Root Architecture Responses: In Search of Phosphate

Péret, Benjamin; Desnos, Thierry; Jost, Ricarda; Kanno, Satomi; Berkowitz, Oliver; Nussaume, Laurent

doi:10.1104/pp.114.244541

Cited by 292Plant nutrient uptake and metabolismPlant Parasitism and ResistancePlant Molecular Biology Research

Root Architecture Responses: In Search of Phosphate

Open access

Péret, Benjamin, Desnos, Thierry, Jost, Ricarda, Kanno, Satomi, Berkowitz, Oliver, Nussaume, Laurent·2014·Plant Physiology

DOI 10.1104/pp.114.244541PMC PMC4256877

Open this paper in CoChat — free account

Abstract

Soil phosphate represents the only source of phosphorus for plants and, consequently, is its entry into the trophic chain. This major component of nucleic acids, phospholipids, and energy currency of the cell (ATP) can limit plant growth because of its low mobility in soil. As a result, root responses to low phosphate favor the exploration of the shallower part of the soil, where phosphate tends to be more abundant, a strategy described as topsoil foraging. We will review the diverse developmental strategies that can be observed among plants by detailing the effect of phosphate deficiency on primary and lateral roots. We also discuss the formation of cluster roots: an advanced adaptive strategy to cope with low phosphate availability observed in a limited number of species. Finally, we will put this work into perspective for future research directions.

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

Crossref · 10.1104/pp.114.244541

Cites

100 of 100 references verified0 citation errors · 0 not checkable

Statistics

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.

Arbuscular mycorrhiza: the mother of plant root endosymbioses
Parniske, M. (2008) · Nature Reviews Microbiology · doi:10.1038/nrmicro1987 · Cited by 2,176 · see citing works
The plastic plant: root responses to heterogeneous supplies of nutrients
Hodge, A. (2004) · New Phytologist · doi:10.1111/j.1469-8137.2004.01015.x · Cited by 1,692 · see citing works
Plant nutrient-acquisition strategies change with soil age
Lambers, H., RAVEN, J., Shaver, G. R., & SMITH, S. (2008) · Trends in Ecology & Evolution · doi:10.1016/j.tree.2007.10.008 · Cited by 1,414 · see citing works
Root Structure and Functioning for Efficient Acquisition of Phosphorus: Matching Morphological and Physiological Traits
Lambers, H., Shane, M. W., Cramer, M. D., Pearse, S. J., & Veneklaas, E. J. (2006) · Annals of Botany · doi:10.1093/aob/mcl114 · Cited by 1,321 · see citing works
Roles of Arbuscular Mycorrhizas in Plant Phosphorus Nutrition: Interactions between Pathways of Phosphorus Uptake in Arbuscular Mycorrhizal Roots Have Important Implications for Understanding and Manipulating Plant Phosphorus Acquisition
Smith, S. E., Jakobsen, I., Grønlund, M., & SMITH, F. A. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.174581 · Cited by 1,250 · see citing works
Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops
Lynch, J. P. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.175414 · Cited by 1,071 · see citing works
Opportunities for improving phosphorus‐use efficiency in crop plants
Veneklaas, E. J., Lambers, H., Bragg, J. G., Finnegan, P. M., Lovelock, C. E., Plaxton, W. C., Price, C. A., Scheible, W., Shane, M. W., White, P. J., et al. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2012.04190.x · Cited by 1,002 · see citing works
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 964 · see citing works
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 871 · see citing works
Arabidopsis lateral root development: an emerging story
Péret, B., Rybel, B. D., 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 819 · see citing works
Self-citation
Phosphate transport in Arabidopsis : Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low‐ and high‐phosphate environments
Shin, H., Shin, H., Dewbre, G. R., & Harrison, M. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02161.x · Cited by 812 · see citing works
The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency
Gamuyao, R., Chin, J. H., Pariasca‐Tanaka, J., Pesaresi, P., Catausan, S., Dalid, C. O., Slamet‐Loedin, I. H., Tecson‐Mendoza, E. M., Wissuwa, M., & Heuer, S. (2012) · Nature · doi:10.1038/nature11346 · Cited by 788 · see citing works
Stress-induced morphogenic responses: growing out of trouble?
Potters, G., Pasternak, T. P., Guisez, Y., Palme, K. J., & Jansen, M. A. K. (2007) · Trends in Plant Science · doi:10.1016/j.tplants.2007.01.004 · Cited by 771 · see citing works
Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System
López‐Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M. F., Simpson, J. K., & Herrera‐Estrella, L. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.010934 · Cited by 760 · see citing works
Phosphate Availability Regulates Root System Architecture in Arabidopsis
Williamson, L. C., Ribrioux, S. P. C. P., FITTER, A. H., & Leyser, O. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.126.2.875 · Cited by 736 · see citing works
OsPHR2 Is Involved in Phosphate-Starvation Signaling and Excessive Phosphate Accumulation in Shoots of Plants
Zhou, J., Jiao, F., Wu, Z., Li, Y., Wang, X., He, X., Zhong, W., & Wu, P. (2008) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.111443 · Cited by 675 · see citing works
Lateral root development in Arabidopsis: fifty shades of auxin
Lavenus, J., Goh, T., Roberts, I., Guyomarc’h, S., Lucas, M., Smet, I. D., Fukaki, H., Beeckman, T., Bennett, M. J., & Laplaze, L. (2013) · Trends in Plant Science · doi:10.1016/j.tplants.2013.04.006 · Cited by 639 · see citing works
Responses of root architecture development to low phosphorus availability: a review
Niu, Y. F., Chai, R. S., Jin, G. L., Wang, H., Tang, C. X., & Zhang, Y. S. (2013) · Annals of Botany · doi:10.1093/aob/mcs285 · Cited by 617 · see citing works
Root tip contact with low-phosphate media reprograms plant root architecture
Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet-Aurigny, A., Nussaume, L., & Desnos, T. (2007) · Nature Genetics · doi:10.1038/ng2041 · Cited by 592 · see citing works
Self-citation
OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes
Hopper, S. D. (2009) · Plant and Soil · doi:10.1007/s11104-009-0068-0 · Cited by 588 · see citing works
Phosphate import in plants: focus on the PHT1 transporters
Nussaume, L. (2011) · Frontiers in Plant Science · doi:10.3389/fpls.2011.00083 · Cited by 560 · see citing works
Self-citation
Phosphate Availability Alters Lateral Root Development inArabidopsisby Modulating Auxin Sensitivity via a Mechanism Involving the TIR1 Auxin Receptor
Pérez-Torres, C.-A., López‐Bucio, J., Cruz‐Ramírez, A., Ibarra‐Laclette, E., Dharmasiri, S., Estelle, M. A., & Herrera‐Estrella, L. (2008) · The Plant Cell · doi:10.1105/tpc.108.058719 · Cited by 551 · see citing works
Root developmental adaptation to phosphate starvation: better safe than sorry
Péret, B., Clément, M., Nussaume, L., & Desnos, T. (2011) · Trends in Plant Science · doi:10.1016/j.tplants.2011.05.006 · Cited by 538 · see citing works
Self-citation
A pathway for lateral root formation in Arabidopsis thaliana.Preprint
Celenza, J. L., Grisafi, P. L., & Fink, G. R. (1995) · Genes & Development · doi:10.1101/gad.9.17.2131 · Cited by 465 · see citing works
Cluster Roots: A Curiosity in Context
Shane, M. W., & Lambers, H. (2005) · Plant and Soil · doi:10.1007/s11104-004-2725-7 · Cited by 418 · see citing works
Cluster roots – an underground adaptation for survival in extreme environments
Neumann, G., & Martinoia, E. (2002) · Trends in Plant Science · doi:10.1016/s1360-1385(02)02241-0 · Cited by 412 · see citing works
Phosphate Starvation Induces a Determinate Developmental Program in the Roots of Arabidopsis thaliana
Sánchez-Calderón, L., López‐Bucio, J., Chacón-López, A., Cruz‐Ramírez, A., Nieto-Jacobo, M. F., DUBROVSKY, J. G., & Herrera‐Estrella, L. (2005) · Plant and Cell Physiology · doi:10.1093/pcp/pci011 · Cited by 382 · see citing works
Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice
Sun, H., Tao, J., Liu, S., Huang, S., Chen, S., Xie, X., Yoneyama, K., Zhang, Y., & Xu, G. (2014) · Journal of Experimental Botany · doi:10.1093/jxb/eru029 · Cited by 377 · see citing works
A Role for Auxin Redistribution in the Responses of the Root System Architecture to Phosphate Starvation in Arabidopsis
Nacry, P., Canivenc, G., Muller, B., Azmi, A., Onckelen, H. A. V., Rossignol, M., & Doumas, P. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.060061 · Cited by 346 · see citing works
Strategies for improving phosphorus acquisition efficiency of crop plants
Ramaekers, L., Remans, R., Rao, I. M., Blair, M. W., & Vanderleyden, J. (2010) · Field Crops Research · doi:10.1016/j.fcr.2010.03.001 · Cited by 342 · see citing works
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 336 · see citing works
Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis
Thibaud, M., Arrighi, J., Bayle, V., Chiarenza, S., Creff, A., Bustos, R., Paz‐Ares, J., Poirier, Y., & Nussaume, L. (2010) · The Plant Journal · doi:10.1111/j.1365-313x.2010.04375.x · Cited by 334 · see citing works
Self-citation
Characterization of a Phosphate-Accumulator Mutant of Arabidopsis thaliana
Delhaize, E., & Randall, P. J. (1995) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.1.207 · Cited by 324 · see citing works
Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris
Bonser, A., Lynch, J. P., & Snapp, S. S. (1996) · New Phytologist · doi:10.1111/j.1469-8137.1996.tb01847.x · Cited by 315 · see citing works
It’s time to make changes: modulation of root system architecture by nutrient signals
Giehl, R. F. H., Gruber, B. D., & Nicolaus Von Wirén, A. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert421 · Cited by 298 · see citing works
Arabidopsis WRKY45 Transcription Factor Activates PHOSPHATE TRANSPORTER1;1 Expression in Response to Phosphate Starvation
Wang, H., Xu, Q., Kong, Y., Chen, Y., Duan, J.-Y., Wu, W., & Chen, Y. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.113.235077 · Cited by 280 · see citing works
Proteaceae from severely phosphorus‐impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus‐use‐efficiency
Lambers, H., Cawthray, G. R., Giavalisco, P., Kuo, J., Laliberté, É., Pearse, S. J., Scheible, W., Stitt, M., Teste, F. P., & Turner, B. L. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2012.04285.x · Cited by 277 · see citing works
ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability
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 262 · see citing works
Self-citation
OsMYB2P-1 , an R2R3 MYB Transcription Factor, Is Involved in the Regulation of Phosphate-Starvation Responses and Root Architecture in Rice
Dai, X., Wang, Y., Yang, A., & Zhang, W. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.194217 · Cited by 257 · see citing works
Identification of tyrosylprotein sulfotransferase in Arabidopsis
Komori, R., Amano, Y., Ogawa, M., & Matsubayashi, Y. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0902801106 · Cited by 251 · see citing works
The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation
Rémy, E., Cabrito, T. R., Batista, R. A., Teixeira, M. C., Sá‐Correia, I., & Duque, P. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2012.04167.x · Cited by 247 · see citing works
Arabidopsis pdr2 reveals a phosphate‐sensitive checkpoint in root development
Ticconi, C. A., Delatorre, C. A., Lahner, B., Salt, D. E., & Abel, S. (2004) · The Plant Journal · doi:10.1111/j.1365-313x.2004.02005.x · Cited by 245 · see citing works
Analysis of the Root System Architecture of Arabidopsis Provides a Quantitative Readout of Crosstalk between Nutritional Signals
Kellermeier, F., Armengaud, P., Seditas, T. J., Danku, J., Salt, D. E., & Anna Amtmann, A. (2014) · The Plant Cell · doi:10.1105/tpc.113.122101 · Cited by 243 · see citing works
Strigolactones and the control of plant development: lessons from shoot branching
Waldie, T., McCulloch, H., & Leyser, O. (2014) · The Plant Journal · doi:10.1111/tpj.12488 · Cited by 242 · see citing works
Structure, ecology and physiology of root clusters – a review
Lamont, B. B. (2003) · Plant and Soil · doi:10.1023/a:1022314613217 · Cited by 241 · see citing works
LEAF TIP NECROSIS1 Plays a Pivotal Role in the Regulation of Multiple Phosphate Starvation Responses in Rice
Hu, B., Zhu, C., Li, F., Tang, J., Wang, Y., Lin, A., Liu, L., Che, R., & Chu, C. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.170209 · Cited by 235 · see citing works
An online database for plant image analysis software tools
Lobet, G., Draye, X., & Périlleux, C. (2013) · Plant Methods · doi:10.1186/1746-4811-9-38 · Cited by 232 · see citing works
Genetic and Genomic Evidence That Sucrose Is a Global Regulator of Plant Responses to Phosphate Starvation in Arabidopsis
Lei, M., Liu, Y., Zhang, B., Zhao, Y.-T., Wang, X., Zhou, Y., Raghothama, K. G., & Liu, D. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.110.171736 · Cited by 229 · see citing works
Phosphorus Nutrition of Proteaceae in Severely Phosphorus-Impoverished Soils: Are There Lessons To Be Learned for Future Crops?
Lambers, H., Finnegan, P. M., Laliberté, É., Pearse, S. J., Ryan, M. H., Shane, M. W., & Veneklaas, E. J. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.174318 · Cited by 221 · see citing works
Linking Development and Determinacy with Organic Acid Efflux from Proteoid Roots of White Lupin Grown with Low Phosphorus and Ambient or Elevated Atmospheric CO2 Concentration1
Watt, M., & Evans, J. R. (1999) · PLANT PHYSIOLOGY · doi:10.1104/pp.120.3.705 · Cited by 221 · see citing works
An RNA-Seq Transcriptome Analysis of Orthophosphate-Deficient White Lupin Reveals Novel Insights into Phosphorus Acclimation in Plants
O’Rourke, J. A., Yang, S. S., Miller, S. S., Bucciarelli, B., Liu, J., Rydeen, A. B., Bozsóki, Z., Uhde‐Stone, C., Tu, Z. J., Allan, D. L., et al. (2012) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.209254 · Cited by 219 · see citing works
The Arabidopsis Purple Acid Phosphatase AtPAP10 Is Predominantly Associated with the Root Surface and Plays an Important Role in Plant Tolerance to Phosphate Limitation
Wang, L., Li, Z., Qian, W., Guo, W., Gao, X., Huang, L., Wang, H., Zhu, H., Wu, J., Wang, D., et al. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.183723 · Cited by 217 · see citing works
Sugar Signaling in Root Responses to Low Phosphorus Availability
Hammond, J. P., & White, P. J. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.175380 · Cited by 203 · see citing works
Phosphite, an Analog of Phosphate, Suppresses the Coordinated Expression of Genes under Phosphate Starvation
Varadarajan, D. K., Karthikeyan, A. S., Matilda, P. D., & Raghothama, K. G. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.010835 · Cited by 199 · see citing works
Conserved and diverse mechanisms in root development
Hochholdinger, F., & Zimmermann, R. (2007) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2007.10.002 · Cited by 196 · see citing works
Ethylene signalling is involved in regulation of phosphate starvation‐induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis
Lei, M., Zhu, C., Liu, Y., Karthikeyan, A. S., Bressan, R. A., Raghothama, K. G., & Liu, D. (2010) · New Phytologist · doi:10.1111/j.1469-8137.2010.03555.x · Cited by 194 · see citing works
Arabidopsis Tyrosylprotein Sulfotransferase Acts in the Auxin/PLETHORA Pathway in Regulating Postembryonic Maintenance of the Root Stem Cell Niche
Zhou, W., Wei, L., Xu, J., Zhai, Q., Jiang, H., Chen, R., Chen, Q., Sun, J., Chu, J., Zhu, L., et al. (2010) · The Plant Cell · doi:10.1105/tpc.110.075721 · Cited by 193 · see citing works
An Auxin Transport Independent Pathway Is Involved in Phosphate Stress-Induced Root Architectural Alterations in Arabidopsis. Identification of BIG as a Mediator of Auxin in Pericycle Cell Activation
López‐Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Pérez-Torres, A., Rampey, R. A., Bartel, B., & Herrera‐Estrella, L. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.104.049577 · Cited by 186 · see citing works
Attenuation of Phosphate Starvation Responses by Phosphite in Arabidopsis
Ticconi, C. A. (2001) · PLANT PHYSIOLOGY · doi:10.1104/pp.127.3.963 · Cited by 183 · see citing works
Developmental Physiology of Cluster-Root Carboxylate Synthesis and Exudation in Harsh Hakea. Expression of Phosphoenolpyruvate Carboxylase and the Alternative Oxidase
Shane, M. W., Cramer, M. D., Funayama‐Noguchi, S., Cawthray, G. R., Millar, A. H., Day, D. A., & Lambers, H. (2004) · PLANT PHYSIOLOGY · doi:10.1104/pp.103.035659 · Cited by 174 · see citing works
Arabidopsis Ferritin 1 (AtFer1) Gene Regulation by the Phosphate Starvation Response 1 (AtPHR1) Transcription Factor Reveals a Direct Molecular Link between Iron and Phosphate Homeostasis
Bournier, M., Tissot, N., Mari, S., Boucherez, J., Lacombe, E., Briat, J., & Gaymard, F. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.482281 · Cited by 165 · see citing works
The peptide growth factor, phytosulfokine, attenuates pattern‐triggered immunity
Igarashi, D., Tsuda, K., & Katagiri, F. (2012) · The Plant Journal · doi:10.1111/j.1365-313x.2012.04950.x · Cited by 161 · see citing works
Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus‐use efficiency of P roteaceae species
Ronan Sulpice, A., Ishihara, H., Schlereth, A., Cawthray, G. R., Encke, B., Giavalisco, P., Ivakov, A. A., Arrivault, S., Jost, R., Krohn, N., et al. (2013) · Plant Cell & Environment · doi:10.1111/pce.12240 · Cited by 160 · see citing works
Self-citation
Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling
Al-Ghazi, Y., Muller, B., Pinloche, S., Tranbarger, T. J., Nacry, P., Rossignol, M., Tardieu, F., & Doumas, P. (2003) · Plant Cell & Environment · doi:10.1046/j.1365-3040.2003.01030.x · Cited by 155 · see citing works
Ethylene in vegetative development: a tale with a riddle
Vandenbussche, F., Vaseva, I., Vissenberg, K., & Straeten, D. V. D. (2012) · New Phytologist · doi:10.1111/j.1469-8137.2012.04100.x · Cited by 155 · see citing works
Shoot P status regulates cluster‐root growth and citrate exudation in Lupinus albus grown with a divided root system
Shane, M. W., de Vos, M., de Roock, S., & Lambers, H. (2003) · Plant Cell & Environment · doi:10.1046/j.1365-3040.2003.00957.x · Cited by 153 · see citing works
The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana
Robinson, W. D., Park, J., Tran, H., Vecchio, H. A. D., Ying, S., Zins, J. L., Patel, K., McKnight, T. D., & Plaxton, W. C. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers309 · Cited by 153 · see citing works
Cluster roots: some ecological considerations
Skene, K. R. (1998) · Journal of Ecology · doi:10.1046/j.1365-2745.1998.00326.x · Cited by 146 · see citing works
Auxin response factor (Os ARF 12), a novel regulator for phosphate homeostasis in rice (Oryza sativa)
Wang, S., Zhang, S., Sun, C., Xu, Y., Chen, Y., Yu, C., Qian, Q., Jiang, D., & Qi, Y. (2013) · New Phytologist · doi:10.1111/nph.12499 · Cited by 141 · see citing works
Biochemical and molecular characterization of AtPAP12 and AtPAP26: the predominant purple acid phosphatase isozymes secreted by phosphate‐starved Arabidopsis thaliana
Tran, H., Qian, W., Hurley, B. A., She, Y., Wang, D., & Plaxton, W. C. (2010) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2010.02184.x · Cited by 138 · see citing works
Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br.
Shane, M. W., de Vos, M., de Roock, S., Cawthray, G. R., & Lambers, H. (2003) · Plant and Soil · doi:10.1023/a:1022320416038 · Cited by 112 · see citing works
Ethylene's Role in Phosphate Starvation Signaling: More than Just a Root Growth Regulator
Nagarajan, V. K., & Smith, A. P. (2011) · Plant and Cell Physiology · doi:10.1093/pcp/pcr186 · Cited by 110 · see citing works
High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities
Shi, L. G., Shi, T., Broadley, M. R., White, P. J., Yan, L., Meng, J., Xu, F., & Hammond, J. P. (2012) · Annals of Botany · doi:10.1093/aob/mcs245 · Cited by 102 · see citing works
A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae)
Shane, M. W., Szota, C., & Lambers, H. (2004) · Plant Cell & Environment · doi:10.1111/j.1365-3040.2004.01204.x · Cited by 101 · see citing works
Phosphate Deprivation in Maize: Genetics and Genomics
Calderón-Vázquez, C. L., Sawers, R. J. H., & Herrera‐Estrella, L. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.174987 · Cited by 91 · see citing works
Expression of Sucrose Transporter cDNAs Specifically in Companion Cells Enhances Phloem Loading and Long-Distance Transport of Sucrose but Leads to an Inhibition of Growth and the Perception of a Phosphate Limitation
Dasgupta, K., Khadilkar, A., Ronan Sulpice, A., Pant, B. D., Scheible, W., Fisahn, J., Stitt, M., & Ayre, B. G. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.238410 · Cited by 90 · see citing works
Phosphate sensing in root development
Abel, S. (2011) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2011.04.007 · Cited by 89 · see citing works
Pattern Formation in Cluster Roots: Some Developmental and Evolutionary Considerations
Skene, K. R. (2000) · Annals of Botany · doi:10.1006/anbo.2000.1140 · Cited by 89 · see citing works
Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone
Li, Z., Xu, C., Li, K., Yan, S., Qu, X., & Zhang, J. (2012) · BMC Plant Biology · doi:10.1186/1471-2229-12-89 · Cited by 86 · see citing works
The morphology and anatomy of proteoid roots in the genus Hakea
Lamont, B. B. (1972) · Australian Journal of Botany · doi:10.1071/bt9720155 · Cited by 81 · see citing works
Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency
Kang, J. G., Yu, H., Tian, C., Zhou, W., Li, C., Jiao, Y., & Liu, D. (2014) · PLANT PHYSIOLOGY · doi:10.1104/pp.114.238725 · Cited by 80 · see citing works
The SABRE gene is required for normal cell expansion in Arabidopsis.Preprint
Aeschbacher, R. A., Hauser, M., Feldmann, K. A., & Benfey, P. N. (1995) · Genes & Development · doi:10.1101/gad.9.3.330 · Cited by 80 · see citing works
Update on White Lupin Cluster Root Acclimation to Phosphorus Deficiency Update on Lupin Cluster Roots
Cheng, L., Bucciarelli, B., Shen, J., Allan, D. L., & Vance, C. P. (2011) · PLANT PHYSIOLOGY · doi:10.1104/pp.111.175174 · Cited by 79 · see citing works
Molecular mechanisms in response to phosphate starvation in rice
Panigrahy, M., Rao, D. N., & Sarla, N. (2009) · Biotechnology Advances · doi:10.1016/j.biotechadv.2009.02.006 · Cited by 73 · see citing works
RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin
Secco, D., Shou, H., Whelan, J., & Berkowitz, O. (2014) · BMC Genomics · doi:10.1186/1471-2164-15-230 · Cited by 71 · see citing works
Self-citation
Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice
Yang, W. T., Baek, D., Yun, D., Hwang, W. H., Park, D. S., Nam, M. H., Chung, E. S., Chung, Y. S., Yi, Y. B., & Kim, D.-H. (2014) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2014.02.024 · Cited by 71 · see citing works
Forest biotechnology – thriving despite controversy
Strauss, S. H. (2004) · New Phytologist · doi:10.1111/j.1469-8137.2004.01103.x · Cited by 60 · see citing works
Reciprocal Control of Anaplerotic Phosphoenolpyruvate Carboxylase by in Vivo Monoubiquitination and Phosphorylation in Developing Proteoid Roots of Phosphate-Deficient Harsh Hakea
Shane, M. W., Fedosejevs, E. T., & Plaxton, W. C. (2013) · PLANT PHYSIOLOGY · doi:10.1104/pp.112.213496 · Cited by 60 · see citing works
Iron deficiency induces cluster (proteoid) root formation in Casuarina glauca
Arahou, M., & Diem, H. G. (1997) · Plant and Soil · doi:10.1023/a:1004268825395 · Cited by 50 · see citing works
The Arabidopsis gene HYPERSENSITIVE TO PHOSPHATE STARVATION 3 encodes ETHYLENE OVERPRODUCTION 1
Wang, L., Dong, J., Gao, Z., & Liu, D. (2012) · Plant and Cell Physiology · doi:10.1093/pcp/pcs072 · Cited by 48 · see citing works
APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability
González-Mendoza, V. M., Zurita‐Silva, A., Sánchez-Calderón, L., Sanchez‐Sandoval, E., Oropeza‐Aburto, A., Gutiérrez-Alanís, D., Alatorre‐Cobos, F., & Herrera‐Estrella, L. (2013) · Plant Science · doi:10.1016/j.plantsci.2012.12.015 · Cited by 44 · see citing works
HPS4/SABRE regulates plant responses to phosphate starvation through antagonistic interaction with ethylene signalling
Yu, H., Luo, N., Sun, L., & Liu, D. (2012) · Journal of Experimental Botany · doi:10.1093/jxb/ers131 · Cited by 41 · see citing works
Acclimation responses of Arabidopsis thaliana to sustained phosphite treatments
Berkowitz, O., Jost, R., Kollehn, D., Fenske, R., Finnegan, P. M., O’Brien, P. A., Hardy, G. E. S. J., & Lambers, H. (2013) · Journal of Experimental Botany · doi:10.1093/jxb/ert037 · Cited by 40 · see citing works
Self-citation
A Novel Rice Gene, NRR Responds to Macronutrient Deficiency and Regulates Root Growth
Zhang, Y., Yan, Y., Wang, L., YANG, K. Y., Xiao, N., Liu, Y., Fu, Y., Sun, Z., Fang, R., & Chen, X.-Y. (2011) · Molecular Plant · doi:10.1093/mp/ssr066 · Cited by 36 · see citing works
Does Ethylene Mediate Cluster Root Formation under Iron Deficiency?
Zaid, H. (2003) · Annals of Botany · doi:10.1093/aob/mcg186 · Cited by 30 · see citing works
Iron deficiency induces changes in metabolism of citrate in lateral roots and cluster roots of Lupinus albus
McCluskey, J., Herdman, L., & Skene, K. R. (2004) · Physiologia Plantarum · doi:10.1111/j.1399-3054.2004.00372.x · Cited by 29 · see citing works
Identification of genes induced in proteoid roots of white lupin under nitrogen and phosphorus deprivation, with functional characterization of a formamidase
Rath, M., Salas, J., Parhy, B., Norton, R. A., Menakuru, H., Sommerhalter, M., Hatlstad, G., Jaimyoung Kwon, B., Allan, D. L., Vance, C. P., et al. (2010) · Plant and Soil · doi:10.1007/s11104-010-0373-7 · Cited by 26 · see citing works
Effect of Phosphorus Deficiency Stress on Rice Lateral Root Growth and Nutrient Absorption
Hai-bo, L., Xia, M., & Wu, P. (2001) · Journal of Integrative Plant Biology · Cited by 26 · see citing works
Cluster Root Formation byLupinus Albusis Modified by Stratified Application of Phosphorus in a Split-Root System
Shu, L., Shen, J., Rengel, Z., Tang, C., & Zhang, F. S. (2007) · Journal of Plant Nutrition · doi:10.1080/01904160601118075 · Cited by 23 · see citing works
Arabidopsis thaliana mutant lpsi reveals impairment in the root responses to local phosphate availability
Karthikeyan, A. S., Jain, A., Nagarajan, V. K., Sinilal, B., Sahi, S. V., & Raghothama, K. G. (2014) · Plant Physiology and Biochemistry · doi:10.1016/j.plaphy.2013.12.009 · Cited by 22 · see citing works

Flagged first, then by citations

Sorted by citations

The molecular–physiological functions of mineral macronutrients and their consequences for deficiency symptoms in plants
de Bang, T. C., Husted, S., Laursen, K. H., Persson, D. P., & Schjoerring, J. K. (2020) · New Phytologist · doi:10.1111/nph.17074 · Cited by 609 · see citing works
Exploring phosphorus fertilizers and fertilization strategies for improved human and environmental health
Bindraban, P. S., Dimkpa, C. O., & Pandey, R. (2020) · Biology and Fertility of Soils · doi:10.1007/s00374-019-01430-2 · Cited by 562 · see citing works
Root-released organic anions in response to low phosphorus availability: recent progress, challenges and future perspectives
Wang, Y., & Lambers, H. (2019) · Plant and Soil · doi:10.1007/s11104-019-03972-8 · Cited by 367 · see citing works
Molecular and Environmental Regulation of Root Development
Motte, H., Vanneste, S., & Beeckman, T. (2019) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050718-100423 · Cited by 357 · see citing works
Root developmental responses to phosphorus nutrition
Liu, D. (2021) · Journal of Integrative Plant Biology · doi:10.1111/jipb.13090 · Cited by 315 · see citing works
Shaping plant architecture
Teichmann, T., & Muhr, M. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00233 · Cited by 228 · see citing works
“Branching in these plants is suppressed and many lateral roots develop near the soil surface, which was termed “topsoil foraging” (Peret et al., 2014).”
Background
Shaping 3D Root System Architecture
Morris, E. C., Griffiths, M., Gołębiowska, A., Mairhofer, S., Burr-Hersey, J. E., Goh, T., von Wangenheim, D., Atkinson, B. S., Sturrock, C. J., Lynch, J. P., et al. (2017) · Current Biology · doi:10.1016/j.cub.2017.06.043 · Cited by 230 · see citing works
Molecular mechanisms of phosphate transport and signaling in higher plants
Wang, F., Deng, M., Xu, J., Zhu, X., & Mao, C. (2017) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2017.06.013 · Cited by 202 · see citing works
Biodiversity hotspots and Ocbil theory
Hopper, S. D., Silveira, F. A. O., & Fiedler, P. L. (2015) · Plant and Soil · doi:10.1007/s11104-015-2764-2 · Cited by 191 · see citing works
The root cap: a short story of life and death
Kumpf, R. P., & Nowack, M. K. (2015) · Journal of Experimental Botany · doi:10.1093/jxb/erv295 · Cited by 184 · see citing works
Phosphate Uptake and Allocation – A Closer Look at Arabidopsis thaliana L. and Oryza sativa L.
Młodzińska, E., & Zboińska, M. (2016) · Frontiers in Plant Science · doi:10.3389/fpls.2016.01198 · Cited by 173 · see citing works
Soil functions and ecosystem services research in the Chinese karst Critical Zone
Green, S. M., Dungait, J. A. J., Tu, C., Buss, H. L., Sanderson, N. K., Hawkes, S. J., Xing, K., Yue, F., Hussey, V. L., Peng, J., et al. (2019) · Chemical Geology · doi:10.1016/j.chemgeo.2019.03.018 · Cited by 153 · see citing works
An Arabidopsis ABC Transporter Mediates Phosphate Deficiency-Induced Remodeling of Root Architecture by Modulating Iron Homeostasis in Roots
Dong, J., Piñeros, M. A., Li, X., Yang, H., Liu, Y., Murphy, A. S., Kochian, L. V., & Liu, D. (2016) · Molecular Plant · doi:10.1016/j.molp.2016.11.001 · Cited by 151 · see citing works
High-throughput three-dimensional visualization of root system architecture of rice using X-ray computed tomography
Teramoto, S., Takayasu, S., Kitomi, Y., Arai‐Sanoh, Y., Tanabata, T., & Uga, Y. (2020) · Plant Methods · doi:10.1186/s13007-020-00612-6 · Cited by 149 · see citing works
Vascular-mediated signalling involved in early phosphate stress response in plants
Zhang, Z., Zheng, Y., Ham, B., Chen, J., Yoshida, A., Kochian, L. V., Fei, Z., & Lucas, W. J. (2016) · Nature Plants · doi:10.1038/nplants.2016.33 · Cited by 147 · see citing works
Early Events in Plant Abiotic Stress Signaling: Interplay Between Calcium, Reactive Oxygen Species and Phytohormones
Mohanta, T. K., Bashir, T., Hashem, A., Allah, E. F. A., Khan, A. L., & Al-Harrasi, A. S. (2018) · Journal of Plant Growth Regulation · doi:10.1007/s00344-018-9833-8 · Cited by 146 · see citing works
Strigolactones Biosynthesis and Their Role in Abiotic Stress Resilience in Plants: A Critical Review
Saeed, W., Naseem, S., & Ali, Z. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.01487 · Cited by 145 · see citing works
Strigolactones are required for nitric oxide to induce root elongation in response to nitrogen and phosphate deficiencies in rice
Sun, H., Bi, Y., Tao, J., Huang, S., Hou, M., Xue, R., Liang, Z., Gu, P., Yoneyama, K., Xie, X., et al. (2016) · Plant Cell & Environment · doi:10.1111/pce.12709 · Cited by 128 · see citing works
Phosphate scouting by root tips
Abel, S. (2017) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2017.04.016 · Cited by 124 · see citing works
The phosphate transporters LjPT4 and MtPT4 mediate early root responses to phosphate status in non mycorrhizal roots
Volpe, V., Giovannetti, M., Sun, X., Fiorilli, V., & Bonfante, P. (2015) · Plant Cell & Environment · doi:10.1111/pce.12659 · Cited by 118 · see citing works
Metabolite profiling and genome‐wide association studies reveal response mechanisms of phosphorus deficiency in maize seedling
Luo, B., Ma, P., Nie, Z., Zhang, X., He, X., Ding, X. S., Feng, X., Lu, Q., Ren, Z., Lin, H., et al. (2018) · The Plant Journal · doi:10.1111/tpj.14160 · Cited by 118 · see citing works
Mechanisms and Impact of Symbiotic Phosphate AcquisitionPreprint
Chiu, C. H., & Paszkowski, U. (2019) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a034603 · Cited by 118 · see citing works
Blue Light-Triggered Chemical Reactions Underlie Phosphate Deficiency-Induced Inhibition of Root Elongation of Arabidopsis Seedlings Grown in Petri Dishes
Zheng, Z. S., Wang, Z., Wang, X., & Liu, D. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.08.001 · Cited by 111 · see citing works
The molecular and genetic regulation of shoot branching
Luo, Z., Janssen, B. J., & Snowden, K. C. (2021) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiab071 · Cited by 104 · see citing works
Detect thy family: Mechanisms, ecology and agricultural aspects of kin recognition in plants
Anten, N. P. R., & Chen, B. J. W. (2021) · Plant Cell & Environment · doi:10.1111/pce.14011 · Cited by 101 · see citing works
Arbuscular Mycorrhizal Fungi Contribute to Phosphorous Uptake and Allocation Strategies of Solidago canadensis in a Phosphorous-Deficient Environment
Qi, S., Wang, J., Wan, L., Dai, Z., Matos, D. M. S., Du, D., Egan, S., Bonser, S. P., Thomas, T., & Moles, A. T. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.831654 · Cited by 102 · see citing works
Os NLA 1, a RING ‐type ubiquitin ligase, maintains phosphate homeostasis in Oryza sativa via degradation of phosphate transporters
Yue, W., Ying, Y., Wang, C., Zhao, Y., Dong, C., Whelan, J., & Shou, H. (2017) · The Plant Journal · doi:10.1111/tpj.13516 · Cited by 101 · see citing works
Arbuscular mycorrhizal colonization outcompetes root hairs in maize under low phosphorus availability
Ma, X., Li, X., & Ludewig, U. (2020) · Annals of Botany · doi:10.1093/aob/mcaa159 · Cited by 99 · see citing works
SPX4 Acts on PHR1-Dependent and -Independent Regulation of Shoot Phosphorus Status in Arabidopsis
Osorio, M. B., Ng, S., Berkowitz, O., Clercq, I. D., Mao, C., Shou, H., Whelan, J., & Jost, R. (2019) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.00594 · Cited by 98 · see citing works
Self-citation
Evolutionary agroecology: Trends in root architecture during wheat breeding
Zhu, Y., Weiner, J., Yu, M., & Li, F. (2018) · Evolutionary Applications · doi:10.1111/eva.12749 · Cited by 96 · see citing works
Root avoidance of toxic metals requires the GeBP‐LIKE 4 transcription factor in Arabidopsis thaliana
Khare, D., Mitsuda, N., Lee, S., Song, W., Hwang, D., Ohme‐Takagi, M., Martinoia, E., Lee, Y., & Hwang, J. (2016) · New Phytologist · doi:10.1111/nph.14242 · Cited by 97 · see citing works
Induced Salt Tolerance of Perennial Ryegrass by a Novel Bacterium Strain from the Rhizosphere of a Desert Shrub Haloxylon ammodendron
He, A.-L., Niu, S., Zhao, Q., Li, Y., Gou, J.-Y., Gao, H.-J., Suo, S.-Z., & Zhang, J. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19020469 · Cited by 95 · see citing works
A reciprocal inhibitory module for Pi and iron signaling
Guo, M., Ruan, W., Zhang, Y., Zhang, Y., Wang, X., Guo, Z., Wang, L., Zhou, T., Paz‐Ares, J., & Yi, K. (2021) · Molecular Plant · doi:10.1016/j.molp.2021.09.011 · Cited by 91 · see citing works
Role of microRNAs involved in plant response to nitrogen and phosphorous limiting conditions
Nguyen, G. N., Rothstein, S. J., SPANGENBERG, G. C., & Kant, S. (2015) · Frontiers in Plant Science · doi:10.3389/fpls.2015.00629 · Cited by 88 · see citing works
The Systems Biology of Lateral Root Formation: Connecting the Dots
Teixeira, J. A. S., & ten Tusscher, K. (2019) · Molecular Plant · doi:10.1016/j.molp.2019.03.015 · Cited by 87 · see citing works
Effects of breeding history and crop management on the root architecture of wheat
Fradgley, N. S., Evans, G., Biernaskie, J. M., Cockram, J., Marr, E., Oliver, A. G., Ober, E. S., & Jones, H. (2020) · Plant and Soil · doi:10.1007/s11104-020-04585-2 · Cited by 85 · see citing works
The Phosphate Starvation Response System: Its Role in the Regulation of Plant–Microbe Interactions
Isidra‐Arellano, M. C., Delaux, P., & Valdés‐López, O. (2021) · Plant and Cell Physiology · doi:10.1093/pcp/pcab016 · Cited by 83 · see citing works
Genetic Dissection of Fe-Dependent Signaling in Root Developmental Responses to Phosphate Deficiency
Wang, X., Wang, Z., Zheng, Z. S., Dong, J., Song, L., Sui, L., Nussaume, L., Desnos, T., & Liu, D. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.00907 · Cited by 82 · see citing works
Self-citation
The good, the bad, and the phosphate: regulation of beneficial and detrimental plant–microbe interactions by the plant phosphate status
Paries, M., & Gutjahr, C. (2023) · New Phytologist · doi:10.1111/nph.18933 · Cited by 81 · see citing works
Transcriptome and metabolome analyses provide insights into root and root-released organic anion responses to phosphorus deficiency in oat
Wang, Y., Lysøe, E., Armarego‐Marriott, T., Erban, A., Paruch, L., van Eerde, A., Bock, R., & Liu‐Clarke, J. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/ery176 · Cited by 79 · see citing works
Arbuscular mycorrhizal fungi have a greater role than root hairs of maize for priming the rhizosphere microbial community and enhancing rhizosphere organic P mineralization
Zhou, J., Zhang, L., Feng, G., & George, T. (2022) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2022.108713 · Cited by 79 · see citing works
The Local Phosphate Deficiency Response Activates Endoplasmic Reticulum Stress-Dependent Autophagy
Naumann, C., Müller, J., Sakhonwasee, S., Wieghaus, A., Hause, G., Heisters, M., Bürstenbinder, K., & Abel, S. (2018) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.01379 · Cited by 78 · see citing works
Phosphatase activity and acidification in lupine and maize rhizosphere depend on phosphorus availability and root properties: Coupling zymography with planar optodes
Ma, X., Liu, Y., Shen, W., & Kuzyakov, Y. V. (2021) · Applied Soil Ecology · doi:10.1016/j.apsoil.2021.104029 · Cited by 76 · see citing works
Diverse Sorghum bicolor accessions show marked variation in growth and transcriptional responses to arbuscular mycorrhizal fungi
Watts‐Williams, S. J., Emmett, B. D., Lévesque-Tremblay, V., MacLean, A. M., Sun, X., Satterlee, J. W., Fei, Z., & Harrison, M. (2018) · Plant Cell & Environment · doi:10.1111/pce.13509 · Cited by 72 · see citing works
Identification of putative QTLs for seedling stage phosphorus starvation response in finger millet (Eleusine coracana L. Gaertn.) by association mapping and cross species synteny analysis
Ramakrishnan, M., Ceasar, S. A., Vinod, K. K., Duraipandiyan, V., Krishna, T. P. A., Upadhyaya, H. D., Al-Dhabi, N. A., & Savarimuthu Ignacimuthu, S. J. (2017) · PLoS ONE · doi:10.1371/journal.pone.0183261 · Cited by 69 · see citing works
Methane Emission from Rice Fields: Necessity for Molecular Approach for Mitigation
Rajendran, S., Park, H., Kim, J., Park, S. J., Shin, D., Lee, J., Song, Y. H., Paek, N., & Kim, C. M. (2023) · Rice Science · doi:10.1016/j.rsci.2023.10.003 · Cited by 67 · see citing works
Plant transporters: roles in stress responses and effects on growth and development
Li, P., Luo, T., Pu, X., Zhou, Y., Yu, J., & Liu, L. (2021) · Plant Growth Regulation · doi:10.1007/s10725-020-00684-3 · Cited by 65 · see citing works
Coupling zymography with pH mapping reveals a shift in lupine phosphorus acquisition strategy driven by cluster roots
Ma, X., Mason‐Jones, K., Liu, Y., Blagodatskaya, E. V., Kuzyakov, Y. V., Guber, A. K., Dippold, M. A., & Razavi, B. S. (2019) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2019.06.001 · Cited by 65 · see citing works
Phosphate Starvation Alters Abiotic-Stress-Induced Cytosolic Free Calcium Increases in Roots
Matthus, E., Wilkins, K. A., Swarbreck, S. M., Doddrell, N. H., Doccula, F. G., Costa, A., & Davies, J. M. (2019) · PLANT PHYSIOLOGY · doi:10.1104/pp.18.01469 · Cited by 64 · see citing works
Characterization of purple acid phosphatases involved in extracellular dNTP utilization in Stylosanthes
Liu, P., Xue, Y., Chen, Z., Liu, G., & Tian, J. (2016) · Journal of Experimental Botany · doi:10.1093/jxb/erw190 · Cited by 64 · see citing works
Role of soil abiotic processes on phosphorus availability and plant responses with a focus on strigolactones in tomato plants
Santoro, V., Schiavon, M., & Celi, L. (2023) · Plant and Soil · doi:10.1007/s11104-023-06266-2 · Cited by 63 · see citing works
One way. Or another? Iron uptake in plants
Tsai, H.-H. M., & Schmidt, W. (2017) · New Phytologist · doi:10.1111/nph.14477 · Cited by 63 · see citing works
Regulation of Ubiquitination Is Central to the Phosphate Starvation Response
Pan, W., Wu, Y., & Xie, Q. (2019) · Trends in Plant Science · doi:10.1016/j.tplants.2019.05.002 · Cited by 62 · see citing works
NRT1.1-centered nitrate signaling in plants
Maghiaoui, A., Gojon, A., & Bach, L. (2020) · Journal of Experimental Botany · doi:10.1093/jxb/eraa361 · Cited by 61 · see citing works
Performance and Limitations of Phosphate Quantification: Guidelines for Plant Biologists
Kanno, S., Cuyas, L., Javot, H., Bligny, R., Gout, E., Dartevelle, T., Hanchi, M., Nakanishi, T., Thibaud, M., & Nussaume, L. (2016) · Plant and Cell Physiology · doi:10.1093/pcp/pcv208 · Cited by 61 · see citing works
Self-citation
Beyond iron-storage pool: functions of plant apoplastic iron during stress
Liu, X. X., Zhu, X. F., Xue, D., Zheng, S. J., & Jin, C. W. (2023) · Trends in Plant Science · doi:10.1016/j.tplants.2023.03.007 · Cited by 58 · see citing works
Up‐regulating GmETO1 improves phosphorus uptake and use efficiency by promoting root growth in soybean
Zhang, H., Yang, Y., Sun, C., Liu, X., Lv, L., Hu, Z., Yu, D., & Zhang, D. (2020) · Plant Cell & Environment · doi:10.1111/pce.13816 · Cited by 56 · see citing works
Coconut Coir as a Sustainable Nursery Growing Media for Seedling Production of the Ecologically Diverse Quercus Species
Mariotti, B., Martini, S., Raddi, S., Tani, A., Jacobs, D. F., Oliet, J. A., & Maltoni, A. (2020) · Forests · doi:10.3390/f11050522 · Cited by 55 · see citing works
Effect of Salinity on Soil Nutrients and Plant Health
Bidalia, A., Vikram, K., Yamal, G., & Rao, K. S. (2019) · Springer eBooks · doi:10.1007/978-981-13-8801-9_13 · Cited by 54 · see citing works
The volatile cedrene from Trichoderma guizhouense modulates Arabidopsis root development through auxin transport and signalling
Li, Y., Shao, J., Fu, Y., Chen, Y., Wang, H., Xu, Z., Feng, H., Xun, W., Liu, Y., Zhang, N., et al. (2021) · Plant Cell & Environment · doi:10.1111/pce.14230 · Cited by 54 · see citing works
Effects of PGPR Co-inoculation on Growth, Phosphorus Nutrition and Phosphatase/Phytase Activities of Faba Bean under Different Phosphorus Availability Conditions
Bechtaoui, N., Raklami, A., Benidire, L., Tahiri, A.-I., Göttfert, M., & Oufdou, K. (2020) · Polish Journal of Environmental Studies · doi:10.15244/pjoes/110345 · Cited by 53 · see citing works
Reshaping Plant Biology: Qualitative and Quantitative Descriptors for Plant Morphology
Balduzzi, M., Binder, B. M., Bucksch, A., Chang, C. C., Hong, L., Iyer‐Pascuzzi, A. S., Pradal, C., & Sparks, E. E. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00117 · Cited by 52 · see citing works
Uncovering How Auxin Optimizes Root Systems Architecture in Response to Environmental StressesPreprint
Leftley, N., Banda, J., Pandey, B. K., Bennett, M. J., & Voß, U. (2021) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a040014 · Cited by 51 · see citing works
Editing of the OsACS locus alters phosphate deficiency-induced adaptive responses in rice seedlings
Lee, H. Y., Chen, Z., Zhang, C., & Yoon, G. M. (2019) · Journal of Experimental Botany · doi:10.1093/jxb/erz074 · Cited by 48 · see citing works
Strigolactones Control Root System Architecture and Tip Anatomy in Solanum lycopersicum L. Plants under P Starvation
Santoro, V., Schiavon, M., Gresta, F., Ertani, A., Cardinale, F., Sturrock, C. J., Celi, L., & Schubert, A. (2020) · Plants · doi:10.3390/plants9050612 · Cited by 49 · see citing works
Mitigating drought stress by application of drought-tolerant Bacillus spp. enhanced root architecture, growth, antioxidant and photosynthetic genes expression in sugarcane
Buqori, D. M. A. I., Sugiharto, B., Suherman, Siswoyo, T. A., & Hariyono, K. (2025) · Scientific Reports · doi:10.1038/s41598-025-89457-4 · Cited by 49 · see citing works
Crop host signatures reflected by co-association patterns of keystone Bacteria in the rhizosphere microbiota
Lewin, S. A., Francioli, D., Ulrich, A., & Kolb, S. (2021) · Environmental Microbiome · doi:10.1186/s40793-021-00387-w · Cited by 48 · see citing works
Bacterial-type ferroxidase tunes iron-dependent phosphate sensing during Arabidopsis root development
Naumann, C., Heisters, M., Brandt, W., Janitza, P., Alfs, C., Tang, N., Nienguesso, A. T., Ziegler, J., Imre, R., Mechtler, K., et al. (2022) · Current Biology · doi:10.1016/j.cub.2022.04.005 · Cited by 47 · see citing works
How functional is a trait? Phosphorus mobilization through root exudates differs little between Carex species with and without specialized dauciform roots
Güsewell, S., & Schroth, M. H. (2017) · New Phytologist · doi:10.1111/nph.14674 · Cited by 46 · see citing works
The Phosphorus-Iron Nexus: Decoding the Nutrients Interaction in Soil and Plant
Yang, X., Liu, C., Liang, C., Wang, T., & Tian, J. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25136992 · Cited by 52 · see citing works
Viroids, infectious long non-coding RNAs with autonomous replication
Gago‐Zachert, S. (2015) · Virus Research · doi:10.1016/j.virusres.2015.08.018 · Cited by 45 · see citing works
Recent Advances in Understanding the Molecular Mechanisms Regulating the Root System Response to Phosphate Deficiency in Arabidopsis
Bouain, N., Doumas, P., & Rouached, H. (2016) · Current Genomics · doi:10.2174/1389202917666160331201812 · Cited by 45 · see citing works
Genetic improvement of legume roots for adaption to acid soils
Li, X., Zhang, X., Zhao, Q., & Liao, H. (2023) · The Crop Journal · doi:10.1016/j.cj.2023.04.002 · Cited by 44 · see citing works
Soil type determines how root and rhizosphere traits relate to phosphorus acquisition in field-grown maize genotypes
Erel, R., Bérard, A., Capowiez, L., Doussan, C., Arnal, D., Souche, G., Gavaland, A., Fritz, C., Visser, E. J. W., Salvi, S., et al. (2016) · Plant and Soil · doi:10.1007/s11104-016-3127-3 · Cited by 43 · see citing works
Heterogeneous phosphate supply influences maize lateral root proliferation by regulating auxin redistribution
Wang, X., Feng, J., White, P. J., Shen, J., & Cheng, L. (2019) · Annals of Botany · doi:10.1093/aob/mcz154 · Cited by 41 · see citing works
Overexpression of OsPIN2 Regulates Root Growth and Formation in Response to Phosphate Deficiency in Rice
Sun, H., Guo, X., Xu, F., Wu, D., Zhang, X., Lou, M., Luo, F., Xu, G., & Zhang, Y. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20205144 · Cited by 39 · see citing works
An Update on Nitric Oxide Production and Role Under Phosphorus Scarcity in Plants
Galatro, A., Ramos-Artuso, F., Luquet, M., Buet, A., & Simontacchi, M. (2020) · Frontiers in Plant Science · doi:10.3389/fpls.2020.00413 · Cited by 38 · see citing works
Can lunar and martian soils support food plant production? Effects of horse/swine monogastric manure fertilisation on regolith simulants enzymatic activity, nutrient bioavailability, and lettuce growth
Caporale, A. G., Amato, M., Duri, L. G., Bochicchio, R., De Pascale, S., Simeone, G. D. R., Palladino, M., Pannico, A., Rao, M. A., Rouphael, Y., et al. (2022) · Plants · doi:10.3390/plants11233345 · Cited by 36 · see citing works
Higher free-living N2 fixation at rock-soil interfaces than topsoils during vegetation recovery in karst soils
Tang, Y., Tian, J., Li, X., Yao, M., Wang, S., Kuzyakov, Y. V., & Dungait, J. A. J. (2021) · Soil Biology and Biochemistry · doi:10.1016/j.soilbio.2021.108286 · Cited by 35 · see citing works
Understanding the Adaptive Mechanisms of Plants to Enhance Phosphorus Use Efficiency on Podzolic Soils in Boreal Agroecosystems
Nadeem, M., Wu, J., Ghaffari, H., Kedir, A. J., Saleem, S., Mollier, A., Singh, J., & Cheema, M. (2022) · Frontiers in Plant Science · doi:10.3389/fpls.2022.804058 · Cited by 34 · see citing works
Prospects of genetics and breeding for low-phosphate tolerance: an integrated approach from soil to cell
Ojeda‐Rivera, J. O., Alejo‐Jacuinde, G., Nájera‐González, H., & López-Arredondo, D. L. (2022) · Theoretical and Applied Genetics · doi:10.1007/s00122-022-04095-y · Cited by 32 · see citing works
The interplay between phosphorus nutrition and abiotic stresses in plants
Zeng, H., Chen, F., Zhu, Q., Ali, S., Du, J., Zhu, Y., & Yi, K. (2025) · Journal of genetics and genomics/Journal of Genetics and Genomics · doi:10.1016/j.jgg.2025.08.008 · Cited by 31 · see citing works
Environmental conditions in the nursery regulate root system development and architecture of forest tree seedlings: a systematic review
Toca, A., Moler, E. R. V., Nelson, A. S., & Jacobs, D. F. (2022) · New Forests · doi:10.1007/s11056-022-09944-8 · Cited by 30 · see citing works
Bacillus subtilis promotes plant phosphorus (P) acquisition through P solubilization and stimulation of root and root hair growth
Jensen, C. N. G., Pang, J. K. Y., Gottardi, M., Kračun, S. K., Svendsen, B. A., Nielsen, K. F., Kovács, Á. T., Moelbak, L., Fimognari, L., Husted, S., et al. (2024) · Physiologia Plantarum · doi:10.1111/ppl.14338 · Cited by 30 · see citing works
Mechanisms and Adaptation Strategies of Tolerance to Phosphorus Deficiency in Legumes
Lazali, M., & Drevon, J. J. (2021) · Communications in Soil Science and Plant Analysis · doi:10.1080/00103624.2021.1885693 · Cited by 30 · see citing works
Maize Transcription Factor ZmARF4 Confers Phosphorus Tolerance by Promoting Root Morphological Development
Li, J., Wu, F., He, Y., He, B., Gong, Y., Yahaya, B. S., Xie, Y., Xie, W., Xu, J., Wang, Q., et al. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23042361 · Cited by 30 · see citing works
Ethylene regulates auxin-mediated root gravitropic machinery and controls root angle in cereal crops
Kong, X., Xiong, Y., Song, X., Wadey, S., Yu, S., Rao, J., Lale, A., Lombardi, M., Fusi, R., Bhosale, R., et al. (2024) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiae134 · Cited by 29 · see citing works
Characterization of the Nicotianamine Exporter ENA1 in Rice
Nozoye, T., von Wirén, N., Sato, Y., Higashiyama, T., Nakanishi, H., & Nishizawa, N. K. (2019) · Frontiers in Plant Science · doi:10.3389/fpls.2019.00502 · Cited by 29 · see citing works
Genetic diversity of rhizobia associated with root nodules of white lupin (Lupinus albus L.) in Tunisian calcareous soils
Tounsi-Hammami, S., Roux, C. L., Dhane, S., de Lajudie, P., Duponnois, R., & Jeddi, F. B. (2019) · Systematic and Applied Microbiology · doi:10.1016/j.syapm.2019.04.002 · Cited by 29 · see citing works
Phosphatidylinositol phosphate 5‐kinase genes respond to phosphate deficiency for root hair elongation in Arabidopsis thaliana
Wada, Y., Kusano, H., Tsuge, T., & Aoyama, T. (2014) · The Plant Journal · doi:10.1111/tpj.12741 · Cited by 28 · see citing works
Endophytic fungus Serendipita indica increased nutrition absorption and biomass accumulation in Cunninghamia lanceolata seedlings under low phosphate
Wu, C. L., Li, B., Wei, Q., Pan, R., & Zhang, W. (2018) · Acta Ecologica Sinica · doi:10.1016/j.chnaes.2018.06.005 · Cited by 28 · see citing works
Developmental responses of roots to limited phosphate availability: Research progress and application in cereals
Lu, H., Ren, M., Lin, R., Jin, K., & Mao, C. (2024) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiae495 · Cited by 27 · see citing works
Acclimation of the crucifer Eutrema salsugineum to phosphate limitation is associated with constitutively high expression of phosphate‐starvation genes
Velasco, V. M. E., Mansbridge, J. F. P., Bremner, S., Carruthers, K., Summers, P. S., Sung, W. W. L., Champigny, M. J., & Weretilnyk, E. A. (2016) · Plant Cell & Environment · doi:10.1111/pce.12750 · Cited by 27 · see citing works
Molecular and genetic basis of plant macronutrient use efficiency: concepts, opportunities, and challenges
López-Arredondo, D. L., Sánchez-Calderón, L., & Yong‐Villalobos, L. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-811308-0.00001-6 · Cited by 27 · see citing works
The PHOSPHATE1 genes participate in salt and Pi signaling pathways and play adaptive roles during soybean evolution
Wang, Y., Gao, H., He, L., Zhu, W., Yan, L., Chen, Q., & He, C. (2019) · BMC Plant Biology · doi:10.1186/s12870-019-1959-8 · Cited by 27 · see citing works
Phenotypic responses of foxtail millet (Setaria italica) genotypes to phosphate supply under greenhouse and natural field conditions
Ceasar, S. A., Ramakrishnan, M., Vinod, K. K., Roch, G. V., Upadhyaya, H. D., Baker, A., & Savarimuthu Ignacimuthu, S. J. (2020) · PLoS ONE · doi:10.1371/journal.pone.0233896 · Cited by 27 · see citing works
Local and systemic responses conferring acclimation of Brassica napus roots to low phosphorus conditions
Li, Y., Yang, X., Liu, H., Wang, W., Wang, C., Ding, G., Xu, F., Wang, S., Cai, H., Hammond, J. P., et al. (2022) · Journal of Experimental Botany · doi:10.1093/jxb/erac177 · Cited by 27 · see citing works
Higher colonization but lower diversity of root-associated arbuscular mycorrhizal fungi in the topsoil than in deep soil
Wang, Z., Zhao, J., Xiao, D., Chen, M., & He, X. (2023) · Applied Soil Ecology · doi:10.1016/j.apsoil.2023.105195 · Cited by 26 · see citing works
A Role for Inositol Pyrophosphates in the Metabolic Adaptations to Low Phosphate in Arabidopsis
Land, E. S., Cridland, C. A., Craige, B., Dye, A. E., Hildreth, S. B., Helm, R. F., Gillaspy, G. E., & Perera, I. Y. (2021) · Metabolites · doi:10.3390/metabo11090601 · Cited by 26 · see citing works
Proteomic Analysis Dissects Molecular Mechanisms Underlying Plant Responses to Phosphorus Deficiency
Zhou, M., Zhu, S., Mo, X., Guo, Q., Li, Y., Tian, J., & Liang, C. (2022) · Cells · doi:10.3390/cells11040651 · Cited by 26 · see citing works

Root developmental adaptation to phosphate starvation: better safe than sorry
Péret, B., Clément, M., Nussaume, L., & Desnos, T. (2011) · Trends in Plant Science · doi:10.1016/j.tplants.2011.05.006 · Cited by 538 · see citing works
Self-citation
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 871 · see citing works
REVIEW: PART OF A SPECIAL ISSUE ON MATCHING ROOTS TO THEIR ENVIRONMENT Responses of root architecture development to low phosphorus availability: a review
Niu, Y. F., Chai, R. S., Jin, G. L., Wang, H., Tang, C. X., & Zhang, Y. S. (2016)
Developmental responses of roots to limited phosphate availability: Research progress and application in cereals
Lu, H., Ren, M., Lin, R., Jin, K., & Mao, C. (2024) · PLANT PHYSIOLOGY · doi:10.1093/plphys/kiae495 · Cited by 27 · see citing works
Understanding the Dynamics of Phosphorus Starvation and Plant Growth
Dar, T. A., Uddin, M., Ali, A., Khan, M. M. A., & Dar, T. U. H. (2017) · Springer eBooks · doi:10.1007/978-3-319-58841-4_7 · Cited by 6 · see citing works

Authors: Péret, B., Desnos, T., Jost, R., Kanno, S., Berkowitz, O., & Nussaume, L.
Affiliations: Centre National de la Recherche Scientifique (FR)
ORCID: Péret, Benjamin
Desnos, Thierry
Jost, Ricarda
Kanno, Satomi
Berkowitz, Oliver
Nussaume, Laurent
Venue: Plant Physiology
Publisher: Oxford University Press (OUP)
Published: 2014-10-23
Volume: 166
Issue: 4
Pages: 1713-1723
ISSN: 0032-0889 (ISSN-L)
1532-2548
DOI: 10.1104/pp.114.244541
PMC: PMC4256877
OpenAlex: W2131102604
Cited by: 292
References: 100
Citations by year: 2026: 22 · 2025: 24 · 2024: 23 · 2023: 28 · 2022: 32 · 2021: 46 · 2020: 27 · 2019: 28 · 2018: 18 · 2017: 21 · 2016: 13 · 2015: 9 · 2014: 1
FWCI: 17.14
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: aspb.org/publications/aspb-journals/open-articles (vor, 404 d)
Locations: PLANT PHYSIOLOGY (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
UWA Profiles and Research Repository (UWA) (submittedVersion, other-oa)
HAL (submittedVersion)
Funders: Agence Nationale de la Recherche (ANR-11-PDOC-0003, ANR-09-BLAN-0118, ANR-11-RSNR-0005)
Japan Society for the Promotion of Science (13J03284)
Topics: Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant nutrient uptake and metabolism
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Parasitism and Resistance
Life Sciences › Agricultural and Biological Sciences › Plant Science › Plant Molecular Biology Research
Keywords: root architecture, phosphate limitation, phosphorus acquisition, lateral roots, primary root, cluster roots, root development, nutrient limitation
MeSH terms: Phosphates, Phosphorus, Plants, Soil, Plant Roots, Plant Development

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

Root Architecture Responses: In Search of Phosphate

Abstract

Integrity signals

Claims the paper makes

Self-check

Cites

Cited by

Related

Record

About these checks