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

  • J. Mithila (a1), J. Christopher Hall (a1), William G. Johnson (a2), Kevin B. Kelley (a3) and Dean E. Riechers (a4)...
Abstract

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.

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Corresponding author's E-mail: riechers@illinois.edu
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I. Abdullah , A. J. Fischer , C. L. Elmore , M. E. Saltveit , and M. Zaki 2006. Mechanism of resistance to quinclorac in smooth crabgrass (Digitaria ischaemum L). Pestic. Biochem. Physiol. 84:3848.

A. Bajguz and A. Piotrowska 2009. Conjugates of auxin and cytokinin. Phytochemistry. 70:957969.

W. D. Beversdorf , D. J. Hume , and M. J. Donnelly-Vanderloo 1988. Agronomic performance of triazine-resistant and susceptible reciprocal spring canola hybrids. Crop Sci. 28:932934.

G. W. Bourdot , D. J. Saville , and G. A. Hurrell 1996. Ecological fitness and the decline of resistance to the herbicide MCPA in a population of Ranunculus acris . J. Appl. Ecol. 33:151160.

L. I. Calderon-Villalobos , X. Tan , N. Zheng , and M. Estelle 2010. Auxin perception–structural insights. Cold Spring Harb. Perspect. Biol. 2:a005546.

E. J. Chapman and M. Estelle 2009. Mechanism of auxin-regulated gene expression in plants. Annu. Rev. Genet. 43:265285.

H. J. Cranston , A. J. Kern , J. L. Hackett , E. K. Miller , B. D. Maxwell , and W. E. Dyer 2001. Dicamba resistance in kochia. Weed Sci. 49:164170.

V. M. Davis , K. D. Gibson , T. T. Bauman , S. C. Weller , and W. G. Johnson 2007. Influence of weed management practices and crop rotation on glyphosate-resistant horseweed population dynamics and crop yield. Weed Sci. 55:508516.

M. D. Devine and A. Shukla 2000. Altered target site as a mechanism of herbicide resistance. Crop Prot. 19:881889.

N. Dharmasiri , S. Dharmasiri , and M. Estelle 2005. The F-box protein TIR1 is an auxin receptor. Nature. 435:441445.

A. J. Diggle , P. B. Neve , and F. P. Smith 2003. Herbicides used in combination can reduce the probability of herbicide resistance in finite weed populations. Weed Res. 43:371382.

L. G. Firbank , P. Rothery , M. J. May , et al. 2006. Effects of genetically modified herbicide-tolerant cropping systems on weed seedbanks in two years of following crops. Biol. Lett. 2:140143.

E. P. Fuerst , T. M. Sterling , M. A. Norman , T. S. Prather , G. P. Irzyk , Y. Wu , N. K. Lownds , and R. H. Callihan 1996. Physiological characterization of picloram resistance in yellow starthistle. Pestic. Biochem. Physiol. 56:149161.

K. Grossman 2000. The mode of action of auxin herbicides: a new ending to a long, drawn out story. Trends Plant Sci. 5:506508.

K. Grossmann and H. Hansen 2001. Ethylene-triggered abscisic acid: a principle in plant growth regulation? Physiol. Plant. 113:914.

K. Grossmann , F. Scheltrup , J. Kwiatkowski , and G. Caspar 1996. Induction of abscisic acid is a common effect of auxin herbicides in susceptible plants. J. Plant Physiol. 149:475478.

T. Guilfoyle 2007. Sticking with auxin. Nature. 446:621622.

D. I. Gustafson 2008. Sustainable use of glyphosate in North American cropping systems. Pest Manag. Sci. 64:409416.

J. C. Hall , S. M. M. Alam , and D. P. Murr 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. 47:3643.

J. C. Hall and M. L. Romano 1995. Morphological and physiological differences between the auxinic herbicide susceptible (S) and resistant (R) wild mustard (Sinapis arvensis) biotypes. Pestic. Biochem. Physiol. 52:149155.

J. C. Hall , S. R. Webb , and S. Deshpande 1996. An overview of auxinic herbicide resistance: wild mustard as a case study. Pages 2843 in T. M. Brown , ed. Molecular Genetics and Evolution of Pesticide Resistance. Washington, DC American Chemical Society.

N. S. Hanson 1962. Weed control practices and research for sugar cane in Hawaii. Weeds. 10:192200.

S. K. Harrison , E. E. Regnier , J. T. Schmoll , and J. E. Webb 2001. Competition and fecundity of giant ragweed in corn. Weed Sci. 49:224229.

B. Johnson , B. Young , J. Matthews , et al. 2010. Weed control in dicamba resistant soybeans. Crop Manag. [Online: DOI:10.1094/CM-2010-0920-01-RS].

K. B. Kelley , K. N. Lambert , A. G. Hager , and D. E. Riechers 2004. Quantitative expression analysis of GH3, a gene induced by plant growth regulator herbicides in soybean. J. Agric. Food Chem. 52:474478.

K. B. Kelley and D. E. Riechers 2007. Recent developments in auxin biology and new opportunities for auxinic herbicide research. Pestic. Biochem. Physiol. 89:111.

S. Kepinski and O. Leyser 2005. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature. 435:446451.

G. R. Kruger , W. G. Johnson , S. C. Weller , M. D. K. Owen , D. R. Shaw , J. W. Wilcut , D. L. Jordan , R. G. Wilson , and B. G. Young 2008. U.S. grower views on problematic weeds and changes in weed pressure in glyphosate-resistant corn, cotton, and soybean cropping systems. Weed Technol. 23:162166.

T. R. Legleiter and K. W. Bradley 2008. Glyphosate and multiple herbicide resistance in waterhemp (Amaranthus rudis) populations from Missouri. Weed Sci. 56:582587.

J. Ludwig-Müller 2011. Auxin conjugates: their role for plant development and in the evolution of land plants. J. Expt. Bot. 62:17571773.

W. B. McCloskey and J. S. Holt 1991. Effect of growth temperature on biomass production of nearly isonuclear triazine-R and S common groundsel (Senecio vulgaris L.). Plant Cell Environ. 14:699705.

J. Mithila and J. C. Hall 2005. Comparison of ABP1 over-expressing Arabidopsis and under-expressing tobacco with an auxinic herbicide-resistant wild mustard (Brassica kaber) biotype. Plant Sci. 169:2128.

K. Mockaitis and M. Estelle 2008. Auxin receptors and plant development: a new signaling paradigm. Annu. Rev. Cell Dev. Biol. 24:5580.

I. N. Morrison and M. D. Devine 1994. Herbicide resistance in the Canadian prairie provinces: five years after the fact. Phytoprotection. 75(Suppl.):516.

M. D. K. Owen and I. A. Zelaya 2005. Herbicide-resistant crops and weed resistance to herbicides. Pest Manag. Sci. 61:301311.

M. G. Peniuk , M. L. Romano , and J. C. Hall 1993. Physiological investigations into the resistance of wild mustard (Sinapis arvensis L) biotype to auxinic herbicides. Weed Res. 33:431440.

S. V. Petersson , A. I. Johansson , M. Kowalczyk , A. Makoveychuk , J. Y. Wang , T. Moritz , M. Grebe , P. N. Benfey , G. Sandberg , and K. Ljung 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. 21:16591668.

S. B. Powles , C. Preston , I. B. Bryan , and A. R. Jutsum 1997. Herbicide resistance: impact and management. Advan. Agron. 58:5793.

C. Preston , D. S. Belles , P. H. Westra , S. J. Nissen , and S. M. Ward 2009. Inheritance of resistance to the auxinic herbicide dicamba in kochia (Kochia scoparia). Weed Sci. 57:4347.

M. C. Romero-Puertas , I. McCarthy , M. Gomez , L. M. Sandalio , F. J. Corpas , L. A. Del Rio , and J. M. Palma 2004. Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ. 27:11351148.

P. H. Rubery 1977. The specificity of carrier-mediated auxin transport by suspension-cultured crown gall cells. Planta. 135:275283.

R. P. Sabba , I. M. Ray , N. Lownds , and T. M. Sterling 2003. Inheritance of resistance to clopyralid and picloram in yellow starthistle (Centaurea solstitialis) is controlled by a single nuclear recessive gene. J. Hered. 94:523527.

D. L. Shaner 2000. The impact of glyphosate-tolerant crops on the use of other herbicides and on resistance management. Pest Manag. Sci. 56:320326.

S. Simon and J. Petrášek 2011. Why plants need more than one type of auxin. Plant Sci. 180:454460.

P. E. Staswick 2009. The tryptophan conjugates of jasmonic and indole-3-acetic acids are endogenous auxin inhibitors. Plant Physiol. 150:13101321.

P. E. Staswick , B. Serban , M. Rowe , I. Tiryaki , M. T. Maldonado , M. C. Maldonado , and W. Suza 2005. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell. 17:616627.

X. Tan , L. I. A. Calderon-Villalobos , M. Sharon , C. Zheng , C. V. Robinson , M. Estelle , and N. Zheng 2007. Mechanism of auxin perception by the TIR1 ubiquitin ligase. Nature. 446:640645.

A. Tromas , I. Paponov , and C. Perrot-Rechenmann 2010. Auxin binding protein 1: functional and evolutionary aspects. Trends Plant Sci. 15:436446.

F. Trucco , D. Zheng , A. J. Woodyard , J. R. Walter , T. C. Tatum , A. L. Rayburn , and P. J. Tranel 2007. Nonhybrid progeny from crosses of dioecious amaranths: implications for gene-flow research. Weed Sci. 55:119122.

J. M. Valenzuela-Valenzuela , N. K. Lownds , and T. M. Sterling 2001. Clopyralid uptake, translocation, metabolism, and ethylene induction in picloram-resistant yellow starthistle (Centaurea solstitislis L.). Pestic. Biochem. Physiol. 71:1119.

J. M. Valenzuela-Valenzuela , N. K. Lownds , and T. M. Sterling 2002. Ethylene plays no role in clopyralid action in yellow starthistle (Centaurea solstitislis L.). Pestic. Biochem. Physiol. 72:142152.

L. L. Van Eerd , M. D. McLean , G. R. Stephenson , and J. C. Hall 2004. Resistance to quinclorac and ALS-inhibitor herbicides in Galium spurium is conferred by two distinct genes. Weed Res. 44:355365.

L. L. Van Eerd , G. R. Stephenson , J. Kwiatkowski , K. Grossmann , and J. C. Hall 2005. Physiological and biochemical characterization of quinclorac and resistance in a false cleavers (Galium spurium) biotype. J. Agric. Food Chem. 53:11441151.

M. J. VanGessel 2001. Glyphosate resistant horseweed from Delaware. Weed Sci. 49:703705.

M. M. Vila-Aiub , P. Neve , and S. B. Powles 2009. Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol. 184:751767.

M. J. Walsh , N. Maguire , and S. B. Powles 2009. Combined effects of wheat competition and 2,4-D amine on phenoxy herbicide resistant Raphanus raphanistrum populations. Weed Res. 49:316325.

T. A. Walsh , R. Neal , A. O. Merlo , M. Honma , G. R. Hicks , K. Wolff , W. Matsumura , and J. P. Davies 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. 142:542552.

S. R. Webb and J. C. Hall 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. 52:137148.

Y. D. Wei , H. G. Zheng , and J. C. Hall 2000. Role of auxinic herbicide-induced ethylene on hypocotyl elongation and root/hypocotyl radial expansion. Pest Manag. Sci. 56:377387.

T. Weinberg , G. R. Stephenson , M. D. McLean , and J. C. Hall 2006. MCPA (4-chloro-2-ethylphenoxyacetate) resistance in hemp-nettle (Galeopsis tetrahit L.). J. Agric. Food Chem. 54:91269134.

Q. Zhang and D. E. Riechers 2008. Proteomics: an emerging technology for weed science research. Weed Sci. 56:306313.

H. G. Zheng and J. C. Hall 2001. Understanding auxinic herbicide resistance in Sinapis arvensis L.: physiological, biochemical and molecular genetic approaches. Weed Sci. 49:276281.

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