilson, R. G., and Young, B. G. 2008. U.S. grower views on problematic weeds and changes in weed pressure in glyphosate-resistant corn, cotton, and soybean cropping systems. Weed Technol. 23:162–166.Google Scholar
Lee, O. C. 1948. The effect of 2,4-D as a selective herbicide in growing corn and sorghums. Proc. North Cent. Weed Sci. Soc. 5:18–21.Google Scholar
Legleiter, T. R. and Bradley, K. W. 2008. Glyphosate and multiple herbicide resistance in waterhemp (Amaranthus rudis) populations from Missouri. Weed Sci. 56:582–587.Google Scholar
Loux, M. M. and Berry, M. A. 1991. Use of a grower survey for estimating weed problems. Weed Technol. 5:460–466.Google Scholar
Lovelace, M. L., Talbert, R. E., Hoagland, R. E., and Scherder, E. F. 2007. Quinclorac absorption and translocation characteristics in quinclorac- and propanil-resistant and -susceptible barnyardgrass (Echinocloa crus-galli) biotypes. Weed Technol. 21:683–687.Google Scholar
Ludwig-Müller, J. 2011. Auxin conjugates: their role for plant development and in the evolution of land plants. J. Expt. Bot. 62:1757–1773.Google Scholar
McCloskey, W. B. and Holt, J. S. 1991. Effect of growth temperature on biomass production of nearly isonuclear triazine-R and S common groundsel (Senecio vulgaris L.). Plant Cell Environ. 14:699–705.Google Scholar
Mithila, J. and Hall, J. C. 2005. Comparison of ABP1 over-expressing Arabidopsis and under-expressing tobacco with an auxinic herbicide-resistant wild mustard (Brassica kaber) biotype. Plant Sci. 169:21–28.Google Scholar
Mockaitis, K. and Estelle, M. 2008. Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24:55–80.Google Scholar
Morrison, I. N. and Devine, M. D. 1994. Herbicide resistance in the Canadian prairie provinces: five years after the fact. Phytoprotection. 75(Suppl.):5–16.Google Scholar
Nice, G. and Johnson, B. 2005. Indiana's Top Ten Most Problematic Weeds. Purdue University Cooperative Extension Services. www.btny.purdue.edu/WeedScience/2005/topten05.pdf. Accessed: October 31, 2010.Google Scholar
Owen, M. D. K. and Zelaya, I. A. 2005. Herbicide-resistant crops and weed resistance to herbicides. Pest Manag. Sci. 61:301–311.Google Scholar
Patzoldt, W. L., Tranel, P. J., and Hager, A. G. 2005. A waterhemp (Amaranthus tuberculatus) biotype with multiple resistances across three herbicide sites of action. Weed Sci. 53:30–36.Google Scholar
Peniuk, M. G., Romano, M. L., and Hall, J. C. 1993. Physiological investigations into the resistance of wild mustard (Sinapis arvensis L) biotype to auxinic herbicides. Weed Res. 33:431–440.Google Scholar
Petersson, S. V., Johansson, A. I., Kowalczyk, M., Makoveychuk, A., Wang, J. Y., Moritz, T., Grebe, M., Benfey, P. N., Sandberg, G., and Ljung, K. 2009. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell. 21:1659–1668.Google Scholar
Powles, S. B. and Preston, C. 2006. Evolved glyphosate resistance in plants: biochemical and genetic basis of resistance. Weed Technol. 20:282–289.Google Scholar
Powles, S. B., Preston, C., Bryan, I. B., and Jutsum, A. R. 1997. Herbicide resistance: impact and management. Advan. Agron. 58:57–93.Google Scholar
Preston, C., Belles, D. S., Westra, P. H., Nissen, S. J., and Ward, S. M. 2009. Inheritance of resistance to the auxinic herbicide dicamba in kochia (Kochia scoparia). Weed Sci. 57:43–47.Google Scholar
Preston, C. and Mallory-Smith, C. A. 2001. Biochemical mechanisms, inheritance, and molecular genetics of herbicide resistance in weeds. Pages 23–60 in Powles, S. B. and Shaner, D. L., eds. Herbicide Resistance in World Grains. Boca Raton, FL CRC Press.Google Scholar
Romero-Puertas, M. C., McCarthy, I., Gomez, M., Sandalio, L. M., Corpas, F. J., Del Rio, L. A., and Palma, J. M. 2004. Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ. 27:1135–1148.Google Scholar
Rubery, P. H. 1977. The specificity of carrier-mediated auxin transport by suspension-cultured crown gall cells. Planta. 135:275–283.Google Scholar
Sabba, R. P., Ray, I. M., Lownds, N., and Sterling, T. M. 2003. Inheritance of resistance to clopyralid and picloram in yellow starthistle (Centaurea solstitialis) is controlled by a single nuclear recessive gene. J. Hered. 94:523–527.Google Scholar
Sabba, R. P., Sterling, T. M., and Lownds, N. 1998. Effect of picloram on R and S yellow starthistle (Centaurea solstitialis): the role of ethylene. Weed Sci. 46:297–300.Google Scholar
Salisbury, F. B. and Ross, C. W. 1992. Plant Physiology. 4th ed. Belmont, CA Wadsworth Publishing Company. 635 p.Google Scholar
Shaner, D. L. 2000. The impact of glyphosate-tolerant crops on the use of other herbicides and on resistance management. Pest Manag. Sci. 56:320–326.Google Scholar
Simon, S. and Petrášek, J. 2011. Why plants need more than one type of auxin. Plant Sci. 180:454–460.Google Scholar
Singh, D. 2009. Understanding 2,4-D resistance in prickly lettuce (Lactuca serriola) and evaluating chemical fallow systems for the inland PNW. Ph.D. dissertation. Pullman, WA Washington State University. 159 p.Google Scholar
Staswick, P. E. 2009. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 150:1310–1321.Google Scholar
Staswick, P. E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M. T., Maldonado, M. C., and Suza, W. 2005. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 17:616–627.Google Scholar
Steckel, L. E. 2007. The dioecious Amaranthus spp.: here to stay. Weed Technol. 21:567–570.Google Scholar
Sterling, T. M. 1994. Mechanisms of herbicide absorption across plant membranes and accumulation in plant cells. Weed Sci. 42:263–276.Google Scholar
Sterling, T. M. and Hall, J. C. 1997. Mechanism of action of natural auxins and the auxinic herbicides. Pages 111–141 in Roe, R. M., Burton, J. D., and Kuhr, R. J., eds. Herbicide Activity: Toxicology, Biochemistry and Molecular Biology. Amsterdam, the Netherlands IOS Press.Google Scholar
Tan, X., Calderon-Villalobos, L. I. A., Sharon, M., Zheng, C., Robinson, C. V., Estelle, M., and Zheng, N. 2007. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature. 446:640–645.Google Scholar
Triplett, G. B. Jr. and Lytle, G. D. 1972. Control and ecology of weeds in continuous corn grown without tillage. Weed Sci. 20:453–457.Google Scholar
Tromas, A., Paponov, I., and Perrot-Rechenmann, C. 2010. Auxin binding protein 1: functional and evolutionary aspects. Trends Plant Sci. 15:436–446.Google Scholar
Trucco, F., Zheng, D., Woodyard, A. J., Walter, J. R., Tatum, T. C., Rayburn, A. L., and Tranel, P. J. 2007. Nonhybrid progeny from crosses of dioecious amaranths: implications for gene-flow research. Weed Sci. 55:119–122.Google Scholar
United States Department of Agriculture - National Agricultural Statistics Service. USDA-NASS. 2008. Agricultural Chemical Use Database. www.pestmanagement.info/nass. Washington, DC: USDA-NASS. Accessed: October 31, 2010.Google Scholar
Valenzuela-Valenzuela, J. M., Lownds, N. K., and Sterling, T. M. 2001. Clopyralid uptake, translocation, metabolism, and ethylene induction in picloram-resistant yellow starthistle (Centaurea solstitislis L.). Pestic. Biochem. Physiol. 71:11–19.Google Scholar
Valenzuela-Valenzuela, J. M., Lownds, N. K., and Sterling, T. M. 2002. Ethylene plays no role in clopyralid action in yellow starthistle (Centaurea solstitislis L.). Pestic. Biochem. Physiol. 72:142–152.Google Scholar
Van Eerd, L. L., McLean, M. D., Stephenson, G. R., and Hall, J. C. 2004. Resistance to quinclorac and ALS-inhibitor herbicides in Galium spurium is conferred by two distinct genes. Weed Res. 44:355–365.Google Scholar
Van Eerd, L. L., Stephenson, G. R., Kwiatkowski, J., Grossmann, K., and Hall, J. C. 2005. Physiological and biochemical characterization of quinclorac and resistance in a false cleavers (Galium spurium) biotype. J. Agric. Food Chem. 53:1144–1151.Google Scholar
VanGessel, M. J. 2001. Glyphosate resistant horseweed from Delaware. Weed Sci. 49:703–705.Google Scholar
Vila-Aiub, M. M., Neve, P., and Powles, S. B. 2009. Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol. 184:751–767.Google Scholar
Walsh, M. J., Maguire, N., and Powles, S. B. 2009. Combined effects of wheat competition and 2,4-D amine on phenoxy herbicide resistant Raphanus raphanistrum populations. Weed Res. 49:316–325.Google Scholar
Walsh, M. J., Powles, S. B., Beard, B. R., Parkin, B. T., and Porter, S. A. 2004. Multiple-herbicide resistance across four modes of action in wild radish (Raphanus raphanistrum). Weed Sci. 52:8–13.Google Scholar
Walsh, T. A., Neal, R., Merlo, A. O., Honma, M., Hicks, G. R., Wolff, K., Matsumura, W., and Davies, J. P. 2006. Mutations in an auxin receptor homolog AFB5 and in SGT1b confer resistance to synthetic picolinate auxins and not to 2,4-dichlorophenoxyacetic acid or indole-3-acetic acid in Arabidopsis . Plant Physiol. 142:542–552.Google Scholar
Webb, S. R. and Hall, J. C. 1995. Auxinic herbicide-resistant and -susceptible wild mustard (Sinapis arvensis L.) biotypes: effect of auxinic herbicides on seedling growth and auxin-binding activity. Pestic. Biochem. Physiol. 52:137–148.Google Scholar
Wei, Y. D., Zheng, H. G., and Hall, J. C. 2000. Role of auxinic herbicide-induced ethylene on hypocotyl elongation and root/hypocotyl radial expansion. Pest Manag. Sci. 56:377–387.Google Scholar
Weinberg, T., Stephenson, G. R., McLean, M. D., and Hall, J. C. 2006. MCPA (4-chloro-2-ethylphenoxyacetate) resistance in hemp-nettle (Galeopsis tetrahit L.). J. Agric. Food Chem. 54:9126–9134.Google Scholar
Went, F. W. 1926. Growth accelerating substances in coleoptile of Avena sativa . Proc. K. Akad. Wet. Amsterdam. 30:10–19.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
Wilson, R. G., Miller, S. D., Westra, P., Kniss, A. R., Stahlman, P. W., Wicks, G. W., and Kachman, S. D. 2007. Glyphosate-induced weed shifts in glyphosate-resistant corn or a rotation of glyphosate-resistant corn, sugarbeet, and spring wheat. Weed Technol. 21:900–909.Google Scholar
Wrubel, R. P. and Gressel, J. 1994. Are herbicide mixtures useful for delaying the rapid evolution of resistance? A case study. Weed Technol. 8:635–648.Google Scholar
Zhang, Q. and Riechers, D. E. 2008. Proteomics: an emerging technology for weed science research. Weed Sci. 56:306–313.Google Scholar
Zheng, H. G. and Hall, J. C. 2001. Understanding auxinic herbicide resistance in Sinapis arvensis L.: physiological, biochemical and molecular genetic approaches. Weed Sci. 49:276–281.Google Scholar