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Field Application of Glyphosate Induces Molecular Changes Affecting Vegetative Growth Processes in Leafy Spurge (Euphorbia esula)

Published online by Cambridge University Press:  20 January 2017

Münevver Doğramacı ,
Greta G. Gramig ,
James V. Anderson ,
Wun S. Chao  and
Michael E. Foley
Münevver Doğramacı*
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Sunflower and Plant Biology Research Unit, Fargo, ND 58102
Greta G. Gramig
Affiliation:
Department of Plant Sciences, North Dakota State University, Fargo, ND 58108
James V. Anderson
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Sunflower and Plant Biology Research Unit, Fargo, ND 58102
Wun S. Chao
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Sunflower and Plant Biology Research Unit, Fargo, ND 58102
Michael E. Foley
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Sunflower and Plant Biology Research Unit, Fargo, ND 58102
*
Corresponding author's E-mail: munevver.dogramaci@ars.usda.gov
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Abstract

Recommended rates of glyphosate for noncultivated areas destroy the aboveground shoots of the perennial plant leafy spurge. However, such applications cause little or no damage to underground adventitious buds (UABs), and thus the plant readily regenerates vegetatively. High concentrations of glyphosate, applied under controlled environmental conditions, have been shown to cause sublethal effects in UABs of leafy spurge that produce stunted and bushy phenotypes in subsequent generations of shoots. We treated leafy spurge plants in the field with glyphosate (0, 1.1, 3.4, or 6.7 kg ai ha−1) to determine its effects on vegetative growth from UABs and on molecular processes. The number of shoots derived from UABs of glyphosate-treated plants was significantly increased compared to controls in subsequent years after application, and new shoots displayed various phenotypical changes, such as stunted and bushy phenotypes. Quantifying the abundance of a selected set of transcripts in UABs of nontreated vs. treated plants (0 vs. 6.7 kg ha−1) indicated that glyphosate impacted molecular processes involved in biosynthesis or signaling of tryptophan or auxin (ARF4, CYP79B2, PIN3, TAA1, TRP6, YUC4), gibberellic acid (GA1/CPS1, GA2/KS), ethylene (ACO1, ACS10), cytokinins (AHP1, AK2, CKX1), and the cell cycle (CDC2A, CDC2B, CYCD3;1). Glyphosate-induced effects on vegetative growth and transcript abundance were persistent for at least 2 yr after treatment. Determining the molecular mechanisms associated with vegetative reproduction in leafy spurge following foliar glyphosate-treatment could identify limiting factors or new targets for manipulation of plant growth and development in perennial weeds.

Keywords

Glyphosate, leafy spurge, Euphorbia esula Lcell cyclefieldgene expressionnatural conditionsphytohormonesqRT-PCRstunted and bushy phenotypetranscript abundance
Type
Weed Biology and Ecology
Information
Weed Science , Volume 64 , Issue 1 , March 2016 , pp. 87 - 100
Copyright
Copyright © Weed Science Society of America 

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Footnotes

Associate Editor for this paper: Patrick J. Tranel, University of Illinois.

References

Literature Cited

Amrhein, N, Deus, B, Gehrke, P, Steinrucken, HC (1980) The site of the inhibition of the shikimate pathway by glyphosate. II. Interference of glyphosate with chorismate formation in vivo and in vitro. Plant Physiol 66:830–834 Google Scholar
Anderson, JV, Gesch, RW, Jia, Y, Chao, WS, Horvath, DP (2005) Seasonal shifts in dormancy status carbohydrate metabolism and related gene expression in crown buds of leafy spurge. Plant Cell Environ 28:1567–1578 Google Scholar
Anderson, JV, Horvath, DP, Chao, WS, Foley, ME (2010) Bud dormancy in perennial plants: a mechanism for survival. Pages 69–90 in Lubzens, E, Cerda, J, Clark, M eds. Dormancy and Resistance in Harsh Environments. Topics in Current Genetics. Hohmann S, series ed. Berlin Springer Google Scholar
Anderson, JV, Horvath, DP, Chao, WS, Foley, ME, Hernandez, AG, Thimmapuram, J, Liu, L, Gong, GL, Band, M, Kim, R, Mikel, MA (2007) Characterization of an EST database for the perennial weed leafy spurge: an important resource for weed biology research. Weed Sci 55:193–203 Google Scholar
Baur, JR (1979) Effect of glyphosate on auxin transport in corn and cotton tissues. Plant Physiol 63:882–886 Google Scholar
Baur, JR, Bovey, RW, Veech, (1977) Growth responses in sorghum and wheat induced by glyphosate. Weed Sci 25:238–240 Google Scholar
Bleecker, AB, Kende, H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol 16:1–18 Google Scholar
Cakmak, I, Yazici, A, Tutus, Y, Ozturk, L (2009) Glyphosate reduced seed and leaf concentrations of calcium, manganese, magnesium, and iron in nonglyphosate resistant soybean. European J Agronomy 31:114–119 Google Scholar
Campbell, WF, Evans, JO, Reed, SC (1976) Effect of glyphosate on chloroplast ultrastructure of quackgrass mesophyll cells. Weed Sci 24:22–25 Google Scholar
Champigny, MJ, Sung, WWL, Catana, V, Salwan, R, Summers, PS, Dudley, SA (2013) RNA-Seq effectively monitors gene expression in Eutrema salsugineum plants growing in an extreme natural habitat and in controlled growth cabinet conditions. BMC Genomics 14:23 Google Scholar
Chao, WS, Doğramacı, M, Foley, ME, Horvath, DP, Anderson, JV (2012) Selection and validation of endogenous reference genes for qRT-PCR analysis in leafy spurge (Euphorbia esula). PLoS ONE 7:e42839 Google Scholar
Chao, WS, Serpe, MD, Anderson, JV, Gesch, RW, Horvath, DP (2006) Sugars, hormones, and environment affect the dormancy status in underground adventitious buds of leafy spurge (Euphorbia esula L.). Weed Sci 54:59–68 Google Scholar
Coupland, D, Caseley, JC (1975) Reduction of silica and increase in tillering induced in Agropyron repens by glyphosate. J Exp Bot 26:138–144 Google Scholar
Della-Cioppa, G, Bauer, SC, Klein, BK, Shah, DM, Fraley, RT, Kishore, G (1986) Translocation of the precursor of 5-enolpyruvylshikimate-3-phosphate synthase into chloroplasts of higher plants in vitro. Proc Natl Acad Sci USA 83:6873–6877 Google Scholar
Doğramacı, M, Anderson, JV, Chao, WS, Foley, ME (2014a) Foliar application of glyphosate affects molecular mechanisms in underground adventitious buds of leafy spurge (Euphorbia esula) and alters their vegetative growth patterns. Weed Sci 62:217–229 Google Scholar
Doğramacı, M, Foley, ME, Chao, WS, Christoffers, MJ, Anderson, JV (2013) Induction of endodormancy in crown buds of leafy spurge (Euphorbia esula L.) implicates a role for ethylene and cross-talk between photoperiod and temperature. Plant Mol Biol 81:577–593 Google Scholar
Doğramacı, M, Foley, ME, Horvath, DP, Hernandez, AG, Khetani, R, Fields, CJ, Mikel, MA, Anderson, JV (2015) Glyphosate's impact on vegetative growth in leafy spurge identifies molecular processes and hormone cross-talk associated with increased branching. BMC Genomics 16:395 Google Scholar
Doğramacı, M, Horvath, DP, Anderson, JV (2014b) Dehydration-induced endodormancy in crown buds of leafy spurge highlights involvement of MAF3- and RVE1-like homologs, and hormone signaling cross-talk. Plant Mol Biol 86:409–424 Google Scholar
Doğramacı, M, Horvath, DP, Chao, WS, Foley, ME, Christoffers, MJ, Anderson, JV (2010) Low temperatures impact dormancy status, flowering competence, and transcript profiles in crown buds of leafy spurge. Plant Mol Biol 73:207–226 Google Scholar
Duke, SO, Powles, SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci 64:319–325 Google Scholar
Gomes, MP, Smedbol, E, Chalifour, A, Hénault-Ethier, L, Labrecque, M, Lepage, L, Lucotte, M, Juneau, P (2014) Alteration of plant physiology by glyphosate and its by-product aminomethylphosphonic acid: an overview. J Exp Bot 65:4691–4703 Google Scholar
Horvath, DP (1998) The role of specific plant organs and polar auxin transport in correlative inhibition of leafy spurge (Euphorbia esula) root buds. Can J Bot 76:1227–1231 Google Scholar
Horvath, DP, Chao, WS, Suttle, JC, Thimmapuram, J, Anderson, JV (2008) Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics 9:536 Google Scholar
Jones, B, Gunnerås, SA, Petersson, SV, Tarkowski, P, Graham, N, May, S, Dolezal, K, Sandberg, G, Ljung, K. (2010) Cytokinin regulation of auxin synthesis in Arabidopsis involves a homeostatic feedback loop regulated via auxin and cytokinin signal transduction. Plant Cell 22:2956–2969 Google Scholar
Krishnaswamy, S, Verma, S, Rahman, MH, Kav, NN (2011) Functional characterization of four APETALA2-family genes (RAP26, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75:107–127 Google Scholar
Lee, TT (1984) Release of lateral buds from apical dominance by glyphosate in soybean and pea seedlings. J Plant Growth Regul 3:227–235 Google Scholar
Leitch, JA, Leistritz, FL, Bangsund, DA (1996) Economic effect of leafy spurge in the Upper Great Plains: methods, models, and results. Impact Assess 14:419–433 Google Scholar
Lym, RG (2000) Leafy spurge (Euphorbia esula) control with glyphosate plus 2,4-D. J Range Manage 53:68–72 Google Scholar
Lym, RG, Messersmith, CG (1985) Leafy spurge control with herbicides in North Dakota: 20-yr summary. J Range Manage 38:149–154 Google Scholar
Lym, RG, Messersmith, CG (2013) Leafy Spurge Identification and Chemical Control. NDSU Extension Service. http://www.ag.ndsu.edu/pubs/plantsci/weeds/w765.pdf. Accessed October 22, 2015Google Scholar
Mason, MG, Ross, JJ, Babst, BA, Wienclaw, BN, Beveridge, CA (2014) Sugar demand, not auxin, is the initial regulator of apical dominance. Proc Natl Acad Sci USA 111:6092–6097 Google Scholar
Maxwell, BD, Foley, ME, Fay, PK (1987) The influence of glyphosate on bud dormancy in leafy spurge (Euphorbia esula). Weed Sci 35:6–10 Google Scholar
Mishra, Y, Johansson-Jänkänpää, H, Kiss, AZ, Funk, C, Schröder, WP, Jansson, S (2012) Arabidopsis plants grown in the field and climate chambers significantly differ in leaf morphology and photosystem components. BMC Plant Biol 12:6 Google Scholar
Mizoi, J, Shinozaki, K, Yamaguchi-Shinozaki, K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96 Google Scholar
Mollenhauer, C, Smart, CC, 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 29:55–65 Google Scholar
North Dakota Agricultural Weather Network Center (2015) North Dakota Agricultural Weather Network. http://ndawn.ndsu.nodak.edu/. Accessed June 8, 2015Google Scholar
Peer, WA (2013) From perception to attenuation: auxin signaling and responses. Curr Opin Plant Biol 23:1–8 Google Scholar
Railton, ID, Fellows, B, West, CA (1984) ent-Kaurene synthesis in chloroplasts from higher plants. Phytochemistry 23:1261–1267 Google Scholar
Sakamoto, T, Miura, K, Itoh, H, Tatsumi, T, Ueguchi-Tanaka, M, Ishiyama, K, Kobayashi, M, Agrawal, GK, Takeda, S, Abe, K, Miyao, A, Hirochika, H, Kitano, H, Ashikari, M, Matsuoka, M (2004) An overview of gibberellin metabolism enzyme genes and their related mutants in rice. Plant Physiol 134:1642–1653 Google Scholar
Sponsel, VM, Hedden, P (2004) Gibberellin biosynthesis and inactivation. Pages 63–94 in Davies, PJ, ed. Plant Hormones: Biosynthesis, Signal Transduction, Action! Dordrecht, The Netherlands Kluwer Academic Publishers Google Scholar
St. John, L, Tilley, D (2014) Plant guide for leafy spurge (Euphorbia esula). USDA-Natural Resources Conservation Service, Plant Materials Center. Aberdeen, Idaho 83210. http://plants.usda.gov/plantguide/pdf/pg_eues.pdf. Accessed October 22, 2015Google Scholar
Steinrücken, HC, Amrhein, N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochem Biophys Res Commun 94:1207–1212 Google Scholar
Ungerer, MC, Johnson, LC, Herman, MA (2008) Ecological genomics: understanding gene and genome function in the natural environment. Heredity 100:178–183 Google Scholar
Vanstraelen, M, Benková, E (2012) Hormonal interactions in the regulation of plant development. Annu Rev Cell Dev Biol 28:463–487 Google Scholar
Yamaguchi, S, Sun, T-p, Kawaide, H, Kamiya, Y (1998) The GA2 locus of Arabidopsis thaliana encodes ent-kaurene synthase of gibberellin biosynthesis. Plant Physiol 116:1271–1278 Google Scholar
Yasuor, H, Abu-abied, M, Belausov, E, Madmony, A, Sadot, E, Riov, J (2006) Glyphosate-induced anther indehiscence in cotton is partially temperature dependent and involves cytoskeleton and secondary wall modifications and auxin accumulation. Plant Physiol 141:1306–1315 Google Scholar
Zhao, Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol 61:49–64 Google Scholar
Zhao, Y, Hull, AK, Gupta, NR, Goss, KA, Alonso, J, Ecker, JR, Normanly, J, Chory, J, Celenza, JL (2002) Trp-dependent auxin biosynthesis in Arabidopsis: involvement of cytochrome P450s CYP79B2 and CYP79B3. Genes Dev 16:3100–3112 Google Scholar
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