11 Effect of Nutrient Availability on Root System Development
Alfredo Cruz-Ramírez
Nacional Laboratory of Genomics for Biodiversity, CINVESTAV Campus Guanajuato, Km. 9.6 Carretera Irapuato-León Z.C. 36500, Irapuato, Guanajuato, México
Search for more papers by this authorCarlos Calderón-Vázquez
Nacional Laboratory of Genomics for Biodiversity, CINVESTAV Campus Guanajuato, Km. 9.6 Carretera Irapuato-León Z.C. 36500, Irapuato, Guanajuato, México
Search for more papers by this authorLuis Herrera-Estrella
Nacional Laboratory of Genomics for Biodiversity, CINVESTAV Campus Guanajuato, Km. 9.6 Carretera Irapuato-León Z.C. 36500, Irapuato, Guanajuato, México
Search for more papers by this authorAlfredo Cruz-Ramírez
Nacional Laboratory of Genomics for Biodiversity, CINVESTAV Campus Guanajuato, Km. 9.6 Carretera Irapuato-León Z.C. 36500, Irapuato, Guanajuato, México
Search for more papers by this authorCarlos Calderón-Vázquez
Nacional Laboratory of Genomics for Biodiversity, CINVESTAV Campus Guanajuato, Km. 9.6 Carretera Irapuato-León Z.C. 36500, Irapuato, Guanajuato, México
Search for more papers by this authorLuis Herrera-Estrella
Nacional Laboratory of Genomics for Biodiversity, CINVESTAV Campus Guanajuato, Km. 9.6 Carretera Irapuato-León Z.C. 36500, Irapuato, Guanajuato, México
Search for more papers by this authorAbstract
Modern-day plant root systems have been modeled from distinct ancestors and by different evolutionary pathways influenced by environmental cues, leading to varied root system architectures. Availability of mineral nutrients has played a major role in evolution and development of the diverse root system architectures. In this chapter, we review the importance of the study of mineral nutrition on root development and describe the physiological, morphological and molecular responses of plant roots to diverse nutrient deficiencies and how the different hormone signaling pathways participate in these responses.
References
- Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C. et al. (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 119, 109–120.
- Allen, E., Xie, Z., Gustafson, A.M. and Carrington, J.C. (2005). microRNA-directed phasing during trans-acting siRNA biogenesis in plants. Cell 121, 207–221.
- Arahou, M. and Diem, H.G. (1997). Iron deficiency induces cluster (proteoid) root formation in Casuarina glauca . Plant Soil 196, 71–79.
- Armengaud, P., Breitling, R. and Amtmann, A. (2004). The potassium-dependent transcriptome of Arabidopsis reveals a prominent role of jasmonic acid in nutrient signaling. Plant Physiol. 136, 2556–2576.
- Ashley, M.K., Grant, M. and Grabov, A. (2006). Plant responses to potassium deficiencies: a role for potassium transport proteins. J. Exp. Bot. 57, 425–436.
- Aung, K., Lin, S.-I., Wu, C.-C., Huang, Y.-T., Su, C.-l. and Chiou, T.-J. (2006). pho2, a phosphate overaccumulator, is caused by a nonsense mutation in a microRNA399 target gene. Plant Physiol. 141, 1000–1011.
- Bar-Yosef, B. (1971). Fluxes of P and Ca into intact corn roots and their dependence on solution concentration and root age. Plant Soil 35, 589–600.
- Bari, R., Pant, B.-D., Stitt, M. and Scheible, W.-R. (2006). PHO2, microRNA399, and PHR1 define a phosphate-signaling pathway in plants. Plant Physiol. 141, 988–999.
- Bariola, P.A., Howard, C.J., Taylor, C.B., Verburg, M.T., Jaglan, V.D. and Green, P.J. (1994). The Arabidopsis ribonuclease gene RNS1 is tightly controlled in response to phosphate limitation. Plant J. 6, 673–685.
- Barker, S.J. and Tagu, D. (2000). The roles of auxins and cytokinins in mycorrhizal symbioses. J. Plant Growth Regul. 19, 144–154.
- Bates, T.R. and Lynch, J.P. (1996). Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell Environ. 19, 529–538.
- Bernhardt, C., Lee, M.M., Gonzalez, A., Zhang, F., Lloyd, A. and Schiefelbein, J. (2003). The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 130, 6431–6439.
- Bienfait, H.F., de Weger, L.A. and Kramer, D. (1987). Control of the development of iron-efficiency reactions in potato as a response to iron deficiency is located in the roots. Plant Physiol. 83, 244–247.
- Blilou, I., Xu, J., Wildwater, M., Willemsen, V., Paponov, I., Friml, J. et al. (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 433, 39–44.
- Bloom, A.J., Jackson, L.E. and Smart, D.R. (1993). Root growth as a function of ammonium and nitrate in the root zone. Plant Cell Environ. 16, 199–206.
- Bloom, A.J., Meyerhoff, P.A., Taylor, A.R. and Rost, T.L. (2003). Root development and absorption of ammonium and nitrate from the rhizosphere. J. Plant Growth Regul. 21, 416–431.
- Boot, R.G.A. and Mensink, M. (1990). Size and morphology of root systems of perennial grasses from contrasting habitats as affected by nitrogen supply. Plant Soil 129, 291–299.
- Buchner, P., Stuiver, C.E.E., Westerman, S., Wirtz, M., Hell, R., Hawkesford, M.J. et al. (2004). Regulation of sulfate uptake and expression of sulfate transporter genes in Brassica oleracea is affected by atmospheric H2S and pedospheric sulfate nutrition. Plant Physiol. 136, 3396–3408.
- Casimiro, I., Beeckman, T., Graham, N., Bhalerao, R., Zhang, H., Casero, P. et al. (2003). Dissecting Arabidopsis lateral root development. Trends Plant Sci. 8, 165–171.
- Casimiro, I., Marchant, A., Bhalerao, R.P., Beeckman, T., Dhooge, S., Swarup, R. et al. (2001). Auxin transport promotes Arabidopsis lateral root initiation. Plant Cell 13, 843–852.
- Colangelo, E.P. and Guerinot, M.L. (2004). The essential basic helix-loop-helix protein FIT1 is required for the iron deficiency response. Plant Cell 16, 3400–3412.
- Connolly, E.L., Fett, J.P. and Guerinot, M.L. (2002). Expression of the IRT1 metal transporter is controlled by metals at the levels of transcript and protein accumulation. Plant Cell 14, 1347–1357.
- Cooper, R.B., Blaser, R.E. and Brown, R.H. (1967). Potassium nutrition effects on net photosynthesis and morphology of alfalfa. Soil Sci. Soc. Am. J. 31, 231–235.
- Cruz-Ramírez, A., López-Bucio, J., Ramírez-Pimentel, G., Zurita-Silva, A., Sánchez-Calderon, L., Ramírez-Chávez, E. et al. (2004). The xipotl mutant of Arabidopsis reveals a critical role for phospholipid metabolism in root system development and epidermal cell integrity. Plant Cell 16, 2020–2034.
- Cruz-Ramírez, A., Oropeza-Aburto, A., Razo-Hernández, F., Ramírez-Chávez, E., and Herrera-Estrella, L. (2006). Phospholipase DZ2 plays an important role in extraplastidic galactolipid biosynthesis and phosphate recycling in Arabidopsis roots. Proc. Natl. Acad. Sci. U. S. A. 103, 6765–6770.
- Curie, C., Panaviene, Z., Loulergue, C., Dellaporta, S.L., Briat, J.-F. and Walker, E.L. (2001). Maize yellow stripe1 encodes a membrane protein directly involved in Fe(III) uptake. Nature 409, 346–349.
- de Groot, C.C., van den Boogaard, R., Marcelis, L.F.M., Harbinson, J. and Lambers, H. (2003). Contrasting effects of N and P deprivation on the regulation of photosynthesis in tomato plants in relation to feedback limitation. J. Exp. Bot. 54, 1957–1967.
- Desbrosses, G., Josefsson, C., Rigas, S., Hatzopoulos, P. and Dolan, L. (2003). AKT1 and TRH1 are required during root hair elongation in Arabidopsis . J. Exp. Bot. 54, 781–788.
- Drew, M.C. and Saker, L.R. (1975). Nutrient supply and the growth of the seminal root system in barley. II. Localized, compensatory increases in lateral root growth and rates of nitrate uptake when nitrate supply is restricted to only part of the root system. J. Exp. Bot. 26, 79–90.
- Drew, M.C., Saker, L.R. and Ashley, T.W. (1973). Nutrient supply and the growth of seminal root system in barley. I. The effect of nitrate concentration on the growth of axes and laterals. J. Exp. Bot. 24, 1189–1202.
- Dubrovsky, J.G. (1997). Determinate primary-root growth in seedlings of Sonoran Desert Cactaceae; its organization, cellular basis, and ecological significance. Planta 203, 85–92.
- Duff, S.M.G., Moorhead, G.B.G., Lefebvre, D.D. and Plaxton, W.C. (1989). Phosphate starvation inducible ‘Bypasses’ of adenylate and phosphate dependent glycolytic enzymes in Brassica nigra suspension cells. Plant Physiol. 90, 1275–1278.
- Dunbabin, V., Rengel, Z. and Diggle, A. (2001). The root growth response to heterogeneous nitrate supply differs for Lupinus angustifolius and Lupinus pilosus . Aust. J. Agric. Res. 52, 495–503.
- Eide, D., Broderius, M., Fett, J. and Guerinot, M.L. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. U. S. A. 93, 5624–5628.
- Epstein, E. and Hagen, C.E. (1952). A kinetic study of the absorption of alkali cations by barley roots. Plant Physiol. 27, 457–474.
- Essigmann, B., Güler, S., Narang, R.A., Linke, D. and Benning, C. (1998). Phosphate availability affects the thylakoid lipid composition and the expression of SQD1, a gene required for sulfolipid biosynthesis in Arabidopsis thaliana . Proc. Natl. Acad. Sci. U. S. A. 95, 1950–1955.
- Evans, J.R. and Poorter, H. (2001). Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ. 24, 755–767.
- Farley, R.A. and Fitter, A.H. (1999). The responses of seven co-occurring woodland herbaceous perennials to localized nutrient-rich patches. J. Ecol. 87, 849–859.
- Filleur, S., Walch-Liu, P., Gan, Y. and Forde, B.G. (2005). Nitrate and glutamate sensing by plant roots. Biochem. Soc. Trans. 33, 283–286.
- Foehse, D. and Jungk, A. (1983). Influence of phosphate and nitrate supply on root hair formation of rape, spinach and tomato plants. Plant Soil 74, 359–368.
- Forde, B. and Lorenzo, H. (2001). The nutritional control of root development. Plant Soil 232, 51–68.
- Franco-Zorrilla, J.M., Valli, A., Todesco, M., Mateos, I., Puga, M.I., Rubio-Somoza, I. et al. (2007). Target mimicry provides a new mechanism for regulation of microRNA activity. Nat. Genet. 39 (8), 1033–1037.
- Friend, A.L., Eide, M.R. and Hinckley, T.M. (1990). Nitrogen stress alters root proliferation in Douglas-fir seedlings. Can. J. For. Res. 20, 1524–1529.
- Fujii, H., Chiou, T.-J., Lin, S.-I., Aung, K. and Zhu, J.-K. (2005). A miRNA involved in phosphate-starvation response in Arabidopsis . Curr. Biol. 15, 2038–2043.
- Fukaki, H., Nakao, Y., Okushima, Y., Theologis, A. and Tasaka, M. (2005). Tissue-specific expression of stabilized SOLITARY-ROOT/IAA14 alters lateral root development in Arabidopsis . Plant J. 44, 382–395.
- Gan, Y., Filleur, S., Rahman, A., Gotensparre, S. and Forde, B.G. (2005). Nutritional regulation of ANR1 and other root-expressed MADS-box genes in Arabidopsis thaliana . Planta 222, 730–742.
- Gastal, F. and Lemaire, G. (2002). N uptake and distribution in crops: an agronomical and ecophysiological perspective. J. Exp. Bot. 53, 789–799.
- Gensel, P.G. and Edwards, D. (2001). Plants Invade the Land. New York, Columbia University Press, 304 pp.
- Goldbach, E., Goldbach, H., Wagner, H. and Michael, G. (1975). Influence of N-deficiency on the abscisic acid content of sunflower plant. Physiol. Plant. 34, 138–140.
- Granato, T.C. and Raper, C.D., Jr. (1989). Proliferation of maize (Zea maize L.) roots in response to localized supply of nitrate. J. Exp. Bot. 40, 263–275.
- Guo, F.-Q., Wang, R., Chen, M. and Crawford, N.M. (2001). The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is activated and functions in nascent organ development during vegetative and reproductive growth. Plant Cell 13, 1761–1777.
- Guo, F.-Q., Wang, R. and Crawford, N.M. (2002). The Arabidopsis dual-affinity nitrate transporter gene AtNRT1.1 (CHL1) is regulated by auxin in both shoots and roots. J. Exp. Bot. 53, 835–844.
- Hawker, J.S., Marschner, H. and Downton, W.J.S. (1974). Effects of sodium and potassium on starch synthesis in leaves. Aust. J. Plant Physiol. 1, 491–501.
- He, Y., Liao, H. and Yan, X. (2003). Localized supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil 248, 247–256.
- Heldt, H.W., Chon, C.J., Maronde, D., Herold, A., Stankovic, Z.S., Walker, D.A. et al. (1977). Role of orthophosphate and other factors in the regulation of starch formation in leaves and isolated chloroplasts. Plant Physiol. 59, 1146–1155.
- Hemsley, A.R. and Poole, I. (2004). The Evolution of Plant Physiology (Linnean Society Symposium Series No. 21). Amsterdam, Elsevier Academic Press.
- Himanen, K., Boucheron, E., Vanneste, S., de Almeida Engler, J., Inzé, D. and Beeckman, T. (2002). Auxin-mediated cell cycle activation during early lateral root initiation. Plant Cell 14, 2339–2351.
- Hirai, M.Y., Fujiwara, T., Awazuhara, M., Kimura, T., Noji, M. and Saito, K. (2003). Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J. 33, 651–663.
- Hochholdinger, F., Guo, L. and Schnable, P.S. (2004). Lateral roots affect the proteome of the primary root of maize (Zea mays L.). Plant Mol. Biol. 56, 397–412.
- Hodge, A. (2004). The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytol. 162, 9–24.
- Huang, G., Yi, K.K., Wu, Y.R., Zhu, L., Mao, C.Z. and Wu, P. (2004). QTLs for nitrate induced elongation and initiation of lateral roots in rice (Oryza sativa L.). Plant Soil 263, 229–237.
- Johnson, J.F., Vance, C.P. and Allan, D.L. (1996). Phosphorus deficiency in Lupinus albus. Altered lateral root development and enhanced expression of phosphoenolpyruvate carboxylase. Plant Physiol. 112, 31–41.
- Jones, M.A., Raymond, M.J. and Smirnoff, N. (2006). Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis . Plant J. 45, 83–100.
- Jones-Rhoades, M.W. and Bartel, D.P. (2004). Computational identification of plant microRNAs and their targets, including a stress-induced miRNA. Mol. Cell 14, 787–799.
- Jungk, A. (2001). Root hairs and the acquisition of plant nutrients from soil. J. Plant Nutr. Soil Sci. 164, 121–129.
- Karmoker, J.L., Clarkson, D.T., Saker, L.R., Rooney, J.M. and Purves, J.V. (1991). Sulphate deprivation depresses the transport of nitrogen to the xylem and the hydraulic conductivity of barley (Hordeum vulgare L.) roots. Planta 185, 269–278.
- Kataoka, T., Hayashi, N., Yamaya, T. and Takahashi, H. (2004). Root-to-shoot transport of sulfate in Arabidopsis. Evidence for a role of SULTR3;5 as a component of low-affinity sulfate transport system in the root vasculature. Plant Physiol. 136, 4198–4204.
- Kutz, A., Müller, A., Hennig, P., Kaiser, W.M., Piotrowski, M. and Weiler, E.W. (2002). A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana . Plant J. 30, 95–106.
- Lappartient, A.G., Vidmar, J.J., Leustek, T., Glass, A.D.M. and Touraine, B. (1999). Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. Plant J. 18, 89–95.
- Lauter, F.-R., Ninnemann, O., Bucher, M., Riesmeier, J.W. and Frommer, W.B. (1996). Preferential expression of an ammonium transporter and of two putative nitrate transporters in root hairs of tomato. Proc. Natl. Acad. Sci. U. S. A. 93, 8139–8144.
- Leigh, R.A. and Wyn Jones, R.G. (1984). A hypothesis relating critical potassium concentrations for growth to the distribution and functions of this ion in the plant cell. New Phytol. 97, 1–13.
- Li, M., Qin, C., Welti, R. and Wang, X. (2006). Double knockouts of phospholipases Dζ1 and Dζ2 in Arabidopsis affect root elongation during phosphate-limited growth but do not affect root hair patterning. Plant Physiol. 140, 761–770.
- Lin, S.-I., Chiang, S.-F., Lin, W.-Y., Chen, J.-W., Tseng, C.-Y., Wu, P.-C. et al. (2008). Regulatory network of microRNA399 and PHO2 by systemic signaling. Plant Physiol. 147, 732–746.
- Ling, H.-Q., Bauer, P., Bereczky, Z., Keller, B. and Ganal, M. (2002). The tomato fer gene encoding a bHLH protein controls iron-uptake responses in roots. Proc. Natl. Acad. Sci. U. S. A. 99, 13938–13943.
- Linkohr, B.I., Williamson, L.C., Fitter, A.H. and Leyser, H.M.O. (2002). Nitrate and phosphate availability and distribution have different effects on root system architecture of Arabidopsis . Plant J. 29, 751–760.
- Little, D.Y., Rao, H., Oliva, S., Daniel-Vedele, F., Krapp, A. and Malamy, J.E. (2005). The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues. Proc. Natl. Acad. Sci. U. S. A. 102, 13693–13698.
- López-Bucio, J., Cruz-Ramírez, A. and Herrera-Estrella, L. (2003). The role of nutrient availability in regulating root architecture. Curr. Opin. Plant Biol. 6, 280–287.
- López-Bucio, J., Hernández-Abreu, E., Sánchez-Calderón, L., Nieto-Jacobo, M.F., Simpson, J. and Herrera-Estrella, L. (2002). Phosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system. Plant Physiol. 129, 244–256.
- Lynch, J. (1995). Root architecture and plant productivity. Plant Physiol. 109, 7–13.
- Lynch, J.P. and Brown, K.M. (2001). Topsoil foraging – an architectural adaptation of plants to low phosphorus availability. Plant Soil 237, 225–237.
- Ma, Z., Bielenberg, D.G., Brown, K.M. and Lynch, J.P. (2001). Regulation of root hair density by phosphorus availability in Arabidopsis thaliana . Plant Cell Environ. 24, 459–467.
- Maathuis, F.J.M. and Sanders, D. (1997). Regulation of K+ absorption in plant root cells by external K+: interplay of different plasma membrane K+ transporters. J. Exp. Bot. 48 (Special issue), 451–458.
- Malamy, J.E. (2005). Intrinsic and environmental response pathways that regulate root system architecture. Plant Cell Environ. 28, 67–77.
- Malamy, J.E. and Ryan, K.S. (2001). Environmental regulation of lateral root initiation in Arabidopsis . Plant Physiol. 127, 899–909.
- Maruyama-Nakashita, A., Inoue, E., Watanabe-Takahashi, A., Yamaya, T. and Takahashi, H. (2003). Transcriptome profiling of sulfur-responsive genes in Arabidopsis reveals global effects of sulfur nutrition on multiple metabolic pathways. Plant Physiol. 132, 597–605.
- Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T. and Takahashi, H. (2004a). A novel regulatory pathway of sulfate uptake in Arabidopsis roots: implication of CRE1/WOL/AHK4-mediated cytokinin-dependent regulation. Plant J. 38, 779–789.
- Maruyama-Nakashita, A., Nakamura, Y., Yamaya, T. and Takahashi, H. (2004b). Regulation of high-affinity sulphate transporters in plants: towards systematic analysis of sulphur signalling and regulation. J. Exp. Bot. 55, 1843–1849.
- Masucci, J.D., Rerie, W.G., Foreman, D.R., Zhang, M., Galway, M.E., Marks, M.D. et al. (1996). The homeobox gene GLABRA 2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana . Development 122, 1253–1260.
- Miller, A.J., Fan, X., Shen, Q. and Smith, S.J. (2008). Amino acids and nitrate as signals for the regulation of nitrogen acquisition. J. Exp. Bot. 59(1), 111–119.
- Misson, J., Raghothama, K.G., Jain, A., Jouhet, J., Block, M.A., Bligny, R. et al. (2005). A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl. Acad. Sci. U. S. A. 102, 11934–11939.
- Miura, K., Rus, A., Sharkhuu, A., Yokoi, S., Karthikeyan, A.S., Raghothama, K.G. et al. (2005). The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc. Natl. Acad. Sci. U. S. A. 102, 7760–7765.
- Müller, M. and Schmidt, W. (2004). Environmentally induced plasticity of root hair development in Arabidopsis . Plant Physiol. 134, 409–419.
- Nacry, P., Canivenc, G., Muller, B., Azmi, A., Van Onckelen, H., Rossignol, M. et al. (2005). A role for auxin redistribution in the responses of the root system architecture to phosphate starvation in Arabidopsis . Plant Physiol. 138, 2061–2074.
- Nakajima, K. and Benfey, P.N. (2002). Signaling in and out: control of cell division and differentiation in the shoot and root. Plant Cell 14 (Suppl), S265–S276.
- Neumann, G. and Martinoia, E. (2002). Cluster roots – an underground adaptation for survival in extreme environments. Trends Plant Sci. 7, 162–167.
- Nikiforova, V., Freitag, J., Kempa, S., Adamik, M., Hesse, H. and Hoefgen, R. (2003). Transcriptome analysis of sulfur depletion in Arabidopsis thaliana: interlacing of biosynthetic pathways provides response specificity. Plant J. 33, 633–650.
- Ohashi, Y., Oka, A., Rodrigues-Pousada, R., Possenti, M., Ruberti, I., Morelli, G. et al. (2003). Modulation of phospholipid signaling by GLABRA2 in root-hair pattern formation. Science 300, 1427–1430.
- Owen, A.G. and Jones, D.L. (2001). Competition for amino acids between wheat roots and rhizosphere microorganisms and the role of amino acids in plant N acquisition. Soil Biol. Biochem. 33, 651–657.
- Pant, B.D., Buhtz, A., Kehrand, J. and Scheible, W.-R. (2008). MicroRNA399 is a long-distance signal for the regulation of plant phosphate homeostasis. Plant J. 53, 731–738.
- Penazzio, S. (2005). Mineral nutrition of plants: a short history of plant physiology. Riv. Biol. 98, 215–236.
- Perry, P., Linke, B. and Schmidt, W. (2007). Reprogramming of root epidermal cells in response to nutrient deficiency. Biochem. Soc. Trans. 35, 161–163.
- Rae, A.L. and Smith, F.W. (2002). Localisation of expression of a high-affinity sulfate transporter in barley roots. Planta 215, 565–568.
- Raghothama, K.G. (1999). Phosphate acquisition. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 665–693.
- Raven, J.A. and Edwards, D. (2001). Roots: evolutionary origins and biogeochemical significance. J. Exp. Bot. 52, 381–401.
- Remans, T., Nacry, P., Pervent, M., Girin, T., Tillard, P., Lepetit, M. et al. (2006). A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis . Plant Physiol. 140, 909–921.
- Rennenberg, H., Schmitz, K. and Bergmann, L. (1979). Long-distance transport of sulfur in Nicotiana tabacum . Planta 147, 57–62.
- Rigas, S., Debrosses, G., Haralampidis, K., Vicente-Agullo, F., Feldmann, K.A., Grabov, A. et al. (2001). TRH1 encodes a potassium transporter required for tip growth in Arabidopsis root hairs. Plant Cell 13, 139–151.
- Riley, D. and Barber, S.A. (1971). Effect of ammonium and nitrate fertilization on phosphorus uptake as related to root-induced pH changes at the root-soil interface. Soil Sci. Soc. Am. J. 35, 301–306.
- Robinson, D. and Rorison, I.H. (1987). Root hairs and plant growth at low nitrogen availabilities. New Phytol. 107, 681–693.
- Robinson, N.J., Procter, C.M., Connolly, E.L. and Guerinot, M.L. (1999). A ferric-chelate reductase for iron uptake from soils. Nature 397, 694–697.
- Rodríguez-Rodríguez, J.F., Shishkova, S., Napsucialy-Mendivil, S. and Dubrovsky, J.G. (2003). Apical meristem organization and lack of establishment of the quiescent center in Cactaceae roots with determinate growth. Planta 217, 849–857.
- Rook, F., Hadingham, S.A., Li, Y. and Bevan, M.W. (2006). Sugar and ABA response pathways and the control of gene expression. Plant Cell Environ. 29, 426–434.
- Rubio, V., Linhares, F., Solano, R., Martín, A.C., Iglesias, J., Leyva, A. et al. (2001). A conserved MYB transcription factor involved in phosphate starvation signaling both in vascular plants and in unicellular algae. Genes Dev. 15, 2122–2133.
- Sabatini, S., Beis, D., Wolkenfelt, H., Murfett, J., Guilfoyle, T., Malamy, J. et al. (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell 99, 463–472.
- Saltini, A. (1984). Storia delle Scienze Agrarie. Vol. 1: Dalle Origini al Rinascimento. Bologna, Edagricole.
- Samuelson, M.E., Eliasson, L. and Larsson, C.-M. (1992). Nitrate-regulated growth and cytokinin responses in seminal roots of barley. Plant Physiol. 98, 309–315.
- Sánchez-Calderón, L., López-Bucio, J., Chacón-López, A., Cruz-Ramírez, A., Nieto-Jacobo, F., Dubrovsky, J.G. et al. (2005). Phosphate starvation induces a determinate developmental program in the roots of Arabidopsis thaliana . Plant Cell Physiol. 46, 174–184.
- Sattelmacher, B., Gerendas, J., Thoms, K., Brück, H. and Bagdady, N.H. (1993). Interaction between root growth and mineral nutrition. Environ. Exp. Bot. 33, 63–73.
- Satter, R.L. and Galston, A.W. (1971). Phytochrome-controlled nyctinasty in Albizzia julibrissin. III. Interactions between an endogenous rhythm and phytochrome in control of potassium flux and leaflet movement. Plant Physiol. 48, 740–746.
- Scheible, W.-R., González-Fontes, A., Lauerer, M., Müller-Röber, B., Caboche, M. and Stitt, M. (1997). Nitrate acts as a signal to induce organic acid metabolism and repress starch metabolism in tobacco. Plant Cell 9, 783–798.
- Schiefelbein, J. (2003). Cell-fate specification in the epidermis: a common patterning mechanism in the root and shoot. Curr. Opin. Plant Biol. 6, 74–78.
- Schikora, A. and Schmidt, W. (2001). Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability. Plant Physiol. 125, 1679–1687.
- Schmidt, W. and Schikora, A. (2001). Different pathways are involved in phosphate and iron stress-induced alterations of root epidermal cell development. Plant Physiol. 125, 2078–2084.
- Shin, R., Berg, R.H. and Schachtman, D.P. (2005). Reactive oxygen species and root hairs in Arabidopsis root response to nitrogen, phosphorus and potassium deficiency. Plant Cell Physiol. 46, 1350–1357.
- Shin, R. and Schachtman, D.P. (2004). Hydrogen peroxide mediates plant root cell response to nutrient deprivation. Proc. Natl. Acad. Sci. U. S. A. 101, 8827–8832.
- Shishkova, S., Rost, T.L. and Dubrovsky, J.G. (2008). Determinate root growth and meristem maintenance in angiosperms. Ann. Bot. 101, 319–340.
- Signora, L., De Smet, I., Foyer, C.H. and Zhang, H. (2001). ABA plays a central role in mediating the regulatory effects of nitrate on root branching in Arabidopsis . Plant J. 28, 655–662.
- Skene, K.R., Kierans, M., Sprent, J.I. and Raven, J.A. (1996). Structural aspects of cluster root development and their possible significance for nutrient acquisition in Grevillea robusta (Proteaceae). Ann. Bot. 77, 443–451.
- Sorgonà, A., Abenavoli, M.R. and Cacco, G. (2005). A comparative study between two citrus rootstocks: effect of nitrate on the root morpho-topology and net nitrate uptake. Plant Soil 270, 257–267.
- Stitt, M. and Feil, R. (1999). Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: consequences for the regulation of biomass partitioning between shoots and root. Plant Soil 215, 143–153.
- Thimm, O., Essigmann, B., Kloska, S., Altmann, T. and Buckhout, T.J. (2001). Response of Arabidopsis to iron deficiency stress as revealed by microarray analysis. Plant Physiol. 127, 1030–1043.
- Tian, Q., Chen, F., Zhang, F. and Mi, G. (2005). Possible involvement of cytokinin in nitrate-mediated root growth in maize. Plant Soil 277, 185–196.
- Tranbarger, T.J., Al-Ghazi, Y., Muller, B., Teyssendier de la Serve, B., Doumas, P. and Touraine, B. (2003). Transcription factor genes with expression correlated to nitrate-related root plasticity of Arabidopsis thaliana . Plant Cell Environ. 26, 459–469.
- Trolldenier, G. (1977). Mineral nutrition and reduction processes in the rhizosphere of rice. Plant Soil 47, 193–202.
- Vange, M.S., Holmern, K. and Nissen, P. (1974). Multiphasic uptake of sulfate by barley roots. I. Effects of analogues, phosphate, and pH. Physiol. Plant. 31, 291–301.
- Veit, B. (2004). Determination of cell fate in apical meristems. Curr. Opin. Plant Biol. 7, 57–64.
- Vert, G., Grotz, N., Dédaldéchamp, F., Gaymard, F., Guerinot, M.L., Briat, J.-F. et al. (2002). IRT1, an Arabidopsis transporter essential for iron uptake from the soil and for plant growth. Plant Cell 14, 1223–1233.
- Vert, G.A., Briat, J.-F. and Curie, C. (2003). Dual regulation of the Arabidopsis high-affinity root iron uptake system by local and long-distance signals. Plant Physiol. 132, 796–804.
- Véry, A.-A. and Sentenac, H. (2003). Molecular mechanisms and regulation of K+ transport in higher plants. Annu. Rev. Plant Biol. 54, 575–603.
- Vicente-Agullo, F., Rigas, S., Desbrosses, G., Dolan, L., Hatzopoulos, P. and Grabov, A. (2004). Potassium carrier TRH1 is required for auxin transport in Arabidopsis roots. Plant J. 40, 523–535.
- Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K. et al. (2002). Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development 129, 5409–5419.
- Wada, T., Tachibana, T., Shimura, Y. and Okada, K. (1997). Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC . Science 277, 1113–1116.
- Walch-Liu, P., Ivanov, I.I., Filleur, S., Gan, Y., Remans, T. and Forde, B.G. (2006). Nitrogen regulation of root branching. Ann. Bot. 97, 875–881.
- Wang, X. (2004). Lipid signaling. Curr. Opin. Plant Biol. 7, 329–336.
- Williamson, L.C., Ribrioux, S.P.C.P., Fitter, A.H. and Leyser, H.M.O. (2001). Phosphate availability regulates root system architecture in Arabidopsis . Plant Physiol. 126, 875–882.
- Wilson, A.K., Pickett, F.B., Turner, J.C. and Estelle, M. (1990). A dominant mutation in Arabidopsis confers resistance to auxin, ethylene and abscisic acid. Mol. Gen. Genet. 222, 377–383.
- Wu, C., Fan, Z. and Wang, Z. (2004). Effect of phosphorus stress on chlorophyll biosynthesis, photosynthesis and biomass partitioning pattern of Fraxinus mandchurica seedlings. Ying Yong Sheng Tai Xue Bao 15, 935–940 (in Chinese).
- Yoshimoto, N., Takahashi, H., Smith, F.W., Yamaya, T. and Saito, K. (2002). Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. Plant J. 29, 465–473.
- Zhang, H. and Forde, B.G. (1998). An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279, 407–409.
- Zhang, H. and Forde, B.G. (2000). Regulation of Arabidopsis root development by nitrate availability. J. Exp. Bot. 51, 51–59.
- Zhang, H., Jennings, A., Barlow, P.W. and Forde, B.G. (1999). Dual pathways for regulation of root branching by nitrate. Proc. Natl. Acad. Sci. U. S. A. 96, 6529–6534.
- Zhang, Y.-J., Lynch, J.P. and Brown, K.M. (2003). Ethylene and phosphorus availability have interacting yet distinct effects on root hair development. J. Exp. Bot. 54, 2351–2361.
Browse other articles of this reference work: