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Glycine Betaine Biosynthesis Is Induced by Salt Stress but Repressed by Auxinic Herbicides in Kochia scoparia.

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Abstract

Kochia scoparia biotypes that are susceptible or resistant to the auxinic herbicide dicamba were used to characterize expression levels of choline monooxygenase (CMO) and glycine betaine accumulation in response to salt stress and herbicide treatment. A 1180-bp cDNA was isolated using differential display and 3′ RACE with a deduced amino acid sequence that was more than 90% similar to the carboxy terminal 290 residues of CMOs from four related plant species. Salt stress led to a substantial increase in CMO mRNA and enzyme levels in K. scoparia biotypes, and the accumulation of up to 80 μmol g−1 fresh weight glycine betaine. In contrast, dicamba treatment was followed by the rapid attenuation of CMO message and protein levels, with a recovery of expression in the resistant but not the susceptible biotype. CMO mRNA and enzyme levels similarly declined, and recovered in the resistant biotype, after dicamba treatment of plants that were previously salt stressed for 4 days. The opposing effects of these two stresses may represent a regulatory scheme in which competition for the substrate choline leads to a repression of glycine betaine biosynthesis to make sufficient choline available for auxin-mediated growth processes.

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References

  1. SF Altschul TL Madden AA Schäffer J Zhang Z Zhang W Miller DJ Lipman (1997) ArticleTitleGapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 3389–3402 Occurrence Handle10.1093/nar/25.17.3389 Occurrence Handle1:CAS:528:DyaK2sXlvFyhu7w%3D Occurrence Handle9254694

    Article  CAS  PubMed  Google Scholar 

  2. FM Ashton AS Crafts (1981) Mode of Action of Herbicides, EditionNumber2nd Ed John Wiley and Sons New York 525

    Google Scholar 

  3. FM Ausubel R Brent RE Kingston DD Moore JG Seidman JA Smith K Struhl (1987) Current Protocols in Molecular Biology. John Wiley and Sons New York

    Google Scholar 

  4. DA Becker (1978) ArticleTitleStem abscission in tumbleweeds of the Chenopodiaceae: Kochia. Amer. J. Bot. 65 375–383

    Google Scholar 

  5. S Berger E Bell A Sadka JE Mullet (1995) ArticleTitleArabidopsis thaliana Atvsp is homologous to soybean VspA and VspB, genes encoding vegetative storage protein acid phosphatases and is regulated similarly by methyl jasmonate, wounding, sugars, light and phosphate. Plant Mol. Biol. 27 933–942 Occurrence Handle1:CAS:528:DyaK2MXmtFSgsL8%3D Occurrence Handle7766883

    CAS  PubMed  Google Scholar 

  6. HJ Bohnert P Ayoubi C Borchert RA Bressan RL Burnap JC Cushman MA Cushman M Deyholos R Fischer DW Galbraith PM Hasegawa M Jenks S Kawasaki H Koiwa S Koreeda BH Lee CB Michalowski E Misawa M Nomura N Ozturk B Postier R Prade CP Song Y Tanaka H Wang JK Zhu (2001) ArticleTitleA genomics approach towards salt stress tolerance. Plant Physiol. Biochem. 39 295–311 Occurrence Handle10.1016/S0981-9428(00)01237-7 Occurrence Handle1:CAS:528:DC%2BD3MXjtFajsL4%3D

    Article  CAS  Google Scholar 

  7. MM Bradford (1976) ArticleTitleA rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Anal. Biochem 72 248–254 Occurrence Handle10.1006/abio.1976.9999 Occurrence Handle1:CAS:528:DyaE28XksVehtrY%3D Occurrence Handle942051

    Article  CAS  PubMed  Google Scholar 

  8. M Burnet PJ Lafontaine AD Hanson (1995) ArticleTitleAssay, purification, and partial characterization of choline monooxygenase from spinach. Plant Physiol. 108 581–588 Occurrence Handle1:CAS:528:DyaK2MXmtlaqsr4%3D Occurrence Handle12228495

    CAS  PubMed  Google Scholar 

  9. C Catala JKC Rose WS York PS William P Albersheim AG Darvill AB Bennett (2001) ArticleTitleCharacterization of a tomato xyloglucan endotransglycosylase gene that is down-regulated by auxin in etiolated hypocotyls. Plant Physiol. 127 1180–1192 Occurrence Handle10.1104/pp.127.3.1180 Occurrence Handle1:CAS:528:DC%2BD3MXos1Kmtr8%3D Occurrence Handle11706197

    Article  CAS  PubMed  Google Scholar 

  10. HJ Cranston AJ Kern JL Hackett EK Miller BD Maxwell WE Dyer (2001) ArticleTitleDicamba resistance in kochia. Weed Sci. 49 164–170 Occurrence Handle1:CAS:528:DC%2BD3MXlsVejtL4%3D

    CAS  Google Scholar 

  11. N Datta PR LaFayette PA Kroner RT Nagao J Key (1993) ArticleTitleIsolation and characterization of three families of auxin down-regulated cDNA clones. Plant Mol. Biol. 21 859–869 Occurrence Handle1:CAS:528:DyaK3sXkt1Wqt7Y%3D Occurrence Handle8096772

    CAS  PubMed  Google Scholar 

  12. SR Downie DS Katz-Downie KJ Cho (1997) ArticleTitleRelationships in the Caryophyllales as suggested by phylogenetic analyses of partial chloroplast DNA ORF2280 homolog sequences. Am. J. Bot. 84 253–273 Occurrence Handle1:CAS:528:DyaK2sXhvVygtbs%3D

    CAS  Google Scholar 

  13. RM Durham JW Durham (1979) Kochia: Its potential for forage production. Proceedings, Arid Land Plant Resource. J. R. Goodin D. K. Northington (Eds) . International Center for Arid and Semi Arid Land Studies . 443–451

    Google Scholar 

  14. CV Eberlein ZQ Fore (1984) ArticleTitleKochia biology. Weeds Today 15 5–6

    Google Scholar 

  15. TWM Fan TD Colmer AN Lane RM Higashi (1993) ArticleTitleDetermination of metabolites by proton NMR and GC: Analysis for organic osmolytes in crude tissue extracts. Anal. Biochem. 214 260–271 Occurrence Handle10.1006/abio.1993.1486 Occurrence Handle1:CAS:528:DyaK3sXms1Gqsrw%3D Occurrence Handle8250233

    Article  CAS  PubMed  Google Scholar 

  16. PJ Franks GD Farquhar (2001) ArticleTitleThe effect of exogenous abscisic acid on stomatal development, stomatal mechanics, and leaf gas exchange in Tradescantia virginiana. Plant Physiol. 125 935–942 Occurrence Handle10.1104/pp.125.2.935 Occurrence Handle1:CAS:528:DC%2BD3MXhs1Kltrg%3D Occurrence Handle11161050

    Article  CAS  PubMed  Google Scholar 

  17. CM Grieve EV Maas (1984) ArticleTitleBetaine accumulation in salt-stressed sorghum. Physiol. Plant. 61 167–171 Occurrence Handle1:CAS:528:DyaL2cXks12lsLk%3D

    CAS  Google Scholar 

  18. RD Guy PG Warne D Reid (1984) ArticleTitleGlycinebetaine content of halophytes: improved analysis by liquid chromatography and interpretation of results. Physiol. Plant. 61 195–202 Occurrence Handle1:CAS:528:DyaL2cXks12gu7k%3D

    CAS  Google Scholar 

  19. AD Hanson D Rhodes (1983) ArticleTitle14 C tracer evidence for synthesis of choline and betaine via phosphoryl base intermediates in salinized sugarbeet leaves. Plant Physiol. 71 692–700 Occurrence Handle1:CAS:528:DyaL3sXhvFGjsbo%3D

    CAS  Google Scholar 

  20. CL Hitchcock A Cronquist M Ownbey JW Thompson (1964) Vascular Plants of the Pacific Northwest. Part 2. Salicaceae to Saxifragacae. University of Washington Press Seattle

    Google Scholar 

  21. M Ishitani T Nakamura SY Han T Takabe (1995) ArticleTitleExpression of the betaine aldehyde dehydrogenase gene in barley in response to osmotic stress and abscisic acid. Plant Mol. Biol. 27 307–315 Occurrence Handle1:CAS:528:DyaK2MXkt1Kgs78%3D Occurrence Handle7888620

    CAS  PubMed  Google Scholar 

  22. SE Jacobsen NE Olszewski (1996) ArticleTitleGibberellins regulate the abundance of RNAs with sequence similarity to proteinase inhibitors, dioxygenases, and dehydrogenases. Planta 198 78–86 Occurrence Handle1:CAS:528:DyaK2MXhtVSntbrP Occurrence Handle8580773

    CAS  PubMed  Google Scholar 

  23. RK Jain N Saini S Jain (2003) ArticleTitleEngineering salinity tolerance in crop plants: A reality. Physiol. Mol. Biol. Plants. 9 29–39

    Google Scholar 

  24. AB Jensen PK Busk M Figueras MM Alba G Peracchia R Messeguer A Goday M Pages MM Alba E Belhassen (1996) ArticleTitleDrought signal transduction in plants. J. Plant Growth Reg. 20 105–110 Occurrence Handle1:CAS:528:DyaK2sXlsVClsw%3D%3D

    CAS  Google Scholar 

  25. H Jiang RE Parales NA Lynch DT Gibson (1996) ArticleTitleSite-directed mutagenesis of conserved amino acids in the alpha subunit of toluene dioxygenase: potential mononuclear non-heme iron coordination sites. J. Bacteriol. 178 3133–3139 Occurrence Handle1:CAS:528:DyaK28Xjt1Kmtb4%3D Occurrence Handle8655491

    CAS  PubMed  Google Scholar 

  26. Kern AJ. 2002. Characterization of gene expression patterns and regulation of choline monooxygenase in dicamba-resistant and susceptible Kochia scoparia. Ph.D. Dissertation. Montana State University-Bozeman. 265 pp.

  27. JA Kreps Y Wu HS Chang T Zhu X Wang JF Harper (2002) ArticleTitleTranscriptome changes for Arabidopsis in response to salt, osmotic, and cold stress. Plant Physiol. 130 2129–2141 Occurrence Handle10.1104/pp.008532 Occurrence Handle1:CAS:528:DC%2BD3sXktlym Occurrence Handle12481097

    Article  CAS  PubMed  Google Scholar 

  28. J Legaria R Rajisbaum RA Munoz-Clares N Villegas-Sepulveda J Simpson G Iturriaga (1998) ArticleTitleMolecular characterization of two genes encoding betaine aldehyde dehydrogenase from amaranth. Expression in leaves under short-term exposure to osmotic stress or abscisic acid. Gene 218 69–76 Occurrence Handle10.1016/S0378-1119(98)00381-3 Occurrence Handle1:CAS:528:DyaK1cXmsFKrtb4%3D Occurrence Handle9751804

    Article  CAS  PubMed  Google Scholar 

  29. A Maggio S Miyazaki P Veronese T Fujita JI Ibeas B Damsz ML Narasimhan PM Hasegawa RJ Joly RA Bressan (2002) ArticleTitleDoes proline accumulation play an active role in stress-induced growth reduction? Plant J. 31 699–712 Occurrence Handle10.1046/j.1365-313X.2002.01389.x Occurrence Handle1:CAS:528:DC%2BD38XotFyjsLY%3D Occurrence Handle12220262

    Article  CAS  PubMed  Google Scholar 

  30. EK Miller TM Myers LJ Hackett WE Dyer (1997) ArticleTitleDicamba resistance in kochia (Kochia Scoparia L. Schrad): Preliminary studies. Proc. West. Soc. Weed Sci. 50 81

    Google Scholar 

  31. Mulugeta D. 1991. Management, inheritance, and gene flow of resistance to chlorsulfuron in Kochia scoparia L. (Schrad). M.S. Thesis, Montana State University, Bozeman. 134 pp.

  32. ML Nuccio BL Russell KD Nolte B Bathinasabapathi DA Gage AD Hanson (1998) ArticleTitleThe endogenous choline supply limits glycine betaine synthesis in transgenic tobacco expressing choline monooxygenase. Plant J. 16 487–496 Occurrence Handle10.1046/j.1365-313x.1998.00316.x Occurrence Handle1:CAS:528:DyaK1MXitVentw%3D%3D Occurrence Handle9881168

    Article  CAS  PubMed  Google Scholar 

  33. Y Ozeki A Komamine Y Tanaka (1990) ArticleTitleInduction and repression of phenylalanine ammonia-lyase and chalcone synthase enzyme proteins and mRNA in carrot cell suspension cultures regulated by 2,4-D. Physiol. Plant. 78 400–408 Occurrence Handle10.1034/j.1399-3054.1990.780314.x Occurrence Handle1:CAS:528:DyaK3cXitlamtLo%3D

    Article  CAS  Google Scholar 

  34. GC Papageorgiou N Murata (1995) ArticleTitleThe unusually strong stabilizing effects of glycine betaine on the structure and function of the oxygen-evolving photosystem II complex. Photosynthesis Res. 44 243–252 Occurrence Handle1:CAS:528:DyaK2MXnvVeiurk%3D

    CAS  Google Scholar 

  35. G Pasquali OJM Goddijn A Waal Particlede R Verpoorte RA Schilperoort HJC Hoge J Memelink (1992) ArticleTitleCoordinated regulation of two indole alkaloid biosynthetic genes from Catharanthus roseus by auxin and elicitors. Plant Mol. Biol. 18 1121–1131 Occurrence Handle1:CAS:528:DyaK3sXitlShs7o%3D Occurrence Handle1600148

    CAS  PubMed  Google Scholar 

  36. MM Primiani JC Cotterman LL Saari (1990) ArticleTitleResistance of Kochia scoparia to sulfonylurea and imidazolinone herbicides. Weed Technol. 4 169–172 Occurrence Handle1:CAS:528:DyaK3cXktVWqtLo%3D

    CAS  Google Scholar 

  37. B Rathinasabapathi M Burnet BL Russell DA Gage PC Liao GJ Nye P Scott JH Golbeck AD Hanson (1997) ArticleTitleCholine monooxygenase, an unusual iron-sulfur enzyme catalyzing the first step of glycine betaine synthesis in plants: prosthetic group characterization and cDNA cloning. Proc. Nat. Acad. Sci. (USA) 94 3454–3458 Occurrence Handle10.1073/pnas.94.7.3454 Occurrence Handle1:CAS:528:DyaK2sXisVKnsLw%3D

    Article  CAS  Google Scholar 

  38. D Rhodes AD Hanson (1993) ArticleTitleQuaternary ammonium and tertiary sulfonium compounds in higher plants. Ann. Rev. Plant Physiol. Plant Mol. Biol. 44 357–384 Occurrence Handle10.1146/annurev.pp.44.060193.002041 Occurrence Handle1:CAS:528:DyaK3sXltlGmtr8%3D

    Article  CAS  Google Scholar 

  39. BL Russell B Rathinasabapathi AD Hanson (1998) ArticleTitleOsmotic stress induces expression of choline monooxygenase in sugar beet and amaranth. Plant Physiol. 116 859–865 Occurrence Handle10.1104/pp.116.2.859 Occurrence Handle1:CAS:528:DyaK1cXht1aisLo%3D Occurrence Handle9489025

    Article  CAS  PubMed  Google Scholar 

  40. A Sakamoto N Murata (2000) ArticleTitleGenetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance. J. Exp. Bot. 51 81–88 Occurrence Handle10.1093/jexbot/51.342.81 Occurrence Handle1:CAS:528:DC%2BD3cXpslKjtQ%3D%3D Occurrence Handle10938798

    Article  CAS  PubMed  Google Scholar 

  41. GH Salekdeh J Siopongco LJ Wade B Ghareyazie J Bennett (2002) ArticleTitleA proteomic approach to analyzing drought- and salt-responsiveness in rice. Field Crops Res. 76 199–219 Occurrence Handle10.1016/S0378-4290(02)00040-0

    Article  Google Scholar 

  42. J Sambrook EF Fritsch T Maniatis (1989) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Laboratory Press Cold Spring Harbor, New York

    Google Scholar 

  43. G Selvaraj RK Jain DJ Olson R Hirjl S Jana LR Hogge (1995) ArticleTitleGlycinebetaine in oilseed rape and flax leaves: Detection by liquid chromatography/continous flow secondary ion-massspectrometry. Phytochem. 38 1143–1146 Occurrence Handle10.1016/0031-9422(94)00758-L Occurrence Handle1:CAS:528:DyaK2MXlsVGqsb0%3D

    Article  CAS  Google Scholar 

  44. DL Swofford (2002) PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates Sunderland, Massachusetts

    Google Scholar 

  45. R Vögelie-Lange C Fründt CM Hart F Nagy F Meins (1994) ArticleTitleDevelopmental, hormonal, and pathogenesis-related regulation of the tobacco class 1 β-1, 3-glucanase B promoter. Plant Mol. Biol. 25 299–311 Occurrence Handle8018877

    PubMed  Google Scholar 

  46. Y Wang YL Meng H Ishikawa T Hibino Y Tanaka N Nii T Takabe (1999) ArticleTitlePhotosynthetic adaptation to salt stress in three-color leaves of a C4 plant Amaranthus tricolor. Plant Cell Physiol. 40 668–674 Occurrence Handle1:CAS:528:DyaK1MXkvVarsbw%3D

    CAS  Google Scholar 

  47. EA Weretilnyk AD Hanson (1990) ArticleTitleMolecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought. Proc. Nat. Acad. Sci. (USA) 87 2745–2749 Occurrence Handle1:CAS:528:DyaK3cXksFent78%3D

    CAS  Google Scholar 

  48. AJ Wood H Saneoka D Rhodes RJ Joly PB Goldsbrough (1996) ArticleTitleBetaine aldehyde dehydrogenase in sorghum. Plant Physiol. 110 1301–1308 Occurrence Handle10.1104/pp.110.4.1301 Occurrence Handle1:CAS:528:DyaK28XitlWjtLw%3D Occurrence Handle8934627

    Article  CAS  PubMed  Google Scholar 

  49. PH Yancey (1994) Compatible and counteracting solutes. K Strange (Eds) Cellular and Molecular Physiology of Cell Volume Regulation. CRC Press Boca Raton, FL 81–109

    Google Scholar 

  50. X Yin Y Zhao D Luo H Zhang (2002) ArticleTitleIsolating the promoter of a stress-induced gene encoding betaine aldehyde dehydrogenase from the halophyte Atriplex centralasiatica Iljin. Biochim. Biophys. Acta. 1577 452–456 Occurrence Handle10.1016/S0167-4781(02)00495-5 Occurrence Handle1:CAS:528:DC%2BD38XnsVSmtb0%3D Occurrence Handle12359336

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Montana Department of Agriculture Noxious Weed Trust Fund and the Montana Agricultural Experiment Station and has been assigned Journal Series No. 2002-72. The excellent technical assistance of Dr. Scott Busse (for GB NMR), Christie Flechsenhar, and Tracey Meyers is gratefully acknowledged.

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  1. Anthony J. Kern

    Present address: Department of Biology, Northland College, Ashland, WI, 54806, USA

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  1. Department of Plant Sciences and Plant Pathology, Montana State University Bozeman, Bozeman, Montana, 59717-0312, USA

    Anthony J. Kern & William E. Dyer

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Kern, A.J., Dyer, W.E. Glycine Betaine Biosynthesis Is Induced by Salt Stress but Repressed by Auxinic Herbicides in Kochia scoparia.. J Plant Growth Regul 23, 9–19 (2004). https://doi.org/10.1007/s00344-003-0045-4

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