Hidden branches: developments in root system architecture.

The root system is fundamentally important for plant growth and survival because of its role in water and nutrient uptake. Therefore, plants rely on modulation of root system architecture (RSA) to respond to a changing soil environment. Although RSA is a highly plastic trait and varies both between and among species, the basic root system morphology and its plasticity are controlled by inherent genetic factors. These mediate the modification of RSA, mostly at the level of root branching, in response to a suite of biotic and abiotic factors. Recent progress in the understanding of the molecular basis of these responses suggests that they largely feed through hormone homeostasis and signaling pathways. Novel factors implicated in the regulation of RSA in response to the myriad endogenous and exogenous signals are also increasingly isolated through alternative approaches such as quantitative trait locus analysis.

[1]  W. Park,et al.  Maize root system and genetic analysis of its formation. , 2002 .

[2]  X. Deng,et al.  A Rice Glutamate Receptor–Like Gene Is Critical for the Division and Survival of Individual Cells in the Root Apical Meristem[W] , 2005, The Plant Cell Online.

[3]  Reeta Prusty,et al.  Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. , 2006, Plant & cell physiology.

[4]  Anna N. Stepanova,et al.  A Link between Ethylene and Auxin Uncovered by the Characterization of Two Root-Specific Ethylene-Insensitive Mutants in Arabidopsis , 2005, The Plant Cell Online.

[5]  N. Graham,et al.  Auxin cross-talk: integration of signalling pathways to control plant development. , 2002 .

[6]  J. Keurentjes,et al.  Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[7]  D. Inzé,et al.  The peri-cell-cycle in Arabidopsis. , 2001, Journal of experimental botany.

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

[9]  J. Lynch Root Architecture and Plant Productivity , 1995, Plant physiology.

[10]  Alastair H. Fitter,et al.  AN ARCHITECTURAL APPROACH TO THE COMPARATIVE ECOLOGY OF PLANT ROOT SYSTEMS , 2008 .

[11]  U. Paszkowski,et al.  Rice phosphate transporters include an evolutionarily divergent gene specifically activated in arbuscular mycorrhizal symbiosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  Ottoline Leyser,et al.  Dynamic Integration of Auxin Transport and Signalling , 2006, Current Biology.

[13]  J. Malamy,et al.  Intrinsic and environmental response pathways that regulate root system architecture. , 2005, Plant, cell & environment.

[14]  Xiangdong Fu,et al.  Auxin promotes Arabidopsis root growth by modulating gibberellin response , 2003, Nature.

[15]  A. Nordheim,et al.  Proteomic analysis of shoot‐borne root initiation in maize (Zea mays L.) , 2006, Proteomics.

[16]  S. Takatsuto,et al.  Roots and shoots of tomato produce 6-deoxo-28-norcathasterone, 6-deoxo-28-nortyphasterol and 6-deoxo-28-norcastasterone, possible precursors of 28-norcastasterone. , 2001, Phytochemistry.

[17]  G. Fink,et al.  Arabidopsis ALF4 encodes a nuclear-localized protein required for lateral root formation. , 2004, The Plant journal : for cell and molecular biology.

[18]  P. Tillard,et al.  A Central Role for the Nitrate Transporter NRT2.1 in the Integrated Morphological and Physiological Responses of the Root System to Nitrogen Limitation in Arabidopsis1 , 2006, Plant Physiology.

[19]  H. Fukaki,et al.  Lateral root formation is blocked by a gain-of-function mutation in the SOLITARY-ROOT/IAA14 gene of Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[20]  Yun-Wei Yang,et al.  A novel function of abscisic acid in the regulation of rice (Oryza sativa L.) root growth and development. , 2006, Plant & cell physiology.

[21]  J. Malamy,et al.  Environmental regulation of lateral root initiation in Arabidopsis. , 2001, Plant physiology.

[22]  B. Scheres,et al.  Root-Specific CLE19 Overexpression and the sol1/2 Suppressors Implicate a CLV-like Pathway in the Control of Arabidopsis Root Meristem Maintenance , 2003, Current Biology.

[23]  R. Amasino,et al.  The PLETHORA Genes Mediate Patterning of the Arabidopsis Root Stem Cell Niche , 2004, Cell.

[24]  C. Foyer,et al.  Modulation of plant morphology, root architecture, and cell structure by low vitamin C in Arabidopsis thaliana. , 2006, Journal of experimental botany.

[25]  B. Scheres,et al.  Cellular organisation of the Arabidopsis thaliana root. , 1993, Development.

[26]  B. Hetrick Mycorrhizas and root architecture , 1991, Experientia.

[27]  M. Estelle,et al.  The axr4 auxin-resistant mutants of Arabidopsis thaliana define a gene important for root gravitropism and lateral root initiation. , 1995, The Plant journal : for cell and molecular biology.

[28]  J. G. Dubrovsky,et al.  Mutations in the Diageotropica (Dgt) gene uncouple patterned cell division during lateral root initiation from proliferative cell division in the pericycle. , 2006, The Plant journal : for cell and molecular biology.

[29]  J. Schiefelbein Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. , 2003, Current opinion in plant biology.

[30]  B. Forde,et al.  An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. , 1998, Science.

[31]  Mark C. Brundrett,et al.  Coevolution of roots and mycorrhizas of land plants. , 2002, The New phytologist.

[32]  Claudia van den Berg,et al.  Short-range control of cell differentiation in the Arabidopsis root meristem , 1997, Nature.

[33]  Ping Wu,et al.  ARL1, a LOB-domain protein required for adventitious root formation in rice. , 2005, The Plant journal : for cell and molecular biology.

[34]  Karen S. Osmont,et al.  BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth , 2006, Nature.

[35]  F. Daniel-Vedele,et al.  The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[36]  Pascal Gantet,et al.  Transcription Factor Networks. Pathways to the Knowledge of Root Development , 2004, Plant Physiology.

[37]  Rüdiger Simon,et al.  Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis , 2003, Development Genes and Evolution.

[38]  Valérie Laucou,et al.  Cytokinin-Deficient Transgenic Arabidopsis Plants Show Multiple Developmental Alterations Indicating Opposite Functions of Cytokinins in the Regulation of Shoot and Root Meristem Activity Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.014928 , 2003, The Plant Cell Online.

[39]  Zhenbiao Yang,et al.  Brassinosteroids Interact with Auxin to Promote Lateral Root Development in Arabidopsis1 , 2004, Plant Physiology.

[40]  C. Foyer,et al.  ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[41]  S. May,et al.  Expression studies on AUX1-like genes in Medicago truncatula suggest that auxin is required at two steps in early nodule development. , 2001, Molecular plant-microbe interactions : MPMI.

[42]  T. Altmann,et al.  Brassinosteroids Promote Root Growth in Arabidopsis , 2003, Plant Physiology.

[43]  A. Müller,et al.  A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. , 2002, The Plant journal : for cell and molecular biology.

[44]  G. Ponce,et al.  Auxin and ethylene interactions control mitotic activity of the quiescent centre, root cap size, and pattern of cap cell differentiation in maize. , 2005, Plant, cell & environment.

[45]  V. Rubio,et al.  A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. , 2001, Genes & development.

[46]  D. Weijers,et al.  Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem. , 2004, Gene.

[47]  C. Dean,et al.  Embryonic origin of the Arabidopsis primary root and root meristem initials , 1994 .

[48]  E. Aloni,et al.  Role of cytokinin and auxin in shaping root architecture: regulating vascular differentiation, lateral root initiation, root apical dominance and root gravitropism. , 2006, Annals of botany.

[49]  E. Blancaflor,et al.  Developmental anatomy and auxin response of lateral root formation in Ceratopteris richardii. , 2004, Journal of experimental botany.

[50]  A. Bleecker,et al.  A Mutation Altering Auxin Homeostasis and Plant Morphology in Arabidopsis. , 1995, The Plant cell.

[51]  A. Nordheim,et al.  Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1 , 2006, Proteomics.

[52]  Jinxiang Wang,et al.  Interactions between ethylene, gibberellin and abscisic acid regulate emergence and growth rate of adventitious roots in deepwater rice , 2006, Planta.

[53]  C. Steindler,et al.  Shade avoidance responses are mediated by the ATHB-2 HD-zip protein, a negative regulator of gene expression. , 1999, Development.

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

[55]  J. Malamy,et al.  Osmotic regulation of root system architecture. , 2005, The Plant journal : for cell and molecular biology.

[56]  C. Hardtke,et al.  Natural genetic variation in Arabidopsis identifies BREVIS RADIX , a novel regulator of cell proliferation and elongation in the root , 2004 .

[57]  L. Lamattina,et al.  Nitric oxide plays a central role in determining lateral root development in tomato , 2004, Planta.

[58]  W. Frommer,et al.  Analysis of the Arabidopsis rsr4-1/pdx1-3 Mutant Reveals the Critical Function of the PDX1 Protein Family in Metabolism, Development, and Vitamin B6 Biosynthesis[W] , 2006, The Plant Cell Online.

[59]  M. Sauter,et al.  Adventitious root growth and cell-cycle induction in deepwater rice , 1999, Plant physiology.

[60]  H. Nusbaum,et al.  Formation of lateral root meristems is a two-stage process. , 1995, Development.

[61]  T. Mockler,et al.  Interdependency of Brassinosteroid and Auxin Signaling in Arabidopsis , 2004, PLoS biology.

[62]  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.

[63]  J. Schiefelbein,et al.  Responses to iron deficiency in Arabidopsis thaliana: The Turbo iron reductase does not depend on the formation of root hairs and transfer cells , 2004, Planta.

[64]  Gerhard K. H. Przemeck,et al.  Studies on the role of the Arabidopsis gene MONOPTEROS in vascular development and plant cell axialization , 2004, Planta.

[65]  G. Sandberg,et al.  Dissecting Arabidopsis lateral root development. , 2003, Trends in plant science.

[66]  Brian G Forde,et al.  Nitrogen regulation of root branching. , 2006, Annals of botany.

[67]  D. Inzé,et al.  Lateral Root Initiation or the Birth of a New Meristem , 2006, Plant Molecular Biology.

[68]  G. Sandberg,et al.  AXR4 Is Required for Localization of the Auxin Influx Facilitator AUX1 , 2006, Science.

[69]  C. Hardtke Root development--branching into novel spheres. , 2006, Current opinion in plant biology.

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

[71]  L. Herrera-Estrella,et al.  The role of nutrient availability in regulating root architecture. , 2003, Current opinion in plant biology.

[72]  G. Hagen,et al.  Overlapping and non-redundant functions of the Arabidopsis auxin response factors MONOPTEROS and NONPHOTOTROPIC HYPOCOTYL 4 , 2004, Development.

[73]  E. Liscum,et al.  MASSUGU2 Encodes Aux/IAA19, an Auxin-Regulated Protein That Functions Together with the Transcriptional Activator NPH4/ARF7 to Regulate Differential Growth Responses of Hypocotyl and Formation of Lateral Roots in Arabidopsis thaliana , 2004, The Plant Cell Online.

[74]  P W Barlow,et al.  Dual pathways for regulation of root branching by nitrate. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[75]  S. Fujioka,et al.  Microarray Analysis of Brassinosteroid-Regulated Genes in Arabidopsis , 2002, Plant Physiology.

[76]  Makoto Matsuoka,et al.  Crown rootless1, Which Is Essential for Crown Root Formation in Rice, Is a Target of an AUXIN RESPONSE FACTOR in Auxin Signalingw⃞ , 2005, The Plant Cell Online.

[77]  T. Schmülling,et al.  Arabidopsis Cytokinin Receptor Mutants Reveal Functions in Shoot Growth, Leaf Senescence, Seed Size, Germination, Root Development, and Cytokinin Metabolism[W] , 2005, The Plant Cell Online.

[78]  M. Mccully,et al.  ROOTS IN SOIL: Unearthing the Complexities of Roots and Their Rhizospheres. , 1999, Annual review of plant physiology and plant molecular biology.

[79]  Ilda Casimiro,et al.  Lateral root initiation by asymmetrical transverse divisions of pericycle cells in four plant species:Raphanus sativus, Helianthus annuus, Zea mays, andDaucus carota , 1995, Protoplasma.

[80]  S. Salvi,et al.  To clone or not to clone plant QTLs: present and future challenges. , 2005, Trends in plant science.

[81]  H. Leyser,et al.  Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis. , 2002, The Plant journal : for cell and molecular biology.

[82]  M Koornneef,et al.  Naturally occurring variation in Arabidopsis: an underexploited resource for plant genetics. , 2000, Trends in plant science.

[83]  Peter McCourt,et al.  The ABSCISIC ACID INSENSITIVE 3 (ABI3) gene is modulated by farnesylation and is involved in auxin signaling and lateral root development in Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[84]  P. Benfey,et al.  Organization and cell differentiation in lateral roots of Arabidopsis thaliana. , 1997, Development.

[85]  Dirk Inzé,et al.  Auxin-Mediated Cell Cycle Activation during Early Lateral Root Initiation Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.004960. , 2002, The Plant Cell Online.

[86]  D. Inzé,et al.  Transcript profiling of early lateral root initiation. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[87]  K. Ljung,et al.  Auxin and Light Control of Adventitious Rooting in Arabidopsis Require ARGONAUTE1w⃞ , 2005, The Plant Cell Online.

[88]  R. Hussey,et al.  Cotton root growth as influenced by phosphorus nutrition and vesicular–arbuscular mycorrhizas , 1989 .

[89]  Chun-Lin Su,et al.  Regulation of Phosphate Homeostasis by MicroRNA in Arabidopsis[W] , 2005, The Plant Cell Online.

[90]  Lewis J. Feldman,et al.  The Maize Root , 1994 .

[91]  M. Drew,et al.  COMPARISON OF THE EFFECTS OF A LOCALISED SUPPLY OF PHOSPHATE, NITRATE, AMMONIUM AND POTASSIUM ON THE GROWTH OF THE SEMINAL ROOT SYSTEM, AND THE SHOOT, IN BARLEY , 1975 .

[92]  S. Kikuchi,et al.  Isolation and Characterization of a Rice Dwarf Mutant with a Defect in Brassinosteroid Biosynthesis1 , 2002, Plant Physiology.

[93]  F. Van Gijsegem,et al.  Induction of lateral root structure formation on petunia roots: A novel effect of GMI1000 Ralstonia solanacearum infection impaired in Hrp mutants. , 2006, Molecular plant-microbe interactions : MPMI.

[94]  D. Inzé,et al.  A new D-type cyclin of Arabidopsis thaliana expressed during lateral root primordia formation , 1999, Planta.

[95]  Woong June Park,et al.  From weeds to crops: genetic analysis of root development in cereals. , 2004, Trends in plant science.

[96]  M. Stitt,et al.  PHO2, MicroRNA399, and PHR1 Define a Phosphate-Signaling Pathway in Plants1[W][OA] , 2006, Plant Physiology.

[97]  Yukihisa Shimada,et al.  Brassinolide Induces IAA5, IAA19, and DR5, a Synthetic Auxin Response Element in Arabidopsis, Implying a Cross Talk Point of Brassinosteroid and Auxin Signaling , 2003, Plant Physiology.

[98]  C. Hardtke,et al.  The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. , 2004, The Plant journal : for cell and molecular biology.

[99]  A. Hirsch,et al.  What makes the rhizobia-legume symbiosis so special? , 2001, Plant physiology.

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

[101]  A. Trubuil,et al.  Quantitative trait loci controlling root growth and architecture in Arabidopsis thaliana confirmed by heterogeneous inbred family , 2005, Theoretical and Applied Genetics.

[102]  D. Inzé,et al.  Auxin Transport Promotes Arabidopsis Lateral Root Initiation , 2001, Plant Cell.

[103]  D. Bird,et al.  Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses. , 2004, The Plant journal : for cell and molecular biology.

[104]  D. Inzé,et al.  An abscisic acid-sensitive checkpoint in lateral root development of Arabidopsis. , 2003, The Plant journal : for cell and molecular biology.

[105]  X. Deng,et al.  An Auxin-Inducible F-Box Protein CEGENDUO Negatively Regulates Auxin-Mediated Lateral Root Formation in Arabidopsis , 2006, Plant Molecular Biology.

[106]  Melissa D. Lehti-Shiu,et al.  Identification of Quantitative Trait Loci That Regulate Arabidopsis Root System Size and Plasticity , 2006, Genetics.

[107]  L. Laplaze,et al.  Armadillo-related proteins promote lateral root development in Arabidopsis , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[108]  M. Matsuoka,et al.  Where do gibberellin biosynthesis and gibberellin signaling occur in rice plants? , 2003, The Plant journal : for cell and molecular biology.

[109]  J. Harada,et al.  Quantitative trait loci for adventitious and lateral roots in rice , 2006 .

[110]  T. Altmann,et al.  Brassinosteroid-Regulated Gene Expression , 2002, Plant Physiology.

[111]  J. Giraudat,et al.  Interactions between Abscisic Acid and Ethylene Signaling Cascades , 2000, Plant Cell.

[112]  M. J. Harrison,et al.  Signaling in the arbuscular mycorrhizal symbiosis. , 2005, Annual review of microbiology.

[113]  Ho Bang Kim,et al.  The Regulation of DWARF4 Expression Is Likely a Critical Mechanism in Maintaining the Homeostasis of Bioactive Brassinosteroids in Arabidopsis1 , 2006, Plant Physiology.

[114]  M. Okamoto,et al.  The regulation of nitrate and ammonium transport systems in plants. , 2002, Journal of experimental botany.

[115]  Jian-Kang Zhu,et al.  A miRNA Involved in Phosphate-Starvation Response in Arabidopsis , 2005, Current Biology.

[116]  D. Inzé,et al.  Superroot, a recessive mutation in Arabidopsis, confers auxin overproduction. , 1995, The Plant cell.

[117]  M. Yano,et al.  An SNP Caused Loss of Seed Shattering During Rice Domestication , 2006, Science.

[118]  P. Schnable,et al.  Isolation, Characterization, and Pericycle-Specific Transcriptome Analyses of the Novel Maize Lateral and Seminal Root Initiation Mutant rum11[w] , 2005, Plant Physiology.