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Understanding auxinic herbicide resistance in wild mustard: physiological, biochemical, and molecular genetic approaches

Published online by Cambridge University Press:  20 January 2017

Hong-gang Zheng
Affiliation:
Department of Environmental Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada

Abstract

The incidence of auxinic herbicide resistance in plants has increased worldwide. Auxinic herbicides were the first selective organic herbicides developed and have been used in agriculture for over 50 yr, primarily for the selective control of broadleaf weeds in cereal crops. However, the mode of action of auxinic herbicides and the molecular basis of auxinic herbicide resistance remain unknown, although an auxin-binding protein (ABP) is proposed to be the primary target site. Using auxinic herbicide-resistant (R) and -susceptible (S) biotypes of wild mustard as a model system, we have extensively studied the mode of action of auxinic herbicides and the resistance mechanisms at the physiological, biochemical, and molecular genetic levels. There are no differences in uptake, transport, and metabolism of auxinic herbicides between the R and S biotypes. Based on these results, as well as the studies on the role of auxin-enhanced ethylene biosynthesis and calcium in mediating the auxinic herbicide resistance, we hypothesize that resistance of the R biotype to auxinic herbicides is due to an altered target site, possibly an auxin receptor. We have identified and characterized a small ABP gene family as well as their cDNAs from both R and S of wild mustard. Amino acid changes were found in the ABP of the R biotype. Functional and mutational analyses of these genes are underway to determine the role of ABP in mediating auxinic herbicide resistance. In this review, we focus on the mode of action of auxinic herbicides and the molecular basis of auxinic herbicide resistance in wild mustard.

Type
Symposium
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Anai, T., Takai, R., Miyata, M., Uchida, H., Kosemura, S., Yamamura, S., Ishizaki, R., and Hasegawa, K. 1997. Isolation and characterization of an auxin-binding protein gene from radish, and its expression in insect cells. Physiol. Plant. 101:606611.Google Scholar
Barbier-Brygoo, H., Ephritikhine, G., Klämbt, D., Ghislain, M., and Guern, J. 1989. Functional evidence for an auxin receptor at the plasmalemma of tobacco mesophyll protoplasts. Proc. Natl. Acad. Sci. USA 86:891895.Google Scholar
Bourdot, G. W., Harrington, K. C., and Popay, A. I. 1989. The appearance of phenoxy-herbicide resistance in New Zealand pasture weeds. Proc. Br. Crop Prot. Conf. Weeds 1:309316.Google Scholar
Bourdot, G. W., Hurrell, G. A., and Saville, D. J. 1990. Variation in MCPA-resistance in Ranunculus acris L. subsp. acris and its correlation with historical exposure to MCPA. Weed Res. 30:449457.Google Scholar
Callihan, R. H., Prather, T. S., and Northam, F. E. 1989. Invasion by yellow starthistle. Proc. Knapweed Symp. 45:7378.Google Scholar
Chen, R., Hilson, P., Sedbrook, J., Rosen, E., Caspar, T., and Masson, P. H. 1998. The Arabidopsis thaliana AGRAVITROPIC1 gene encodes a component of the polar-auxin-transport efflux carrier. Proc. Natl. Acad. Sci. USA 95:1511215117.Google Scholar
Choi, S.-Y. 1996. Molecular cloning and expression of the hot pepper ERabp1 gene encoding auxin-binding protein. Plant Mol. Biol. 32:995997.Google Scholar
Darmency, H. 1994. Genetics of herbicide resistance in weeds and crops. Pages 263297 In Powles, S. and Holtum, J., eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: Lewis.Google Scholar
del Pozo, J. C., Timpte, C., Tan, S., Callis, J., and Estelle, M. 1998. The ubiquitin-related protein RUB1 and auxin response in Arabidopsis . Science 280:17601763.Google Scholar
Deshpande, S. and Hall, J. C. 1995. Comparison of flash-induced lightscattering transients and proton efflux from auxinic-herbicide resistant and susceptible wild mustard protoplasts: a possible role for calcium in mediating auxinic herbicide resistance. Biochem. Biophys. Acta 1244:6978.Google Scholar
Deshpande, S. and Hall, J. C. 1996. ATP-dependent auxin- and auxinic herbicide-induced volume changes in isolated protoplast suspensions from Sinapis arvensis L. Pestic. Biochem. Physiol. 56:2643.Google Scholar
Deshpande, S. and Hall, J. C. 2000. Auxinic herbicide resistance may be modulated at the auxin-binding site in wild mustard (Sinapis arvensis L.): a light scattering study. Pestic. Biochem. Physiol. 66:4148.Google Scholar
Devine, M. D., Duke, S. O., and Fedtke, C. 1993. Physiology of Herbicide Action. Englewood Cliffs, NJ: Prentice Hall. pp. 295309.Google Scholar
Estelle, M. A. and Somerville, C. 1987. Auxin-resistant mutants of Arabidopsis thaliana with an altered morphology. Mol. Gen. Genet. 206:200206.Google Scholar
Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A., and Palme, K. 1998. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282:22262230.CrossRefGoogle ScholarPubMed
Goldsmith, M.H.M. 1993. Cellular signaling: new insights into the action of the plant growth hormone auxin. Proc. Natl. Acad. Sci. USA 90:1144211445.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. 47:3643.Google Scholar
Hall, J. C. and Romano, M. L. 1995. Morophological and physiological differences between the auxinic herbicide-susceptible (S) and -resistant (R) wild mustard (Sinapis arvensis L.) biotypes. Pestic. Biochem. Physiol. 52:149155.Google Scholar
Hall, J. C., Webb, S. R., and Deshpande, S. 1996. An overview of auxinic herbicide resistance: wild mustard (Sinapis arvensis L.) as a case study. Pages 2843 In Brown, T. M., ed. Molecular Genetics and Evolution of Pesticide Resistance. Washington, DC: American Chemical Society.Google Scholar
Heap, I. M. 1997. The occurence of herbicide-resistant weeds worldwide. Pestic. Sci. 51:235243.3.0.CO;2-N>CrossRefGoogle Scholar
Heap, I. M. 2000. International Survey of Herbicide Resistant Weeds. Online at www.weedscience.com. Accessed March 23, 2000.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. Weed Sci. Soc. Am. Abstr. 32:164.Google Scholar
Hesse, T., Feldwisch, J., Balshüsemann, D., et al. 1989. Molecular cloning and structural analysis of a gene from Zea mays (L) coding for a putative receptor for the plant hormone auxin. Eur. Mol. Biol. Org. J. 8:24532461.Google Scholar
Hobbie, L., McGovern, M., Hurwitz, L. R., Pierro, A., Liu, N. Y., Bandyopadhyay, A., and Estelle, M. A. 2000. The axr6 mutants of Arabidopsis thaliana define a gene involved in auxin response and early development. Development 127:2332.Google Scholar
Holt, J. S. and LeBaron, H. M. 1990. Significance and distribution of herbicide resistance. Weed Technol. 4:141149.Google Scholar
Inohara, N., Shimomura, S., Fukui, T., and Futai, M. 1989. Auxin-binding protein located in the endoplasmic reticulum of maize shoots: molecular cloning and complete primary structure. Proc. Natl. Acad. Sci. USA 86:35643568.Google Scholar
Jasieniuk, M., Morrison, I. N., and Brûlé-Babel, A. L. 1995. Inheritance of dicamba resistance in wild mustard (Brassica kaber). Weed Sci. 43:192195.Google Scholar
Jones, A. M. 1994. Auxin-binding proteins. Annu. Rev. Plant Physiol. Plant Mol. Biol. 45:393420.Google Scholar
Jones, A. M. and Herman, E. 1993. KDEL-containing auxin-binding protein is secreted to the plasma membrane and cell wall. Plant Physiol. 101:595606.Google Scholar
Jones, A. M., Im, K.-H., Savka, M. A., Wu, M.-J., DeWitt, N. G., Shillito, R., and Binns, A. N. 1998. Auxin-dependent cell expansion mediated by overexpressed auxin-binding protein 1. Science 282:11141117.Google Scholar
Kovtun, Y., Chiu, W. L., Zeng, W., and Sheen, J. 1998. Suppression of auxin signal transduction by a MAPK cascade in higher plants. Nature 395:716720.Google Scholar
Lazarus, C. M. and Macdonald, H. 1996. Characterization of a strawberry gene for auxin-binding protein, and its expression in insect cells. Plant Mol. Biol. 31:267277.Google Scholar
LeBaron, H. M. 1991. Distribution and seriousness of herbicide-resistant weed infestations worldwide, Pages 2743 In Caseley, J. C., Cussans, G. W., and Atkins, R. K., eds. Herbicide Resistance in Weeds and Crops. Oxford, UK: Butterworth-Heinemann.Google Scholar
Leblanc, N., Roux, C., Pradier, J.-M., and Perrot-Rechenmann, C. 1997. Characterization of two cDNAs encoding auxin-binding proteins in Nicotiana tabacum . Plant Mol. Biol. 33:697–689.CrossRefGoogle ScholarPubMed
Leyser, H.M.O. 1998. Auxin signaling: protein stability as a versatile control target. Curr. Biol. 8:R305R307.Google Scholar
Leyser, H.M.O., Lincoln, C., Timpte, C. A., Lammer, D., Turner, J., and Estelle, M. 1993. Arabidopsis auxin-resistance gene AXR1 encodes a protein related to ubiquitin-activating enzyme E1. Nature 364:161164.Google Scholar
Luschnig, C., Gaxiola, R. A., Grisafi, P., and Fink, G. R. 1998. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana . Genes Dev. 12:21752187.Google Scholar
Lutman, P.J.W. and Lovegrove, A. W. 1985. Variations in the tolerance of Galium aparine (cleavers) and Stellaria media (chickweed) to mecoprop. Proc. Br. Crop Prot. Conf. Weeds. 1:411418.Google Scholar
Lutman, P.J.W. and Snow, H. S. 1987. Further investigations into the resistance of chickweed (Stellaria media) to mecoprop. Proc. Br. Crop Prot. Conf. Weeds. 3:901908.Google Scholar
Marchant, A., Kargul, J., May, S. T., Muller, P., Delbarre, A., Perrot-Rechenmann, C., and Bennett, M. J. 1999. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 18:20662073.Google Scholar
Migo, T. R., Mercado, B. L., and De Datta, S. K. 1986. Response of Sphenoclea zeylanica to 2,4-D and other recommended herbicides for weed control in lowland rice. Philipp. J. Weed Sci. 13:2838.Google Scholar
Müller, A., Guan, C., Gälweiler, L., Huijser, P., Marchant, A., Parry, G., Bennett, M. J., Wisman, E., and Palme, K. 1998. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17:69036911.Google Scholar
Mulligan, R. M., Chory, J., and Ecker, J. R. 1997. Signaling in plants. Proc. Natl. Acad. Sci. USA 94:27932795.Google Scholar
Palme, K., Hesse, T., Campos, N., Garbers, C., Yanofsky, M. F., and Schell, J. 1992. Molecular analysis of an auxin binding protein gene located on chromosome 4 of Arabidopsis . Plant Cell 4:193201.Google ScholarPubMed
Peniuk, M. G., Romano, M. L., and Hall, J. C. 1993. Physiological investigations into the resistance of a wild mustard (Sinapis arvensis L.) biotype to auxinic herbicide. Weed Res. 33:431440.Google Scholar
Pozo, J. C., Timpte, C., Tan, S., Callis, J., and Estelle, M. 1998. The ubiquitin-related protein RUB1 and auxin response in Arabidopsis . Science 280:17601763.Google Scholar
Rouse, D., Mackay, P., Stirnberg, P., Estelle, M., and Leyser, O. 1998. Changes in auxin response from mutations in an AUX/IAA gene. Science 279:13711373.Google Scholar
Sterling, T. M. and Hall, J. C. 1997. Mechanism of action of natural auxins and the auxinic herbicides. Pages 111141 In Roe, R. M., Burton, J. D., and Kuhr, R. J., eds. Herbicide Activity: Toxicology, Biochemistry and Molecular Biology. Amsterdam: IOS Press.Google Scholar
Thiel, G., Blatt, M. R., Fricker, M. D., White, I. R., and Millner, P. 1993. Modulation of K+ channels in Vicia stomatal guard cells by peptide homologs to the auxin-binding protein C-terminus. Proc. Natl. Acad. Sci. USA 90:1149311497.CrossRefGoogle Scholar
Venis, M. A. and Napier, R. M. 1995. Auxin receptors and auxin binding proteins. Crit. Rev. Plant Sci. 14:2747.Google Scholar
Wang, Y., Deshpande, S., and Hall, J. C. 2001. Calcium may mediate auxinic herbicide resistance in wild mustard. Weed Sci. 49:27.Google Scholar
Watanabe, S. and Shimomura, S. 1998. Cloning and expression of two genes encoding auxin-binding proteins from tobacco. Plant Mol. Biol. 36:6374.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. 52:137148.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. 56:377387.Google Scholar
Went, T. W. 1928. Wuchstoff and Wachstum. Rec. Trav. Bot. Neerl. 29:379396.Google Scholar
Yang, S. F. and Hoffman, N. E. 1984. Ethylene biosynthesis and its regulation in higher plants. Annu. Rev. Plant Physiol. 35:155189.Google Scholar
Yang, T. and Poovaiah, B. W. 2000. Molecular and biochemical evidence for the involvement of calcium/calmodulin in auxin action. J. Biol. Chem. 275:31373143.Google Scholar