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Dicamba-responsive genes in herbicide-resistant and susceptible biotypes of kochia (Kochia scoparia)

Published online by Cambridge University Press:  20 January 2017

Anthony J. Kern ,
Marta E. Chaverra ,
Harwood J. Cranston  and
William E. Dyer
Anthony J. Kern
Affiliation:
Department of Biology, Northland College, Ashland, WI 54806
Marta E. Chaverra
Affiliation:
Department of Cell Biology and Neuroscience, Montana State University–Bozeman, Bozeman, MT 59717-0312
Harwood J. Cranston
Affiliation:
Department of Cell Biology and Neuroscience, Montana State University–Bozeman, Bozeman, MT 59717-0312
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Abstract

The herbicide resistance to dicamba (HRd) biotype of kochia is resistant to several auxinic herbicides and is impaired in shoot gravitropism and other auxin-mediated responses. To better characterize the biotype and investigate its mechanism of resistance, we used messenger RNA (mRNA) differential display to compare patterns of dicamba-induced gene expression in HRd and susceptible (S1) plants. More than 60,000 complementary DNA fragments were generated and examined, 106 of which were isolated and used as probes on Northern blots to confirm gene expression levels. Steady-state levels of > 90% of mRNAs did not change after dicamba application. However, several mRNAs were detected whose levels were decreased, increased, or differentially regulated between the biotypes within minutes of dicamba treatment. The abundance of three mRNAs decreased after treatment, two of which had significant sequence similarity to choline monooxygenase and 5,10-methylenetetrahydrofolate reductase, respectively. Conversely, increased expression levels were observed for a putative chloride channel protein, 1-aminocyclopropane-1-carboxylate synthase, and an unknown gene. Genes differentially expressed between HRd and S1 plants included those similar to a putative translation initiation factor, xyloglucan endotransglycosylase, and a hypothetical protein cloned from several organisms. The results demonstrate that mRNA differential display is a useful technique for discovering genes that are rapidly regulated as part of a physiological response, and that this approach may provide insight into the mechanism of auxinic herbicide resistance in kochia.

Keywords

Dicambakochia, Kochia scoparia L. Schrad. KCHSCAuxinic herbicidedifferential displaygene expressionherbicide resistance
Type
Physiology, Chemistry, and Biochemistry
Information
Weed Science , Volume 53 , Issue 2 , April 2005 , pp. 139 - 145
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Altschul, S. F., Madden, T. L., Schäffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402.CrossRefGoogle ScholarPubMed
Assman, S. M. 1993. The guard cell-environment connection. Plant Physiol 102:711–715.Google Scholar
Ausubel, F. M., Brent, R., Kingston, R. E., Moore, D. D., Seidman, J. G., Smith, J. A., and Struhl, K. 1987. Current Protocols in Molecular Biology. New York: J. Wiley. Pp. 4.3.1–4.3.3.Google Scholar
Babourina, O., Shabala, S., and Newman, I. 1998. Auxin stimulates Cl− uptake by oat coleoptiles. Ann. Bot 82:331–336.Google Scholar
Botella, J. R., Arteca, J. M., Schlagnhaufer, C. D., Arteca, R. N., and Phillips, A. T. 1992. Identification and characterization of a full-length cDNA encoding for an auxin-induced 1-aminocyclopropane-1-carboxylate synthase from etiolated mung bean hypocotyl segments and expression of its mRNA in response to indole-3-acetic acid. Plant Mol. Biol 20:425–436.Google Scholar
Bourdôt, G. W., Hurrell, G. A., and Saville, D. J. 1990. Variation in MCPA-resistance in Ranunculus acris L. subsp. acris and its correlation with historical exposure to MCPA. Weed Res 30:449–457.Google Scholar
Chan, K. L., New, D., Ghandhi, S., Wong, F., Lam, C. M. C., and Wong, J. T. Y. 2002. Transcript levels of the eukaryotic translation initiation factor 5A gene peak at early G1 phase of the cell cycle in the dinoflagellate Crypthecodinium cohnii . Appl. Environ. Microbiol 68:2278–2284.Google Scholar
Coupland, D., Cooke, D. T., and James, C. S. 1991. Effects of 4-chloro-2-methylphenoxypropionate (an auxin analogue) on plasma membrane ATPase activity in herbicide-resistant and herbicide-susceptible biotoypes of Stellaria media L. J. Exp. Bot 42:1065–1071.CrossRefGoogle Scholar
Coupland, D. and Jackson, M. B. 1991. Effects of mecoprop (an auxin analogue) on ethylene evolution and epinasty in two biotypes of Stellaria media . Ann. Bot 68:167–172.CrossRefGoogle Scholar
Cox, K., Robertson, D., and Fites, R. 1999. Mapping and expression of a bifunctional thymidylate synthase, dihydrofolate reductase gene from maize. Plant Mol. Biol 41:733–739.Google Scholar
Cranston, H. J., Kern, A. J., Hackett, J. L., Miller, E. K., Maxwell, B. D., and Dyer, W. E. 2001. Dicamba resistance in kochia. Weed Sci 49:164–170.Google Scholar
Dargeviciute, A., Roux, C., Decreux, A., Sitbon, F., and Perrot-Rechenmann, C. 1998. Molecular cloning and expression of the early auxin-responsive Aux/IAA gene family in Nicotiana tabacum . Plant Cell Physiol 39:993–1002.CrossRefGoogle ScholarPubMed
Datta, N., LaFayette, P. R., Kroner, P. A., Nagao, R. T., and Key, J. 1993. Isolation and characterization of three families of auxin down-regulated cDNA clones. Plant Mol. Biol 21:859–869.Google Scholar
Delbarre, A., Muller, P., Imhoff, V., and Guern, J. 1996. Comparisons of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta 198:532–541.Google Scholar
Devine, M., Duke, S. O., and Fedtke, C. 1993. Physiology of Herbicide Action. Eaglewood Cliffs, NJ: Prentice Hall. 441 p.Google Scholar
Fuerst, E. P., Sterling, T. M., Norman, M. A., Prather, T. S., Irzyk, G. P., Wu, Y., Lownds, N. K., and Callihan, R. H. 1996. Physiological characterization of picloram resistance in yellow starthistle. Pestic. Biochem. Physiol 56:149–161.CrossRefGoogle 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.CrossRefGoogle Scholar
Grossmann, K. 2000. Mode of action of auxin herbicides: a new ending to a long, drawn out story. Trends Plant Sci 5:506–508.CrossRefGoogle ScholarPubMed
Haas, B. J., Volfovsky, N., Town, C. D., Troukhan, M., Alexandrov, N., Feldmann, K. A., Flavell, R. B., White, O., and Salzberg, S. L. 2002. Full-length messenger RNA sequences greatly improve genome annotation. Genome Biol. 3(6):RESEARCH0029. Epub 2002 May 30.Google Scholar
Hajouj, T., Michelis, R., and Gepstein, S. 2000. Cloning and characterization of a receptor-like protein kinase gene associated with senescence. Plant Physiol 124:1305–1314.CrossRefGoogle ScholarPubMed
Hall, J. C., Alan, S. M. M., and Murr, D. P. 1993. Ethylene biosynthesis following foliar application of picloram to biotypes of wild mustard (Sinapsis arvensis L.) susceptible or resistant to auxinic herbicides. Pestic. Biochem. Physiol 47:36–43.CrossRefGoogle Scholar
Hall, J. C. and Romano, M. L. 1995. Morphological and physiological differences between susceptible (S) and resistant (R) wild mustard (Sinapis arvensis) biotypes. Pestic. Biochem. Physiol 52:149–155.Google Scholar
Heap, I. and Morrison, I. N. 1992. Resistance to auxin-type herbicides in wild mustard (Sinapis arvensis L.) populations in western Canada. Weed Sci. Soc. Am. Abstr 32:164.Google Scholar
Henskens, J. A. M., Rouwendal, G. J. A., Have, A. T., and Woltering, E. J. 1994. Molecular cloning of two different ACC synthase PCR fragments in carnation flowers and organ-specific expression of the corresponding genes. Plant Mol. Biol 26:453–458.Google Scholar
Hutchison, K. W., Singer, P. B., McInnis, S., Diaz, S. C., and Greenwood, M. S. 1999. Expansins are conserved in conifers and expressed in hypocotyls in response to exogenous auxin. Plant Physiol 120:827–831.Google Scholar
Iwahara, M., Saito, T., Ishida, S., Takahashi, Y., and Nagata, T. 1998. Isolation and characterization of a cytokinin up-regulated gene from tobacco mesophyll protoplasts. Plant Cell Physiol 39:859–864.CrossRefGoogle ScholarPubMed
Jasieniuk, M., Brûle-Babel, A. L., and Morrison, I. N. 1996. The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:176–193.CrossRefGoogle Scholar
Johnson, R. R., Cranston, H. J., Chaverra, M. E., and Dyer, W. E. 1995. Screening for differentially expressed genes in dormant and nondormant A. fatua embryos. Plant Mol. Biol 28:113–122.CrossRefGoogle Scholar
Keller, C. P. and van Volkenburgh, E. 1996. The electrical response of Avena coleoptiles to auxins: evidence in vivo for activation of a Cl− conductance. Planta 198:404–412.Google Scholar
Kern, A. J. and Dyer, W. E. 2003. Glycine betaine biosynthesis is induced by salt stress but repressed by auxinic herbicides in Kochia scoparia . J. Plant Growth Regul 23:9–19.Google Scholar
Kim, W. T., Silverstone, A., Yip, W. K., Dong, J. G., and Yang, S. F. 1992. Induction of 1-aminocyclopropane-1-carboxylate synthase mRNA by auxin in mung bean hypocotyls and cultured apple shoots. Plant Physiol 98:465–471.Google Scholar
LeBaron, H. M. 1991. Distribution and seriousness of herbicide-resistant weed infestations worldwide. Pages 27–43 in Caseley, J. C., Cussans, G. W., and Atkins, R. K. eds. Herbicide Resistance in Weeds and Crops. Oxford, UK: Butterworth-Heinemann.Google Scholar
Leyser, O. 1997. Auxins: lessons from a mutant weed. Physiol. Plant 100:407–414.Google Scholar
Liang, Pl and Pardee, A. B. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257:967–971.Google Scholar
Lutman, P. J. W. and Snow, H. S. 1987. Further investigations into the resistance of chickweed (Stellaria media) to mecoprop. Proc. Br. Crop Prot. Conf. Weeds 3:901–908.Google Scholar
Migo, T. R., Mercado, B. L., and De Datta, S. K. 1986. Response of Sphenoclea zeylanica to 2,4-D and other recommended herbicides for weed control in lowland rice. Philipp. J. Weed Sci 13:28–38.Google Scholar
Miller, E. K., Myers, T. M., Hackett, J. L., and Dyer, W. E. 1997. Dicamba resistance in kochia (Kochia scoparia L. Schrad): preliminary studies. Proc. West. Soc. Weed Sci 50:81.Google Scholar
Mulugeta, D. 1991. Management, Inheritance, and Gene Flow of Resistance to Chlorsulfuron in Kochia scoparia L. (Schrad). , Montana State University, Bozeman, MT. 134 p.Google Scholar
Nakamura, T., Ishitani, M., Harinasut, P., Nomura, M., Takabe, T., and Takabe, T. 1996. Distribution of glycinebetaine in old and young leaf blades of salt-stressed barley plants. Plant Cell Physiol 37:873–877.Google Scholar
Olson, D. C., Oetiker, J. H., and Yang, S. F. 1995. Analysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants. J. Biol. Chem 270:14056–14061.Google Scholar
Peck, S. C. and Kende, H. 1995. Sequential induction of ethylene biosynthetic enzymes by indole-3-acetic acid in etiolated peas. Plant Mol. Biol 28:293–301.Google Scholar
Peniuk, M. G., Romano, M. L., and Hall, J. C. 1993. Absorption, translocation, and metabolism are not the basis for differential selectivity of wild mustard (Sinapis arvensis L.) to auxinic herbicides. Weed Sci. Soc. Am. Abstr 32:55.Google Scholar
Rathinasabapathi, B., Burnet, M., Russell, B. L., Gage, D. A., Liao, P. C., Nye, G. J., Scott, P., Golbeck, J. H., and Hanson, A. D. 1997. Choline monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc. Natl. Acad. Sci. USA 94:3454–3458.Google Scholar
Rubinstein, B. and Light, E. N. 1973. Indoleacetic-acid-enhanced chloride uptake into coleoptile cells. Planta 110:43–56.Google Scholar
Russell, B. L., Rathinasabapathi, B., and Hanson, A. D. 1998. Osmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol 116:859–865.Google Scholar
Sambrook, J., Fritsch, E. F., and Maniatis, T. 1989. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press. 863 p.Google Scholar
Sterling, T. M. and Hall, J. C. 1997. Mechanism of action of natural auxins and the auxinic herbicides. Pages 205–263 in Roe, R. M., Burton, J. D., and Kuhr, R. J. eds. Herbicide Activity: Toxicology, Biochemistry, and Molecular Biology. Amsterdam, The Netherlands: IOS.Google Scholar
Trebitsh, T., Staub, J. E., and O'Neill, S. D. 1997. Identification of a 1-aminocyclopropane-1-carboxylic acid synthase gene linked to the Female (F) locus that enhances female sex expression in cucumber. Plant Physiol 113:987–995.CrossRefGoogle Scholar
van der Straeten, D., Rodrigues-Pousada, R. A., Villarroel, R., Hanley, S., Goodman, H. M., and van Montagu, M. 1992. Cloning, genetic mapping, and expression analysis of an Arabidopsis thaliana gene that encodes 1-aminocyclopropane-1-carboxylate synthase. Proc. Natl. Acad. Sci. USA 89:9969–9973.Google Scholar
van der Zaal, E. J., Droog, F. N., Boot, C. J. M., Hensgens, L. A., Hoge, J. H., Schilperoort, R. A., and Libbenga, K. R. 1991. Promoters of auxin-induced genes from tobacco can lead to auxin-inducible and root tip-specific expression. Plant Mol. Biol 16:983–998.Google Scholar
Walden, R. and Lubenow, H. 1996. Genetic dissection of auxin action: more questions than answers? Trends Plant Sci 1:335–339.Google Scholar
Wang, T. W. and Arteca, R. N. 1995. Identification and characterization of cDNAs encoding ethylene biosynthetic enzymes from Pelargonium × hortorum cv snow mass leaves. Plant Physiol 109:627–636.CrossRefGoogle ScholarPubMed
Xu, W., Purugganan, M. M., Polisensky, D. H., Antosiewicz, D. M., Fry, S. C., and Braam, J. 1995. Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycosylase. Plant Cell 7:1555–1567.Google Scholar
Yancey, P. H. 1994. Compatible and counteracting solutes. Pages 81–109 in Strange, K. ed. Cellular and Molecular Physiology of Cell Volume Regulation. Boca Raton, FL: CRC.Google Scholar
Yoon, I. S., Mori, H., Kim, J. H., Kang, B. G., and Imaseki, H. 1997. VR-ACS6 is an auxin-inducible 1-aminocyclopropane-1-carboxylate synthase gene in mungbean (Vigna radiata). Plant Cell Physiol 38:217–224.Google Scholar
Yoshida, S., Ito, M., Nishida, I., and Watanabe, A. 2001. Isolation and RNA gel blot analysis of genes that could serve as potential molecular markers for leaf senescence in Arabidopsis thaliana . Plant Cell Physiol 42:170–178.CrossRefGoogle ScholarPubMed
Zegzouti, H., Jones, B., Frasse, P., Marty, C., Maitre, B., Latche, A., Pech, J. C., and Bouzayen, M. 1999. Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening-related genes isolated by differential display. Plant J 18:589–600.CrossRefGoogle ScholarPubMed
Zegzouti, H., Marty, C., Jones, B., Bouquin, T., Latche, A., Pech, J. C., and Bouzayen, M. 1997. Improved screening of cDNAs generated by mRNA differential display enables the selection of true positives and the isolation of weakly expressed messages. Plant Mol. Biol. Rep 15:236–245.Google Scholar
Zheng, H. G. and Hall, J. C. 2001. Understanding auxinic herbicide resistance in wild mustard: physiological, biochemical, and molecular genetic approaches. Weed Sci 49:276–281.CrossRefGoogle Scholar