Hostname: page-component-84b7d79bbc-2l2gl Total loading time: 0 Render date: 2024-07-26T10:13:35.148Z Has data issue: false hasContentIssue false

Role of Translocation as A Mechanism of Resistance to Glyphosate

Published online by Cambridge University Press:  20 January 2017

Dale L. Shaner*
Affiliation:
U.S. Department of Agriculture–Agricultural Research Service, Water Management Research Unit, 2150 Centre Avenue, Building D, Suite 320, Fort Collins, CO 80526
*
Corresponding author's E-mail: dale.shaner@ars.usda.gov

Abstract

The continuous use of glyphosate has resulted in the selection of glyphosate-resistant (GR) biotypes in 13 weed species. Decreased translocation of glyphosate to the meristematic tissue is the primary mechanism of resistance in horseweed, hairy fleabane, rigid ryegrass, and Italian ryegrass, and the resistance is inherited as a single, semidominant nuclear trait. The question is: What role does decreased translocation play in glyphosate resistance, and what is the actual mechanism(s)? The enzyme 5-enol-pyruvylshikimate-3-phosphate synthase (EPSPS), the target site of glyphosate, preferentially accumulates in the active meristems of plants. Inhibition of EPSPS results in the accumulation of shikimate. Leaf disc assays across a number of species show that the maximum accumulation of shikimate occurs in young, rapidly expanding tissue. Gene expression studies have also shown that the gene encoding EPSPS is maximally expressed in meristems. Thus, glyphosate needs to translocate to the growing points of plants to be effective. In some GR weed biotypes, glyphosate moves in the treated leaf via the transpiration stream; but instead of being loaded into the phloem, it is trapped in the distal portion of the leaf. These results suggest that there is some type of inhibition of glyphosate-loading into the phloem in GR plants. However, this mechanism may involve uptake of glyphosate at the cellular level. Shikimate accumulation in isolated leaf discs occurs at high glyphosate concentrations in both susceptible and GR biotypes of horseweed and Italian ryegrass; but at low concentrations, shikimate accumulation occurs only in susceptible biotypes. Decreased cellular uptake of glyphosate might occur by one of four mechanisms: (1) the active uptake system no longer recognizes glyphosate, (2) an active efflux system pumps glyphosate out of the cell into the apoplast, (3) an active efflux system pumps glyphosate out of the chloroplast into the cytoplasm, or (4) glyphosate is pumped into the vacuole and sequestered in the cell.

Type
Special Topics
Copyright
Copyright © Weed Science Society of America 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Literature Cited

Amrhein, N., Deus, B., Gehrke, P., and Steinrucken, H. C. 1980. The site of inhibition of the shikimate pathway by glyphosate, II: interference of glyphosate with chorismate formation in vivo and in vitro. Plant Physiol. 66:830834.CrossRefGoogle ScholarPubMed
Bradshaw, L. D., Padgette, S. R., Kimball, S. L., and Wells, B. H. 1997. Perspectives on glyphosate resistance. Weed Technol. 11:189198.Google Scholar
Bromilow, R. H. and Chamberlain, K. 2000. The herbicide glyphosate and related molecules: physicochemical and structural factors determining their mobility in phloem. Pest Manag. Sci. 56:368373.Google Scholar
Christy, A. L. and Ferrier, J. M. 1973. A mathematical treatment of Munch's pressure flow hypothesis of phloem translocation. Plant Physiol. 52:531538.Google Scholar
Culpepper, A. S., 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. 54:620626.Google Scholar
Daram, P., Brunner, S., Persson, B. L., Amrhein, N., and Bucher, M. 1999. Pht2;1 encodes a low affinity phosphate transporter from Arabidopsis . Plant Cell. 11:21532166.CrossRefGoogle ScholarPubMed
Denis, M-H. and Delrot, S. 1993. Carrier-mediated uptake of glyphosate in broad bean (Vicia faba) via a phosphate transporter. Physiol. Plant. 87:569575.Google Scholar
Dinelli, G., Marotti, I., Catizone, P., Bonetti, A., Urbano, J. M., and Barnes, J. 2008. Physiological and molecular basis of glyphosate resistance in C. bonariensis (L.) Cronq. biotypes from Spain. Weed Res. 48:257265.CrossRefGoogle Scholar
Feng, P. C. C., Chiu, T., and Sammons, R. D. 2003. Glyphosate efficacy is contributed by its tissue concentration and sensitivity in velvetleaf (Abutilon theophrasti). Pestic. Biochem. Physiol. 77:8391.CrossRefGoogle Scholar
Feng, P. C., Tran, M., Chiu, T., Sammons, R. D., Heck, G. R., and CaJacob, C. A. 2004. Investigation into GR horseweed (Conyza canadensis): retention, uptake, translocation and metabolism. Weed Sci. 52:498505.CrossRefGoogle Scholar
Fuerst, E. P. and Vaughn, K. C. 1990. Mechanisms of paraquat resistance. Weed Technol. 4:150156.Google Scholar
Geiger, D. R., Shieh, W-J., and Fuchs, M. A. 1999. Causes of self-limited translocation of glyphosate in Beta vulgaris plants. Pestic. Biochem. Physiol. 64:124133.CrossRefGoogle Scholar
Gianessi, L. P. 2004. Economic and herbicide use impacts of GR crops. Pest Manag. Sci. 61:241245.CrossRefGoogle Scholar
Gougler, J. A. and Geiger, D. R. 1981. Uptake and distribution of N-phosphonomethylglycine in sugar beet plants. Plant Physiol. 68:668672.Google Scholar
Gout, E., Bligny, R., Genix, P., Tissut, M., and Dounce, R. Effect of glyphosate on plant cell metabolism: 31P and 13C NMR studies. Biochimie. 74:875882.Google Scholar
Heap, I. 2008. The International Survey of Herbicide Resistant Weeds. http://www.weedscience.com Accessed: February 21, 2008.Google Scholar
Henton, S. M., Greaves, A. J., Piller, G. J., and Minchin, P. E. H. 2002. Revisiting the Munch pressure-flow hypothesis for long-distance transport of carbohydrates: modeling the dynamics of solute transport inside a semipermeable tube. J. Exp. Bot. 53:14111419.Google ScholarPubMed
Hetherington, P. R., Marshall, G., Kirkwood, R. C., and Warner, J. M. 1998. Absorption and efflux of glyphosate by cell suspensions. J. Exp. Bot. 49:527533.Google Scholar
Ibaoui, H., Delrot, E. S., Besson, J., and Bonnemain, J-L. 1986. Uptake and release of phloem-mobile (glyphosate) and of non-phloem-mobile (iprodione) xenobiotic by broadbean leaf tissues. Physiol. Veg. 24:431442.Google Scholar
Jasieniuk, M. 1995. Constraints on the evolution of glyphosate resistance in weeds. Resistant Pest Manag. 3132.Google Scholar
Koger, C. H. and Reddy, K. N. 2005. Role of absorption and translocation in the mechanism of glyphosate resistance in horseweed (Conyza canadensis). Weed Sci. 53:8489.Google Scholar
Koger, C. H., Shaner, D. L., Henry, W. B., Nadler-Hassar, T., Thomas, W. E. T., and Wilcut, J. W. 2005. Assessment of two nondestructive assays for detecting glyphosate resistance in horseweed (Conyza canadensis). Weed Sci. 53:438445.Google Scholar
Lalonde, S., Tegeder, M., Throne-Holst, M., Frommer, W. B., and Patrick, J. W. 2003. Phloem loading and unloading of sugars and amino acids. Plant Cell Environ. 26:3759.Google Scholar
McAllister, R. S. and Haderlie, L. C. 1985. Translocation of 14C-glyphosate and 14CO2-labeled photoassimilates in Canada thistle (Cirsium arvense). Weed Sci. 33:153159.CrossRefGoogle Scholar
Mollenhauer, C., Smart, C. C., and Amrhein, N. 1987. Glyphosate toxicity in the shoot apical region of the tomato plant I. plastid swelling is the initial ultrastructural feature following in vivo inhibition of 5-enolpyruvylshikimic acid-3-phosphate synthase. Pestic. Biochem. Physiol. 29:5565.Google Scholar
Morin, F., Vera, V., Nurit, F., Tissut, M., and Marigo, G. 1997. Glyphosate uptake in Catharanthus roseus cells: Role of a phosphate transporter. Pestic. Biochem. Physiol. 58:1322.CrossRefGoogle Scholar
Nandula, V. K., Reddy, K. N., Poston, D. H., Rimando, A. M., and Duke, S. O. 2008. Glyphosate-tolerance mechanisms in Italian ryegrass (Lolium multiflorum) from Mississippi. Weed Sci. 56:344349.CrossRefGoogle Scholar
Padgette, S. R., Re, D. B., Barry, G. F., Eichholtz, D. E., Delannay, X., Fuchs, R. L., Kishore, G. M., and Fraley, R. T. 1996. New weed control opportunities: development of soybeans with a Roundup Ready gene. Pages 5384. in Duke, S. O. Herbicide Resistant Crops: Agricultural, Environmental, Economic, Regulatory, and Technical Aspects. Boca Raton, FL CRC Lewis Publishers.Google Scholar
Pedersen, B. P., Neve, P., Andreasen, C., and Powles, S. B. 2007. Ecological fitness of a glyphosate resistant Lolium rigidum population: growth and seed production along a competition gradient. Basic Appl. Ecol. 8:258268.CrossRefGoogle Scholar
Perez, A., Alister, C., and Kogan, M. 2004. Absorption, translocation and allocation of glyphosate in resistant and susceptible Chilean biotypes of Lolium multiflorum . Weed Biol. Manag. 4:5658.Google Scholar
Perez-Jones, A., Park, K. W., Colquhoun, J., Mallory-Smith, C., and Shaner, D. L. 2005. Identification of glyphosate-resistant Italian ryegrass (Lolium multiflorum) in Oregon. Weed Science. 53:775779.CrossRefGoogle Scholar
Perez-Jones, A., Park, K-W., Polge, N., Colquhoun, J., and Mallory-Smith, C. A. 2007. Investigating the mechanisms of glyphosate resistance in Lolium multiflorum . Planta. 226:395404.CrossRefGoogle ScholarPubMed
Powles, S. B. and Preston, C. 2006. Evolved glyphosate resistance in plants: biochemical and genetic basis of resistance. Weed Technol. 20:282289.CrossRefGoogle Scholar
Rae, A. L., Cybinski, D. H., Jarney, J. M., and Smith, F. W. 2003. Characterization of two phosphate transporters from barley; evidence for diverse function and kinetic properties among members of the Pht1. Plant Mol. Biol. 53:2736.CrossRefGoogle ScholarPubMed
Rausch, C. and Bucher, M. 2002. Molecular mechanisms of phosphate transport in plants. Planta. 216:2337.CrossRefGoogle ScholarPubMed
Rausch, C., Zimmermann, P., Amrhein, N., and Bucher, M. 2004. Expression analysis suggests novel roles for the plastidic phosphate transporter Pht2;1 in auto- and heterotrophic tissues in potato and Arabidopsis . Plant J. 39:1328.CrossRefGoogle ScholarPubMed
Schulz, A., Munder, T., Hollander-Czytko, H., and Amrhein, N. 1990. Glyphosate transport and early effects on shikimate metabolism and its compartmentation in sink leaves of tomato and spinach plants. Z. Naturforsch. 45c:529534.Google Scholar
Shaner, D. L., Nadler-Hassar, T., Henry, W. B., and Koger, C. H. 2005. A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci. 53:769774.CrossRefGoogle Scholar
Simarmata, M., Kaufmann, J. E., and Penner, D. 2003. Potential basis of glyphosate resistance in California rigid ryegrass (Lolium rigidum). Weed Sci. 51:678682.Google Scholar
Simarmata, M. and Penner, D. 2008. The basis for glyphosate resistance in rigid ryegrass (Lolium rigidum) from California. Weed Sci. 56:181188.CrossRefGoogle Scholar
van Bel, A. J. E., Gamalei, Y. V., Ammerlaan, A., and Bik, L. P. M. 1992. Dissimilar phloem loading in leaves with symplasmic or apoplasmic minor-vein configurations. Planta. 186:518525.Google Scholar
Vaughn, K. C. and Duke, S. O. 1986. Ultrastructural effects of glyphosate on Glycine max seedling. Pestic. Biochem. Physiol. 26:5665.CrossRefGoogle Scholar
Wakelin, A. M. and Preston, C. 2006. Inheritance of glyphosate resistance in several populations of rigid ryegrass (Lolium rigidum) from Australia. Weed Sci. 54:212219.CrossRefGoogle Scholar
Wakelin, A. M., Lorraine-Colwill, D. F., and Preston, C. 2004. Glyphosate resistance in four different populations of Lolium rigidum as associated with reduced translocation of glyphosate to meristematic zones. Weed Res. 44:453459.CrossRefGoogle Scholar
Weaver, L. M. and Hermann, K. M. 1997. Dynamics of the shikimate pathway in plants. Trends Plant Sci. 2:346351.Google Scholar
Yu, Q., Cairns, A., and Powles, S. 2007. Glyphosate, paraquat and ACCase multiple herbicide resistance in a Lolium rigidum biotype. Planta. 225:499513.Google Scholar
Yuan, J. S., Tranel, P. J., and Stewart, C. N. Jr. 2007. Non-target-site herbicide resistance: a family business. Trends Plant Sci. 12:613.Google Scholar
Zelaya, I. A., Owen, M. D. K., and VanGessel, M. J. 2004. Inheritance of evolved glyphosate resistance in Conyza canadensis (L.) Cronq. Theor. Appl. Genet. 110:5870.CrossRefGoogle ScholarPubMed