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Functional Genomics Analysis of Horseweed (Conyza canadensis) with Special Reference to the Evolution of Non–Target-Site Glyphosate Resistance

Published online by Cambridge University Press:  20 January 2017

Joshua S. Yuan ,
Laura L. G. Abercrombie ,
Yongwei Cao ,
Matthew D. Halfhill ,
Xin Zhou ,
Yanhui Peng ,
Jun Hu ,
Murali R. Rao ,
Gregory R. Heck  and
Thomas J. Larosa
...Show all authors
Joshua S. Yuan
Affiliation:
Department of Plant Pathology and Microbiology, Institute of Plant Genomics and Microbiology, Texas A&M University, College Station, TX 77843
Laura L. G. Abercrombie
Affiliation:
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996
Yongwei Cao
Affiliation:
Monsanto Company, Saint Louis, MO 63167
Matthew D. Halfhill
Affiliation:
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996 Department of Biology, St. Ambrose University, Davenport, IA 52803
Xin Zhou
Affiliation:
Department of Plant Pathology and Microbiology, Institute of Plant Genomics and Microbiology, Texas A&M University, College Station, TX 77843
Yanhui Peng
Affiliation:
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996
Jun Hu
Affiliation:
Department of Plant Pathology and Microbiology, Institute of Plant Genomics and Microbiology, Texas A&M University, College Station, TX 77843 Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996
Murali R. Rao
Affiliation:
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996
Gregory R. Heck
Affiliation:
Monsanto Company, Saint Louis, MO 63167
Thomas J. Larosa
Affiliation:
Monsanto Company, Saint Louis, MO 63167
R. Douglas Sammons
Affiliation:
Monsanto Company, Saint Louis, MO 63167
Xinwang Wang
Affiliation:
Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN 37996
Priya Ranjan
Affiliation:
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996 Environmental Science Division, Oak Ridge National Laboratory, Oak Ridge, TN
Denita H. Johnson
Affiliation:
Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN 37996
Phillip A. Wadl
Affiliation:
Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN 37996
Brian E. Scheffler
Affiliation:
U.S. Department of Agriculture–Agricultural Research Service–Gemonics and Bioinformatics Research Unit; Mid-South Area, Genomics Laboratory, 141 Experiment Station Rd., Stoneville, MS 38776
Timothy A. Rinehart
Affiliation:
U.S. Department of Agriculture–Agricultural Research Service Southern Horticultural Laboratory, 810 Highway 26 West, Poplarville, MS 39470
Robert N. Trigiano
Affiliation:
Department of Entomology and Plant Pathology, University of Tennessee, Knoxville, TN 37996
C. Neal Stewart Jr.*
Affiliation:
Department of Plant Sciences, University of Tennessee, Knoxville, TN 37996
*
Corresponding author's E-mail: [email protected]
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Abstract

The evolution of glyphosate resistance in weedy species places an environmentally benign herbicide in peril. The first report of a dicot plant with evolved glyphosate resistance was horseweed, which occurred in 2001. Since then, several species have evolved glyphosate resistance and genomic information about nontarget resistance mechanisms in any of them ranges from none to little. Here, we report a study combining iGentifier transcriptome analysis, cDNA sequencing, and a heterologous microarray analysis to explore potential molecular and transcriptomic mechanisms of nontarget glyphosate resistance of horseweed. The results indicate that similar molecular mechanisms might exist for nontarget herbicide resistance across multiple resistant plants from different locations, even though resistance among these resistant plants likely evolved independently and available evidence suggests resistance has evolved at least four separate times. In addition, both the microarray and sequence analyses identified non–target-site resistance candidate genes for follow-on functional genomics analysis.

Keywords

Glyphosatehorseweed, Conyza canadensis (L.) Cronq. ERICABioinformaticsherbicide resistancephylogeographysystems biologytranscriptomics
Type
Research Article
Information
Weed Science , Volume 58 , Issue 2 , June 2010 , pp. 109 - 117
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Abercrombie, L. G., Anderson, C. M., Baldwin, B. G., et al. 2009. Permanent genetic resources added to Molecular Ecology Resources database 1 January 2009–30 April 2009. Mol. Ecol. Resourc. 9:1375–1379.Google Scholar
Ahmadian, A., Ehn, M., and Hober, S. 2006. Pyrosequencing: history, biochemistry and future. Clin. Chim. Acta. 363:83–94.Google Scholar
Basu, C., Halfhill, M. D., Mueller, T. C., and Stewart, C. N. Jr. 2004. Weed genomics: new tools to understand weed biology. Trends Plant Sci. 9:391–398.CrossRefGoogle ScholarPubMed
Baucom, R. S. and Mauricio, R. 2008. Constraints on the evolution of tolerance to herbicide in the common morning glory: resistance and tolerance are mutually exclusive. Evolution. 62:2842–2854.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.CrossRefGoogle Scholar
Dauer, J. T., Mortensen, D. A., and VanGessel, M. J. 2007. Temporal and spatial dynamics of long-distance Conyza canadensis seed dispersal. J. Appl. Ecol. 44:105–114.Google Scholar
Dill, G. M. 2005. Glyphosate-resistant crops: history, status and future. Pest Manag. Sci. 61:219–224.CrossRefGoogle ScholarPubMed
Dill, G. M., Cajacob, C. A., and Padgette, S. R. 2008. Glyphosate-resistant crops: adoption, use and future considerations. Pest Manag. Sci. 64:326–331.Google Scholar
Duke, S. O. and Powles, S. B. 2008a. Glyphosate-resistant weeds and crops. Pest Manag. Sci. 64:317–318.Google Scholar
Duke, S. O. and Powles, S. B. 2008b. Glyphosate: a once-in-a-century herbicide. Pest Manag. Sci. 64:319–325.Google Scholar
Feng, P. C. C. and Chiu, T. 2005. Distribution of C14 glyphosate in mature glyphosate-resistant cotton from application to a single leaf or over-the-top spray. Pestic. Biochem. Physiol. 82:36–45.Google Scholar
Feng, P. C. C., Chiu, T., and Sammons, R. D. 2003a. Glyphosate efficacy is contributed by its tissue concentration and sensitivity in velvetleaf (Abutilon theophrasti). Pestic. Biochem. Physiol. 77:83–91.CrossRefGoogle Scholar
Feng, P. C. C., Chiu, T., Sammons, R. D., and Ryerse, J. S. 2003b. Droplet size affects glyphosate retention, absorption, and translocation in corn. Weed Sci. 51:443–448.CrossRefGoogle Scholar
Feng, P. C. C., Pratley, J. E., and Bohn, J. A. 1999. Resistance to glyphosate in Lolium rigidum. II. Uptake, translocation, and metabolism. Weed Sci. 47:412–415.Google Scholar
Feng, P. C. C., Sandbrink, J. J., and Sammons, R. D. 2000. Retention, uptake, and translocation of C14-glyphosate from track-spray applications and correlation to rainfastness in velvetleaf (Abutilon theophrasti). Weed Technol. 14:127–132.Google Scholar
Feng, P. C. C., Tran, M., Chiu, T., Sammons, R. D., Heck, G. R., and Cajacob, C. A. 2004. Investigations into glyphosate-resistant horseweed (Conyza canadensis): retention, uptake, translocation, and metabolism. Weed Sci. 52:498–505.CrossRefGoogle Scholar
Fischer, A., Lenhard, A., Tronecker, H., et al. 2007. iGentifier: indexing and large-scale profiling of unknown transcriptomes. Nucleic Acids Res. 35:4640–4648.Google Scholar
Funke, T., Yang, Y., Han, H., Healy-Fried, M., Olesen, S., Becker, A., and Schonbrunn, E. 2009. Structural basis of glyphosate resistance resulting from the double mutation Thr97 → Ile and Pro101 → Ser in 5-enolpyruvylshikimate-3-phosphate synthase from Escherichia coli . J. Biol. Chem. 284:9854–9860.Google Scholar
Goudet, J. 1995. FSTAT (Version 1.2): a computer program to calculate F-statistics. J. Heredity. 86:485–486.Google Scholar
Gressel, J. 2009. Crops with target-site herbicide resistance for Orobanche and Striga control. Pest Manag. Sci. 65:560–565.CrossRefGoogle ScholarPubMed
Gressel, J. and Valverde, B. E. 2009. A strategy to provide long-term control of weedy rice while mitigating herbicide resistance transgene flow, and its potential use for other crops with related weeds. Pest Manag. Sci. 65:723–731.Google Scholar
Halfhill, M. D., Good, L. L., Basu, C., Burris, J., Main, C. L., Mueller, T. C., and Stewart, C. N. Jr. 2007. Transformation and segregation of GFP fluorescence and glyphosate resistance in horseweed (Conyza canadensis) hybrids. Plant Cell Reports. 26:303–311.CrossRefGoogle ScholarPubMed
Heap, I. 2010. International Survery of Herbicide Resistant Weeds. www.weedscience.org. Accessed: February 15, 2010.Google Scholar
Hong, F. X., Breitling, R., McEntee, C. W., Wittner, B. S., Nemhauser, J. L., and Chory, J. 2006. RankProd: a bioconductor package for detecting differentially expressed genes in meta-analysis. Bioinformatics. 22:2825–2827.Google Scholar
Hu, J., Tranel, P. J., Stewart, C. N. Jr., and Yuan, J. S. 2009. Molecular and genomic mechanisms of non-target site herbicide resistance. Pages 149–161. In Stewart, C. N. Jr. Genomics of Weedy and Invasive Plants. Ames, IA Blackwell Scientific.Google Scholar
Ito, K., Oleschuk, C. J., Westlake, C., Vasa, M. Z., Deeley, R. G., and Cole, S. P. C. 2001. Mutation of Trp1254 in the multispecific organic anion transporter, multidrug resistance protein 2 (MRP2) (ABCC2), alters substrate specificity and results in loss of methotrexate transport activity. J. Biol. Chem. 276:38,101–38,114.CrossRefGoogle ScholarPubMed
Kang, B-G., Ye, X., Osburn, L. D., Stewart, C. N. Jr., and Cheng, Z-M. 2010. Transgenic hybrid aspen overexpressing the Atwbc19 gene encoding an ATP binding cassette transporter confers resistance to four aminoglycoside antibiotics. Plant Cell Rep. In press.Google Scholar
Klein, M., Burla, B., and Martinoia, E. 2006. The multidrug resistance-associated protein (MRP/ABCC) subfamily of ATP-binding cassette transporters in plants. FEBS Lett. 580:1112–1122.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. 53:84–89.Google Scholar
Langella, O. 2002. Populations, a Free Population Genetics Software. https://launchpad.net/∼olivier-langella/+archive/ppa. Accessed: September 14, 2009.Google Scholar
Lee, H. S., Wang, J., Tian, L., et al. 2004. Sensitivity of 70-Mer oligonucleotides and cDNAs for microarray analysis of gene expression in Arabidopsis and its related species. Plant Biotechnol. J. 2:45–57.Google Scholar
Linton, K. J. and Higgins, C. F. 2007. Structure and function of ABC transporters: the ATP switch provides flexible control. Pflügers Arch. Eur. J. Physiol. 453:555–567.Google Scholar
Liu, G., Sanchez-Fernandez, R., Li, Z. S., and Rea, P. A. 2001. Enhanced multispecificity of Arabidopsis vacuolar multidrug resistance-associated protein-type ATP-binding cassette transporter, AtMRP2. J. Biol. Chem. 276:8648–8656.CrossRefGoogle ScholarPubMed
Ma, J. F. and Yamaji, N. 2008. Functions and transport of silicon in plants. Cell. Mol. Life Sci. 65:3049–3057.CrossRefGoogle ScholarPubMed
Main, C. L., Mueller, T. C., Hayes, R. M., and Wilkerson, J. B. 2004. Response of selected horseweed (Conyza canadensis (L.) cronq.) populations to glyphosate. J. Agric. Food Chem. 52:879–883.Google Scholar
Mallory-Smith, C. and Zapiola, M. 2008. Gene flow from glyphosate resistant crops. Pest Manag. Sci. 64:428–440.CrossRefGoogle ScholarPubMed
Margulies, M., Egholm, M., Altman, W. E., et al. 2005. Genome sequencing in microfabricated high-density picolitre reactors. Nature. 437:376–380.Google Scholar
Maurel, C., Verdoucq, L., Luu, D. T., and Santoni, V. 2008. Plant aquaporins: membrane channels with multiple integrated functions. Ann. Rev. Plant Biol. 59:595–624.CrossRefGoogle ScholarPubMed
Mentewab, A. and Stewart, C. N. Jr. 2005. Overexpression of an Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nat. Biotechnol. 23:1177–1180.Google Scholar
Mueller, T. C., Massey, J. H., Hayes, R. M., Main, C. L., and Stewart, C. N. Jr. 2003. Shikimate accumulates in both glyphosate sensitive and glyphosate resistant horseweed (Conyza canadensis L. Cronq.). J. Agric. Food Chem. 51:680–684.CrossRefGoogle ScholarPubMed
Nei, M. 1972. Genetic distance between populations. Amer. Nat. 106:283.Google Scholar
Owen, M. D. and Zelaya, I. A. 2005. Herbicide resistant crops and weed resistance to herbicides. Pest Manag. Sci. 61:301–311.Google Scholar
Özvegy, C., Váradi, A., and Sarkadi, B. 2002. Characterization of drug transport, ATP hydrolysis, and nucleotide trapping by the human ABCG2 multidrug transporter modulation of subtrate specifically by a point of mutation. J. Biol. Chem. 277:47,980–47,990.Google Scholar
Page, R. D. 1996. TreeView: an application to display phylogenetic trees on personal computers. Comp. Appl. Biosci. 12:357–358.Google Scholar
Powles, S. B. 2008. Evolved glyphosate resistant weeds around the world: lessons to be learnt. Pest Manag. Sci. 64:360–365.Google Scholar
Preston, C. 2009. Herbicide resistance: target site mutations. Pages 127–148. In Stewart, C. N. Jr. Genomics of Weedy and Invasive Plants. Ames, IA Blackwell Scientific.Google Scholar
Preston, C. and Wakelin, A. M. 2008. Resistance to glyphosate from altered herbicide translocation patterns. Pest Manag. Sci. 64:372–376.Google Scholar
Rao, M. R., Halfhill, M. D., Abercrombie, L. G., Ranjan, P., Abercrombie, J. M., Gouffon, J. S., Saxton, A. M., and Stewart, C. N. Jr. 2009. Phytoremediation and phytosensing of chemical contaminants, RDX and TNT: identification of the required target genes. Funct. Integr. Genom. 9:537–547.Google Scholar
Ryerse, J. S., Downer, R. A., Sammons, R. D., and Feng, P. C. C. 2004. Effect of glyphosate spray droplets on leaf cytology in velvetleaf (Abutilon theophrasti). Weed Sci. 52:302–309.Google Scholar
Saitou, N. and Nei, M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4:406–425.Google Scholar
Sammons, R. D., Heering, D. C., Dinicola, N., Glick, H., and Elmore, G. A. 2007. Sustainability and stewardship of glyphosate and glyphosate-resistant crops. Weed Technol. 21:347–354.Google Scholar
Sanchez-Fernandez, R., Davies, T. G. E., Coleman, J. O. D., and Rea, P. A. 2001. The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J. Biol. Chem. 276:30,231–30,244.Google Scholar
Scheiber, P., Tran, M., and Duncan, D. 2006. Tissue culture and transient transformation of marestail (Conyza canadensis (L.) Cronquist). Plant Cell Rep. 25:507–512.Google Scholar
Schulz, B. and Kolukisaglu, H. U. 2006. Genomics of plant ABC transporters: the alphabet of photosynthetic life forms or just holes in membranes? FEBS Lett. 580:1010–1016.Google Scholar
Shaner, D. 2009. Role of translocation as a mechanism of resistance to glyphosate. Weed Sci. 57:118–123.Google Scholar
Shendure, J., Porreca, G. J., Reppas, N. B., et al. 2005. Accurate multiplex polony sequencing of an evolved bacterial genome. Science. 309:1728–1732.Google Scholar
Shields, E. J., Dauer, J. T., VanGessel, M. J., and Neuman, G. 2006. Horseweed (Conyza canadensis) seed collected in the planetary boundary layer. Weed Sci. 54:1063–1067.CrossRefGoogle Scholar
Smith, T. F., Gaitatzes, C., Saxena, K., and Neer, E. J. 1999. The WD repeat: a common architecture for diverse functions. Trends Biochem. Sci. 24:181–185.Google Scholar
Stewart, C. N. Jr. 2009. Weedy and Invasive Plant Genomics. Ames, IA Wiley-Blackwell. 253.Google Scholar
Stewart, C. N. Jr., Tranel, P. J., Horvath, D. P., Anderson, J. V., Rieseberg, L. H., Westwood, J. H., Mallory-Smith, C. A., Zapiola, M. L., and Dlugosch, K. M. 2009. Evolution of weediness and invasiveness: charting the course for weed genomics. Weed Sci. 57:451–462.Google Scholar
VanGessel, M. J. 2001. Glyphosate-resistant horseweed from Delaware. Weed Sci. 49:703–705.Google Scholar
Vila-Aiub, M. M., Vidal, R. A., Balbi, M. C., Gundel, P. E., Trucco, F., and Ghersa, C. M. 2008. Glyphosate-resistant weeds of South American cropping systems: an overview. Pest Manag. Sci. 64:366–371.Google Scholar
Wakelin, A. M. and Preston, C. 2006. A target-site mutation is present in a glyphosate-resistant Lolium rigidum population. Weed Res. 46:432–440.Google Scholar
Williams, G. M., Kroes, R., and Munro, I. C. 2000. Safety evaluation and risk assessment of the herbicide Roundup and its active ingredient, glyphosate, for humans. Regul. Toxicol. Pharmacol. 31:117–165.Google Scholar
Yuan, J. S., Galbraith, D. W., Dai, S. Y., Griffin, P., and Stewart, C. N. Jr. 2008. Plant systems biology comes of age. Trends Plant Sci. 13:165–171.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. 12:6–13.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 (1):58–70.CrossRefGoogle ScholarPubMed
Zhou, X., Su, Z., Sammons, R. D., Peng, Y., Tranel, P. J., Stewart, C. N. Jr., and Yuan, J. S. 2009. Novel software package for cross-platform transcriptome analysis (CPTRA). BMC Bioinformatics. 10 (Suppl. 11):S16.Google Scholar
Zhu, J., Patzoldt, W. L., Shealy, R. T., Vodkin, L. O., Clough, S. J., and Tranel, P. J. 2008. Transcriptome response to glyphosate in sensitive and resistant soybean. J. Agric. Food Chem. 56:6355–6363.Google Scholar
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