Root Architecture Responses: In Search of Phosphate1

Root development alters in response to phosphate availability, which affects the production of cluster roots in a limited number of species. 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.

[1]  O. Leyser,et al.  Strigolactones and the control of plant development: lessons from shoot branching. , 2014, The Plant journal : for cell and molecular biology.

[2]  D. Yun,et al.  Overexpression of OsMYB4P, an R2R3-type MYB transcriptional activator, increases phosphate acquisition in rice. , 2014, Plant physiology and biochemistry : PPB.

[3]  Caihuan Tian,et al.  Suppression of Photosynthetic Gene Expression in Roots Is Required for Sustained Root Growth under Phosphate Deficiency1[W][OPEN] , 2014, Plant Physiology.

[4]  J. Fisahn,et al.  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 Limitation1[W][OPEN] , 2014, Plant Physiology.

[5]  A. Karthikeyan,et al.  Arabidopsis thaliana mutant lpsi reveals impairment in the root responses to local phosphate availability. , 2014, Plant physiology and biochemistry : PPB.

[6]  Fabian Kellermeier,et al.  Analysis of the Root System Architecture of Arabidopsis Provides a Quantitative Readout of Crosstalk between Nutritional Signals[W][OPEN] , 2014, Plant Cell.

[7]  D. Secco,et al.  RNA-seq analysis identifies an intricate regulatory network controlling cluster root development in white lupin , 2014, BMC Genomics.

[8]  K. Yoneyama,et al.  Strigolactones are involved in phosphate- and nitrate-deficiency-induced root development and auxin transport in rice , 2014, Journal of experimental botany.

[9]  N. von Wirén,et al.  It's time to make changes: modulation of root system architecture by nutrient signals. , 2014, Journal of experimental botany.

[10]  Wei-Hua Wu,et al.  Arabidopsis WRKY45 Transcription Factor Activates PHOSPHATE TRANSPORTER1;1 Expression in Response to Phosphate Starvation1[W][OPEN] , 2014, Plant Physiology.

[11]  M. Stitt,et al.  Low levels of ribosomal RNA partly account for the very high photosynthetic phosphorus-use efficiency of Proteaceae species , 2013, Plant, cell & environment.

[12]  Q. Qian,et al.  Auxin response factor (OsARF12), a novel regulator for phosphate homeostasis in rice (Oryza sativa). , 2014, The New phytologist.

[13]  Xavier Draye,et al.  An online database for plant image analysis software tools , 2013, Plant Methods.

[14]  M. Lucas,et al.  Lateral root development in Arabidopsis: fifty shades of auxin. , 2013, Trends in plant science.

[15]  Swetlana Friedel,et al.  Plasticity of the Arabidopsis Root System under Nutrient Deficiencies1[C][W][OPEN] , 2013, Plant Physiology.

[16]  J. Briat,et al.  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* , 2013, The Journal of Biological Chemistry.

[17]  Luis Herrera-Estrella,et al.  APSR1, a novel gene required for meristem maintenance, is negatively regulated by low phosphate availability. , 2013, Plant science : an international journal of experimental plant biology.

[18]  Eric T. Fedosejevs,et al.  Reciprocal Control of Anaplerotic Phosphoenolpyruvate Carboxylase by in Vivo Monoubiquitination and Phosphorylation in Developing Proteoid Roots of Phosphate-Deficient Harsh Hakea1[W][OA] , 2013, Plant Physiology.

[19]  H. Lambers,et al.  Acclimation responses of Arabidopsis thaliana to sustained phosphite treatments , 2013, Journal of experimental botany.

[20]  Huan Wang,et al.  Responses of root architecture development to low phosphorus availability: a review , 2012, Annals of botany.

[21]  Yan Long,et al.  High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities , 2012, Annals of botany.

[22]  Benjamin L Turner,et al.  Proteaceae from severely phosphorus-impoverished soils extensively replace phospholipids with galactolipids and sulfolipids during leaf development to achieve a high photosynthetic phosphorus-use-efficiency. , 2012, The New phytologist.

[23]  Carroll P. Vance,et al.  An RNA-Seq Transcriptome Analysis of Orthophosphate-Deficient White Lupin Reveals Novel Insights into Phosphorus Acclimation in Plants1[W][OA] , 2012, Plant Physiology.

[24]  W. Plaxton,et al.  The secreted purple acid phosphatase isozymes AtPAP12 and AtPAP26 play a pivotal role in extracellular phosphate-scavenging by Arabidopsis thaliana , 2012, Journal of experimental botany.

[25]  P. Pesaresi,et al.  The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency , 2012, Nature.

[26]  F. Katagiri,et al.  The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. , 2012, The Plant journal : for cell and molecular biology.

[27]  Jason G. Bragg,et al.  Opportunities for improving phosphorus-use efficiency in crop plants. , 2012, The New phytologist.

[28]  Miguel C. Teixeira,et al.  The Pht1;9 and Pht1;8 transporters mediate inorganic phosphate acquisition by the Arabidopsis thaliana root during phosphorus starvation. , 2012, The New phytologist.

[29]  Filip Vandenbussche,et al.  Ethylene in vegetative development: a tale with a riddle. , 2012, The New phytologist.

[30]  Dong Liu,et al.  The Arabidopsis gene hypersensitive to phosphate starvation 3 encodes ethylene overproduction 1. , 2012, Plant & cell physiology.

[31]  Dong Liu,et al.  HPS4/SABRE regulates plant responses to phosphate starvation through antagonistic interaction with ethylene signalling , 2012, Journal of experimental botany.

[32]  An Yang,et al.  OsMYB2P-1, an R2R3 MYB Transcription Factor, Is Involved in the Regulation of Phosphate-Starvation Responses and Root Architecture in Rice1[C][W][OA] , 2012, Plant Physiology.

[33]  Aaron P. Smith,et al.  Ethylene's role in phosphate starvation signaling: more than just a root growth regulator. , 2012, Plant & cell physiology.

[34]  Yuman Zhang,et al.  A novel rice gene, NRR responds to macronutrient deficiency and regulates root growth. , 2012, Molecular plant.

[35]  Z. Li,et al.  Phosphate starvation of maize inhibits lateral root formation and alters gene expression in the lateral root primordium zone , 2012, BMC Plant Biology.

[36]  L. Nussaume,et al.  Phosphate Import in Plants: Focus on the PHT1 Transporters , 2011, Front. Plant Sci..

[37]  Daowen Wang,et al.  The Arabidopsis Purple Acid Phosphatase AtPAP10 Is Predominantly Associated with the Root Surface and Plays an Important Role in Plant Tolerance to Phosphate Limitation1[W][OA] , 2011, Plant Physiology.

[38]  L. Nussaume,et al.  Root developmental adaptation to phosphate starvation: better safe than sorry. , 2011, Trends in plant science.

[39]  S. Abel Phosphate sensing in root development. , 2011, Current opinion in plant biology.

[40]  L. Herrera-Estrella,et al.  Phosphate Deprivation in Maize: Genetics and Genomics1 , 2011, Plant Physiology.

[41]  Jonathan P Lynch,et al.  Root Phenes for Enhanced Soil Exploration and Phosphorus Acquisition: Tools for Future Crops , 2011, Plant Physiology.

[42]  H. Lambers,et al.  Phosphorus Nutrition of Proteaceae in Severely Phosphorus-Impoverished Soils: Are There Lessons To Be Learned for Future Crops?1 , 2011, Plant Physiology.

[43]  J. Hammond,et al.  Sugar Signaling in Root Responses to Low Phosphorus Availability1 , 2011, Plant Physiology.

[44]  I. Jakobsen,et al.  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 Acquisition1 , 2011, Plant Physiology.

[45]  Jianbo Shen,et al.  Update on lupin cluster roots. Update on white lupin cluster root acclimation to phosphorus deficiency. , 2011, Plant physiology.

[46]  A. Karthikeyan,et al.  Ethylene signalling is involved in regulation of phosphate starvation-induced gene expression and production of acid phosphatases and anthocyanin in Arabidopsis. , 2011, The New phytologist.

[47]  Mingguang Lei,et al.  Genetic and Genomic Evidence That Sucrose Is a Global Regulator of Plant Responses to Phosphate Starvation in Arabidopsis1[W][OA] , 2011, Plant Physiology.

[48]  Bin Hu,et al.  LEAF TIP NECROSIS1 Plays a Pivotal Role in the Regulation of Multiple Phosphate Starvation Responses in Rice1[W][OA] , 2011, Plant Physiology.

[49]  Y. Poirier,et al.  Dissection of local and systemic transcriptional responses to phosphate starvation in Arabidopsis. , 2010, The Plant journal : for cell and molecular biology.

[50]  Daowen Wang,et al.  Biochemical and molecular characterization of AtPAP12 and AtPAP26: the predominant purple acid phosphatase isozymes secreted by phosphate-starved Arabidopsis thaliana. , 2010, Plant, cell & environment.

[51]  Hongling Jiang,et al.  Arabidopsis Tyrosylprotein Sulfotransferase Acts in the Auxin/PLETHORA Pathway in Regulating Postembryonic Maintenance of the Root Stem Cell Niche[W][OA] , 2010, Plant Cell.

[52]  M. Blair,et al.  Strategies for improving phosphorus acquisition efficiency of crop plants. , 2010 .

[53]  Jaimyoung Kwon,et al.  Identification of genes induced in proteoid roots of white lupin under nitrogen and phosphorus deprivation, with functional characterization of a formamidase , 2010, Plant and Soil.

[54]  Y. Matsubayashi,et al.  Identification of tyrosylprotein sulfotransferase in Arabidopsis , 2009, Proceedings of the National Academy of Sciences.

[55]  C. Ticconi,et al.  ER-resident proteins PDR2 and LPR1 mediate the developmental response of root meristems to phosphate availability , 2009, Proceedings of the National Academy of Sciences.

[56]  Stephen D. Hopper,et al.  OCBIL theory: towards an integrated understanding of the evolution, ecology and conservation of biodiversity on old, climatically buffered, infertile landscapes , 2009, Plant and Soil.

[57]  M. Panigrahy,et al.  Molecular mechanisms in response to phosphate starvation in rice. , 2009, Biotechnology advances.

[58]  Tom Beeckman,et al.  Arabidopsis lateral root development: an emerging story. , 2009, Trends in plant science.

[59]  L. Herrera-Estrella,et al.  Phosphate Availability Alters Lateral Root Development in Arabidopsis by Modulating Auxin Sensitivity via a Mechanism Involving the TIR1 Auxin Receptor[C][W][OA] , 2008, The Plant Cell Online.

[60]  Martin Parniske,et al.  Arbuscular mycorrhiza: the mother of plant root endosymbioses , 2008, Nature Reviews Microbiology.

[61]  B. Lahner,et al.  The Effect of Iron on the Primary Root Elongation of Arabidopsis during Phosphate Deficiency1[W][OA] , 2008, Plant Physiology.

[62]  Ping Wu,et al.  OsPHR2 Is Involved in Phosphate-Starvation Signaling and Excessive Phosphate Accumulation in Shoots of Plants1[C][W][OA] , 2008, Plant Physiology.

[63]  Frank Hochholdinger,et al.  Conserved and diverse mechanisms in root development. , 2008, Current opinion in plant biology.

[64]  H. Lambers,et al.  Plant nutrient-acquisition strategies change with soil age. , 2008, Trends in ecology & evolution.

[65]  Laurent Nussaume,et al.  Root tip contact with low-phosphate media reprograms plant root architecture , 2007, Nature Genetics.

[66]  K. Palme,et al.  Stress-induced morphogenic responses: growing out of trouble? , 2007, Trends in plant science.

[67]  Fusuo Zhang,et al.  Cluster Root Formation by Lupinus Albus is Modified by Stratified Application of Phosphorus in a Split-Root System , 2007 .

[68]  Erik J Veneklaas,et al.  Root structure and functioning for efficient acquisition of phosphorus: Matching morphological and physiological traits. , 2006, Annals of botany.

[69]  Bertrand Muller,et al.  A Role for Auxin Redistribution in the Responses of the Root System Architecture to Phosphate Starvation in Arabidopsis1 , 2005, Plant Physiology.

[70]  L. Herrera-Estrella,et al.  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 Activation1 , 2005, Plant Physiology.

[71]  L. Herrera-Estrella,et al.  Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana. , 2005, Plant & cell physiology.

[72]  Hans Lambers,et al.  Cluster Roots: A Curiosity in Context , 2005, Plant and Soil.

[73]  H. Lambers,et al.  A root trait accounting for the extreme phosphorus sensitivity of Hakea prostrata (Proteaceae) , 2004 .

[74]  Keith R. Skene,et al.  Iron deficiency induces changes in metabolism of citrate in lateral roots and cluster roots of Lupinus albus , 2004 .

[75]  M. J. Harrison,et al.  Phosphate transport in Arabidopsis: Pht1;1 and Pht1;4 play a major role in phosphate acquisition from both low- and high-phosphate environments. , 2004, The Plant journal : for cell and molecular biology.

[76]  S. Strauss Forest biotechnology – thriving despite controversy , 2004 .

[77]  A. Millar,et al.  Developmental Physiology of Cluster-Root Carboxylate Synthesis and Exudation in Harsh Hakea. Expression of Phosphoenolpyruvate Carboxylase and the Alternative Oxidase1 , 2004, Plant Physiology.

[78]  Angela Hodge,et al.  The plastic plant: root responses to heterogeneous supplies of nutrients , 2004 .

[79]  B. Lahner,et al.  Arabidopsis pdr2 reveals a phosphate-sensitive checkpoint in root development. , 2004, The Plant journal : for cell and molecular biology.

[80]  J. Lynch,et al.  Topsoil foraging – an architectural adaptation of plants to low phosphorus availability , 2001, Plant and Soil.

[81]  H. G. Diem,et al.  Iron deficiency induces cluster (proteoid) root formation in Casuarina glauca , 1997, Plant and Soil.

[82]  H. Lambers,et al.  Effects of external phosphorus supply on internal phosphorus concentration and the initiation, growth and exudation of cluster roots in Hakea prostrata R.Br. , 2004, Plant and Soil.

[83]  B. Lamont Structure, ecology and physiology of root clusters – a review , 2004, Plant and Soil.

[84]  H. G. Diem,et al.  Does ethylene mediate cluster root formation under iron deficiency? , 2003, Annals of botany.

[85]  François Tardieu,et al.  Temporal responses of Arabidopsis root architecture to phosphate starvation: evidence for the involvement of auxin signalling , 2003 .

[86]  H. Lambers,et al.  Shoot P status regulates cluster‐root growth and citrate exudation in Lupinus albus grown with a divided root system , 2003 .

[87]  A. Karthikeyan,et al.  Phosphite, an Analog of Phosphate, Suppresses the Coordinated Expression of Genes under Phosphate Starvation1 , 2002, Plant Physiology.

[88]  Luis Herrera-Estrella,et al.  Phosphate Availability Alters Architecture and Causes Changes in Hormone Sensitivity in the Arabidopsis Root System1 , 2002, Plant Physiology.

[89]  G. Neumann,et al.  Cluster roots--an underground adaptation for survival in extreme environments. , 2002, Trends in plant science.

[90]  Wu Ping,et al.  Effect of Phosphorus Deficiency Stress on Rice Lateral Root Growth and Nutrient Absorption , 2001 .

[91]  C. Ticconi,et al.  Attenuation of phosphate starvation responses by phosphite in Arabidopsis. , 2001, Plant physiology.

[92]  H. Leyser,et al.  Phosphate availability regulates root system architecture in Arabidopsis. , 2001, Plant physiology.

[93]  L. Hai Effect of Phosphorus Deficiency Stress on Rice Lateral Root Growth and Nutrient Absorption , 2001 .

[94]  Keith R. Skene Pattern Formation in Cluster Roots: Some Developmental and Evolutionary Considerations , 2000 .

[95]  M. Watt,et al.  Linking development and determinacy with organic acid efflux from proteoid roots of white lupin grown with low phosphorus and ambient or elevated atmospheric CO2 concentration , 1999, Plant physiology.

[96]  Keith R. Skene Cluster roots: some ecological considerations , 1998 .

[97]  J. Lynch,et al.  Effect of phosphorus deficiency on growth angle of basal roots in Phaseolus vulgaris. , 1996, The New phytologist.

[98]  G. Fink,et al.  A pathway for lateral root formation in Arabidopsis thaliana. , 1995, Genes & development.

[99]  P. Benfey,et al.  The SABRE gene is required for normal cell expansion in Arabidopsis. , 1995, Genes & development.

[100]  E. Delhaize,et al.  Characterization of a Phosphate-Accumulator Mutant of Arabidopsis thaliana , 1995, Plant Physiology.

[101]  B. Lamont The morphology and anatomy of proteoid roots in the genus Hakea , 1972 .