Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-16T11:15:31.022Z Has data issue: false hasContentIssue false
  • English
  • Français

Evaluation of auxin-responsive genes in soybean for detection of off-target plant growth regulator herbicides

Published online by Cambridge University Press:  20 January 2017

Kevin B. Kelley ,
Qin Zhang ,
Kris N. Lambert  and
Dean E. Riechers
Kevin B. Kelley
Affiliation:
Department of Crop Sciences, University of Illinois, Urbana, IL 61801
Qin Zhang
Affiliation:
Department of Crop Sciences, University of Illinois, Urbana, IL 61801
Kris N. Lambert
Affiliation:
Department of Crop Sciences, University of Illinois, Urbana, IL 61801
Get access Rights & Permissions [Opens in a new window]

Abstract

The expression of a candidate auxin-responsive gene was evaluated for use in a diagnostic assay for plant growth regulator (PGR) herbicide injury in soybean leaves. Expression of GH3, a primary auxin-responsive gene, was evaluated in response to dicamba and clopyralid at the RNA and protein levels, and proteomic analysis evaluated global expression of proteins in response to dicamba. Expression of GH3 was also analyzed in response to heat, drought, salt stress, and infection by soybean mosaic virus (SMV) and bean pod mottle virus (BPMV) to determine the specificity of GH3 expression as a diagnostic marker for PGR herbicide injury. At the RNA level, GH3 was strongly induced by dicamba and clopyralid within 8 h after application. Expression peaked 1 to 3 d after treatment (DAT) in response to 10% and 1% of a labeled dose of dicamba and clopyralid, with higher expression levels detected at higher herbicide rates. At the protein level, GH3 expression was also strongly induced at 1, 2, and 3 DAT by 10% vs. 1% of a labeled dose of dicamba and clopyralid. Heat, drought, and salt stress and infection with SMV or BPMV had no effect on GH3 expression at either the RNA or protein level. Proteomic analysis identified three proteins that were up-regulated in response to dicamba. Two were induced for less than 7 DAT, and a third was identified as a stress-response enzyme (superoxide dismutase) that is likely not specific to PGR herbicide injury. Expression of GH3 was highly induced by PGR herbicides at the RNA and protein level and was not affected by environmental stresses or viral infection, indicating that GH3 expression has excellent potential for use in a diagnostic assay for PGR herbicide injury.

Keywords

Clopyraliddicambasoybean, Glycine max L. MerrAuxinic herbicidesdiagnostic assaygene expressionGH3immunoassaymolecular markerreal-time RT-PCR
Type
Physiology, Chemistry, Biochemistry
Information
Weed Science , Volume 54 , Issue 2 , April 2006 , pp. 220 - 229
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

Andersen, S. M., Clay, S. A., Wrage, L. J., and Matthees, D. 2004. Soybean foliage residues of dicamba and 2,4-D and correlation to application rates and yield. Agron. J 96:750–760.Google Scholar
Auch, D. E. and Arnold, W. E. 1978. Dicamba use and injury on soybeans (Glycine max) in South Dakota. Weed Sci 26:471–475.Google Scholar
Behens, R. and Lueschen, W. E. 1979. Dicamba volatility. Weed Sci 27:486–493.CrossRefGoogle Scholar
Bierfreund, N. M., Tintelnot, S., Reski, R., and Decker, E. L. 2004. Loss of GH3 function does not affect phytochrome-mediated development in a moss, Physcomitrella patens . J. Plant Physiol 161:823–835.Google Scholar
Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem 72:248–254.Google Scholar
Comba, M. E., Benavides, M. P., and Tomaro, M. L. 1998. Effect of salt stress on antioxidant defense system in soybean root nodules. Aust. J. Plant Physiol 25:665–671.Google Scholar
Converse, R. H. and Martin, R. R. 1990. ELISA methods for plant viruses. Pages 179–196 in Hampton, R., Ball, E., and De Boer, S. eds. Serological Methods for Detection and Identification of Viral and Bacterial Plant Pathogens. St. Paul, MN: APS Press.Google Scholar
Doyle, E. A. and Lambert, K. N. 2002. Cloning and characterization of an esophageal gland–specific pectate lyase from the root-knot nematode Meloidogyne javanica . Mol. Plant Microb. Interact 15:549–556.Google Scholar
Ferris, R., Wheeler, T. R., Ellis, R. H., and Hadley, P. 1999. Seed yield after environmental stress in soybean grown under elevated CO2 . Crop Sci 39:710–718.Google Scholar
Franzen, D. W., O'Barr, J. H., and Zollinger, R. K. 2004. Influence of certain postemergence broadleaf herbicides on soybean stressed from iron deficiency chlorosis. Agron. J 96:1357–1363.Google Scholar
Gee, M. A., Hagen, G., and Guilfoyle, T. J. 1991. Tissue-specific and organ-specific expression of soybean auxin-responsive transcripts GH3 and SAURs. Plant Cell 3:419–430.Google Scholar
Ghorbanli, M., Ebrahimzadeh, H., and Sharifi, M. 2004. Effects of NaCl and mycorrhizal fungi on antioxidative enzymes in soybean. Biol. Plant 48:575–581.Google Scholar
Giesler, L. J., Ghabrial, S. A., Hunt, T. E., and Hill, J. H. 2002. Bean pod mottle virus: a threat to U.S. soybean production. Plant Dis 86:1280–1289.Google Scholar
Goda, H., Sawa, S., Asami, T., Fujioka, S., Shimada, Y., and Yoshida, S. 2004. Comprehensive comparison of auxin-regulated and brassinosteroid-regulated genes in Arabidopsis . Plant Physiol 134:1555–1573.Google Scholar
Goss, G. A. and Dyer, W. E. 2003. Physiological characterization of auxinic herbicide-resistant biotypes of kochia (Kochia scoparia). Weed Sci 51:839–844.Google Scholar
Greenbaum, D., Colangelo, C., Williams, K., and Gerstein, M. 2003. Comparing protein abundance and mRNA expression levels on a genomic scale. Genome Biol 4:117. genomebiology.com/2003/4/9/117.Google Scholar
Gunduza, I., Buss, G. R., Chena, P., and Tolin, S. A. 2002. Characterization of SMV-resistance genes in Tousan 140 and Hourei soybean. Crop Sci 42:90–95.Google Scholar
Gygi, S. P., Corthals, G. L., Zhany, Y., Rochon, Y., and Aebersold, R. 2000. Evaluation of two-dimensional gel electrophoresis-based proteome analysis technology. Proc. Natl. Acad Sci. U S A 97:9390–9395.CrossRefGoogle ScholarPubMed
Hagen, G. and Guilfoyle, T. J. 1985. Rapid induction of selective transcription by auxins. Mol. Cell. Biol 5:1197–1203.Google ScholarPubMed
Hagen, G., Kleinschmidt, A., and Guilfoyle, T. 1984. Auxin-regulated gene expression in intact soybean hypocotyl and excised hypocotyl sections. Planta 162:147–153.CrossRefGoogle ScholarPubMed
Hagen, G., Martin, G., Li, Y., and Guilfoyle, T. J. 1991. Auxin-induced expression of the soybean GH3-promoter in transgenic tobacco plants. Plant Mol. Biol 17:567–79.Google Scholar
Hager, A. and Nordby, D. 2004. Soybean leaf cupping. Pest Manag. Crop Dev. Bull 15:133–135. www.ipm.uiuc.edu/bulletin/index.php.Google Scholar
Hanson, A. D. and Gregory, J. F. 2002. Synthesis and turnover of folates in plants. Curr. Opin. Plant Biol 5:244–249.Google Scholar
Himanen, K., Vuylsteke, M., Vercruysse, S., Boucheron, E., Alard, P., Chiqui, D., Van Montagu, M., Inze, D., and Beeckman, T. 2004. Transcript profiling of early lateral root initiation. Proc. Natl. Acad. Sci. USA 101:5146–5151.Google Scholar
Hoagland, D. R. and Arnon, D. I. 1953. The water culture method for growing plants without soil. Calif. Agric. Exp. Stn. Univ. Calif. Berkeley Circ. 347.Google Scholar
Hong, Y. and Pak, Y. 1999. Identification of chiro-inositol-containing phospholipids and changes in their metabolism upon salt stress in soybean seedlings. Phytochemistry 51:861–866.Google Scholar
Huangpu, J., Pak, J. H., Graham, M. C., Rickle, S. A., and Graham, J. S. 1996. Purification and molecular analysis of an extracellular gamma-glutamyl hydrolase present in young tissues of the soybean plant. Biochem. Biophys. Res. Commun 228:1–6.Google Scholar
Irwin, M. E. and Schultz, G. A. 1981. Soybean mosaic virus. Plant Protect. Bull 29:41–55.Google Scholar
Ivnitski, D., O'Neil, D. J., Gattuso, A., Schlicht, R., Calidonna, M., and Fisher, R. 2003. Nucleic acid approaches for detection and identification of biological warfare and infectious disease agents. BioTechniques 35:862–869.Google Scholar
Kelley, K. B., Lambert, K. N., Hager, A. G., and Riechers, D. E. 2004. Quantitative expression analysis of GH3, a gene induced by plant growth regulator herbicides in soybean. J. Agric. Food Chem 52:474–478.CrossRefGoogle ScholarPubMed
Kelley, K. B., Wax, L. M., Hager, A. G., and Riechers, D. E. 2005. Soybean response to plant growth regulator herbicides is affected by other postemergence herbicides. Weed Sci 53:101–112.CrossRefGoogle Scholar
Kokado, A., Arakawa, H., and Maeda, M. 2002. Chemiluminescent assay of alkaline phosphatase using dihydroxyacetone phosphate as substrate detected with lucigenin. Luminescence 17:5–10.CrossRefGoogle ScholarPubMed
Koning, G., TeKrony, D. M., Ghabrial, S. A., and Pfeiffer, T. W. 2002. Soybean mosaic virus (SMV) and the SMV resistance gene (Rsv1 ): influence on Phomopsis spp. seed infection in an aphid free environment. Crop Sci 42:178–185.Google Scholar
Kuo, H. F., Tsai, Y. F., Young, L. S., and Lin, C. Y. 2000. Ethanol treatment triggers a heat shock-like response but no thermotolerance in soybean (Glycine max cv. Kaohsiung No. 8) seedlings. Plant Cell Environ 23:1099–1108.Google Scholar
Lahey, K., Yuan, R., Burns, J. K., Ueng, P. P., Timmer, L. W., and Chung, K-R. 2004. Induction of phytohormones and differential gene expression in citrus flowers infected by the fungus Colletotrichum acutatum . Mol. Plant Microbe Interact 17:1394–1401.Google Scholar
Mahajan, S. D., Schwartz, S. A., and Nair, M. P. N. 2003. Immunological assays for chemokine detection in in vitro culture of CNS cells. Biol. Proced. Online 5:90–102.CrossRefGoogle ScholarPubMed
Nishizono, I., Iida, S., Suzuki, N., Kawada, H., Murakami, H., Ashihara, Y., and Okada, M. 1991. Rapid and sensitive chemiluminescent enzyme immunoassay for measuring tumor markers. Clin. Chem 37:1639–1644.Google Scholar
Porcel, R. and Ruiz-Lozano, J. M. 2004. Arbuscular mycorrhizal influence on leaf water potential, solute accumulation, and oxidative stress in soybean plants subjected to drought stress. J. Exp. Bot 55:1743–1750.CrossRefGoogle ScholarPubMed
Proost, R., Boerboom, C., and Schmidt, R. 2004. Dicamba Injury to Soybean. Integrated Pest and Crop Management, University of Wisconsin-Madison. ipcm.wisc.edu/pubs/pest/Dicamba2004.htm.Google Scholar
Raghavan, C., Kok Ong, E., Dalling, M. J., and Stevenson, T. W. 2005. Effect of herbicidal application of 2,4-dichlorophenoxyacetic acid in Arabidopsis . Funct. Integr. Genomics 5:4–17.Google Scholar
Riccardi, F., Gazeau, P., de Vienne, D., and Zivy, M. 1998. Protein changes in response to progressive water deficit in maize. Plant Physiol 117:1253–1263.CrossRefGoogle ScholarPubMed
Riechers, D. E., Zhang, Q., Xu, F., and Vaughn, K. C. 2003. Tissue-specific expression and localization of safener-induced glutathione S-transferase proteins in Triticum tauschii . Planta 217:831–840.Google Scholar
Ritchie, S. W., Hanway, J. J., Thompson, H. E., and Benson, G. O. 1997. How a Soybean Plant Develops. Ames, IA: Iowa State University Special Rep. 53. 20 p.Google Scholar
Romero-Puertas, M. C., McCarthy, I., Gomez, M., Sandalio, L. M., Corpas, F. J., Del Rio, L. A., and Palma, J. M. 2004. Reactive oxygen species-mediated enzymatic systems involved in the oxidative action of 2,4-dichlorophenoxyacetic acid. Plant Cell Environ 27:1135–1148.Google Scholar
Roux, C. and Perrot-Rechenmann, C. 1997. Isolation by differential display and characterization of a tobacco auxin-responsive cDNA Nt-gh3, related to GH3 . FEBS Lett 419:131–136.Google Scholar
Rubtsova, M. Y., Wittmann, C., Egorov, A. M., and Schmid, R. D. 1997. Chemiluminescent immunoassay: application of a portable scanning luminometer for the determination of 2,4-dichlorophenoxyacetic acid in microtiter and membrane strip format. Food Agric. Immunol 9:235–247.Google Scholar
Sawa, S., Ohgishi, M., Goda, H., Higuchi, K., Shimada, Y., Yoshida, S., and Koshiba, T. 2002. The HAT2 gene, a member of the HD-Zip gene family, isolated as an auxin-inducible gene by DNA microarray screening, affects auxin response in Arabidopsis . Plant J 32:1011–1022.Google Scholar
Singh, M. and Singh, R. P. 1996. Factors affecting detection of PVY in dormant tubers by reverse transcription polymerase chain reaction and nucleic acid spot hybridization. J. Virol. Methods 60:47–57.Google Scholar
Singh, R. P., Nie, X., Singh, M., Coffin, R., and Duplessis, P. 2002. Sodium sulphite inhibition of potato and cherry polyphenolics in nucleic acid extraction for virus detection by RT-PCR. J. Virol. Methods 99:123–131.Google Scholar
Staswick, P. E., Serban, B., Rowe, M., Tiryaki, I., Maldonado, M. T., Maldonado, M. C., and Suza, W. 2005. Characterization of an Arabidopsis enzyme family that conjugates amino acids to indole-3-acetic acid. Plant Cell 17:616–627.Google Scholar
Tian, Q., Uhlir, N. J., and Reed, J. W. 2002. Arabidopsis SHY2/IAA3 inhibits auxin-regulated gene expression. Plant Cell 14:301–319.Google Scholar
Tsang, E. W. T., Bowler, C., Herouart, D., Van Camp, W., Villarroel, R., Genetello, C., Van Montagu, M., and Inze, D. 1991. Differential regulation of superoxide dismutases in plants exposed to environmental stress. Plant Cell 3:783–792.Google ScholarPubMed
Tuteja, J. H., Clough, S. J., Chin, W-C., and Vodkin, L. O. 2004. Tissue specific gene silencing mediated by a naturally occurring chalcone synthase gene cluster in (Glycine max). Plant Cell 16:819–835.Google Scholar
Umezawa, T., Mizuno, K., and Fujimura, T. 2002. Discrimination of genes expressed in response to the ionic or osmotic effect of salt stress in soybean with cDNA-AFLP. Plant Cell Environ 25:1617–1625.Google Scholar
Valenzuela-Valenzuela, J. M., Lownds, N. K., and Sterling, T. M. 2001. Clopyralid uptake, translocation, metabolism, and ethylene induction in picloram-resistant yellow starthistle (Centaurea solstitialis L). Pestic. Biochem. Physiol 71:11–19.Google Scholar
Walz, C., Giavalisco, P., Schad, M., Juenger, M., Klose, J., and Keh, J. 2004. Proteomics of curcurbit phloem exudate reveals a network of defense proteins. Phytochemistry 65:1795–1804.Google Scholar
Wax, L. M., Knuth, L. A., and Slife, F. W. 1969. Response of soybean to 2,4-D, dicamba, and picloram. Weed Sci 17:388–393.Google Scholar
Winicov, I. 1998. New molecular approaches to improving salt tolerance in crop plants. Anal. Bot 82:703–710.Google Scholar
Wright, R. M., Hagen, G., and Guilfoyle, T. 1987. An auxin-induced polypeptide in dicotyledonous plants. Plant Mol. Biol 9:625–634.Google Scholar
Yajima, W., Hall, J. C., and Kav, N. V. 2004. Proteome-level differences between auxinic herbicide–susceptible and –resistant wild mustard (Sinapis arvensis L). J. Agric. Food Chem 52:5063–5070.Google Scholar
Yao, R., Nimec, Z., Ryan, T. J., and Galivan, J. 1996. Identification, cloning, and sequencing of a cDNA coding for rat γ-glutamyl hydrolase. J. Biol. Chem 271:8525–8528.Google Scholar
Zheng, H. and Hall, J. C. 2001. Understanding auxinic herbicide resistance in wild mustard: physiological, biochemical, and molecular genetic approaches. Weed Sci 49:276–281.Google Scholar
Zhang, Q. and Riechers, D. E. 2004. Proteomic characterization of herbicide safener-induced proteins in the coleoptile of Triticum tauschii seedlings. Proteomics 4:2058–2071.Google Scholar