|
|
|
|
|
| Excessive ammonia inhibited transcription of MsU2 gene and furthermore affected accumulation distribution of allantoin and amino acids in alfalfa Medicago sativa |
| WANG Li, JIANG Lin-lin, Nomura Mika, Tajima Shigeyuki, CHENG Xian-guo |
1、College of Life Science, Shanxi Normal University, Linfen 041004, P.R.China
2、Key Laboratory of Plant Nutrition and Fertilizers, Agriculture of Ministry/Insititute of Agricultural Resources and Regional Planning,Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
3、Faculty of Agriculture, Kagawa University, 2393 Ikenobe, Miki-cho, Kita-gun, Kagawa, 761-0795, Japan |
|
|
|
摘要 In legume plants, uricase gene (Nodulin-35) plays a positive role in metabolism of ureide and amide compounds in symbiotic nitrogen-fixing in the nodules. In this study, a pot experiment was performed to examine the effects of ammonium application on the transcription of MsU2 gene and distribution of major nitrogen compounds in alfalfa Medicago sativa. Data showed that alfalfa plant has a significant difference in contents of nitrogen compounds in xylem saps compared with soybean plant, and belongs to typical amide type legume plants with little ureide accumulation, and the accumulation of asparagines and ureide in the tissues of alfalfa is mainly gathered in the nodules. Northern blotting showed that excessive ammonium significantly inhibited the transcription of MsU2 gene in the nodules and roots, and mRNA accumulation of MsU2 gene in the plants exposed to excessive ammonium decreased gradually with culture time extension, indicating that application of ammonium significantly inhibited the transcription of MsU2 gene in the alfalfa plants. Although the application of excessive ammonium increased the contents of amino acids in various tissues of alfalfa, the accumulation of allantoin reflecting the strength of uricase activity is remarkably reduced in the xylem saps, stems and nodules when alfalfa plants exposed to excessive ammonium, suggesting that application of excessive ammonium generated a negative effect on symbiosis fixing-nitrogen system due to inhibition of ammonium ion on uricase activity in the nodules of alfalfa. This result seems to imply that application of excessive ammonium in legume plants should not be proposed to avoid affecting the ability of fixing nitrogen in the nodules of legume plants, and reasonable dose of ammonium should be recommended to effectively utilize the fixed N from atmosphere in legume plant production.
Abstract In legume plants, uricase gene (Nodulin-35) plays a positive role in metabolism of ureide and amide compounds in symbiotic nitrogen-fixing in the nodules. In this study, a pot experiment was performed to examine the effects of ammonium application on the transcription of MsU2 gene and distribution of major nitrogen compounds in alfalfa Medicago sativa. Data showed that alfalfa plant has a significant difference in contents of nitrogen compounds in xylem saps compared with soybean plant, and belongs to typical amide type legume plants with little ureide accumulation, and the accumulation of asparagines and ureide in the tissues of alfalfa is mainly gathered in the nodules. Northern blotting showed that excessive ammonium significantly inhibited the transcription of MsU2 gene in the nodules and roots, and mRNA accumulation of MsU2 gene in the plants exposed to excessive ammonium decreased gradually with culture time extension, indicating that application of ammonium significantly inhibited the transcription of MsU2 gene in the alfalfa plants. Although the application of excessive ammonium increased the contents of amino acids in various tissues of alfalfa, the accumulation of allantoin reflecting the strength of uricase activity is remarkably reduced in the xylem saps, stems and nodules when alfalfa plants exposed to excessive ammonium, suggesting that application of excessive ammonium generated a negative effect on symbiosis fixing-nitrogen system due to inhibition of ammonium ion on uricase activity in the nodules of alfalfa. This result seems to imply that application of excessive ammonium in legume plants should not be proposed to avoid affecting the ability of fixing nitrogen in the nodules of legume plants, and reasonable dose of ammonium should be recommended to effectively utilize the fixed N from atmosphere in legume plant production.
|
|
Received: 11 August 2014
Accepted:
|
|
Corresponding Authors:
CHENG Xian-guo, Tel: +86-10-82105028, E-mail: chengxianguo@caas.cn
E-mail: chengxianguo@caas.cn
|
| About author: WANG Li, Mobile: +86-13593524238, E-mail: wangli11882003@
126.com; |
Cite this article:
WANG Li, JIANG Lin-lin, Nomura Mika, Tajima Shigeyuki, CHENG Xian-guo.
2015.
Excessive ammonia inhibited transcription of MsU2 gene and furthermore affected accumulation distribution of allantoin and amino acids in alfalfa Medicago sativa. Journal of Integrative Agriculture, 14(7): 1269-1282.
|
| Alamillo J M, Diaz-Leal J L, Sanchez-Moran M V, Pineda M.2010. Molecular analysis of ureide accumulation underdrought stress in Phaseolus vulgaris L. Plant, Cell andEnvironment, 33, 1828-1837Andrea K W, Claus-Peter W. 2011. The biochemistry of nitrogenmobilization: Purine ring catabolism. Trends in PlantScience, 16, 381-387Atkins C A. 1982. Ureide metabolism and the significanceof ureides in legumes. In: N S S Rao, ed., Advances inAgriculture. Microbiology. Oxford and IBH Publishing Co.,New Dehli, India. pp. 25-51Atkins C A, Smith P M, Storer P J. 1997. Reexamination ofthe intracellular localization of de novo purine synthesis incowpea nodules. Plant Physiology, 113, 127-135.Atkins C A, Smith P M C. 2000. Ureide synthesis in legumenodules. In: EJ Triplett, ed, Prokaryotic Nitrogen Fixation:A Model System for the Analysis of a Biological Process.Horizon Scientific Press, Wymondham, Norfolk, UK, pp.559-587Berger M G, Klaus R E, Fock H P. 1986. Assimilation of gaseousammonia by sunflower leaves during photosynthesis.Australian Journal of Plant Physiology, 13, 211-219Bisseling T, Ven den Bos R C, Kammen A V. 1978. The effectof ammonium nitrate on the synthesis of nitrogenase andthe concentration of leghaemoglobin in pea root nodulesinduced by Rhizobium leguminosarum. Biochimica etBiophysica Acta, 539, 1-11Brontonegoro S. 1974. Nitrogen fixation and nitrogenase activityof Azotobacter chroococuum. Communication AgricultureUniversity of Wagenningen, 74-10, 1–76Charlson D V, Korth K L, Purcell L C. 2009. Allantoateamidohydrolase transcript expression is independent ofdrought tolerance in soybean. Journal of ExperimentalBotany, 60, 847-851Cheng X G, Nomura M, Takane K, Kouchi H, Tajima S. 2000. Expression of two uricase (Nodulin-35) genes in a nonureidetype legume, Medicago sativa. Plant Cell Physiology,41, 104-109Christopher D T, Peter A T, Dale G B, Pedro P, Manuel P, Joe CP. 2006. Update on ureide degradation in legumes. Journalof Experimental Botany, 57, 5-12Claus-Peter W. 2011. Urea metabolism in plants. Plant Science,180, 431-438Day D A, Poole P S, Tyerman S D, Rosendahl L. 2001.Ammonia and amino acid transport across symbioticmembranes in nitrogen-fixing legume nodules. Journal ofCellular and Molecular Life Sciences, 58, 61-71Du H, Kim S, Hee K N, Lee M S, Son O, Lee S H , Cheon CI. 2010. Identification of uricase as a potential target ofplant thioredoxin: Implication in the regulation of noduledevelopment. Biochemical and Biophysical ResearchCommunications, 39, 722-726Erena G Q, Estíbaliz L A S, Juan L D, Josefa M A, Manuel P,Cesar A I, Stefanie W, Esther M G. 2013. Local inhibition ofnitrogen fixation and nodule metabolism in drought-stressedsoybean. Journal of Experimental Botany, 64, 2171-2182Francisco P, Akao S. 1993. The 2,4-D-induced wheat paranodulesare modified lateral roots with structure enhancedby rhizobial inoculation. Plant and Soil, 157, 121-129George T, Ladha J K, Buresh R J, Garrity D P. 1992. Managingnative and legume-fixed nitrogen in lowland rice-basedcropping systems. Plant and Soil, 141, 69-91Groat R G, Vance C P. 1981. Root nodule enzymes of ammoniaassimilation in alfalfa (Medicago sativa L.). Plant Physiology,67, 1198-1203Groat R G, Vance C P. 1982. Root and nodule enzymes ofammonia assimilation in two plant-conditioned symbioticallyineffective genotypes of alfalfa (Medicago sativa L.). PlantPhysiology, 69, 614-618Hélène C P, Anke F, Marcelo D, Karin S, Mechthild T. 2004.PvUPS1, an allantoin transporter in nodulated roots offrench bean. Plant Physiology, 134, 664-675Herridge D F. 1982. Use of the ureide technique to describethe nitrogen economy of field-grown soybeans. PlantPhysiology, 70, 7-11Herridge D F. 1984. Effects of nitrate and plant developmenton the abundance of nitrogenous solutes in root-bleedingand vacuum-extracted exudates in soybean. Crop Science.25, 173-179.Houwaard F. 1978. Influence of ammonium chloride onthe nitrogenase activity of nodulated pea plants (Pisumsativium). Applied and Environmental Microbiology, 35,1061-1065Jeudy C, Ruffel S, Freixes S, Tillard P, Santoni A L, Morel S,Journet E P, Duc G, Gojon A, Lepetit M, Salon C. 2010.Adaptation of Medicago truncatula to nitrogen limitation ismodulated via local and systemic nodule developmentalresponses. New Phytologist, 185, 817-828Juan L D L, Gregorio G V, Javier F, Manuel P, Josefa M A.2012. Developmental effects on ureide levels are mediatedby tissue-specific regulation of allantoinase in Phaseolusvulgaris L. Journal of Experimental Botany, 63, 4095-4106James W, Jurgen P, Euan K J, Philip P. 2007. Nutrient sharingbetween symbionts. Plant Physiology, 144, 604-614Kim K, Kim M I I, Chung J, Ahn J H, Rhee S. 2009. Crystalstructure of metal-dependent allantoinase from Escherichiacoli. Journal of Molecular Cell Biology, 387, 1067-1074King C A, Purcell L C. 2005. Inhibition of N2 fixation in soybeanis associated with elevated ureides and amino acids. PlantPhysiology, 137, 1389-1396Lanquar V, Loque D, Hormann F, Yuan L, Bohner A,Engelsberger W R, Lalonde S, Schulze W X, Von W N,Frommer W B. 2009. Feedback inhibition of ammoniumuptake by a phospho-dependent allosteric mechanism inArabidopsis. The Plant Cell, 21, 3610-3622Li Y, Richard P, David A D, Fraser J B. 2002. Reassessmentof major products of N2 fixation by bacteroids from soybeanroot nodules. Microbiology, 148, 1959-1966Ligero F, Caba J M, Lluch C, Olivares J. 1991. Nitrate inhibitionof nodulation can be overcome by the ethylene inhibitoraminoethoxyvinylglycine. Plant Physiology, 97, 1221-1225Lodwig E M, Hosie A H F, Bourdes A, Findlay K, Allaway D,Karunakaran R, Downie J A, Poole P S. 2003. Amino-acidcycling drives nitrogen fixation in the legume-Rhizobiumsymbiosis. Nature, 422, 722-726Lodwig E , Poole P. 2003. Metabolism of Rhizobium bacteroids.Critical Reviews in Plant Sciences, 22, 37-78Loqué D, von Wirén N. 2004. Regulatory levels for the transportof ammonium in plant roots. Journal of ExperimentalBiology, 55, 1293-1305McClure, P R, Israel D W. 1979. Transport of nitrogen in thexylem of soybean plants. Plant Physiology, 64, 411-416Modric N, Derome A E, Ashcroft S J H, Poje M. 1992. Tracingand identification of uricase reaction intermediates.Tetrahedron Letter, 33, 6691-6694Ohtake N, Nishiwaki T, Mizukoshi K, Minagawa R, TakahashiY, Chinushi T, Ohyama T. 1995. Amino acid compositionin xylem sap of soybean related to the evaluation of N2fixation by the relative ureide method. Soil Science andPlant Nutrition, 41, 95-102.Peter G, Carroll V. 2003. Nitrogen fixation in soils (Symbiotic).Encyclopedia of Environmental Microbiology, doi:10.1002/0471263397Pineda M, Fernandez E, Cardenas J. 1984. Urate oxidase ofChlamydomonas-reinhardii. Physiologia Plantarum, 62,453-457Ruffel S, Freixes S, Balzergue S, Tillard P, Jeudy C, Marie L MM, Margaretha J M, Klementina K, Jerôme G, Alisdair R F,Michael U, Christophe S, Alain G, Marc L. 2008. Systemicsignaling of the plant nitrogen status triggers specifictranscriptome responses depending on the nitrogen sourcein Medicago truncatula. Plant Physiololgy, 146, 2020-2035Sato T, Yashima H, Ohtake N, Sueyoshi K, Akao S, Harper JE and Ohyama T. 1998. Determination of leghemoglobincomponents and xylem sap composition by capillaryelectrophoresis in hypernodulation soybean mutantscultivated in the field. Soil Science and Plant Nutrition, 44, 635-645.Seiffert B, Ecke W, Lohaus G, Wallbraun M, Zhou Z, MollersC. 1999. Strategies for the Investigation of N-efficiencyin Oilseed Rape. In: G. Gissel-Nielsen, A. Jensen, eds.,Plant Nutrition—Molecular Biology and Genetics. KluwerAcademic Publishers: Dordrecht, The Netherlands. pp.425-432Senecoff J F, McKinney E C, Meagher R B. 1996. De novopurine synthesis in Arabidopsis thaliana. Plant Physiology,112, 905-917Serraj R, Vadez V, Denison R F, Sinclair T R. 1999. Involvementof ureide in nitrogen fixation inhibition in soybean. PlantPhysiology, 119, 289-296Schweiger P, Hofer M, Hartl W, Wanek W, Vollmann J. 2012.N2 fixation by organically grown soybean in Central Europe:Method of quantification and agronomic effects. EuropeanJournal of Agronomy, 41, 11-17Smith M T, Emerich D W. 1993. Alanine dehydrogenase fromsoybean nodule bacteroids, kinetics, mechanism and pHstudies. Journal of Biological Chemistry, 268, 10746-10753Smith P M C, Atkins C A. 2002. Purine biosynthesis. Big incell division, even bigger in nitrogen assimilation. PlantPhysiology, 128, 793-802.Sonia G, Laurence L, Alain G, Olaf N, Wolf B F, Nicolaus von W.1999. Three functional transporters for constitutive, diurnallyregulated, and starvation-induced uptake of ammonium intoArabidopsis roots. The Plant Cell, 11, 937-947Stacey G L, Vodkin W A P, Shoemaker R C. 2004. Nationalscience foundation-sponsored workshop report. Draft planfor soybean genomics. Plant Physiology, 135, 59-70Streeter V, Wong J, Streeter P, Wong P. 1988. Inhibition oflegume nodule formation and nitrogen fixation by nitrate.CRC Critical Reviews in Plant Sciences, 7, 1-23Streeter J G. 2003. Effects of drought on nitrogen fixation insoybean root nodules. Plant, Cell and Environment, 26,1199-1204Sulieman S, Schlze J. 2010. Phloem-derived γ-aminobutyricacid (GABA) is involved in up-regulating nodule N2 fixationefficiency in the model legume Medicago truncatula. Plant,Cell and Environment, 33, 2162-2172Suzuki H, Verma D P. 1991. Soybean nodule-specific uricase(nodulin-35) is expressed and assembled into a functionaltetrameric holoenzyme in Escherichia coli. Plant Physiology,95, 384-389Takane K, Tajima S, Kouchi H. 1997. Two distinct uricase II(Nodulin 35) genes are differentially expressed in soybeanplants. Molecular Plant-Microbe Interactions, 10, 735-741Tajima S, Yamamoto Y. 1977. Regulation of uricase activityin developing roots of Glycine max, non-nodulating varietyA62-2. Plant & Cell Physiology, 18, 247-253Uwe L, Benjamin N, Marek D. 2007. Molecular mechanismsof ammonium transport and accumulation in plants. FEBSLetters, 581, 2301-2308Wang P, Kong C H, Hu F, Xu X. 2007. Allantoin involved inspecies interactions with rice and other organisms in paddysoil. Plant and Soil, 296, 43-51Wang P, Kong C H, Sun B, Xu X H. 2012. Distribution andfunction of allantoin (5-ureidohydantoin) in rice grains.Journal of Agricultural and Food Chemistry, 60, 2793-2798Werner A K, Romeis T, Witte C P. 2010. Ureide catabolism inArabidopsis thaliana and Escherichia coli. Nature ChemicalBiology, 6, 19-21Wright P A. 1995. Nitrogen excretion: Three end products, manyphysiological roles. The Journal of Experimental Biology,198, 273-281Yang J Y, Drury C F, Yang X M, Jong R D, Huffman E C,Campbell C A, Kirkwood V. 2010. Estimating biological N2fixation in Canadian agricultural land using legume yields.Agriculture, Ecosystems and Environment, 137, 192-201Yemm E W, Cocking E C. 1955. The determination of aminoacids with ninhdrin. Analyist, 80, 209-213Young G and Conway C F. 1942. On the estimation of allantoinby the Rimini-Schryver reaction. Journal of BiologicalChemistry, 142, 839-853.Yuan L, Dominique L, Soichi K, Sabine R, Keiki I, Eri I, HidekiT, von Nicolaus W. 2007. The organization of high-affinityammonium uptake in arabidopsis roots depends on thespatial arrangement and biochemical properties of AMT1-type transporters. The Plant Cell, 19, 2636-2652 |
| No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
| |
Shared |
|
|
|
|
| |
Discussed |
|
|
|
|
