The DOI matches its Crossref record; 87 of the 87 references it cites were found in a registry or an index.
It’s time to make changes: modulation of root system architecture by nutrient signals
Open accessAbstract
Root growth and development are of outstanding importance for the plant's ability to acquire water and nutrients from different soil horizons. To cope with fluctuating nutrient availabilities, plants integrate systemic signals pertaining to their nutritional status into developmental pathways that regulate the spatial arrangement of roots. Changes in the plant nutritional status and external nutrient supply modulate root system architecture (RSA) over time and determine the degree of root plasticity which is based on variations in the number, extension, placement, and growth direction of individual components of the root system. Roots also sense the local availability of some nutrients, thereby leading to nutrient-specific modifications in RSA, that result from the integration of systemic and local signals into the root developmental programme at specific steps. An in silico analysis of nutrient-responsive genes involved in root development showed that the majority of these specifically responded to the deficiency of individual nutrients while a minority responded to more than one nutrient deficiency. Such an analysis provides an interesting starting point for the identification of the molecular players underlying the sensing and transduction of the nutrient signals that mediate changes in the development and architecture of root systems.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
GENEVESTIGATOR. Arabidopsis Microarray Database and Analysis Toolbox
Zimmermann, P., Hirsch-Hoffmann, M., Hennig, L., & Gruissem, W. (2004) · Plant Physiology · doi:10.1104/pp.104.046367 · Cited by 2,462
Root Architecture and Plant Productivity
Lynch, J. (1995) · Plant Physiology · doi:10.1104/pp.109.1.7 · Cited by 1,905
The role of nutrient availability in regulating root architecture
López-Bucio, J., Cruz-Ramı́rez, A., & Herrera-Estrella, L. (2003) · Current Opinion in Plant Biology · doi:10.1016/s1369-5266(03)00035-9 · Cited by 1,522
An Auxin-Dependent Distal Organizer of Pattern and Polarity in the Arabidopsis Root
Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J., Benfey, P., Leyser, O., Bechtold, N., Weisbeek, P., et al. (1999) · Cell · doi:10.1016/s0092-8674(00)81535-4 · Cited by 1,388
Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems
Lynch, J. P. (2013) · Annals of Botany · doi:10.1093/aob/mcs293 · Cited by 1,385
Roots of the Second Green Revolution
Lynch, J. P. (2007) · Australian Journal of Botany · doi:10.1071/bt06118 · Cited by 1,282
How do plants respond to nutrient shortage by biomass allocation?
Hermans, C., Hammond, J. P., White, P. J., & Verbruggen, N. (2006) · Trends in Plant Science · doi:10.1016/j.tplants.2006.10.007 · Cited by 1,238
An Arabidopsis MADS Box Gene That Controls Nutrient-Induced Changes in Root Architecture
Zhang, H., & Forde, B. G. (1998) · Science · doi:10.1126/science.279.5349.407 · Cited by 1,234
The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche
Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y.-S., Amasino, R., & Scheres, B. (2004) · Cell · doi:10.1016/j.cell.2004.09.018 · Cited by 1,213
The SHORT-ROOT Gene Controls Radial Patterning of the Arabidopsis Root through Radial Signaling
Helariutta, Y., Fukaki, H., Wysocka-Diller, J., Nakajima, K., Jung, J., Sena, G., Hauser, M.-T., & Benfey, P. N. (2000) · Cell · doi:10.1016/s0092-8674(00)80865-x · Cited by 1,133
ARF7 and ARF19 Regulate Lateral Root Formation via Direct Activation of LBD/ASL Genes in Arabidopsis
Okushima, Y., Fukaki, H., Onoda, M., Theologis, A., & Tasaka, M. (2007) · The Plant Cell · doi:10.1105/tpc.106.047761 · Cited by 1,076
Auxin Transport Promotes Arabidopsis Lateral Root Initiation
Casimiro, I., Marchant, A., Bhalerao, R. P., Beeckman, T., Dhooge, S., Swarup, R., Graham, N., Inzé, D., Sandberg, G., Casero, P. J., et al. (2001) · The Plant Cell · doi:10.1105/tpc.13.4.843 · Cited by 1,060
Nitrate-Regulated Auxin Transport by NRT1.1 Defines a Mechanism for Nutrient Sensing in Plants
Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E., Hoyerova, K., Tillard, P., Leon, S., Ljung, K., et al. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.05.008 · Cited by 1,054
Intrinsic and environmental response pathways that regulate root system architecture
MALAMY, J. E. (2005) · Plant, Cell & Environment · doi:10.1111/j.1365-3040.2005.01306.x · Cited by 1,018
Plasticity of the Arabidopsis Root System under Nutrient Deficiencies
Gruber, B. D., Giehl, R. F. H., Friedel, S., & von Wirén, N. (2013) · Plant Physiology · doi:10.1104/pp.113.218453 · Cited by 944
Self-citationA Genetic Framework for the Control of Cell Division and Differentiation in the Root Meristem
Ioio, R. D., Nakamura, K., Moubayidin, L., Perilli, S., Taniguchi, M., Morita, M. T., Aoyama, T., Costantino, P., & Sabatini, S. (2008) · Science · doi:10.1126/science.1164147 · Cited by 944
DREW, M. C. (1975) · New Phytologist · doi:10.1111/j.1469-8137.1975.tb01409.x · Cited by 929
PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development
Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R., & Scheres, B. (2007) · Nature · doi:10.1038/nature06206 · Cited by 899
Topsoil foraging – an architectural adaptation of plants to low phosphorus availability
Lynch, J. P., & Brown, K. M. (2001) · Plant and Soil · doi:10.1023/a:1013324727040 · Cited by 868
Cytokinins Determine Arabidopsis Root-Meristem Size by Controlling Cell Differentiation
Dello Ioio, R., Linhares, F. S., Scacchi, E., Casamitjana-Martinez, E., Heidstra, R., Costantino, P., & Sabatini, S. (2007) · Current Biology · doi:10.1016/j.cub.2007.02.047 · Cited by 834
Arabidopsis lateral root development: an emerging story
Péret, B., De Rybel, B., Casimiro, I., Benková, E., Swarup, R., Laplaze, L., Beeckman, T., & Bennett, M. J. (2009) · Trends in Plant Science · doi:10.1016/j.tplants.2009.05.002 · Cited by 818
The auxin influx carrier LAX3 promotes lateral root emergence
Swarup, K., Benková, E., Swarup, R., Casimiro, I., Péret, B., Yang, Y., Parry, G., Nielsen, E., De Smet, I., Vanneste, S., et al. (2008) · Nature Cell Biology · doi:10.1038/ncb1754 · Cited by 817
The responses of plants to non‐uniform supplies of nutrients
ROBINSON, D. (1994) · New Phytologist · doi:10.1111/j.1469-8137.1994.tb02969.x · Cited by 817
López-Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M. F., Simpson, J., & Herrera-Estrella, L. (2002) · Plant Physiology · doi:10.1104/pp.010934 · Cited by 756
Root system architecture: opportunities and constraints for genetic improvement of crops
de Dorlodot, S., Forster, B., Pagès, L., Price, A., Tuberosa, R., & Draye, X. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.08.012 · Cited by 739
Phosphate Availability Regulates Root System Architecture in Arabidopsis
Williamson, L. C., Ribrioux, S. P. C. P., Fitter, A. H., & Leyser, H. M. O. (2001) · Plant Physiology · doi:10.1104/pp.126.2.875 · Cited by 732
SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem
Sabatini, S., Heidstra, R., Wildwater, M., & Scheres, B. (2003) · Genes & Development · doi:10.1101/gad.252503 · Cited by 731
Dual pathways for regulation of root branching by nitrate
Zhang, H., Jennings, A., Barlow, P. W., & Forde, B. G. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.11.6529 · Cited by 700
Control of Arabidopsis Root Development
Petricka, J. J., Winter, C. M., & Benfey, P. N. (2012) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-042811-105501 · Cited by 672
Linkohr, B. I., Williamson, L. C., Fitter, A. H., & Leyser, H. M. O. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01251.x · Cited by 640
Auxin acts as a local morphogenetic trigger to specify lateral root founder cells
Dubrovsky, J. G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, M. G., Friml, J., Shishkova, S., Celenza, J., & Benková, E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712307105 · Cited by 634
Solute Movement in the Rhizosphere
Tinker, P. B., & Nye, P. (2000) · Oxford University Press eBooks · doi:10.1093/oso/9780195124927.001.0001 · Cited by 620
Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis
De Smet, I., Tetsumura, T., De Rybel, B., Frey, N. F. D., Laplaze, L., Casimiro, I., Swarup, R., Naudts, M., Vanneste, S., Audenaert, D., et al. (2007) · Development · doi:10.1242/dev.02753 · Cited by 620
Cui, H., Levesque, M. P., Vernoux, T., Jung, J. W., Paquette, A. J., Gallagher, K. L., Wang, J. Y., Blilou, I., Scheres, B., & Benfey, P. N. (2007) · Science · doi:10.1126/science.1139531 · Cited by 600
Oscillating Gene Expression Determines Competence for Periodic Arabidopsis Root Branching
Moreno-Risueno, M. A., Van Norman, J. M., Moreno, A., Zhang, J., Ahnert, S. E., & Benfey, P. N. (2010) · Science · doi:10.1126/science.1191937 · Cited by 596
Beemster, G. T. S., & Baskin, T. I. (1998) · Plant Physiology · doi:10.1104/pp.116.4.1515 · Cited by 560
Fagard, M., Desnos, T., Desprez, T., Goubet, F., Refregier, G., Mouille, G., McCann, M., Rayon, C., Vernhettes, S., & Höfte, H. (2000) · The Plant Cell · doi:10.1105/tpc.12.12.2409 · Cited by 559
Hidden Branches: Developments in Root System Architecture
Osmont, K. S., Sibout, R., & Hardtke, C. S. (2007) · Annual Review of Plant Biology · doi:10.1146/annurev.arplant.58.032806.104006 · Cited by 556
Remans, T., Nacry, P., Pervent, M., Filleur, S., Diatloff, E., Mounier, E., Tillard, P., Forde, B. G., & Gojon, A. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0605275103 · Cited by 554
Pérez-Torres, C.-A., López-Bucio, J., Cruz-Ramírez, A., Ibarra-Laclette, E., Dharmasiri, S., Estelle, M., & Herrera-Estrella, L. (2009) · The Plant Cell · doi:10.1105/tpc.108.058719 · Cited by 545
Embryonic origin of the Arabidopsis primary root and root meristem initials
Scheres, B., Wolkenfelt, H., Willemsen, V., Terlouw, M., Lawson, E., Dean, C., & Weisbeek, P. (1994) · Development · doi:10.1242/dev.120.9.2475 · Cited by 519
Cailliatte, R., Schikora, A., Briat, J.-F., Mari, S., & Curie, C. (2010) · The Plant Cell · doi:10.1105/tpc.109.073023 · Cited by 506
Control of auxin-regulated root development by the Arabidopsis thaliana SHY2/IAA3 gene
Tian, Q., & Reed, J. W. (1999) · Development · doi:10.1242/dev.126.4.711 · Cited by 500
DREW, M. C., & SAKER, L. R. (1975) · Journal of Experimental Botany · doi:10.1093/jxb/26.1.79 · Cited by 497
Hormone interactions during lateral root formation
Fukaki, H., & Tasaka, M. (2009) · Plant Molecular Biology · doi:10.1007/s11103-008-9417-2 · Cited by 476
The nutritional control of root development
Forde, B., & Lorenzo, H. (2001) · Plant and Soil · doi:10.1023/a:1010329902165 · Cited by 474
A pathway for lateral root formation in Arabidopsis thaliana.
Celenza, J. L., Grisafi, P. L., & Fink, G. R. (1995) · Genes & Development · doi:10.1101/gad.9.17.2131 · Cited by 465
Expansive growth of plant cell walls
Cosgrove, D. J. (2000) · Plant Physiology and Biochemistry · doi:10.1016/s0981-9428(00)00164-9 · Cited by 461
Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth
Sozzani, R., Cui, H., Moreno-Risueno, M. A., Busch, W., Van Norman, J. M., Vernoux, T., Brady, S. M., Dewitte, W., Murray, J. A. H., & Benfey, P. N. (2010) · Nature · doi:10.1038/nature09143 · Cited by 438
The nutritional control of root development
Forde, B., & Lorenzo, H. (2002) · Interactions in the Root Environment: An Integrated Approach · doi:10.1007/978-94-010-0566-1_6 · Cited by 429
Cytokinin regulates root meristem activity via modulation of the polar auxin transport
Růžička, K., Šimášková, M., Duclercq, J., Petrášek, J., Zažímalová, E., Simon, S., Friml, J., Van Montagu, M. C. E., & Benková, E. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0900060106 · Cited by 419
Root System Architecture from Coupling Cell Shape to Auxin Transport
Laskowski, M., Grieneisen, V. A., Hofhuis, H., Hove, C. A. T., Hogeweg, P., Marée, A. F. M., & Scheres, B. (2008) · PLoS Biology · doi:10.1371/journal.pbio.0060307 · Cited by 405
Sánchez-Calderón, L., López-Bucio, J., Chacón-López, A., Cruz-Ramírez, A., Nieto-Jacobo, F., Dubrovsky, J. G., & Herrera-Estrella, L. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci011 · Cited by 380
Chen, W. W., Yang, J. L., Qin, C., Jin, C. W., Mo, J. H., Ye, T., & Zheng, S. J. (2010) · Plant Physiology · doi:10.1104/pp.110.161109 · Cited by 373
Ethylene Mediates Response and Tolerance to Potassium Deprivation in Arabidopsis
Jung, J.-Y., Shin, R., & Schachtman, D. P. (2009) · The Plant Cell · doi:10.1105/tpc.108.063099 · Cited by 370
Receptor-Like Kinase ACR4 Restricts Formative Cell Divisions in the Arabidopsis Root
De Smet, I., Vassileva, V., De Rybel, B., Levesque, M. P., Grunewald, W., Van Damme, D., Van Noorden, G., Naudts, M., Van Isterdael, G., De Clercq, R., et al. (2008) · Science · doi:10.1126/science.1160158 · Cited by 370
Nitrate signaling: adaptation to fluctuating environments
Krouk, G., Crawford, N. M., Coruzzi, G. M., & Tsay, Y.-F. (2010) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2009.12.003 · Cited by 367
Plant root proliferation in nitrogen–rich patches confers competitive advantage
Robinson, D., Hodge, A., Griffiths, B. S., & FITTER, A. H. (1999) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1999.0656 · Cited by 364
Terasaka, K., Blakeslee, J. J., Titapiwatanakun, B., Peer, W. A., Bandyopadhyay, A., Makam, S. N., Lee, O. R., Richards, E. L., Murphy, A. S., Sato, F., et al. (2005) · The Plant Cell · doi:10.1105/tpc.105.035816 · Cited by 360
Sun, J., Xu, Y., Ye, S., Jiang, H., Chen, Q., Liu, F., Zhou, W., Chen, R., Li, X., Tietz, O., et al. (2009) · The Plant Cell · doi:10.1105/tpc.108.064303 · Cited by 344
The Effect of Iron on the Primary Root Elongation of Arabidopsis during Phosphate Deficiency
Ward, J. T., Lahner, B., Yakubova, E., Salt, D. E., & Raghothama, K. G. (2008) · Plant Physiology · doi:10.1104/pp.108.118562 · Cited by 335
Lima, J. E., Kojima, S., Takahashi, H., & von Wirén, N. (2010) · The Plant Cell · doi:10.1105/tpc.110.076216 · Cited by 325
Self-citationHodge, A., Robinson, D., Griffiths, B. S., & Fitter, A. H. (1999) · Plant, Cell & Environment · doi:10.1046/j.1365-3040.1999.00454.x · Cited by 316
Schumacher, K., Vafeados, D., McCarthy, M., Sze, H., Wilkins, T., & Chory, J. (1999) · Genes & Development · doi:10.1101/gad.13.24.3259 · Cited by 314
Goh, T., Joi, S., Mimura, T., & Fukaki, H. (2012) · Development · doi:10.1242/dev.071928 · Cited by 299
Physiological characterization of Mg deficiency in Arabidopsis thaliana
Hermans, C., & Verbruggen, N. (2005) · Journal of Experimental Botany · doi:10.1093/jxb/eri215 · Cited by 287
Fukaki, H., Nakao, Y., Okushima, Y., Theologis, A., & Tasaka, M. (2005) · The Plant Journal · doi:10.1111/j.1365-313x.2005.02537.x · Cited by 282
Jackson, R. B., & Caldwell, M. M. (1989) · Oecologia · doi:10.1007/bf00379798 · Cited by 278
Ticconi, C. A., Lucero, R. D., Sakhonwasee, S., Adamson, A. W., Creff, A., Nussaume, L., Desnos, T., & Abel, S. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0901778106 · Cited by 263
A role for nitrilase 3 in the regulation of root morphology in sulphur‐starving Arabidopsis thaliana
Kutz, A., Müller, A., Hennig, P., Kaiser, W. M., Piotrowski, M., & Weiler, E. W. (2002) · The Plant Journal · doi:10.1046/j.1365-313x.2002.01271.x · Cited by 242
The IAA1 protein is encoded by AXR5 and is a substrate of SCFTIR1
Yang, X., Lee, S., So, J., Dharmasiri, S., Dharmasiri, N., Ge, L., Jensen, C., Hangarter, R., Hobbie, L., & Estelle, M. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02254.x · Cited by 226
Lally, D., Ingmire, P., Tong, H.-Y., & He, Z.-H. (2001) · The Plant Cell · doi:10.1105/tpc.010075 · Cited by 211
Hirota, A., Kato, T., Fukaki, H., Aida, M., & Tasaka, M. (2007) · The Plant Cell · doi:10.1105/tpc.107.050674 · Cited by 206
Root growth and nitrate utilization of maize cultivars under field conditions
Wiesler, F., & Horst, W. J. (1994) · Plant and Soil · doi:10.1007/bf00007976 · Cited by 193
Giehl, R. F. H., Lima, J. E., & von Wirén, N. (2012) · The Plant Cell · doi:10.1105/tpc.111.092973 · Cited by 190
Self-citationWu, G., Lewis, D. R., & Spalding, E. P. (2007) · The Plant Cell · doi:10.1105/tpc.106.048777 · Cited by 179
Scheres, B., Benfey, P. N., & Dolan, L. (2002) · The Arabidopsis Book · doi:10.1199/tab.0101 · Cited by 169
Lateral root initiation: one step at a time
De Smet, I. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2011.03996.x · Cited by 162
Lally, D. (2001) · THE PLANT CELL ONLINE · doi:10.1105/tpc.13.6.1317 · Cited by 160
Burns, I. G. (1980) · Journal of Soil Science · doi:10.1111/j.1365-2389.1980.tb02073.x · Cited by 155
An Auxin Transport Mechanism Restricts Positive Orthogravitropism in Lateral Roots
Rosquete, M. R., von Wangenheim, D., Marhavý, P., Barbez, E., Stelzer, E. H. K., Benková, E., Maizel, A., & Kleine‐Vehn, J. (2013) · Current Biology · doi:10.1016/j.cub.2013.03.064 · Cited by 129
Plant root growth and the marginal value theorem
McNickle, G. G., & Cahill, J. F. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0807971106 · Cited by 110
Richard‐Molard, C., Krapp, A., Brun, F., Ney, B., Daniel‐Vedele, F., & Chaillou, S. (2008) · Journal of Experimental Botany · doi:10.1093/jxb/erm363 · Cited by 88
Developmental plasticity in plants: implications of non-cognitive behavior
Novoplansky, A. (2002) · Evolutionary Ecology · doi:10.1023/a:1019617409133 · Cited by 66
Genetic analysis of the gravitropic set-point angle in lateral roots of arabidopsis
Mullen, J. L., & Hangarter, R. P. (2003) · Advances in Space Research · doi:10.1016/s0273-1177(03)00249-7 · Cited by 50
Granato, T. C., Raper, C. D., & Wilkerson, G. G. (1989) · Physiologia Plantarum · doi:10.1111/j.1399-3054.1989.tb06213.x · Cited by 26
Recent Advances in Nutrient Sensing and Signaling
Schachtman, D. P. (2012) · Molecular Plant · doi:10.1093/mp/sss109 · Cited by 14
Cited by
Root Architecture Responses: In Search of Phosphate
Péret, B., Desnos, T., Jost, R., Kanno, S., Berkowitz, O., & Nussaume, L. (2014) · Plant Physiology · doi:10.1104/pp.114.244541 · Cited by 292
Metadata
- Authors
- Giehl, R. F. H., Gruber, B. D., & von Wirén, N.
- Venue
- Journal of Experimental Botany
- Publisher
- Oxford University Press (OUP)
- Published
- 2013-12-18
- Volume
- 65
- Issue
- 3
- Pages
- 769-778
- ISSN
- 0022-0957 (ISSN-L)
- 1460-2431
- OpenAlex
- W2103247929
- Cited by
- 295
- References
- 87
- FWCI
- 17.58
- Type
- journal article
- Language
- en
- Open access
- bronze
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
Data sources
Bibliographic data: Semantic Scholar, OpenAlex, Crossref.
Contains information from the Semantic Scholar Academic Graph Datasets, made available under the ODC Attribution License (ODC-BY 1.0).
Semantic Scholar’s data is described in: Kinney, R., et al. (2023). The Semantic Scholar Open Data Platform. arXiv:2301.10140.