Skip to main content Accessibility help
×
Home

Foliar Application of Glyphosate Affects Molecular Mechanisms in Underground Adventitious Buds of Leafy Spurge (Euphorbia esula) and Alters Their Vegetative Growth Patterns

  • Münevver Doğramacı (a1), James V. Anderson (a1), Wun S. Chao (a1) and Michael E. Foley (a1)

Abstract

Long-term control of leafy spurge with glyphosate requires multiple applications because the plant reproduces vegetatively from abundant underground adventitious buds, referred to as crown and root buds. Determining the molecular mechanisms involved in controlling vegetative reproduction in leafy spurge following foliar glyphosate treatment could identify limiting factors or new targets for manipulation of plant growth and development in invasive perennial species. Thus, we treated leafy spurge plants with 0 or 2.24 kg ai ha−1 glyphosate to determine its impact on selected molecular processes in crown buds derived from intact plants and plants decapitated at the soil surface 7 d after glyphosate treatment. New shoot growth from crown buds of foliar glyphosate-treated plants was significantly reduced compared with controls after growth-inducing decapitation, and had a stunted or bushy phenotype. Quantification of a selected set of transcripts involved in hormone biosynthesis and signaling pathways indicated that glyphosate had the most significant impact on abundance of ENT-COPALYL DIPHOSPHATE SYNTHETASE 1, which is involved in a committed step for gibberellin biosynthesis, and auxin transporters including PINs, PIN-LIKES, and ABC TRANSPORTERS. Foliar glyphosate treatment also reduced the abundance of transcripts involved in cell cycle processes, which would be consistent with altered growth patterns observed in this study. Overall, these results suggest that interplay among phytohormones such as auxin, ethylene, and gibberellins affect vegetative growth patterns from crown buds of leafy spurge in response to foliar glyphosate treatment.

Copyright

Corresponding author

Corresponding author's E-mail: munevver.dogramaci@ars.usda.gov.

References

Hide All
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. 66:830834
Anderson, JV, Davis, DG (2004) Abiotic stress alters transcript profiles and activity of glutathione S-transferase, glutathione peroxidase, and glutathione reductase in Euphorbia esula . Physiol Plant. 120:421433
Anderson, JV, Dogramaci, M, Horvath, DP, Foley, ME, Chao, WS, Suttle, JC, Thimmapuram, J, Hernandez, AG, Ali, S, Mikel, MA (2012) Auxin and ABA act as central regulators of developmental networks associated with paradormancy in Canada thistle (Cirsium arvense). Funct Integr Genomics. 12:515531
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. 28:15671578
Anderson, JV, Horvath, DP, Chao, WS, Foley, ME, Hernandez, A, 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. 55:193203
Barbez, E, Kubeš, M, Rolčík, J, Béziat, C, Pěnčík, A, Wang, B, Rosquete, MR, Zhu, J, Dobrev, PI, Lee, Y, Zažímalovà, E, Petrášek, J, Geisler, M, Friml, J, Kleine-Vehn, J (2012) A novel putative auxin carrier family regulates intracellular auxin homeostasis in plants. Nature. 485:119122
Bleecker, AB, Kende, H (2000) Ethylene: a gaseous signal molecule in plants. Annu Rev Cell Dev Biol. 16:118
Blilou, I, Xu, J, Wildwater, M, Willemsen, V, Paponov, I, Friml, J, Heidstra, R, Aida, M, Palme, K, Scheres, B (2005) The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 433:3944
Boocock, MR, Coggins, JR (1983) Kinetics of 5-enolpyruvyl-shikimate-3 phosphate synthase inhibition by glyphosate. FEBS Lett. 154:127133
Campbell, WF, Evans, JO, Reed, SC (1976) Effect of glyphosate on chloroplast ultrastructure of quackgrass mesophyll cells. Weed Sci. 24:2225
Cebeci, O, Budak, H (2009) Global expression patterns of three Festuca species exposed to different doses of glyphosate using the Affymetrix GeneChip wheat genome array. Comp Funct Genomics. 2009:110
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
Dai, C, Xuea, HW (2010) Rice early flowering1, a CKI, phosphorylates DELLA protein SLR1 to negatively regulate gibberellin signaling. EMBO J. 29:19161927
Davidson, SE, Elliott, RC, Helliwell, CA, Poole, AT, Reid, JB (2003) The pea gene NA encodes ent-kaurenoic acid oxidase. Plant Physiol. 131:335344
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 U S A. 83:68736877
Denis, MH, Delrot, S (1993) Carrier-mediated uptake of glyphosate in broad bean (Vicia faba) via a phosphate transporter. Physiol Planta. 87:569575
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. 81:577593
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. 73:207226
Doğramacı, M, Horvath, DP, Christoffers, MJ, Anderson, JV (2011) Dehydration and vernalization treatments identify overlapping molecular networks impacting endodormancy maintenance in leafy spurge crown buds. Funct Integr Genomics. 11:611626
Duke, SO, Powels, SB (2008) Glyphosate: a once-in-a-century herbicide. Pest Manag Sci. 64:319325
Feraru, E, Vosolsobě, S, Feraru, MI, Petrášek, J, Kleine-Vehn, J (2012) Evolution and structural diversification of PILS putative auxin carriers in plants. Front Plant Sci. 3:227
Fleet, CM, Yamaguchi, S, Hanada, A, Kawaide, H, David, CJ, Kamiya, Y, Sun, TP (2003) Overexpression of AtCPS and AtKS in Arabidopsis confers increased ent-kaurene production but no increase in bioactive gibberellins. Plant Physiol. 132:830839
Foley, ME, Anderson, JV, Horvath, DP (2009) The effects of temperature photoperiod and vernalization on regrowth and flowering competence in Euphorbia esula (Euphorbiaceae) crown buds. Botany. 87:986992
Franz, JE, Mao, MK, Sikorski, JA (1997) Glyphosate: a unique global herbicide. Am Chem Soc Monogr. 189:521615
Gaines, TA, Zhang, W, Wang, D, Bukun, B, Chisholm, ST, Shaner, DL, Nissen, SJ, Patzoldt, WL, Tranel, PJ, Culpepper, AS, Grey, TL, Webster, TM, Vencill, WK, Sammons, RD, Jiang, J, Preston, C, Leach, JE, Westra, P (2010) Gene amplification confers glyphosate resistance in Amaranthus palmeri . Proc Natl Acad Sci U S A. 107:10291034
Ge, X, d'Avignon, DA, Ackerman, JJH, Sammons, RD (2010) Rapid vacuolar sequestration: the horseweed glyphosate resistance mechanism. Pest Manag Sci. 66:345348
Gottrup, O, O'Sullivan, PA, Schraa, RJ, Vanden Bobn, WH (1976) Uptake, translocation, metabolism and selectivity of glyphosate in Canada thistle and leafy spurge. Weed Res. 16:197201
Gruys, KJ, Walker, MC, Sikorski, JA (1992) Substrate synergism and the steady-state kinetic reaction mechanism for EPSP synthase from Escherichia coli . Biochemistry. 31:55345544
Harberd, NP, Belfield, E, Yasumura, Y (2009) The angiosperm gibberellin-GID1-DELLA growth regulatory mechanism: how an “inhibitor of an inhibitor” enables flexible response to fluctuating environments. Plant Cell. 21:13281339
Hedden, P, Phillips, AL (2000) Gibberellin metabolism: new insights revealed by the genes. Trends Plant Sci. 5:523530
Herrmann, KM, Weaver, LM (1999) The shikimate pathway. Annu Rev Plant Physiol Plant Mol Biol. 50:473503
Kang, J, Park, J, Choi, H, Burla, B, Kretzschmar, T, Lee, Y, Martinoia, E (2011) Plant ABC transporters. Arabidopsis Book. 9:e0153
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. 75:107127
Lang, GA, Early, JD, Martin, GC, Darnell, RL (1987) Endo-, para-, and eco-dormancy: physiological terminology and classification for dormancy research. Hort Sci. 22:371377
Lym, RG (2000) Leafy spurge (Euphorbia esula) control with glyphosate plus 2,4-D. J Range Manage. 53:6872
Lym, RG, Messersmith, CG (2013) Leafy spurge identification and chemical control. NDSU Extension Service, http://www.ag.ndsu.edu/pubs/plantsci/weeds/w765.pdf
Lym, RG, Nelson, JA (2002) Integration of Aphthona spp. flea beetles and herbicides for leafy spurge (Euphorbia esula) control. Weed Sci. 50:812819
Magome, H, Yamaguchi, S, Hanada, A, Kamiya, Y, Oda, K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis . Plant J. 56:613626
Maxwell, BD, Foley, ME, Fay, PK (1987) The influence of glyphosate on bud dormancy in leafy spurge (Euphorbia esula). Weed Sci. 35:610
Mizoi, J, Shinozaki, K, Yamaguchi-Shinozaki, K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta. 1819:8696
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. 29:5565
Peer, WA (2013) From perception to attenuation: auxin signaling and responses. Curr Opin Plant Biol. 23:18
Peng, Y, Abercrombie, LL, Yuan, JS, Riggins, CW, Sammons, RD, Tranel, PJ, Stewart, CN Jr. (2010) Characterization of the horseweed (Conyza canadensis) transcriptome using GS-FLX 454 pyrosequencing and its application for expression analysis of candidate non-target herbicide resistance genes. Pest Manag Sci. 66:10531062
Raju, MVS, Steeves, TA, Coupland, RT (1964) On the regeneration of root fragments of leafy spurge (Euphorbia esula L.). Weed Res. 4:211
Riechers, DE, Wax, LM, Liebl, RA, Bush, DA (1994) Surfactant-increased glyphosate uptake into plasma membrane vesicles isolated from common lambsquarters leaves. Plant Physiol. 105:14191425
Riggins, CW, Peng, Y, Stewart, CN Jr., Tranel, PJ (2010) Characterization of de novo transcriptome for waterhemp (Amaranthus tuberculatus) using GS-FLX 454 pyrosequencing and its application for studies of herbicide target-site genes. Pest Manag Sci. 66:10421052
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. 134:16421653
Shaner, DL (2009) The role of translocation as a mechanism of resistance to glyphosate. Weed Sci. 57:118123
Shinohara, N, Taylor, C, Leyser, O (2013) Strigolactone can promote or inhibit shoot branching by triggering rapid depletion of the auxin efflux protein PIN1 from the plasma membrane. PLoS Biol. 11(1):e1001474
Sponsel, VM, Hedden, P (2004) Gibberellin biosynthesis and inactivation. Pages 6394 in Davies, PJ ed. Plant Hormones: Biosynthesis, Signal Transduction, Action. Dordrecht, The Netherlands Kluwer Academic Publishers
Staub, JM, Brand, L, Tran, M, Kong, Y, Rogers, SG (2012) Bacterial glyphosate resistance conferred by overexpression of an Escherichia coli membrane efflux transporter. J Ind Microbiol Biotechnol. 39:641647
Steinrücken, HC, Amrhein, N (1980) The herbicide glyphosate is a potent inhibitor of 5-enolpyruvylshikimic acid-3-phosphate synthase. Biochem Biophys Res Commun. 94:12071212
Tong, Z, Hong, B, Yang, Y, Li, Q, Ma, N, Ma, C, Gao, J (2009) Overexpression of two chrysanthemum DgDREB1 group genes causing delayed flowering or dwarfism in Arabidopsis . Plant Mol Biol. 71:115129
Wyrill, JB III, Burnside, OC (1976) Absorption, translocation, and metabolism of 2,4-D and glyphosate in common milkweed and hemp dogbane. Weed Sci. 24:557566
Yuan, JS, Abercrombie, LLG, Cao, Y, Halfhill, MD, Zhou, X, Peng, Y, Hu, J, Rao, MR, Heck, GR, Larosa, TJ, Sammons, RD, Wang, X, Ranjan, P, Johnson, DH, Wadl, PA, ScheZer, BE, Rinehart, TA, Trigiano, RN, Stewart, CN Jr. (2010) Functional genomics analysis of horseweed (Conyza canadensis) with special reference to the evolution of non-target-site glyphosate resistance. Weed Sci. 58:109117
Yuan, JS, Tranel, PJ, Stewart, CN Jr. (2007) Non-target-site herbicide resistance: a family business. Trends Plant Sci. 12:613
Zhao, Y (2010) Auxin biosynthesis and its role in plant development. Annu Rev Plant Biol. 61:4964
Zhu, J, Patzoldt, WL, Shealy, RT, Vodkin, LO, Clough, SJ, Tranel, PJ (2008) Transcriptome response to glyphosate in sensitive and resistant soybean. J Agric Food Chem. 56:63556363

Keywords

Type Description Title
UNKNOWN
Supplementary materials

Doğramacı et al. supplementary material
Supplementary Material

 Unknown (214 KB)
214 KB

Metrics

Altmetric attention score

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed