Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T11:18:18.652Z Has data issue: false hasContentIssue false

Herbicide symptomology and the mechanism of action of methiozolin

Published online by Cambridge University Press:  03 December 2020

Chad Brabham
Affiliation:
Former Graduate Student, Department of Horticulture, University of Kentucky, Lexington, KY, USA
Philipp Johnen
Affiliation:
Team Leader, BASF SE, Limburgerhof, Germany
Janneke Hendriks
Affiliation:
Senior Scientist, BASF Metabolome Solutions GmbH, Berlin, Germany
Michael Betz
Affiliation:
Team Leader, BASF SE, Ludwigshafen am Rhein, Germany
Alexandra Zimmermann
Affiliation:
Team Leader, BASF SE, Limburgerhof, Germany
Jarrad Gollihue
Affiliation:
Graduate Student, Department of Horticulture, University of Kentucky, Lexington, KY, USA
William Serson
Affiliation:
Assistant Professor, Department of Biology, Ave Maria University, Ave Maria, FL, USA
Chase Kempinski
Affiliation:
Former Graduate Student, Department of Pharmaceutical Science Lexington, KY, USA
Michael Barrett*
Affiliation:
Professor, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY, USA
*
Author for correspondence: Michael Barrett, Department of Plant and Soil Sciences, University of Kentucky, Lexington, KY40546-0312. (Email: mbarrett@uky.edu)

Abstract

Methiozolin is a new herbicide with an unknown mechanism of action (MOA) for control of annual bluegrass (Poa annua L.) in several warm- and cool-season turfgrasses. In the literature, methiozolin was proposed to be a pigment inhibitor via inhibition of tyrosine aminotransferases (TATs) or a cellulose biosynthesis inhibitor (CBI). Here, exploratory research was conducted to characterize the herbicide symptomology and MOA of methiozolin. Arabidopsis (Arabidopsis thaliana L.) and P. annua exhibited a similar level of susceptibility to methiozolin, and arrest of meristematic growth was the most characteristic symptomology. For example, methiozolin inhibited A. thaliana root growth (GR50 8 nM) and shoot emergence (GR80 ˜50 nM), and apical meristem growth was completely arrested at rates greater than 500 nM. We concluded that methiozolin was neither a TAT nor a CBI inhibitor. Methiozolin had a minor effect on chlorophyll and alpha-tocopherol content in treated seedlings (<500 nM), and supplements in the proposed TAT pathway could not lessen phytotoxicity. Examination of microscopic images of roots revealed that methiozolin-treated (100 nM) and untreated seedlings had similar root cell lengths. Thus, methiozolin inhibits cell proliferation and not elongation from meristematic tissue. Subsequently, we suspected methiozolin was an inhibitor of the mevalonic acid (MVA) pathway, because its herbicidal symptomologies were nearly indistinguishable from those caused by lovastatin. However, methiozolin did not inhibit phytosterol production, and MVA pathway metabolites did not rescue treated seedlings. Further experiments showed that methiozolin produced a physiological profile very similar to cinmethylin across a number of assays, a known inhibitor of fatty-acid synthesis through inhibition of thioesterases (FATs). Experiments with lesser duckweed (Lemna aequinoctialis Welw.; syn. Lemna paucicostata Hegelm.) showed that methiozolin also reduced fatty-acid content in Lemna with a profile similar, but not identical, to cinmethylin. However, there was no difference in fatty-acid content between treated (1 µM) and untreated A. thaliana seedlings. Methiozolin also bound to both A, thaliana and L. aequinoctialis FATs in vitro. Modeling suggested that methiozolin and cinmethylin have comparable and overlapping FAT binding sites. While there was a discrepancy in the effect of methiozolin on fatty-acid content between L. aequinoctialis and A. thaliana, the overall evidence indicates that methiozolin is a FAT inhibitor and acts in a similar manner as cinmethylin.

Type
Research Article
Copyright
© The Author(s), 2020. Published by Cambridge University Press on behalf of the 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.)

Footnotes

Associate Editor: Franck E. Dayan, Colorado State University

References

Anonymous (2019a) Molecular Operating Environment (MOE). Version 2019.01. Montreal, QC, Canada: Chemical Computing GroupGoogle Scholar
Anonymous (2019b) U.S. Environmental Protection Agency Registration of PoaCure SC. EPA Registration # 089633-5. https://www3.epa.gov/pesticides/chem_search/ppls/089633-00005-20191209.pdf Google Scholar
Askew, SD, McNulty, BMS (2014) Methiozolin and cumyluron for preemergence annual bluegrass (Poa annua) control on creeping bentgrass (Agrostis stolonifera) putting greens. Weed Technol 28:535542 CrossRefGoogle Scholar
Bao, X, Focke, M, Pollard, M, Ohlrogge, J (2000) Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue. Plant J 22:3950 CrossRefGoogle ScholarPubMed
Baum, SF, Karanastasis, L, Rost, TL (1998) Morphogenetic effect of the herbicide Cinch on Arabidopsis thaliana root development. J Plant Growth Regul 14:107114 CrossRefGoogle Scholar
Bonaventure, G, Bao, X, Ohlrogge, J, Pollard, M (2004) Metabolic responses to the reduction in palmitate caused by disruption of the FATB gene in Arabidopsis . Plant Physiol 135:12691279 CrossRefGoogle ScholarPubMed
Brabham, C, Debolt, S (2012) Chemical genetics to examine cellulose biosynthesis. Front Plant Sci 3:309 Google ScholarPubMed
Brabham, C, Lei, L, Gu, Y, Stork, J, Barrett, M, Debolt, S (2014) Indaziflam herbicidal action: a potent cellulose biosynthesis inhibitor. Plant Physiol 166:11771185 CrossRefGoogle ScholarPubMed
Brosnan, JT, Calvache, S, Breeden, GK, Sorochan, JC (2013) Rooting depth, soil types, and application rate effects on creeping bentgrass injury with amicarbazone and methiozolin. Crop Sci 53:655659 CrossRefGoogle Scholar
Campe, R, Hollenbach, E, Kammerer, L, Hendriks, J, Hoffken, HW, Kraus, H, Lerchl, J, Mietzner, T, Tresch, S, Witschel, M, Hutzler, (2018) A new herbicidal site of action: cinmethylin binds to acyl-ACP thioesterase and inhibits plant fatty acid biosynthesis. Pest Biochem Phys 148:116125 CrossRefGoogle ScholarPubMed
Cutler, SR, Ehrhardt, DW, Griffitts, JS, Somerville, CR (2000) Random GFP:cDNA fusions enable visualization of subcellular structures in cells of Arabidopsis at a high frequency. Proc Natl Acad Sci USA 97:37183723 CrossRefGoogle ScholarPubMed
DellaPenna, D., Pogson, BJ (2006) Vitamin synthesis in plants: tocopherols and carotenoids. Annu Rev Plant Biol 57:711–38CrossRefGoogle ScholarPubMed
El-Deek, MH, Hess, FD (1986) Inhibited miotic entry is the cause of growth inhibition by cinmethylin. Weed Sci 34:684688 CrossRefGoogle Scholar
Flessner, ML, Wehtje, GR, McElroy, JS (2013) Methiozolin absorption and translocation in annual bluegrass (Poa annua). Weed Sci 61:201208 Google Scholar
Gendreau, E, Traas, J, Desnos, T, Grandjean, O, Caboche, M, Hofte, H (1997) Cellular basis of hypoctyl growth in Arabidopsis thaliana. Plant Physiol 114:295305 CrossRefGoogle ScholarPubMed
Gigon, A, Matos, A-R, Laffray, D, Zuily-Fodil, Y, Pham-Thi, A-T (2004) Effect of drought stress on lipid metabolism in the leaves of Arabidopsis thaliana (Ecotype Columbia). Ann Bot 94:345351 CrossRefGoogle Scholar
Grossmann, K (2005) What it takes to get a herbicide’s mode of action. Physionomics, a classical approach in a new complexion. Pest Manag Sci 61:423431 CrossRefGoogle Scholar
Grossmann, K, Hutzler, J, Tresch, S, Christiansen, N, Looser, R, Ehrhardt, T (2012) On the mode of action of the herbicides cinmethlyin and 5-benyloxymethyl-1,2-isoxazolines: putative inhibitors of plant tyrosine aminotransferase. Pest Manag Sci 68:482492 CrossRefGoogle ScholarPubMed
Grossmann, K, Niggeweg, R, Christiansen, N, Looser, R, Ehrhardt, T (2010) The herbicide saflufenacil (Kixor™) is a new inhibitor of protoporphyrinogen IX oxidase activity. Weed Sci 58:19 CrossRefGoogle Scholar
Guo, DA, Venkatramesh, M, Nes, WD (1995) Developmental regulation of sterol biosynthesis in Zea mays . Lipid 30:2032019 CrossRefGoogle ScholarPubMed
Hartmann, MA (1998) Plant sterols and the membrane environment. Trends Plant Sci 3:170175 CrossRefGoogle Scholar
Hoisington, NR, Flessner, ML, Schiavon, M, McElroy, JS, Baird, JH (2014) Tolerance of bentgrass (Agrostis) species and cultivars to methiozolin. Weed Technol 28:501509 CrossRefGoogle Scholar
Holländer-Czytko, H, Grabowski, J, Sandorf, I, Weckermann, K, Weiler, EW (2005) Tocopherol content and activities of tyrosine aminotransferase and cysteine lyase in Arabidopsis under stress conditions. J Plant Physiol 162:767770 CrossRefGoogle Scholar
Huang, T, Tohge, T, Lytovchenko, A, Fernie, AR, Jander, G (2010) Pleiotropic physiological consequences of feedback-insensitive phenylalanine biosynthesis in Arabidopsis thaliana. Plant J 63:823835 CrossRefGoogle ScholarPubMed
Hwang, IT, Kim, HR, Jeon, DJ, Hong, KS, Song, JH, Cho, KY (2005) 5-(2,6-Difluorobenzyl)oxymethyl-5-methyl-3-(3-methylthiophen-2-yl)-1,2-isoxazoline as a useful rice herbicide. J Agric Food Chem 53:86398643 CrossRefGoogle Scholar
Istvan, ES, Deisenhofer, J (2001) Structural mechanism for statin inhibition of HMG-CoA Reductase. Science 292:1601164 CrossRefGoogle ScholarPubMed
Iverson, SJ, Lang, SLC, Cooper, MH (2001) Comparison of the Bligh and Dyer and Folch methods for total lipid determination in a broad range of marine tissue. Lipids 36:1283 CrossRefGoogle Scholar
Jiang, Z, Kempinski, C, Chappell, J (2016) Extraction and analysis of terpenes/terpenoids. Curr Protoc Plant Biol 1:345358 CrossRefGoogle ScholarPubMed
Jones, G, Willett, P, Glen, RC, Leach, AR, Taylor, R (1997) Development and validation of a genetic algorithm for flexible docking. J Mol Biol 267:727748 CrossRefGoogle ScholarPubMed
Kobayashi, K, Suzuki, M, Tang, J, Nagata, N, Ohyama, K, Seki, H, Kiuchi, R, Kaneko, Y, Nakazawa, M, Matsui, M, Matsumoto, S, Yoshida, S, Muranaka, T (2007) LOVASTATIN INSENSITIVE 1, a novel pentatricopeptide repeat protein, is a potential regulatory factor of isoprenoid biosynthesis in Arabidopsis . Plant Cell Physiol 48:322331 CrossRefGoogle ScholarPubMed
Koo, SJ, Hwang, KH, Jeon, MS, Kim, SH, Lim, J, Lee, DG, Cho, NG (2014) Methiozolin [5-(2,6-difluorobenzyl)oxymethyl-5-methyl-3,3(3-methylthiophen-2-yl)-1,2-isoxazoline], a new annual bluegrass (Poa annua L.) herbicide for turfgrasses. Pest Manag Sci 70:156162 CrossRefGoogle ScholarPubMed
Layton, CJ, Hellinga, HW (2010) Thermodynamic analysis of ligand-induced changes in protein thermal unfolding applied to high-throughput determination of ligand affinities with extrinsic fluorescent dyes. Biochemistry 49:1083110841 CrossRefGoogle Scholar
Lee, JN, Koo, SJ, Hwang, KH, Hwang, IT, Jeon, DJ, Kim, HR (2007) Mode of action of a new isoxazoline compound. Pages 597601 in Proceedings of the 21st Asian Pacific Weed Science Society Conference. Colombo, Sri Lanka: Asian Pacific Weed Science SocietyGoogle Scholar
McCullough, PE, Barreda, DG, Yu, J (2013) Selectivity of methiozolin for annual bluegrass (Poa annua) control in creeping bentgrass as influenced by temperature and application timing. Weed Sci 61:209216 CrossRefGoogle Scholar
Porfirova, S, Bergmuller, E, Tropf, S, Lemke, R, Dormann, P (2002) Isolation of an Arabidopsis mutant lacking vitamin E and identification of a cyclase essential for all tocopherol biosynthesis Proc Natl Acad Sci USA 99:1249512500 CrossRefGoogle ScholarPubMed
Riewe, D, Koohi, M, Lisec, J, Pfeiffer, M, Lippman, R, Schmeichel, J, Willmitzer, L, Altmann, T (2012) A tyrosine aminotransferase involved in tocopherol synthesis in Arabidopsis . Plant J 71:850859 CrossRefGoogle ScholarPubMed
Ritchie, RJ (2006) Consistent sets of spectrophotometric chlorophyll equations for acetone, methanol and ethanol solvents. Photosynth Res 89:2741 CrossRefGoogle ScholarPubMed
Ritz, C, Baty, F, Streibig, JC, Gerhand, D (2015) Dose-response analysis using R. PLoS ONE 10: e01460251 CrossRefGoogle ScholarPubMed
Rodriguez-Concepcion, M, Fores, O, Martinex-Garcia, JF, Gonzalez, V, Phillipis, M, Ferrer, A, Boronat, A (2004) Distinct-light-mediated pathways regulate the biosynthesis and exchange of isoprenoid precursors during Arabidopsis seedling development. Plant Cell 16:144156 CrossRefGoogle ScholarPubMed
Ryu, EK, Kim, HR, Jeon, DJ, Song, JW, Kim, KM, Lee, JN, Kim, HC, Hong, SH, inventors; Korea Research Institute of Chemical Technology, assignee (2002) September 7. Preparation of herbicidial 5-benzyloxymethyl-1,2-isoxazoline derivates of weed control in rice. US patent WO200209185Google Scholar
Sabba, RP, Vaughn, KC (1999) Herbicides that inhibit cellulose biosynthesis. Weed Sci 47:757763 CrossRefGoogle Scholar
Sánchez-Martín, J, Canales, FJ, Tweed, JKS, Lee, MRF, Rubiales, D, Gómez-Cadenas, A, Arbona, V, Mur, LAJ, Prats, E (2004) Fatty acid profile changes during gradual soil water depletion in oats suggests a role for jasmonates in coping with drought. Front Plant Sci 9:1077 CrossRefGoogle Scholar
Schaller, H (2003) The role of sterols in plant growth and development. Prog Lipid Res 42:163175 CrossRefGoogle ScholarPubMed
Schneider, CA, Rasband, WS, Eliceiri, KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9:671675 CrossRefGoogle ScholarPubMed
Shaner, DL, ed (2014) Herbicide Handbook. 10th ed. Lawrence, KS: Weed Science Society of America. Pp 12, 413 Google Scholar
Soto, G, Stritzler, M, Lisi, C, Alleva, K, Pagano, ME, Ardila, F, Mozzicafreddo, M, Cuccioloni, M, Angeletti, M, Ayub, ND (2011) Acetoacetyl-CoA thiolase regulates the mevalonate pathway during abiotic stress adaptation. J Exp Bot 62:5699–711CrossRefGoogle ScholarPubMed
Suzuki, M, Kamide, Y, Nagata, N, Seki, H, Ohyama, K, Kato, H, Masuda, K, Sato, S, Kato, T, Tabata, S, Yoshida, S, Muranaka, T (2004) Loss of function of 3-hydroxy-3-methyldlutaryl coenzyme A reductase 1 (HMG1) in Arabidopsis leads to dwarfing, early senescence and male sterility, and reduced sterol levels. Plant J 37:750761 CrossRefGoogle Scholar
Venner, KA (2015) Evaluating Methiozolin Programs for Golf Putting Greens and Investigating Potential Modes of Action. Ph.D dissertation. Blackburg, VA: Virgina Tech. 165 pGoogle Scholar
Vranova, E, Coman, D, Gruissem, W (2013) Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu Rev Plant Biol 64:665700 CrossRefGoogle ScholarPubMed
Xu, Z (2002) Analysis of tocopherols and tocotrienols. Curr Protoc Food Anal Chem 4:D1.5.1-D1.5.1.2CrossRefGoogle Scholar
Yu, J, McCullough, PE (2014) Methiozolin efficacy, absorption, and fate in six cool-season grasses. Crop Sci 54:12111219 CrossRefGoogle Scholar
Supplementary material: PDF

Brabham et al. supplementary material

Brabham et al. supplementary material 1

Download Brabham et al. supplementary material(PDF)
PDF 191.2 KB
Supplementary material: File

Brabham et al. supplementary material

Brabham et al. supplementary material 2

Download Brabham et al. supplementary material(File)
File 33.8 KB