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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Insights into the functional relationship between cytokinin-induced root system phenotypes and nitrate uptake in Brassica napus

Qianqian Guo A , Jonathan Love A , Jiancheng Song B , Jessica Roche A , Matthew H. Turnbull A and Paula E. Jameson A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand.

B School of Life Sciences, Yantai University, 30 Qingquan Road, Yantai 264005, China.

C Corresponding author. Email: paula.jameson@canterbury.ac.nz

Functional Plant Biology 44(8) 832-844 https://doi.org/10.1071/FP16435
Submitted: 16 December 2016  Accepted: 27 May 2017   Published: 29 June 2017

Abstract

Root system architecture is the spatial arrangement of roots that impacts the capacity of plants to access nutrients and water. We employed pharmacologically generated morphological and molecular phenotypes and used in situ 15N isotope labelling, to investigate whether contrasting root traits are of functional interest in relation to nitrate acquisition. Brassica napus L. were grown in solidified phytogel culture media containing 1 mM KNO3 and treated with the cytokinin, 6-benzylaminopurine, the cytokinin antagonist, PI-55, or both in combination. The pharmacological treatments inhibited root elongation relative to the control. The contrasting root traits induced by PI-55 and 6-benzylaminopurine were strongly related to 15N uptake rate. Large root proliferation led to greater 15N cumulative uptake rather than greater 15N uptake efficiency per unit root length, due to a systemic response in the plant. This relationship was associated with changes in C and N resource distribution between the shoot and root, and in expression of BnNRT2.1, a nitrate transporter. The root : shoot biomass ratio was positively correlated with 15N cumulative uptake, suggesting the functional utility of root investment for nutrient acquisition. These results demonstrate that root proliferation in response to external nitrate is a behaviour which integrates local N availability and the systemic N status of the plant.

Additional keywords: NO3, N uptake, PI-55, root system architecture (RSA).


References

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 |

Berntson G (1994) Modelling root architecture: are there tradeoffs between efficiency and potential of resource acquisition? New Phytologist 127, 483–493.
Modelling root architecture: are there tradeoffs between efficiency and potential of resource acquisition?Crossref | GoogleScholarGoogle Scholar |

Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T (2005) Immediate‐early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome‐wide expression profiling reveal novel cytokinin‐sensitive processes and suggest cytokinin action through transcriptional cascades. The Plant Journal 44, 314–333.
Immediate‐early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome‐wide expression profiling reveal novel cytokinin‐sensitive processes and suggest cytokinin action through transcriptional cascades.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtFyhsb%2FO&md5=39417cdcc6157892dce3995862523852CAS |

Crawford NM, Glass AD (1998) Molecular and physiological aspects of nitrate uptake in plants. Trends in Plant Science 3, 389–395.
Molecular and physiological aspects of nitrate uptake in plants.Crossref | GoogleScholarGoogle Scholar |

Dathe A, Postma J, Postma-Blaauw M, Lynch J (2016) Impact of axial root growth angles on nitrogen acquisition in maize depends on environmental conditions. Annals of Botany 118, 401–414.
Impact of axial root growth angles on nitrogen acquisition in maize depends on environmental conditions.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2s3lvFymsw%3D%3D&md5=6e8ff81b782b9e72ac6601027331e2cbCAS |

Davidson E, David MB, Galloway JN, Goodale CL, Haeuber R, Harrison JA, Howarth RW, Jaynes DB, Lowrance RR, Thomas NB (2011) Excess nitrogen in the US environment: trends, risks, and solutions. Issues in Ecology 15,

de Ruiter J, Wilson D, Maley S, Fletcher AL, Fraser T, Scott WR, Berryman S, Dumbleton A, Nichol W (2009) ‘Management practices for forage brassicas.’ (Forage Brassica Development Group: Christchurch)

de Vries W, Kros J, Kroeze C, Seitzinger SP (2013) Assessing planetary and regional nitrogen boundaries related to food security and adverse environmental impacts. Current Opinion in Environmental Sustainability 5, 392–402.
Assessing planetary and regional nitrogen boundaries related to food security and adverse environmental impacts.Crossref | GoogleScholarGoogle Scholar |

Del Bianco M, Giustini L, Sabatini S (2013) Spatiotemporal changes in the role of cytokinin during root development. New Phytologist 199, 324–338.
Spatiotemporal changes in the role of cytokinin during root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXpvFars7c%3D&md5=9f8493d836e5d2c80c74d331e66f394dCAS |

Dubrovsky JG, Forde BG (2012) Quantitative analysis of lateral root development: pitfalls and how to avoid them. The Plant Cell 24, 4–14.
Quantitative analysis of lateral root development: pitfalls and how to avoid them.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOlu78%3D&md5=495e2d29d1634488225608b0e7727f8cCAS |

Forde BG (2002) Local and long-range signaling pathways regulating plant responses to nitrate. Annual Review of Plant Biology 53, 203–224.
Local and long-range signaling pathways regulating plant responses to nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlsVWhtbk%3D&md5=d37baeb615d110b16b5871e875ef087eCAS |

Fransen B, Blijjenberg J, de Kroon H (1999) Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches. Plant and Soil 211, 179–189.
Root morphological and physiological plasticity of perennial grass species and the exploitation of spatial and temporal heterogeneous nutrient patches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXntlKisL0%3D&md5=c1f951bdb81399ac694e05f29c4a1cc6CAS |

Freixes S, Thibaud MC, Tardieu F, Muller B (2002) Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings. Plant, Cell & Environment 25, 1357–1366.
Root elongation and branching is related to local hexose concentration in Arabidopsis thaliana seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XotVCqsrk%3D&md5=ceb2f6c785cc1e9c32d2b3e779e0d8c5CAS |

Gabrielle B, Justes E, Denoroy P (1998) Modelling of temperature and nitrogen effects on the rooting dynamics of winter oilseed rape. In ‘16th International Society of Soil Science Congress’. Montpellier, France.

Gaudin A, Mcclymont SA, Holmes BM, Lyons E, Raizada MN (2011) Novel temporal, fine‐scale and growth variation phenotypes in roots of adult‐stage maize (Zea mays L.) in response to low nitrogen stress. Plant, Cell & Environment 34, 2122–2137.
Novel temporal, fine‐scale and growth variation phenotypes in roots of adult‐stage maize (Zea mays L.) in response to low nitrogen stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Glt7nE&md5=945381af8d23ace9eea64b1552acd8d2CAS |

Giehl RF, von Wirén N (2014) Root nutrient foraging. Plant Physiology 166, 509–517.
Root nutrient foraging.Crossref | GoogleScholarGoogle Scholar |

Giehl RF, Gruber BD, von Wirén N (2014) It’s time to make changes: modulation of root system architecture by nutrient signals. Journal of Experimental Botany 65, 769–778.
It’s time to make changes: modulation of root system architecture by nutrient signals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXisFOjtrw%3D&md5=a98cc20542a8205238a4c26b5e4f853fCAS |

Gruber BD, Giehl RF, Friedel S, von Wirén N (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiology 163, 161–179.
Plasticity of the Arabidopsis root system under nutrient deficiencies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsVygsbjM&md5=b01ee32e55d71f258de3f2abfc1ddf1bCAS |

Guo Q, Love J, Roche J, Song J, Turnbull MH, Jameson PE (2017a) A RootNav analysis of morphological changes in Brassica napus L. roots in response to different nitrogen forms. Plant Growth Regulation
A RootNav analysis of morphological changes in Brassica napus L. roots in response to different nitrogen forms.Crossref | GoogleScholarGoogle Scholar |

Guo Q, Turnbull MH, Song JC, Roche J, Novák O, Späth J, Jameson PE, Love J (2017b) Depletion of carbohydrate reserves limits nitrate uptake during early regrowth in Lolium perenne L. Journal of Experimental Botany 68, 1569–1583.
Depletion of carbohydrate reserves limits nitrate uptake during early regrowth in Lolium perenne L.Crossref | GoogleScholarGoogle Scholar |

Hamburger D, Rezzonico E, Petétot JM-C, Somerville C, Poirier Y (2002) Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. The Plant Cell 14, 889–902.
Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjsFWktro%3D&md5=5d150e10091ba19db1970da87d74b9bbCAS |

Han Y-L, Song H-X, Liao Q, Yu Y, Jian S-F, Lepo JE, Liu Q, Rong X-M, Tian C, Zeng J (2016) Nitrogen use efficiency is mediated by vacuolar nitrate sequestration capacity in roots of Brassica napus. Plant Physiology 3, 1684–1698.

Hayes JM (2004) ‘An introduction to isotopic calculations.’ (Woods Hole Oceanographic Institution: Woods Hole, MA, USA)

Hewelt A, Prinsen E, Schell J, Onckelen H, Schmülling T (1994) Promoter tagging with a promoterless ipt gene leads to cytokinin‐induced phenotypic variability in transgenic tobacco plants: implications of gene dosage effects. The Plant Journal 6, 879–891.
Promoter tagging with a promoterless ipt gene leads to cytokinin‐induced phenotypic variability in transgenic tobacco plants: implications of gene dosage effects.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjsFyqurc%3D&md5=460f9d405082e3e21e7fafa7b4ed4f00CAS |

Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proceedings of the National Academy of Sciences of the United States of America 101, 8821–8826.
In planta functions of the Arabidopsis cytokinin receptor family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXltFKkt78%3D&md5=dfe962f7357e9a0819c15f1dedbf8fd8CAS |

Ho C-H, Lin S-H, Hu H-C, Tsay Y-F (2009) CHL1 functions as a nitrate sensor in plants. Cell 138, 1184–1194.
CHL1 functions as a nitrate sensor in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVyrsbvF&md5=cea8ad9d696ab222e0d4edb518ebd512CAS |

Huang N-C, Liu K-H, Lo H-J, Tsay Y-F (1999) Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake. The Plant Cell 11, 1381–1392.
Cloning and functional characterization of an Arabidopsis nitrate transporter gene that encodes a constitutive component of low-affinity uptake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXmtVWmurc%3D&md5=8b943088201f6b6f8803bf1390025bb7CAS |

Ioio RD, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S (2007) Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Current Biology 17, 678–682.
Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation.Crossref | GoogleScholarGoogle Scholar |

Kiba T, Krapp A (2016) Plant nitrogen acquisition under low availability: regulation of uptake and root architecture. Plant & Cell Physiology 57, 707–714.
Plant nitrogen acquisition under low availability: regulation of uptake and root architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsFSrtLnO&md5=11d65b334be423a2489cc225c8d15660CAS |

Kiba T, Kudo T, Kojima M, Sakakibara H (2011) Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin. Journal of Experimental Botany 62, 1399–1409.
Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhs1Gjtrs%3D&md5=bb2b2f42844e51ab7f9b8a69403f313dCAS |

Kiba T, Feria-Bourrellier A-B, Lafouge F, Lezhneva L, Boutet-Mercey S, Orsel M, Bréhaut V, Miller A, Daniel-Vedele F, Sakakibara H (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. The Plant Cell 24, 245–258.
The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVOksrc%3D&md5=9940b31d561e5b6abea8f0734d59f2fdCAS |

Kuderová A, Urbánková I, Válková M, Malbeck J, Brzobohatý B, Némethová D, Hejátko J (2008) Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant & Cell Physiology 49, 570–582.
Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar |

Laplaze L, Benkova E, Casimiro I, Maes L, Vanneste S, Swarup R, Weijers D, Calvo V, Parizot B, Herrera-Rodriguez MB (2007) Cytokinins act directly on lateral root founder cells to inhibit root initiation. The Plant Cell 19, 3889–3900.
Cytokinins act directly on lateral root founder cells to inhibit root initiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhvF2htrc%3D&md5=daa4903c173b05cafd3d864d78081f1bCAS |

Lemaire L, Deleu C, Le Deunff E (2013) Modulation of ethylene biosynthesis by ACC and AIB reveals a structural and functional relationship between the K15NO3 uptake rate and root absorbing surfaces. Journal of Experimental Botany 64, 2725–2737.
Modulation of ethylene biosynthesis by ACC and AIB reveals a structural and functional relationship between the K15NO3 uptake rate and root absorbing surfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtVaks7%2FN&md5=36dd4fb783137a0536e20b8012db367eCAS |

Li X, Mo X, Shou H, Wu P (2006) Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis. Plant & Cell Physiology 47, 1112–1123.
Cytokinin-mediated cell cycling arrest of pericycle founder cells in lateral root initiation of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XpsFKnsLY%3D&md5=593f6e50ff15327e92728c98a50a2b83CAS |

Li J-Y, Fu Y-L, Pike SM, Bao J, Tian W, Zhang Y, Chen C-Z, Zhang Y, Li H-M, Huang J (2010) The Arabidopsis nitrate transporter NRT1. 8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance. The Plant Cell 22, 1633–1646.
The Arabidopsis nitrate transporter NRT1. 8 functions in nitrate removal from the xylem sap and mediates cadmium tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptVeguro%3D&md5=03310147a56ca8df2b240279ef5b9bb7CAS |

Lin S-H, Kuo H-F, Canivenc G, Lin C-S, Lepetit M, Hsu P-K, Tillard P, Lin H-L, Wang Y-Y, Tsai C-B (2008) Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport. The Plant Cell 20, 2514–2528.
Mutation of the Arabidopsis NRT1.5 nitrate transporter causes defective root-to-shoot nitrate transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCnsLjE&md5=745013cd604f644281a30708c31ce605CAS |

Linkohr BI, Williamson LC, Fitter AH, Leyser H (2002) Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. The Plant Journal 29, 751–760.
Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjs12msr8%3D&md5=5735c7430ef37fe0b39d70e97c406badCAS |

Long C, Held M, Hayward A, Nisler J, Spíchal L, Neil Emery R, Moffatt BA, Guinel FC (2012) Seed development, seed germination and seedling growth in the R50 (sym16) pea mutant are not directly linked to altered cytokinin homeostasis. Physiologia Plantarum 145, 341–359.
Seed development, seed germination and seedling growth in the R50 (sym16) pea mutant are not directly linked to altered cytokinin homeostasis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotFWlur4%3D&md5=3c4d21dd60c3b00c23fcec0b58aaff48CAS |

López-Bucio J, Cruz-Ramírez A, Herrera-Estrella L (2003) The role of nutrient availability in regulating root architecture. Current Opinion in Plant Biology 6, 280–287.
The role of nutrient availability in regulating root architecture.Crossref | GoogleScholarGoogle Scholar |

Lynch J (1995) Root architecture and plant productivity. Plant Physiology 109, 7–13.
Root architecture and plant productivity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXotFWmsr0%3D&md5=31c9569eb29671038b6ce7f4ffe9983cCAS |

Lynch JP (2013) Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Annals of Botany 112, 347–357.
Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtFSitbfJ&md5=013995236bd80ca90a8d5b88a48231beCAS |

Marhavý P, Duclercq J, Weller B, Feraru E, Bielach A, Offringa R, Friml J, Schwechheimer C, Murphy A, Benková E (2014) Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis. Current Biology 24, 1031–1037.
Cytokinin controls polarity of PIN1-dependent auxin transport during lateral root organogenesis.Crossref | GoogleScholarGoogle Scholar |

McCormack ML, Dickie IA, Eissenstat DM, Fahey TJ, Fernandez CW, Guo D, Helmisaari HS, Hobbie EA, Iversen CM, Jackson RB (2015) Redefining fine roots improves understanding of below‐ground contributions to terrestrial biosphere processes. New Phytologist 207, 505–518.
Redefining fine roots improves understanding of below‐ground contributions to terrestrial biosphere processes.Crossref | GoogleScholarGoogle Scholar |

Medford JI, Horgan R, El-Sawi Z, Klee HJ (1989) Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene. The Plant Cell 1, 403–413.
Alterations of endogenous cytokinins in transgenic plants using a chimeric isopentenyl transferase gene.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXhslWgtA%3D%3D&md5=0a200ba1a93de43a981f219c6892aed1CAS |

Miller A, Cramer M (2005) Root nitrogen acquisition and assimilation. Plant and Soil 274, 1–36.
Root nitrogen acquisition and assimilation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVWiurbF&md5=075b516fd4ba929e2cfe2860afd92763CAS |

Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, Tarkowska D, Tabata S, Sandberg G, Kakimoto T (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proceedings of the National Academy of Sciences of the United States of America 103, 16598–16603.
Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xht1WgtbzL&md5=5f7bd26c7495c57991fc0a87f9235e49CAS |

Novák J, Černý M, Pavlů J, Zemánková J, Skalák J, Plačková L, Brzobohatý B (2015) Roles of proteome dynamics and cytokinin signaling in root to hypocotyl ratio changes induced by shading roots of Arabidopsis seedlings. Plant & Cell Physiology 56, 1006–1018.
Roles of proteome dynamics and cytokinin signaling in root to hypocotyl ratio changes induced by shading roots of Arabidopsis seedlings.Crossref | GoogleScholarGoogle Scholar |

Ohkubo Y, Tanaka M, Tabata R, Ogawa-Ohnishi M, Matsubayashi Y (2017) Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition. Nature Plants 3, 17029
Shoot-to-root mobile polypeptides involved in systemic regulation of nitrogen acquisition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXkvFahtLk%3D&md5=94fbe2fb966afde0bef87cb8c8713181CAS |

Péret B, De Rybel B, Casimiro I, Benková E, Swarup R, Laplaze L, Beeckman T, Bennett MJ (2009) Arabidopsis lateral root development: an emerging story. Trends in Plant Science 14, 399–408.
Arabidopsis lateral root development: an emerging story.Crossref | GoogleScholarGoogle Scholar |

Postma JA, Dathe A, Lynch JP (2014) The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiology 166, 590–602.
The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability.Crossref | GoogleScholarGoogle Scholar |

Pound MP, French AP, Atkinson JA, Wells DM, Bennett MJ, Pridmore T (2013) RootNav: navigating images of complex root architectures. Plant Physiology 162, 1802–1814.
RootNav: navigating images of complex root architectures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhtlWlt73M&md5=4bd2fec8bddce0976c2636f02514d0a8CAS |

Qiao C, Liu L, Hu S, Compton JE, Greaver TL, Li Q (2015) How inhibiting nitrification affects nitrogen cycle and reduces environmental impacts of anthropogenic nitrogen input. Global Change Biology 21, 1249–1257.
How inhibiting nitrification affects nitrogen cycle and reduces environmental impacts of anthropogenic nitrogen input.Crossref | GoogleScholarGoogle Scholar |

Remans T, Nacry P, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006a) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proceedings of the National Academy of Sciences of the United States of America 103, 19206–19211.
The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlChsrjO&md5=d2a8a4a05069c69770998f3822b69ca3CAS |

Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, Gojon A (2006b) A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiology 140, 909–921.
A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xislygsr4%3D&md5=dfe280444e08d8a98cb9842c50323345CAS |

Rosas U, Cibrian-Jaramillo A, Ristova D, Banta JA, Gifford ML, Fan AH, Zhou RW, Kim GJ, Krouk G, Birnbaum KD (2013) Integration of responses within and across Arabidopsis natural accessions uncovers loci controlling root systems architecture. Proceedings of the National Academy of Sciences of the United States of America 110, 15133–15138.
Integration of responses within and across Arabidopsis natural accessions uncovers loci controlling root systems architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFWrs7zP&md5=89fa9e59b5e55d0861abf6f3e8773680CAS |

Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM (2011) Nitrogen economics of root foraging: transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs demand. Proceedings of the National Academy of Sciences of the United States of America 108, 18524–18529.
Nitrogen economics of root foraging: transitive closure of the nitrate–cytokinin relay and distinct systemic signaling for N supply vs demand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFymu7bO&md5=da93a36596358097fe4ba613f69dc29cCAS |

Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3, 1101–1108.
Analyzing real-time PCR data by the comparative CT method.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvVemt7c%3D&md5=b40a697865fa3c52af2e4ad62a61696eCAS |

Siddiqi MY, Glass AD, Ruth TJ, Rufty TW (1990) Studies of the uptake of nitrate in barley I. Kinetics of 13NO3 − influx. Plant Physiology 93, 1426–1432.
Studies of the uptake of nitrate in barley I. Kinetics of 13NO3 influx.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXls12jtLc%3D&md5=407741e6361e8456d385825ec6973a01CAS |

Song J, Jiang L, Jameson PE (2015) Expression patterns of Brassica napus genes implicate IPT, CKX, sucrose transporter, cell wall invertase and amino acid permease gene family members in leaf, flower, silique and seed development. Journal of Experimental Botany 66, 5067–5082.
Expression patterns of Brassica napus genes implicate IPT, CKX, sucrose transporter, cell wall invertase and amino acid permease gene family members in leaf, flower, silique and seed development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVWhsbjI&md5=f3a9f306e334332924ebfe35a7260632CAS |

Spíchal L, Werner T, Popa I, Riefler M, Schmülling T, Strnad M (2009) The purine derivative PI‐55 blocks cytokinin action via receptor inhibition. FEBS Journal 276, 244–253.
The purine derivative PI‐55 blocks cytokinin action via receptor inhibition.Crossref | GoogleScholarGoogle Scholar |

Sutton MA, Howard CM, Erisman JW, Billen G, Bleeker A, Grennfelt P, Van Grinsven H, Grizzetti B (2011) ‘The European nitrogen assessment: sources, effects and policy perspectives.’(Cambridge University Press: Cambridge, UK)

Takei K, Ueda N, Aoki K, Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H (2004) AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis. Plant & Cell Physiology 45, 1053–1062.
AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXns1Sktb4%3D&md5=0b295ea699c1bcff661e5865c5c35b51CAS |

Tsay Y-F, Schroeder JI, Feldmann KA, Crawford NM (1993) The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter. Cell 72, 705–713.
The herbicide sensitivity gene CHL1 of Arabidopsis encodes a nitrate-inducible nitrate transporter.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXit1Oit7k%3D&md5=b8deb22b0e1a62f4a3250c0e45e070d8CAS |

van Vuuren M, Robinson D, Griffiths B (1996) Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil. Plant and Soil 178, 185–192.
Nutrient inflow and root proliferation during the exploitation of a temporally and spatially discrete source of nitrogen in soil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XitVahs7k%3D&md5=86644d9055149fd6f174d3b5eaaf4821CAS |

Wang Y-Y, Tsay Y-F (2011) Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport. The Plant Cell 23, 1945–1957.
Arabidopsis nitrate transporter NRT1.9 is important in phloem nitrate transport.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptFWqsbw%3D&md5=1da426214410df4a89e0ead6b23b7936CAS |

Wang Y-Y, Hsu P-K, Tsay Y-F (2012) Uptake, allocation and signaling of nitrate. Trends in Plant Science 17, 458–467.
Uptake, allocation and signaling of nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XotVeku7o%3D&md5=45d794b26a60a06505c04c60b105bd22CAS |

Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, Schmülling 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=8a547f40c5ec492875f69aea29c3d747CAS |

Xu W, Ding G, Yokawa K, Baluška F, Li Q-F, Liu Y, Shi W, Liang J, Zhang J (2013) An improved agar-plate method for studying root growth and response of Arabidopsis thaliana. Scientific Reports 3, 1273
An improved agar-plate method for studying root growth and response of Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Yokawa K, Kagenishi T, Kawano T, Mancuso S, Baluška F (2011) Illumination of Arabidopsis roots induces immediate burst of ROS production. Plant Signaling & Behavior 6, 1460–1464.
Illumination of Arabidopsis roots induces immediate burst of ROS production.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XjsVGhs70%3D&md5=57210a5b4f342348d6232221523d694aCAS |

York LM, Silberbush M, Lynch JP (2016) Spatiotemporal variation of nitrate uptake kinetics within the maize (Zea mays L.) root system is associated with greater nitrate uptake and interactions with architectural phenes. Journal of Experimental Botany 67, 3763–3775.
Spatiotemporal variation of nitrate uptake kinetics within the maize (Zea mays L.) root system is associated with greater nitrate uptake and interactions with architectural phenes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsF2lsbfM&md5=d2d48cd764761133ce163ea277d627faCAS |

Zhan A, Lynch JP (2015) Reduced frequency of lateral root branching improves N capture from low-N soils in maize. Journal of Experimental Botany 66, 2055–2065.
Reduced frequency of lateral root branching improves N capture from low-N soils in maize.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVGjs7%2FL&md5=39f91d63a8d7883a08dddd82055e6d2bCAS |

Zhang H, Forde BG (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409.
An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmsVShtA%3D%3D&md5=28c42264fa8fa0e6f67ef027b06d90cfCAS |

Zhang H, Jennings A, Barlow PW, Forde BG (1999) Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences of the United States of America 96, 6529–6534.
Dual pathways for regulation of root branching by nitrate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXksFKktbc%3D&md5=742b32efbba1bb087acc3043dd2f1ad1CAS |