Auxin-modulated root growth inhibition in Arabidopsis thaliana seedlings with ammonium as the sole nitrogen source
Huaiyu Yang A B , Jenny von der Fecht-Bartenbach B , Jiří Friml C , Jan U. Lohmann D , Benjamin Neuhäuser A and Uwe Ludewig A B E
+ Author Affiliations
- Author Affiliations
A Institute of Crop Science, Nutritional Crop Physiology, University of Hohenheim, Fruwirthstr. 20, D-70593 Stuttgart, Germany.
B Centre for Molecular Biology of Plants, Plant Physiology, University of Tübingen, Auf der Morgenstelle 1, D-72076 Tübingen, Germany.
C Institute of Science and Technology Austria, Am Campus 1, 3400 Klosterneuburg, Austria.
D Department of Stem Cell Biology, University of Heidelberg, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany.
E Corresponding author. Email: u.ludewig@uni-hohenheim.de
Functional Plant Biology 42(3) 239-251 https://doi.org/10.1071/FP14171
Submitted: 24 June 2014 Accepted: 23 September 2014 Published: 24 October 2014
Abstract
Ammonium is the major nitrogen source in some plant ecosystems but is toxic at high concentrations, especially when available as the exclusive nitrogen source. Ammonium stress rapidly leads to various metabolic and hormonal imbalances that ultimately inhibit root and shoot growth in many plant species, including Arabidopsis thaliana (L.) Heynh. To identify molecular and genetic factors involved in seedling survival with prolonged exclusive NH4+ nutrition, a transcriptomic analysis with microarrays was used. Substantial transcriptional differences were most pronounced in (NH4)2SO4-grown seedlings, compared with plants grown on KNO3 or NH4NO3. Consistent with previous physiological analyses, major differences in the expression modules of photosynthesis-related genes, an altered mitochondrial metabolism, differential expression of the primary NH4+ assimilation, alteration of transporter gene expression and crucial changes in cell wall biosynthesis were found. A major difference in plant hormone responses, particularly of auxin but not cytokinin, was striking. The activity of the DR5::GUS reporter revealed a dramatically decreased auxin response in (NH4)2SO4-grown primary roots. The impaired root growth on (NH4)2SO4 was partially rescued by exogenous auxin or in specific mutants in the auxin pathway. The data suggest that NH4+-induced nutritional and metabolic imbalances can be partially overcome by elevated auxin levels.
Additional keywords: microarray, mitochondria, nitrogen, nitrate.
References
Ameziane R, Bernhard K, Lightfoot DA (2000) Expression of the bacterial gdhA gene encoding a NADPH glutamate dehydrogenase in tobacco affects plant growth and development. Plant and Soil 221, 47–57.| Expression of the bacterial gdhA gene encoding a NADPH glutamate dehydrogenase in tobacco affects plant growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlslyns74%3D&md5=4778348d1f67994f2fc64a79309d1e54CAS |
Balkos KD, Britto DT, Kronzucker HJ (2010) Optimization of ammonium acquisition and metabolism by potassium in rice (Oryza sativa L. cv. IR-72). Plant, Cell & Environment 33, 23–34.
Barth C, Gouzd ZA, Steele HP, Imperio RM (2010) A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis. Journal of Experimental Botany 61, 379–394.
| A mutation in GDP-mannose pyrophosphorylase causes conditional hypersensitivity to ammonium, resulting in Arabidopsis root growth inhibition, altered ammonium metabolism, and hormone homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXktlGnuw%3D%3D&md5=c86c6a93eefe41a05cbb4198646f6219CAS | 20007685PubMed |
Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003) Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell 115, 591–602.
| Local, efflux-dependent auxin gradients as a common module for plant organ formation.Crossref | GoogleScholarGoogle Scholar | 14651850PubMed |
Bhalerao RP, Eklof J, Ljung K, Marchant A, Bennett M, Sandberg G (2002) Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. The Plant Journal 29, 325–332.
| Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhvFOitL8%3D&md5=8e08f4b2d8b5f0a44128b728dd36a456CAS | 11844109PubMed |
Bloom AJ, Sukrapanna SS, Warner RL (1992) Root respiration associated with ammonium and nitrate absorption and assimilation by barley. Plant Physiology 99, 1294–1301.
| Root respiration associated with ammonium and nitrate absorption and assimilation by barley.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK38XlvVygsr0%3D&md5=6b99e0159a1e2479052cb5f6f0daa532CAS | 16669035PubMed |
Breitling R, Armengaud P, Amtmann A, Herzyk P (2004) Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments. FEBS Letters 573, 83–92.
| Rank products: a simple, yet powerful, new method to detect differentially regulated genes in replicated microarray experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFyrtr4%3D&md5=38c72b55d4bf91eccb5ea2556ff74466CAS | 15327980PubMed |
Britto DT, Kronzucker HJ (2002) NH4 + toxicity in higher plants: a critical review. Journal of Plant Physiology 159, 567–584.
| NH4 + toxicity in higher plants: a critical review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvVCrtbc%3D&md5=32cf49614f988ab4a9666e52f9c57d99CAS |
Britto DT, Siddiqi MY, Glass AD, Kronzucker HJ (2001) Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants. Proceedings of the National Academy of Sciences of the United States of America 98, 4255–4258.
| Futile transmembrane NH4 + cycling: a cellular hypothesis to explain ammonium toxicity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1Khurw%3D&md5=2e125b681d267d260c09f9fa21ccd725CAS | 11274450PubMed |
Cao Y, Glass AD, Crawford NM (1993) Ammonium inhibition of Arabidopsis root growth can be reversed by potassium and by auxin resistance mutations aux1, axr1, and axr2. Plant Physiology 102, 983–989.
| Ammonium inhibition of Arabidopsis root growth can be reversed by potassium and by auxin resistance mutations aux1, axr1, and axr2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXlslOltLY%3D&md5=77f87fdb33ea30d2362590f6e16982b7CAS | 8278539PubMed |
Chen G, Guo S, Kronzucker HJ, Shi W (2013) Nitrogen use efficiency (NUE) in rice links to NH4+ toxicity and futile NH4+ cycling in roots. Plant and Soil 369, 351–363.
| Nitrogen use efficiency (NUE) in rice links to NH4+ toxicity and futile NH4+ cycling in roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVyqtLjO&md5=4844a03413c4b3908fbcf69f8646b641CAS |
Dubrovsky JG, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E (2008) Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proceedings of the National Academy of Sciences of the United States of America 105, 8790–8794.
| Auxin acts as a local morphogenetic trigger to specify lateral root founder cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXot1emtb8%3D&md5=edff6c2130fa9391fdfe55aa204deeedCAS | 18559858PubMed |
Dynowski M, Mayer M, Moran O, Ludewig U (2008) Molecular determinants of ammonia and urea conductance in plant aquaporin homologs. FEBS Letters 582, 2458–2462.
| Molecular determinants of ammonia and urea conductance in plant aquaporin homologs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnvVKns7Y%3D&md5=eb332411eb267ae539cb4cf0d4cc1a85CAS | 18565332PubMed |
Escobar MA, Geisler DA, Rasmusson AG (2006) Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate. The Plant Journal 45, 775–788.
| Reorganization of the alternative pathways of the Arabidopsis respiratory chain by nitrogen supply: opposing effects of ammonium and nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1Sjt7o%3D&md5=98a9aa097cad5230668362d237eb77ccCAS | 16460511PubMed |
Feng J, Barker AV (1992) Ethylen evolution and ammonium accumulation by tomato plants with various nitrogen forms and regimes of acidity. Journal of Plant Nutrition 15, 2457–2469.
| Ethylen evolution and ammonium accumulation by tomato plants with various nitrogen forms and regimes of acidity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXitFKntQ%3D%3D&md5=925b1fa31cd635772159d6dfae1a6418CAS |
Findenegg GR (1987) A comparative study of ammonium toxicity at different constant pH of the nutrient solution. Plant and Soil 103, 239–243.
| A comparative study of ammonium toxicity at different constant pH of the nutrient solution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXnsVemtA%3D%3D&md5=5176a03775a34a40c2ae535e6af9cd89CAS |
Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, Hooykaas PJ, Palme K, Offringa R (2004) A PINOID-dependent binary switch in apical–basal PIN polar targeting directs auxin efflux. Science 306, 862–865.
| A PINOID-dependent binary switch in apical–basal PIN polar targeting directs auxin efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXovFamsLk%3D&md5=bc226f1b4bcf5d531e0ffa19cdd55b80CAS | 15514156PubMed |
Gazzarrini S, Lejay L, Gojon A, Ninnemann O, Frommer WB, von Wiren N (1999) Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots. The Plant Cell 11, 937–948.
| Three functional transporters for constitutive, diurnally regulated, and starvation-induced uptake of ammonium into Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjvVajsLg%3D&md5=55cd114a83ff55b227ff7408213c7cfcCAS | 10330477PubMed |
Gerendás J, Zhu Z, Bendixen R, Ratcliffe RG, Sattelmacher B (1997) Physiological and biochemical processes related to ammonium toxicity in higher plants. Zeitschrift für Pflanzenernährung und Bodenkunde 160, 239–251.
| Physiological and biochemical processes related to ammonium toxicity in higher plants.Crossref | GoogleScholarGoogle Scholar |
Givan CV (1979) Metabolic detoxification of ammonia in tissues of higher plants. Phytochemistry 18, 375–382.
| Metabolic detoxification of ammonia in tissues of higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXltVGisrc%3D&md5=5c391f196caeb8fb5b05b5b6335c561eCAS |
Hachiya T, Watanabe CK, Fujimoto M, Ishikawa T, Takahara K, Kawai-Yamada M, Uchimiya H, Uesono Y, Terashima I, Noguchi K (2012) Nitrate addition alleviates ammonium toxicity without lessening ammonium accumulation, organic acid depletion and inorganic cation depletion in Arabidopsis thaliana shoots. Plant & Cell Physiology 53, 577–591.
| Nitrate addition alleviates ammonium toxicity without lessening ammonium accumulation, organic acid depletion and inorganic cation depletion in Arabidopsis thaliana shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjslehu7o%3D&md5=db8bba22127050f23d3ca487be7f8c65CAS |
Ishiyama K, Inoue E, Watanabe-Takahashi A, Obara M, Yamaya T, Takahashi H (2004) Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis. The Journal of Biological Chemistry 279, 16 598–16 605.
| Kinetic properties and ammonium-dependent regulation of cytosolic isoenzymes of glutamine synthetase in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXivF2qtbc%3D&md5=820413a6c278f0c05db8df991924c4eeCAS |
Jadid N, Mialoundama AS, Heintz D, Ayoub D, Erhardt M, Mutterer J, Meyer D, Alioua A, Van Dorsselaer A, Rahier A, Camara B, Bouvier F (2011) DOLICHOL PHOSPHATE MANNOSE SYNTHASE1 mediates the biogenesis of isoprenyl-linked glycans and influences development, stress response, and ammonium hypersensitivity in Arabidopsis. The Plant Cell 23, 1985–2005.
| DOLICHOL PHOSPHATE MANNOSE SYNTHASE1 mediates the biogenesis of isoprenyl-linked glycans and influences development, stress response, and ammonium hypersensitivity in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWqsbs%3D&md5=2181e3f7885d44b59ed13a29c54b9d1bCAS | 21558543PubMed |
Kempinski CF, Haffar R, Barth C (2011) Toward the mechanism of NH4 + sensitivity mediated by Arabidopsis GDP-mannose pyrophosphorylase. Plant, Cell & Environment 34, 847–858.
| Toward the mechanism of NH4 + sensitivity mediated by Arabidopsis GDP-mannose pyrophosphorylase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmvVGksLo%3D&md5=466ab60aa826f71176e6db16a736760aCAS |
Kudoyarova G, Farkhutdinov R, Veselov S (1997) Comparison of the effects of nitrate and ammonium forms of nitrogen on auxin content in roots and the growth of plants under different temperature conditions. Plant Growth Regulation 23, 207–208.
| Comparison of the effects of nitrate and ammonium forms of nitrogen on auxin content in roots and the growth of plants under different temperature conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1Snug%3D%3D&md5=bf70f481d49de28b421aa60c57bb1e53CAS |
Lager I, Andreasson O, Dunbar TL, Andreasson E, Escobar MA, Rasmusson AG (2010) Changes in external pH rapidly alter plant gene expression and modulate auxin and elicitor responses. Plant, Cell & Environment 33, 1513–1528.
Lasa B, Frechilla S, Aparicio-Tejo PM, Lamsfus C (2002) Role of glutamate dehydrogenase and phosphoenolpyruvate carboxylase activity in ammonium nutrition tolerance in roots. Plant Physiology and Biochemistry 40, 969–976.
| Role of glutamate dehydrogenase and phosphoenolpyruvate carboxylase activity in ammonium nutrition tolerance in roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFCitr4%3D&md5=1d069c9c98543a719cee88cde627d096CAS |
Li Q, Li BH, Kronzucker HJ, Shi WM (2010) Root growth inhibition by NH4 + in Arabidopsis is mediated by the root tip and is linked to NH4 + efflux and GMPase activity. Plant, Cell & Environment 33, 1529–1542.
| Root growth inhibition by NH4 + in Arabidopsis is mediated by the root tip and is linked to NH4 + efflux and GMPase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtFKru7bF&md5=d019e0792d87ea33cde81e5abecdd6ddCAS |
Li B, Li Q, Su Y, Chen H, Xiong L, Mi G, Kronzucker HJ, Shi W (2011) Shoot-supplied ammonium targets the root auxin influx carrier AUX1 and inhibits lateral root emergence in Arabidopsis. Plant, Cell & Environment 34, 933–946.
| Shoot-supplied ammonium targets the root auxin influx carrier AUX1 and inhibits lateral root emergence in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXos1Sgtb4%3D&md5=0d708e7e834e87efcf89d2bd02d5294fCAS |
Li B, Li Q, Xiong L, Kronzucker HJ, Kramer U, Shi W (2012) Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress. Plant Physiology 160, 2040–2051.
| Arabidopsis plastid AMOS1/EGY1 integrates abscisic acid signaling to regulate global gene expression response to ammonium stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvVKmt7fO&md5=c5c36c68146259402d03e166fcb8af82CAS | 23064408PubMed |
Li G, Li B, Dong G, Feng X, Kronzucker HJ, Shi W (2013) Ammonium-induced shoot ethylene production is associated with the inhibition of lateral root formation in Arabidopsis. Journal of Experimental Botany 64, 1413–1425.
| Ammonium-induced shoot ethylene production is associated with the inhibition of lateral root formation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXktFKqsrs%3D&md5=7a862b7bdac9a9ed71713a6e088f1fa8CAS | 23382554PubMed |
Li B, Li G, Kronzucker HJ, Baluska F, Shi W (2014) Ammonium stress in Arabidopsis: signaling, genetic loci, and physiological targets. Trends in Plant Science 19, 107–114.
Liu Y, Lai N, Gao K, Chen F, Yuan L, Mi G (2013) Ammonium inhibits primary root growth by reducing the length of meristem and elongation zone and decreasing elemental expansion rate in the root apex in Arabidopsis thaliana. PLoS ONE 8, e61031
| Ammonium inhibits primary root growth by reducing the length of meristem and elongation zone and decreasing elemental expansion rate in the root apex in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXmtlSmsbo%3D&md5=04071ba3fcc5e9a29a4c691c89d716b6CAS | 23577185PubMed |
Lukowitz W, Nickle TC, Meinke DW, Last RL, Conklin PL, Somerville CR (2001) Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 98, 2262–2267.
| Arabidopsis cyt1 mutants are deficient in a mannose-1-phosphate guanylyltransferase and point to a requirement of N-linked glycosylation for cellulose biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslKntLc%3D&md5=f0d785ed8dd0ffe6fd7d4fb69ca8dc4dCAS | 11226227PubMed |
Luschnig C, Gaxiola RA, Grisafi P, Fink GR (1998) EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes & Development 12, 2175–2187.
| EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXltVShs7Y%3D&md5=23744b58b0e806735be8b5ddf785aa3fCAS |
Marschner P (2011) ‘Marschner’s mineral nutrition of higher plants.’ (Academic Press: London)
Martin A, Lee J, Kichey T, Gerentes D, Zivy M, Tatout C, Dubois F, Balliau T, Valot B, Davanture M, Terce-Laforgue T, Quillere I, Coque M, Gallais A, Gonzalez-Moro MB, Bethencourt L, Habash DZ, Lea PJ, Charcosset A, Perez P, Murigneux A, Sakakibara H, Edwards KJ, Hirel B (2006) Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production. The Plant Cell 18, 3252–3274.
| Two cytosolic glutamine synthetase isoforms of maize are specifically involved in the control of grain production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1Crtg%3D%3D&md5=3114db26ab31415953265c8667c10ec7CAS | 17138698PubMed |
Masakapalli SK, Kruger NJ, Ratcliffe RG (2013) The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a complex response to changes in nitrogen supply. The Plant Journal 74, 569–582.
| The metabolic flux phenotype of heterotrophic Arabidopsis cells reveals a complex response to changes in nitrogen supply.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnsVKqs7g%3D&md5=efe26f827e355384815c9abed3271406CAS | 23406511PubMed |
Michniewicz M, Zago MK, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler MG, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz EM, Luschnig C, Offringa R, Friml J (2007) Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell 130, 1044–1056.
| Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtFKnurvK&md5=b73d640e28f4ce5778a70737c76a101cCAS | 17889649PubMed |
Miflin BJ, Habash DZ (2002) The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops. Journal of Experimental Botany 53, 979–987.
| The role of glutamine synthetase and glutamate dehydrogenase in nitrogen assimilation and possibilities for improvement in the nitrogen utilization of crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XivFSnur8%3D&md5=598f95b4622bc8777b13d4ddd532eb6cCAS | 11912240PubMed |
Negi S, Ivanchenko MG, Muday GK (2008) Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana. The Plant Journal 55, 175–187.
| Ethylene regulates lateral root formation and auxin transport in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptlalsrk%3D&md5=585fde972c923f7c017a86abfeb94903CAS | 18363780PubMed |
Neuhauser B, Dynowski M, Mayer M, Ludewig U (2007) Regulation of NH4 + transport by essential cross talk between AMT monomers through the carboxyl tails. Plant Physiology 143, 1651–1659.
| Regulation of NH4 + transport by essential cross talk between AMT monomers through the carboxyl tails.Crossref | GoogleScholarGoogle Scholar | 17337531PubMed |
Nielsen KH, Schjoerring JK (1998) Regulation of apoplastic NH4 + concentration in leaves of oilseed rape. Plant Physiology 118, 1361–1368.
| Regulation of apoplastic NH4 + concentration in leaves of oilseed rape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht10%3D&md5=7c9b7e423ba53f8c2de2864a419e054cCAS | 9847110PubMed |
Ottenschlager I, Wolff P, Wolverton C, Bhalerao RP, Sandberg G, Ishikawa H, Evans M, Palme K (2003) Gravity-regulated differential auxin transport from columella to lateral root cap cells. Proceedings of the National Academy of Sciences of the United States of America 100, 2987–2991.
| Gravity-regulated differential auxin transport from columella to lateral root cap cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXitVaiu7g%3D&md5=0e60c781aa6a735a5427c2cad9eba797CAS | 12594336PubMed |
Patterson K, Cakmak T, Cooper A, Lager I, Rasmusson AG, Escobar MA (2010) Distinct signalling pathways and transcriptome response signatures differentiate ammonium- and nitrate-supplied plants. Plant, Cell & Environment 33, 1486–1501.
Petrasek J, Mravec J, Bouchard R, Blakeslee JJ, Abas M, Seifertova D, Wisniewska J, Tadele Z, Kubes M, Covanoa M, Dhonukshe P, Skupa P, Benkova E, Perry L, Krecek P, Lee OR, Fink GR, Geisler M, Murphy AS, Luschnig C, Zazimalova E, Friml J (2006) PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 312, 914–918.
| PIN proteins perform a rate-limiting function in cellular auxin efflux.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xktlyhs7o%3D&md5=5d0cb5ff8475de49ab59c3b0fef96720CAS | 16601150PubMed |
Pilot G, Stransky H, Bushey DF, Pratelli R, Ludewig U, Wingate VP, Frommer WB (2004) Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves. The Plant Cell 16, 1827–1840.
| Overexpression of GLUTAMINE DUMPER1 leads to hypersecretion of glutamine from hydathodes of Arabidopsis leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmtFSqtLo%3D&md5=22a4093b1192a8b391334bc229c60326CAS | 15208395PubMed |
Qin C, Qian W, Wang W, Wu Y, Yu C, Jiang X, Wang D, Wu P (2008) GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 105, 18 308–18 313.
| GDP-mannose pyrophosphorylase is a genetic determinant of ammonium sensitivity in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVyhsrrN&md5=8ff0c8bdbce8574479f5525a8e452110CAS |
Rahayu YS, Walch-Liu P, Neumann G, Römheld V, von Wiren N, Bangerth F (2005) Root-derived cytokinins as long-distance signals for NO3 −-induced stimulation of leaf growth. Journal of Experimental Botany 56, 1143–1152.
| Root-derived cytokinins as long-distance signals for NO3 −-induced stimulation of leaf growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisVGqs70%3D&md5=419a7757ceaa2c9d524ea943f80e2f5eCAS | 15710629PubMed |
Rashotte AM, DeLong A, Muday GK (2001) Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth. The Plant Cell 13, 1683–1697.
| Genetic and chemical reductions in protein phosphatase activity alter auxin transport, gravity response, and lateral root growth.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXlsFKlt7c%3D&md5=c408ba294dafac949e70f7ba2870bbc5CAS | 11449059PubMed |
Roosta HR, Schjoerring JK (2007) Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants. Journal of Plant Nutrition 30, 1933–1951.
| Effects of ammonium toxicity on nitrogen metabolism and elemental profile of cucumber plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyntrnP&md5=3ac31120e64af7e105645558ab8f0a4eCAS |
Roosta HR, Schjoerring JK (2008) Root carbon enrichment alleviates ammonium toxicity in cucumber plants. Journal of Plant Nutrition 31, 941–958.
| Root carbon enrichment alleviates ammonium toxicity in cucumber plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXnsVSmsL4%3D&md5=1b9ea4b1b97ef97246450448744f3f2fCAS |
Swarup R, Friml J, Marchant A, Ljung K, Sandberg G, Palme K, Bennett M (2001) Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex. Genes & Development 15, 2648–2653.
| Localization of the auxin permease AUX1 suggests two functionally distinct hormone transport pathways operate in the Arabidopsis root apex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVWksLk%3D&md5=4215c2e98255299cf81249ced213416cCAS |
Taylor AR, Bloom AJ (1998) Ammonium, nitrate, and proton fluxes along the maize root. Plant, Cell & Environment 21, 1255–1263.
| Ammonium, nitrate, and proton fluxes along the maize root.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1Wmt78%3D&md5=aacbe9e48bd466f647ae198b6b5ff0b3CAS |
Tian QY, Chen FJ, Liu JX, Zhang FS, Mi GH (2008) Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots. Journal of Plant Physiology 165, 942–951.
| Inhibition of maize root growth by high nitrate supply is correlated with reduced IAA levels in roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXptlagurc%3D&md5=2d703216e14b5009dd3960db2010b8d7CAS |
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ (1997) Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. The Plant Cell 9, 1963–1971.
| Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXnsl2mtrc%3D&md5=9b39f6bd89dcd4c57c3b36bd00af9059CAS | 9401121PubMed |
Usadel B, Nagel A, Thimm O, Redestig H, Blaesing OE, Palacios-Rojas N, Selbig J, Hannemann J, Piques MC, Steinhauser D, Scheible WR, Gibon Y, Morcuende R, Weicht D, Meyer S, Stitt M (2005) Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses. Plant Physiology 138, 1195–1204.
| Extension of the visualization tool MapMan to allow statistical analysis of arrays, display of corresponding genes, and comparison with known responses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmvV2ltbY%3D&md5=f18b4ee2be7e653e974e4eba15f8f493CAS | 16009995PubMed |
van den Berg LJ, Dorland E, Vergeer P, Hart MA, Bobbink R, Roelofs JG (2005) Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH. New Phytologist 166, 551–564.
| Decline of acid-sensitive plant species in heathland can be attributed to ammonium toxicity in combination with low pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktlWqsLY%3D&md5=860d4b18f49f9de82f6cca800a67f63cCAS | 15819917PubMed |
Vanneste S, Friml J (2009) Auxin: a trigger for change in plant development. Cell 136, 1005–1016.
| Auxin: a trigger for change in plant development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltFSntro%3D&md5=c3dc615b27f2c56f79fd8ce13911d80cCAS | 19303845PubMed |
Walch-Liu P, Neumann G, Bangerth F, Engels C (2000) Rapid effects of nitrogen form on leaf morphogenesis in tobacco. Journal of Experimental Botany 51, 227–237.
| Rapid effects of nitrogen form on leaf morphogenesis in tobacco.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsVOjs7o%3D&md5=a8c7ea74ab694709b8f6beacc36ea64fCAS | 10938829PubMed |
Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmulling T (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. The Plant Cell 15, 2532–2550.
| Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpt1Ortbw%3D&md5=824ac581f9664969cfff1988ebebf4edCAS | 14555694PubMed |
Wu Z, Irizarry RA, Gentleman R, Murillo FM, Spencer FA (2004) ‘A model based background adjustment for oligonucleotide expression arrays.’ Working paper 1. (Department of Biostatistics Working Papers, Johns Hopkins University: Baltimore).
