1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Plant Biology
  4. Volume 67, 2016
  5. Article

Annual Review of Plant Biology

Volume 67, 2016

Environmental Control of Root System Biology

Abstract

The plant root system traverses one of the most complex environments on earth. Understanding how roots support plant life on land requires knowing how soil properties affect the availability of nutrients and water and how roots manipulate the soil environment to optimize acquisition of these resources. Imaging of roots in soil allows the integrated analysis and modeling of environmental interactions occurring at micro- to macroscales. Advances in phenotyping of root systems is driving innovation in cross-platform-compatible methods for data analysis. Root systems acclimate to the environment through architectural changes that act at the root-type level as well as through tissue-specific changes that affect the metabolic needs of the root and the efficiency of nutrient uptake. A molecular understanding of the signaling mechanisms that guide local and systemic signaling is providing insight into the regulatory logic of environmental responses and has identified points where crosstalk between pathways occurs.

Keyword(s): root modeling, root system architecture, root-environment interactions
Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-043015-111848
2016-04-29
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/arplant/67/1/annurev-arplant-043015-111848.html?itemId=/content/journals/10.1146/annurev-arplant-043015-111848&mimeType=html&fmt=ahah

Literature Cited

  1. Araya T, Miyamoto M, Wibowo J, Suzuki A, Kojima S. 1.  et al. 2014. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. PNAS 111:2029–34 [Google Scholar]
  2. Babé A, Lavigne T, Séverin JP, Nagel KA, Walter A. 2.  et al. 2012. Repression of early lateral root initiation events by transient water deficit in barley and maize. Philos. Trans. R. Soc. B 367:1534–41 [Google Scholar]
  3. Bao Y, Aggarwal P, Robbins NE, Sturrock CJ, Thompson MC. 3.  et al. 2014. Plant roots use a patterning mechanism to position lateral root branches toward available water. PNAS 111:9319–24 [Google Scholar]
  4. Bari R, Datt Pant B, Stitt M, Scheible WR. 4.  2006. PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141:988–99 [Google Scholar]
  5. Bateman RM, Crane PR, DiMichele WA, Kenrick PR, Rowe NP. 5.  et al. 1998. Early evolution of land plants: phylogeny, physiology, and ecology of the primary terrestrial radiation. Annu. Rev. Ecol. Evol. Syst. 29:263–92 [Google Scholar]
  6. Baxter I, Brazelton JN, Yu D, Huang YS, Lahner B. 6.  et al. 2010. A coastal cline in sodium accumulation in Arabidopsis thaliana is driven by natural variation of the sodium transporter AtHKT1;1. PLOS Genet. 6:e1001193 [Google Scholar]
  7. Bayuelo-Jiménez JS, Gallardo-Valdéz M, Pérez-Decelis VA, Magdaleno-Armas L, Ochoa I, Lynch JP. 7.  2011. Genotypic variation for root traits of maize (Zea mays L.) from the Purhepecha Plateau under contrasting phosphorus availability. Field Crops Res. 121:350–62 [Google Scholar]
  8. Benfey PN. 8.  2012. Toward a systems analysis of the root. Cold Spring Harb. Symp. Quant. Biol. 77:91–96 [Google Scholar]
  9. Bennett MJ, Marchant A, Green HG, May ST, Ward SP. 9.  et al. 1996. Arabidopsis AUX1 gene: a permease-like regulator of root gravitropism. Science 273:948–50 [Google Scholar]
  10. Berner RA. 10.  1997. Geochemistry and geophysics: the rise of plants and their effect on weathering and atmospheric CO2. Science 276:544–46 [Google Scholar]
  11. Bisseling T, Scheres B. 11.  2014. Nutrient computation for root architecture. Science 346:300–301 [Google Scholar]
  12. Bodner G, Leitner D, Nakhforoosh A, Sobotik M, Moder K, Kaul HP. 12.  2013. A statistical approach to root system classification. Front. Plant Sci. 4:292 [Google Scholar]
  13. Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M. 13.  2015. Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants 1:15015 [Google Scholar]
  14. Bournier M, Tissot N, Mari S, Boucherez J, Lacombe E. 14.  et al. 2013. 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. J. Biol. Chem. 288:22670–80 [Google Scholar]
  15. Brady NC, Weil RR. 15.  2008. The Nature and Properties of Soils Upper Saddle River, NJ: Prentice Hall, 14th ed..
  16. Brady SM, Orlando DA, Lee JY, Wang JY, Koch J. 16.  et al. 2007. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 318:801–6 [Google Scholar]
  17. Busoms S, Teres J, Huang X, Bomblies K, Danku J. 17.  et al. 2015. Salinity is an agent of divergent selection driving local adaptation of Arabidopsis thaliana to coastal habitats. Plant Physiol. 168:915–29 [Google Scholar]
  18. Cai J, Zeng Z, Connor JN, Huang CY, Melino V. 18.  et al. 2015. RootGraph: a graphic optimization tool for automated image analysis of plant roots. J. Exp. Bot. 66:6551–62 [Google Scholar]
  19. Caldwell MM, Richards JH. 19.  1989. Hydraulic lift: water efflux from upper roots improves effectiveness of water uptake by deep roots. Oecologia 79:1–5 [Google Scholar]
  20. Chen YL, Dunbabin VM, Postma JA, Diggle AJ, Siddique KHM, Rengel Z. 20.  2013. Modelling root plasticity and response of narrow-leafed lupin to heterogeneous phosphorus supply. Plant Soil 372:319–37 [Google Scholar]
  21. Chitwood DH, Topp CN. 21.  2015. Revealing plant cryptotypes: defining meaningful phenotypes among infinite traits. Curr. Opin. Plant Biol. 24:54–60 [Google Scholar]
  22. Digby J, Firn RD. 22.  1995. The gravitropic set-point angle (GSA): the identification of an important developmentally controlled variable governing plant architecture. Plant Cell Environ. 18:1434–40 [Google Scholar]
  23. Dinneny JR. 23.  2014. A gateway with a guard: how the endodermis regulates growth through hormone signaling. Plant Sci. 214:14–19 [Google Scholar]
  24. Dinneny JR, Long TA, Wang JY, Jung JW, Mace D. 24.  et al. 2008. Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science 320:942–45 [Google Scholar]
  25. Doebley J, Stec A, Gustus C. 25.  1995. Teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–46 [Google Scholar]
  26. Downie H, Holden N, Otten W, Spiers AJ, Valentine TA, Dupuy L. 26.  2012. Transparent soil for imaging the rhizosphere. PLOS ONE 7:1–6 [Google Scholar]
  27. Draye X, Kim Y, Lobet G, Javaux M. 27.  2010. Model-assisted integration of physiological and environmental constraints affecting the dynamic and spatial patterns of root water uptake from soils. J. Exp. Bot. 61:2145–55 [Google Scholar]
  28. Drew M. 28.  1975. 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. New Phytol. 75:479–90 [Google Scholar]
  29. Duan L, Dietrich D, Ng CH, Chan PMY, Bhalerao R. 29.  et al. 2013. Endodermal ABA signaling promotes lateral root quiescence during salt stress in Arabidopsis seedlings. Plant Cell 25:324–41 [Google Scholar]
  30. Dunbabin VM, Postma JA, Schnepf A, Pagès L, Javaux M. 30.  et al. 2013. Modelling root-soil interactions using three-dimensional models of root growth, architecture and function. Plant Soil 372:93–124 [Google Scholar]
  31. Dupuy L, Fourcaud T, Stokes A, Danjon F. 31.  2005. A density-based approach for the modelling of root architecture: application to Maritime pine (Pinus pinaster Ait.) root systems. J. Theor. Biol. 236:323–34 [Google Scholar]
  32. Dupuy L, Gregory PJ, Bengough AG. 32.  2010. Root growth models: towards a new generation of continuous approaches. J. Exp. Bot. 61:2131–43 [Google Scholar]
  33. Dupuy L, Vignes M, McKensie BM, White PJ. 33.  2010. The dynamics of root meristem distribution in the soil. Plant Cell Environ. 33:358–69 [Google Scholar]
  34. Durrett TP, Gassmann W, Rogers EE. 34.  2007. The FRD3-mediated efflux of citrate into the root vasculature is necessary for efficient iron translocation. Plant Physiol. 144:197–205 [Google Scholar]
  35. Eshel A, Waisel Y. 35.  1996. Multiform and multifunction of various constituents of one root system. Plant Roots: The Hidden Half Y Waisel, A Eshel, U Kafkafi 175–92 New York: Marcel Dekker [Google Scholar]
  36. Fang S, Clark RT, Zheng Y, Iyer-Pascuzzi AS, Weitz JS. 36.  et al. 2013. Genotypic recognition and spatial responses by rice roots. PNAS 110:2670–75 [Google Scholar]
  37. Fitter AH. 37.  1987. An architectural approach to the comparative ecology of plant root systems. New Phytol. 106:61–77 [Google Scholar]
  38. Fitter AH, Stickland TR, Harvey ML, Wilson GW. 38.  1991. Architectural analysis of plant root systems 1. Architectural correlates of exploitation efficiency. New Phytol. 118:375–82 [Google Scholar]
  39. Flowers T, Yeo A. 39.  1995. Breeding for salinity resistance in crop plants: Where next?. Aust. J. Plant Physiol. 22:875 [Google Scholar]
  40. Furbank RT, Tester M. 40.  2011. Phenomics technologies to relieve the phenotyping bottleneck. Trends Plant Sci. 16:635–44 [Google Scholar]
  41. Galkovskyi T, Mileyko Y, Bucksch A, Moore B, Symonova O. 41.  et al. 2012. GiA Roots: software for the high throughput analysis of plant root system architecture. BMC Plant Biol. 12:116 [Google Scholar]
  42. Gaudin ACM, McClymont SA, Soliman SSM, Raizada MN. 42.  2014. The effect of altered dosage of a mutant allele of Teosinte branched 1 (tb1-ref) on the root system of modern maize. BMC Genet. 15:23 [Google Scholar]
  43. Ge Z, Rubio G, Lynch JP. 43.  2000. The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218:159–71 [Google Scholar]
  44. Geldner N. 44.  2013. The endodermis. Annu. Rev. Plant Biol. 64:531–58 [Google Scholar]
  45. Geng Y, Wu R, Wee CW, Xie F, Wei X. 45.  et al. 2013. A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25:2132–54 [Google Scholar]
  46. Giehl R, von Wirén N. 46.  2014. Root nutrient foraging. Plant Physiol. 166:509–17 [Google Scholar]
  47. Godin C, Sinoquet H. 47.  2005. Functional-structural plant modelling. New Phytol. 166:705–8 [Google Scholar]
  48. Gruber BD, Giehl RFH, Friedel S, von Wirén N. 48.  2013. Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163:161–79 [Google Scholar]
  49. Hackett C, Rose DA. 49.  1972. A model of the extension and branching of a seminal root of barley, and its use in studying relations between root dimensions. I. The model. Aust. J. Biol. Sci. 25:681–90 [Google Scholar]
  50. Hamburger D, Rezzonico E, MacDonald-Comber Petétot J, Somerville C, Poirier Y. 50.  2002. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell 14:889–902 [Google Scholar]
  51. Heppell J, Talboys P, Payvandi S, Zygalakis KC, Fliege J. 51.  et al. 2014. How changing root system architecture can help tackle a reduction in soil phosphate (P) levels for better plant P acquisition. Plant Cell Environ. 38:118–28 [Google Scholar]
  52. Ho MDB, McCannon C, Lynch JP. 52.  2004. Optimization modeling of plant root architecture for water and phosphorus acquisition. J. Theor. Bot. 226:331–40 [Google Scholar]
  53. Hochholdinger F. 53.  2009. The maize root system: morphology, anatomy, and genetics. Handbook of Maize: Its Biology JL Bennetzen, SC Hake 145–60 New York: Springer [Google Scholar]
  54. Hohmann-Marriott MF, Blankenship RE. 54.  2011. Evolution of photosynthesis. Annu. Rev. Plant Biol. 62:515–48 [Google Scholar]
  55. Huber K, Vanderborght J, Javaux M, Schröder N, Dodd IC, Vereecken H. 55.  2014. Modelling the impact of heterogeneous rootzone water distribution on the regulation of transpiration by hormone transport and/or hydraulic pressures. Plant Soil 384:93–112 [Google Scholar]
  56. Jackson RB, Sperry JS, Dawson TE. 56.  2000. Root water uptake and transport: using physiological processes in global predictions. Trends Plant Sci. 5:482–88 [Google Scholar]
  57. Jaramillo RE, Nord EA, Chimungu JG, Brown KM, Lynch JP. 57.  2013. Root cortical burden influences drought tolerance in maize. Ann. Bot. 112:429–37 [Google Scholar]
  58. Jarvis PG. 58.  1976. The interpretation of the variations in leaf water potential and stomatal conductance found in canopies in the field. Philos. Trans. R. Soc. B 273:593–610 [Google Scholar]
  59. Javaux M, Schroeder T, Vanderborght J, Vereecken H. 59.  2008. Use of a three-dimensional detailed modeling approach for predicting root water uptake. Vadose Zone J. 7:1079–88 [Google Scholar]
  60. Jones VAS, Dolan L. 60.  2012. The evolution of root hairs and rhizoids. Ann. Bot. 110:205–12 [Google Scholar]
  61. Julkowska MM, Hoefsloot HCJ, Mol S, Feron R, de Boer GJ. 61.  et al. 2014. Capturing Arabidopsis root architecture dynamics with ROOT-FIT reveals diversity in responses to salinity. Plant Physiol. 166:1387–402 [Google Scholar]
  62. Karahara I, Ikeda A, Kondo T, Uetake Y. 62.  2004. Development of the Casparian strip in primary roots of maize under salt stress. Planta 219:41–47 [Google Scholar]
  63. Kehr J. 63.  2013. Systemic regulation of mineral homeostasis by micro RNAs. Front. Plant Sci. 4:145 [Google Scholar]
  64. Kehr J, Buhtz A. 64.  2008. Long distance transport and movement of RNA through the phloem. J. Exp. Bot. 59:85–92 [Google Scholar]
  65. Kellermeier F, Armengaud P, Seditas TJ, Danku J, Salt DE, Amtmann A. 65.  2014. Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 26:1480–96 [Google Scholar]
  66. Knee EM, Gong FC, Gao M, Teplitski M, Jones AR. 66.  et al. 2001. Root mucilage from pea and its utilization by rhizosphere bacteria as a sole carbon source. Mol. Plant-Microbe Interact. 14:775–84 [Google Scholar]
  67. Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K. 67.  et al. 2010. Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18:927–37 [Google Scholar]
  68. Lambers H, Finnegan PM, Jost R, Plaxton WC, Shane MW, Stitt M. 68.  2015. Phosphorus nutrition in Proteaceae and beyond. Nat. Plants 1:15109 [Google Scholar]
  69. Lambers H, Hayes PE, Laliberté E, Oliveira RS. 69.  2015. Leaf manganese accumulation and phosphorus-acquisition efficiency. Trends Plant Sci. 20:83–90 [Google Scholar]
  70. Le Marié C, Kirchgessner N, Marschall D, Walter A, Hund A. 70.  2014. Rhizoslides: paper-based growth system for non-destructive, high throughput phenotyping of root development by means of image analysis. Plant Methods 10:13 [Google Scholar]
  71. Leitner D, Klepsch S, Bodner G, Schnepf A. 71.  2010. A dynamic root system growth model based on L-Systems. Plant Soil 332:117–92 [Google Scholar]
  72. Liu KH, Tsay YF. 72.  2003. Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22:1005–13 [Google Scholar]
  73. Lobet G, Draye X. 73.  2013. Novel scanning procedure enabling the vectorization of entire rhizotron-grown root systems. Plant Methods 9:2–10 [Google Scholar]
  74. Lobet G, Pagès L, Draye X. 74.  2014. A modeling approach to determine the importance of dynamic regulation of plant hydraulic conductivities on the water uptake dynamics in the soil-plant. Ecol. Model. 290:65–75 [Google Scholar]
  75. Lobet G, Pound MP, Diener J, Pradal C, Draye X. 75.  et al. 2015. Root System Markup Language: toward a unified root architecture description language. Plant Physiol. 167:617–27 [Google Scholar]
  76. López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L. 76.  2014. Phosphate nutrition: improving low-phosphate tolerance in crops. Annu. Rev. Plant Biol. 65:95–123 [Google Scholar]
  77. Lowry DB, Hall MC, Salt DE, Willis JH. 77.  2009. Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytol. 183:776–88 [Google Scholar]
  78. Lungley DR. 78.  1973. The growth of root systems—a numerical computer simulation model. Plant Soil 38:145–59 [Google Scholar]
  79. Lynch JP. 79.  2011. Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol. 156:1041–49 [Google Scholar]
  80. Lynch JP. 80.  2013. Steep, cheap and deep: an ideotype to optimize water and N acquisition by maize root systems. Ann. Bot. 112:347–57 [Google Scholar]
  81. Lynch JP, Brown KM. 81.  2012. New roots for agriculture: exploiting the root phenome. Philos. Trans. R. Soc. B 367:1598–604 [Google Scholar]
  82. Lynch JP, Nielsen KL, Davis RD, Jablokow AG. 82.  1997. SimRoot: modelling and visualization of root systems. Plant Soil 188:139–51 [Google Scholar]
  83. Lynch JP, Wojciechowski T. 83.  2015. Opportunities and challenges in the subsoil: pathways to deeper rooted crops. J. Exp. Bot. 66:2199–210 [Google Scholar]
  84. Mahner M, Kary M. 84.  1997. What exactly are genomes, genotypes and phenotypes? And what about phenomes?. J. Theor. Biol. 186:55–63 [Google Scholar]
  85. Mairhofer S, Zappala S, Tracy S, Sturrock C, Bennett M. 85.  et al. 2011. RooTrak: automated recovery of three-dimensional plant root architecture in soil from X-ray microcomputed tomography using visual tracking. Plant Physiol. 158:561–69 [Google Scholar]
  86. Marschner P. 86.  2012. Marschner's Mineral Nutrition of Higher Plants San Diego, CA: Academic
  87. Mathieu L, Lobet G, Tocquin P, Périlleux C. 87.  2015. Rhizoponics: a novel hydroponic rhizotron for root system analyses on mature Arabidopsis thaliana plants. Plant Methods 11:1–7 [Google Scholar]
  88. McCully ME. 88.  1999. Roots in soil: unearthing the complexities of roots and their rhizospheres. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50:695–718 [Google Scholar]
  89. McCully ME, Canny MJ. 89.  1988. Pathways and processes of water and nutrient movement in roots. Plant Soil 111:159–70 [Google Scholar]
  90. Medici A, Marshall-Colon A, Ronzier E, Szponarski W, Wang R. 90.  et al. 2015. AtNIGT1/HRS1 integrates nitrate and phosphate signals at the Arabidopsis root tip. Nat. Commun. 6:6274 [Google Scholar]
  91. Metzner R, Eggert A, van Dusschoten D, Pflugfelder D, Gerth S. 91.  et al. 2015. Direct comparison of MRI and X-ray CT technologies for 3D imaging of root systems in soil: potential and challenges for root trait quantification. Plant Methods 11:17 [Google Scholar]
  92. Miguel MA, Postma JA, Lynch JP. 92.  2015. Phene synergism between root hair length and basal root growth angle for phosphorus acquisition. Plant Physiol. 167:1430–39 [Google Scholar]
  93. Moreno-Risueno MA, Van Norman JM, Moreno A, Zhang J, Ahnert SE, Benfey PN. 93.  2010. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 329:1306–11 [Google Scholar]
  94. Moriwaki T, Miyazawa Y, Kobayashi A, Takahashi H. 94.  2013. Molecular mechanisms of hydrotropism in seedling roots of Arabidopsis thaliana (Brassicaceae). Am. J. Bot. 100:25–34 [Google Scholar]
  95. North GB, Nobel PS. 95.  1997. Drought-induced changes in soil contact and hydraulic conductivity for roots of Opuntia ficus-indica with and without rhizosheaths. Plant Soil 191:249–58 [Google Scholar]
  96. Oades J. 96.  1993. The role of biology in the formation, stabilization and degradation of soil structure. Geoderma 56:377–400 [Google Scholar]
  97. Ohyama K, Ogawa M, Matsubayashi Y. 97.  2008. Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J. 55:152–60 [Google Scholar]
  98. Oldroyd GED, Murray JD, Poole PS, Downie JA. 98.  2011. The rules of engagement in the legume-rhizobial symbiosis. Annu. Rev. Genet. 45:119–44 [Google Scholar]
  99. Orman-Ligeza B, Parizot B, Gantet PP, Beeckman T, Bennett MJ, Draye X. 99.  2013. Post-embryonic root organogenesis in cereals: branching out from model plants. Trends Plant Sci. 18:459–67 [Google Scholar]
  100. Osmont KS, Sibout R, Hardtke CS. 100.  2007. Hidden branches: developments in root system architecture. Annu. Rev. Plant Biol. 58:93–113 [Google Scholar]
  101. Pacheco-Villalobos D, Hardtke CS. 101.  2012. Natural genetic variation of root system architecture from Arabidopsis to Brachypodium: towards adaptive value. Philos. Trans. R. Soc. Lond. B 367:1552–58 [Google Scholar]
  102. Pagès L, Bécel C, Boukcim H, Moreau D, Nguyen C, Voisin AS. 102.  2013. Calibration and evaluation of ArchiSimple, a simple model of root system architecture. Ecol. Model. 290:76–84 [Google Scholar]
  103. Pagès L, Vercambre G, Drouet JL, Lecompte F, Collet C, LeBot J. 103.  2004. RootTyp: a generic model to depict and analyse the root system architecture. Plant Soil 258:103–19 [Google Scholar]
  104. Pant BD, Buhtz A, Kehr J, Scheible WR. 104.  2008. MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53:731–38 [Google Scholar]
  105. Peng Y, Li X, Li C. 105.  2012. Temporal and spatial profiling of root growth revealed novel response of maize roots under various nitrogen supplies in the field. PLOS ONE 7:e37726 [Google Scholar]
  106. Pérez-Torres CA, López-Bucio J, Cruz-Ramirez A, Ibarra-Laclette E, Dharmasiri S. 106.  et al. 2008. Phosphate availability alters lateral root development in Arabidopsis by modulating auxin sensitivity via a mechanism involving the TIR1 auxin receptor. Plant Cell 20:3258–72 [Google Scholar]
  107. Pfister A, Barberon M, Alassimone J, Kalmbach L, Lee Y. 107.  et al. 2014. A receptor-like kinase mutant with absent endodermal diffusion barrier displays selective nutrient homeostasis defects. eLife 3:e03115 [Google Scholar]
  108. Postma JA, Dathe A, Lynch JP. 108.  2014. The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability. Plant Physiol. 166:590–602 [Google Scholar]
  109. Postma JA, Lynch JP. 109.  2011. Root cortical aerenchyma enhances the growth of maize on soils with suboptimal availability of nitrogen, phosphorus, and potassium. Plant Physiol. 156:1190–201 [Google Scholar]
  110. Postma JA, Lynch JP. 110.  2011. Theoretical evidence for the functional benefit of root cortical aerenchyma in soils with low phosphorus availability. Ann. Bot. 107:829–41 [Google Scholar]
  111. Puga MI, Mateos I, Charukesi R, Wang Z, Franco-Zorrilla JM. 111.  et al. 2014. SPX1 is a phosphate-dependent inhibitor of PHOSPHATE STARVATION RESPONSE 1 in Arabidopsis. PNAS 111:14947–52 [Google Scholar]
  112. Rasse DP, Rumpel C, Dignac MF. 112.  2005. Is soil carbon mostly root carbon? Mechanisms for a specific stabilisation. Plant Soil 269:341–56 [Google Scholar]
  113. Rellán-Álvarez R, Giner-Martinez-Sierra J, Orduna J, Orera I, Rodríguez-Castrillón JÁ. 113.  et al. 2010. Identification of a tri-iron(III), tri-citrate complex in the xylem sap of iron-deficient tomato resupplied with iron: new insights into plant iron long-distance transport. Plant Cell Physiol. 51:91–102 [Google Scholar]
  114. Rellán-Álvarez R, Lobet G, Lindner H, Pradier PL, Sebastian J. 114.  et al. 2015. GLO-Roots: an imaging platform enabling multidimensional characterization of soil-grown root systems. eLife 4:e07597 [Google Scholar]
  115. Retallack GJ. 115.  1997. Early forest soils and their role in Devonian global change. Science 276:583–85 [Google Scholar]
  116. Robbins NE, Dinneny JR. 116.  2015. The divining root: moisture-driven responses of roots at the micro- and macro-scale. J. Exp. Bot. 66:2145–54 [Google Scholar]
  117. Robbins NE, Trontin C, Duan L, Dinneny JR. 117.  2014. Beyond the barrier: communication in the root through the endodermis. Plant Physiol. 166:551–59 [Google Scholar]
  118. Ron M, Dorrity MW, de Lucas M, Toal T, Hernandez RI. 118.  et al. 2013. Identification of novel loci regulating interspecific variation in root morphology and cellular development in tomato. Plant Physiol. 162:755–68 [Google Scholar]
  119. Rosas U, Cibrian-Jaramillo A, Ristova D, Banta JA, Gifford ML. 119.  et al. 2013. Integration of responses within and across Arabidopsis natural accessions uncovers loci controlling root systems architecture. PNAS 110:15133–38 [Google Scholar]
  120. Rosquete MR, von Wangenheim D, Marhavý P, Barbez E, Stelzer EHK. 120.  et al. 2013. An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr. Biol. 23:817–22 [Google Scholar]
  121. Rost TL. 121.  2011. The organization of roots of dicotyledonous plants and the positions of control points. Ann. Bot. 107:1213–22 [Google Scholar]
  122. Ruffel S, Krouk G, Ristova D, Shasha D, Birnbaum KD, Coruzzi GM. 122.  2011. Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply versus demand. PNAS 108:18524–29 [Google Scholar]
  123. Saengwilai P, Nord EA, Chimungu JG, Brown KM, Lynch JP. 123.  2014. Root cortical aerenchyma enhances nitrogen acquisition from low-nitrogen soils in maize. Plant Physiol. 166:726–35 [Google Scholar]
  124. Schroeder N, Lazarovitch N, Vanderborght J, Vereecken H, Javaux M. 124.  2013. Linking transpiration reduction to rhizosphere salinity using a 3D coupled soil-plant model. Plant Soil 377:277–93 [Google Scholar]
  125. Sieber T, Grünig C. 125.  2013. Fungal root endophytes. Plant Roots: The Hidden Half A Eshel, T Beeckman 38–149 New York: CRC, 4th ed.. [Google Scholar]
  126. Šimůnek J, Hopmans JW. 126.  2009. Modeling compensated root water and nutrient uptake. Ecol. Model. 220:505–21 [Google Scholar]
  127. Singh P, Mohanta TK, Sinha AK. 127.  2015. Unraveling the intricate nexus of molecular mechanisms governing rice root development: OsMPK3/6 and auxin-cytokinin interplay. PLOS ONE 10:e0123620 [Google Scholar]
  128. Svistoonoff S, Creff A, Reymond M, Sigoillot-Claude C, Ricaud L. 128.  et al. 2007. Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39:792–96 [Google Scholar]
  129. Symonova O, Topp CN, Edelsbrunner H. 129.  2015. DynamicRoots: a software platform for the reconstruction and analysis of growing plant roots. PLOS ONE 10:e0127657 [Google Scholar]
  130. Tabata R, Sumida K, Yoshii T, Ohyama K, Shinohara H, Matsubayashi Y. 130.  2014. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science 346:343–46 [Google Scholar]
  131. Tian H, De Smet I, Ding Z. 131.  2014. Shaping a root system: regulating lateral versus primary root growth. Trends Plant Sci. 19:426–31 [Google Scholar]
  132. Topp CN, Iyer-Pascuzzi AS, Anderson JT, Lee CR, Zurek PR. 132.  et al. 2013. 3D phenotyping and quantitative trait locus mapping identify core regions of the rice genome controlling root architecture. PNAS 110:E1695–704 [Google Scholar]
  133. Tracy SR, Black CR, Roberts JA, Sturrock C, Mairhofer S. 133.  et al. 2012. Quantifying the impact of soil compaction on root system architecture in tomato (Solanum lycopersicum) by X-ray micro-computed tomography. Ann. Bot. 110:511–19 [Google Scholar]
  134. Tracy SR, Daly KR, Sturrock CJ, Crout NMJ, Mooney SJ, Roose T. 134.  2015. Three-dimensional quantification of soil hydraulic properties using X-ray Computed Tomography and image-based modeling. Water Resour. Res. 51:1006–22 [Google Scholar]
  135. Tyree MT, Sperry JS. 135.  1989. Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40:19–36 [Google Scholar]
  136. Uga Y, Sugimoto K, Ogawa S, Rane J, Ishitani M. 136.  et al. 2013. Control of root system architecture by DEEPER ROOTING 1 increases rice yield under drought conditions. Nat. Genet. 45:1097–102 [Google Scholar]
  137. Van Norman JM, Xuan W, Beeckman T, Benfey PN. 137.  2013. To branch or not to branch: the role of pre-patterning in lateral root formation. Development 140:4301–10 [Google Scholar]
  138. Verslues PE, Agarwal M, Katiyar-Agarwal S, Zhu J, Zhu JK. 138.  2006. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J. 45:523–39 [Google Scholar]
  139. Walker TS, Bais HP, Grotewold E, Vivanco JM. 139.  2003. Root exudation and rhizosphere biology. Plant Physiol. 132:44–51 [Google Scholar]
  140. Wang Z, Ruan W, Shi J, Zhang L, Xiang D. 140.  et al. 2014. Rice SPX1 and SPX2 inhibit phosphate starvation responses through interacting with PHR2 in a phosphate-dependent manner. PNAS 111:14953–58 [Google Scholar]
  141. Ward JT, Lahner B, Yakubova E, Salt DE, Raghothama KG. 141.  2008. The effect of iron on the primary root elongation of Arabidopsis during phosphate deficiency. Plant Physiol. 147:1181–91 [Google Scholar]
  142. Watt M, McCully M, Canny M. 142.  1994. Formation and stabilization of rhizosheaths of Zea mays L. Plant Physiol. 106:179–86 [Google Scholar]
  143. Yan F, Zhu Y, Müller C, Zörb C, Schubert S. 143.  2002. Adaptation of H+-pumping and plasma membrane H+ ATPase activity in proteoid roots of white lupin under phosphate deficiency. Plant Physiol. 129:50–63 [Google Scholar]
  144. York LM, Nord EA, Lynch JP. 144.  2013. Integration of root phenes for soil resource acquisition. Front. Funct. Plant Ecol. 4:355 [Google Scholar]
  145. Yu J, Li Y, Han G, Zhou D, Fu Y. 145.  et al. 2013. The spatial distribution characteristics of soil salinity in coastal zone of the Yellow River Delta. Environ. Earth Sci. 72:589–99 [Google Scholar]
  146. Zurek PR, Topp CN, Benfey PN. 146.  2015. Quantitative trait locus mapping reveals regions of the maize genome controlling root system architecture. Plant Physiol. 167:1487–96 [Google Scholar]
/content/journals/10.1146/annurev-arplant-043015-111848
Loading
Environmental Control of Root System Biology
Annual Review of Plant Biology 67, 619 (2016); https://doi.org/10.1146/annurev-arplant-043015-111848
/content/journals/10.1146/annurev-arplant-043015-111848
/content/journals/10.1146/annurev-arplant-043015-111848
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error