Strategies for optimization of mineral nutrient transport in plants: Multilevel regulation of nutrient-dependent dynamics of root architecture and transporter activity

Plant and Cell Physiology

Volumn 55, Issue 12, 2014, Pages 2027-2036

  Aibara, Izumi ^a   Miwa, Kyoko ^a,b  

^a HOKKAIDO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Arabidopsis thaliana; Essential element; Gene expression; Nutrient dependent; Root architecture; Transporter

Indexed keywords

ARABIDOPSIS THALIANA;

CARRIER PROTEIN; MINERAL; SOIL; VEGETABLE PROTEIN;

ADAPTATION; ARABIDOPSIS; GENETICS; HOMEOSTASIS; METABOLISM; PLANT; PLANT ROOT; SOIL; TRANSPORT AT THE CELLULAR LEVEL;

ADAPTATION, PHYSIOLOGICAL; ARABIDOPSIS; BIOLOGICAL TRANSPORT; HOMEOSTASIS; MEMBRANE TRANSPORT PROTEINS; MINERALS; PLANT PROTEINS; PLANT ROOTS; PLANTS; SOIL;

EID: 84922452288     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu156     Document Type: Review

References (85)

1. Ahn, S.J., Shin, R. and Schachtman, D.P. (2004) Expression of KT/KUP genes in Arabidopsis and the role of root hairs in K+ uptake. Plant Physiol. 134: 1135-1145.
2. Alvarez, J.M., Riveras, E., Vidal, E.A., Gras, D.E., Contreras-Lopez, O., Tamayo, K.P. et al. (2014) Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J. 80: 1-13.
3. Barberon, M., Dubeaux, G., Kolb, C., Isono, E., Zelazny, E. and Vert, G. (2014) Polarization of IRON-REGULATED TRANSPORTER 1 (IRT1) to the plant-soil interface plays crucial role in metal homeostasis. Proc. Natl Acad. Sci. USA 111: 8293-8298.
4. Barberon, M., Zelazny, E., Robert, S., Conejero, G., Curie, C., Friml, J. et al. (2011) Monoubiquitin-dependent endocytosis of the IRONREGULATED TRANSPORTER 1 (IRT1) transporter controls iron uptake in plants. Proc. Natl Acad. Sci. USA 108: E450-E458.
5. Benito, B., Garciadeblas, B. and Rodriguez-Navarro, A. (2012) HAK transporters from Physcomitrella patens and Yarrowia lipolytica mediate sodium uptake. Plant Cell Physiol. 53: 1117-1123.
6. Bhat, S., Tang, L., Krueger, A., Smith, C., Ford, S., Dickey, L. et al. (2004) The Fed-1 (CAUU)(4) element is a 50 UTR dark-responsive mRNA instability element that functions independently of dark-induced polyribosome dissociation. Plant Mol. Biol. 56: 761-773.
7. Caballero, F., Botella, M.A., Rubio, L., Fernandez, J.A., Martinez, V. and Rubio, F. (2012) A Ca2+-sensitive system mediates low-affinity K+ uptake in the absence of AKT1 in Arabidopsis plants. Plant Cell Physiol. 53: 2047-2059.
8. Chatterjee, M., Tabi, Z., Galli, M., Malcomber, S., Buck, A., Muszynski, M. et al. (2014) The boron efflux transporter ROTTEN EAR is required for maize inflorescence development and fertility. Plant Cell 26: 2962-2977.
9. Chiba, Y., Mineta, K., Hirai, M.Y., Suzuki, Y., Kanaya, S., Takahashi, H. et al. (2013) Changes in mRNA stability associated with cold stress in Arabidopsis cells. Plant Cell Physiol. 54: 180-194.
10. 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.
11. Deng, F., Yamaji, N., Xia, J. and Ma, J.F. (2013) A member of the heavy metal P-type ATPase OsHMA5 is involved in xylem loading of copper in rice. Plant Physiol. 163: 1353-1362.
12. Durbak, A.R., Phillips, K.A., Pike, S., O'Neill, M.A., Mares, J., Gallavotti, A. et al. (2014) Transport of boron by the tassel-less1 aquaporin is critical for vegetative and reproductive development in maize. Plant Cell 26: 2978-2995.
13. Gan, Y., Bernreiter, A., Filleur, S., Abram, B. and Forde, B.G. (2012) Overexpressing the ANR1 MADS-box gene in transgenic plants provides new insights into its role in the nitrate regulation of root development. Plant Cell Physiol. 53: 1003-1016.
14. Garcia-Molina, A., Andres-Colas, N., Perea-Garcia, A., Neumann, U., Dodani, S.C., Huijser, P. et al. (2013) The Arabidopsis COPT6 transport protein functions in copper distribution under copper-deficient conditions. Plant Cell Physiol. 54: 1378-1390.
15. Ge, Z., Rubio, G. and Lynch, J.P. (2000) The importance of root gravitropism for inter-root competition and phosphorus acquisition efficiency: results from a geometric simulation model. Plant Soil 218: 159-171.
16. Giehl, R.F., Lima, J.E. and von Wiren, N. (2012) Localized iron supply triggers lateral root elongation in Arabidopsis by altering the AUX1-mediated auxin distribution. Plant Cell 24: 33-49.
17. Gruber, B.D., Giehl, R.F., Friedel, S. and von Wiren, N. (2013) Plasticity of the Arabidopsis root system under nutrient deficiencies. Plant Physiol. 163: 161-179.
18. Gu, C., Zhang, X., Jiang, J., Guan, Z., Zhao, S., Fang, W. et al. (2014) Chrysanthemum CmNAR2 interacts with CmNRT2 in the control of nitrate uptake. Sci. Rep. 4: 5833.
19. Gu, R., Duan, F., An, X., Zhang, F., von Wiren, N. and Yuan, L. (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant Cell Physiol. 54: 1515-1524.
20. Haro, R., Fraile-Escanciano, A., Gonzalez-Melendi, P. and Rodriguez- Navarro, A. (2013) The potassium transporters HAK2 and HAK3 localize to endomembranes in Physcomitrella patens. HAK2 is required in some stress conditions. Plant Cell Physiol. 54: 1441-1454.
21. Heppell, J., Talboys, P., Payvandi, S., Zygalakis, K.C., Fliege, J., Withers, P.J. 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. (in press).
22. Ho, C.H., Lin, S.H., Hu, H.C. and Tsay, Y.F. (2009) CHL1 functions as a nitrate sensor in plants. Cell 138: 1184-1194.
23. Hong, J.P., Takeshi, Y., Kondou, Y., Schachtman, D.P., Matsui, M. and Shin, R. (2013) Identification and characterization of transcription factors regulating Arabidopsis HAK5. Plant Cell Physiol. 54: 1478-1490.
24. Hsieh, L.C., Lin, S.I., Shih, A.C., Chen, J.W., Lin, W.Y., Tseng, C.Y. et al. (2009) Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 151: 2120-2132.
25. Hsu, P.K. and Tsay, Y.F. (2013) Two phloem nitrate transporters, NRT1.11 and NRT1.12, are important for redistributing xylem-borne nitrate to enhance plant growth. Plant Physiol. 163: 844-856.
26. Ishimaru, Y., Takahashi, R., Bashir, K., Shimo, H., Senoura, T., Sugimoto, K. et al. (2012) Characterizing the role of rice NRAMP5 in manganese, iron and cadmium transport. Sci. Rep. 2: 286.
27. Jobbagy, E.G. and Jackson, R.B. (2001) The distribution of soil nutrients with depth: global patterns and the imprint of plants. Biogeochemistry 53: 51-77.
28. Kasai, K., Takano, J., Miwa, K., Toyoda, A. and Fujiwara, T. (2011) High boron-induced ubiquitination regulates vacuolar sorting of the BOR1 borate transporter in Arabidopsis thaliana. J. Biol. Chem. 286: 6175-6183.
29. Kellermeier, F., Armengaud, P., Seditas, T.J., Danku, J., Salt, D.E. and Amtmann, A. (2014) Analysis of the root system architecture of Arabidopsis provides a quantitative readout of crosstalk between nutritional signals. Plant Cell 26: 1480-1496.
30. Kerkeb, L., Mukherjee, I., Chatterjee, I., Lahner, B., Salt, D.E. and Connolly, E.L. (2008) Iron-induced turnover of the Arabidopsis IRONREGULATED TRANSPORTER1 metal transporter requires lysine residues. Plant Physiol. 146: 1964-1973.
31. Kiba, T., Feria-Bourrellier, A.B., Lafouge, F., Lezhneva, L., Boutet-Mercey, S., Orsel, M. et al. (2012) The Arabidopsis nitrate transporter NRT2.4 plays a double role in roots and shoots of nitrogen-starved plants. Plant Cell 24: 245-258.
32. Kim, M.J., Ruzicka, D., Shin, R. and Schachtman, D.P. (2012) The Arabidopsis AP2/ERF transcription factor RAP2.11 modulates plant response to low-potassium conditions. Mol. Plant 5: 1042-1057.
33. Konishi, M. and Yanagisawa, S. (2013) Arabidopsis NIN-like transcription factors have a central role in nitrate signalling. Nat. Commun. 4: 1617.
34. Krouk, G., Lacombe, B., Bielach, A., Perrine-Walker, F., Malinska, K., Mounier, E. et al. (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell 18: 927-937.
35. Lanquar, V., Loque, D., Hormann, F., Yuan, L., Bohner, A., Engelsberger, W.R. et al. (2009) Feedback inhibition of ammonium uptake by a phosphodependent allosteric mechanism in Arabidopsis. Plant Cell 21: 3610-3622.
36. Leaungthitikanchana, S., Fujibe, T., Tanaka, M., Wang, S., Sotta, N., Takano, J. et al. (2013) Differential expression of three BOR1 genes corresponding to different genomes in response to boron conditions in hexaploid wheat (Triticum aestivum L.). Plant Cell Physiol. 54: 1056-1063.
37. Leonard, A., Holloway, B., Guo, M., Rupe, M., Yu, G., Beatty, M. et al. (2014) tassel-less1 encodes a boron channel protein required for inflorescence development in maize. Plant Cell Physiol. 55: 1044-1054.
38. Lezhneva, L., Kiba, T., Feria-Bourrellier, A.B., Lafouge, F., Boutet-Mercey, S., Zoufan, P. et al. (2014) The Arabidopsis nitrate transporter NRT2.5 plays a role in nitrate acquisition and remobilization in nitrogen-starved plants. Plant J. 80: 230-241.
39. Lin, W.Y., Huang, T.K. and Chiou, T.J. (2013) Nitrogen limitation adaptation, a target of microRNA827, mediates degradation of plasma membrane- localized phosphate transporters to maintain phosphate homeostasis in Arabidopsis. Plant Cell 25: 4061-4074.
40. 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. USA 102: 13693-13698.
41. Liu, K.H., Huang, C.Y. and Tsay, Y.F. (1999) CHL1 is a dual-affinity nitrate transporter of Arabidopsis involved in multiple phases of nitrate uptake. Plant Cell 11: 865-874.
42. Liu, K.H. and Tsay, Y.F. (2003) Switching between the two action modes of the dual-affinity nitrate transporter CHL1 by phosphorylation. EMBO J. 22: 1005-1013.
43. Lopez-Bucio, J., Hernandez-Abreu, E., Sanchez-Calderon, 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.
44. Loque, D., Lalonde, S., Looger, L.L., von Wiren, N. and Frommer, W.B. (2007) A cytosolic trans-activation domain essential for ammonium uptake. Nature 446: 195-198.
45. Lynch, J.P., Nielsen, K.L., Davis, R.D. and Jablokow, A.G. (1997) SimRoot: modelling and visualization of root systems. Plant Soil 188: 139-151.
46. Ma, J.F., Tamai, K., Yamaji, N., Mitani, N., Konishi, S., Katsuhara, M. et al. (2006) A silicon transporter in rice. Nature 440: 688-691.
47. Ma, J.F., Yamaji, N., Mitani, N., Tamai, K., Konishi, S., Fujiwara, T. et al. (2007) An efflux transporter of silicon in rice. Nature 448: 209-212.
48. Ma, W., Li, J., Qu, B., He, X., Zhao, X., Li, B. et al. (2014) Auxin biosynthetic gene TAR2 is involved in low nitrogen-mediated reprogramming of root architecture in Arabidopsis. Plant J. 78: 70-79.
49. Mao, D., Chen, J., Tian, L., Liu, Z., Yang, L., Tang, R. et al. (2014) Arabidopsis transporter MGT6 mediates magnesium uptake and is required for growth under magnesium limitation. Plant Cell 26: 2234-2248.
50. Marchive, C., Roudier, F., Castaings, L., Brehaut, V., Blondet, E., Colot, V. et al. (2013) Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants. Nat. Commun. 4: 1713.
51. Marschner, P. (2011) Marschner's Mineral Nutrition of Higher Plants, 3rd edn. Academic Press, San Diego.
52. Mounier, E., Pervent, M., Ljung, K., Gojon, A. and Nacry, P. (2014) Auxinmediated nitrate signalling by NRT1.1 participates in the adaptive response of Arabidopsis root architecture to the spatial heterogeneity of nitrate availability. Plant Cell Environ. 37: 162-174.
53. Park, B.S., Seo, J.S. and Chua, N.H. (2014) Nitrogen limitation adaptation recruits phosphate2 to target the phosphate transporter PT2 for degradation during the regulation of Arabidopsis phosphate homeostasis. Plant Cell 26: 454-464.
54. Parker, J.L. and Newstead, S. (2014) Molecular basis of nitrate uptake by the plant nitrate transporter NRT1.1. Nature 507: 68-72.
55. Peng, M., Hannam, C., Gu, H., Bi, Y.M. and Rothstein, S.J. (2007) A mutation in NLA, which encodes a RING-type ubiquitin ligase, disrupts the adaptability of Arabidopsis to nitrogen limitation. Plant J. 50: 320-337.
56. Perez-Castro, R., Kasai, K., Gainza-Cortes, F., Ruiz-Lara, S., Casaretto, J.A., Pena-Cortes, H. et al. (2012) VvBOR1, the grapevine ortholog of AtBOR1, encodes an efflux boron transporter that is differentially expressed throughout reproductive development of Vitis vinifera L. Plant Cell Physiol. 53: 485-494.
57. Remans, T., Nacry, P., Pervent, M., Filleur, S., Diatloff, E., Mounier, E. et al. (2006a) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. Proc. Natl Acad. Sci. USA 103: 19206-19211.
58. Remans, T., Nacry, P., Pervent, M., Girin, T., Tillard, P., Lepetit, M. et al. (2006b) 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.
59. Remy, E., Cabrito, T.R., Batista, R.A., Hussein, M.A., Teixeira, M.C., Athanasiadis, A. et al. (2014) Intron retention in the 50UTR of the novel ZIF2 transporter enhances translation to promote zinc tolerance in Arabidopsis. PLoS Genet. 10: e1004375.
60. Roose, T., Fowler, A.C. and Darrah, P.R. (2001) A mathematical model of plant nutrient uptake. J. Math. Biol. 42: 347-360.
61. Rubio, G., Liao, H., Yan, X.L. and Lynch, J.P. (2003) Topsoil foraging and its role in plant competitiveness for phosphorus in common bean. Crop Sci. 43: 598-607.
62. Saito, T., Kobayashi, N.I., Tanoi, K., Iwata, N., Suzuki, H., Iwata, R. et al. (2013) Expression and functional analysis of the CorA-MRS2-ALR-type magnesium transporter family in rice. Plant Cell Physiol. 54: 1673-1683.
63. Sasaki, A., Yamaji, N., Yokosho, K. and Ma, J.F. (2012) Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell 24: 2155-2167.
64. Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K. et al. (2012) Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant Cell Physiol. 53: 213-224.
65. Shin, L.J., Lo, J.C., Chen, G.H., Callis, J., Fu, H. and Yeh, K.C. (2013) IRT1 DEGRADATION FACTOR1, a RING E3 ubiquitin ligase, regulates the degradation of IRONREGULATED TRANSPORTER1 in Arabidopsis. Plant Cell 25: 3039-3051.
66. Sun, J., Bankston, J.R., Payandeh, J., Hinds, T.R., Zagotta, W.N. and Zheng, N. (2014) Crystal structure of the plant dual-affinity nitrate transporter NRT1.1. Nature 507: 73-77.
67. Takano, J., Miwa, K., Yuan, L., von Wiren, N. and Fujiwara, T. (2005) Endocytosis and degradation of BOR1, a boron transporter of Arabidopsis thaliana, regulated by boron availability. Proc. Natl Acad. Sci. USA 102: 12276-12281.
68. Takano, J., Tanaka, M., Toyoda, A., Miwa, K., Kasai, K., Fuji, K. et al. (2010) Polar localization and degradation of Arabidopsis boron transporters through distinct trafficking pathways. Proc. Natl Acad. Sci. USA 107: 5220-5225.
69. Takano, J., Wada, M., Ludewig, U., Schaaf, G., von Wiren, N. and Fujiwara, T. (2006) The Arabidopsis major intrinsic protein NIP5;1 is essential for efficient boron uptake and plant development under boron limitation. Plant Cell 18: 1498-1509.
70. Tanaka, M., Takano, J., Chiba, Y., Lombardo, F., Ogasawara, Y., Onouchi, H. et al. (2011) Boron-dependent degradation of NIP5;1 mRNA for acclimation to excess boron conditions in Arabidopsis. Plant Cell 23: 3547-3559.
71. Tanaka, N., Uraguchi, S., Saito, A., Kajikawa, M., Kasai, K., Sato, Y. et al. (2013) Roles of pollen-specific boron efflux transporter, OsBOR4, in the rice fertilization process. Plant Cell Physiol. 54: 2011-2019.
72. Uehara, M., Wang, S., Kamiya, T., Shigenobu, S., Yamaguchi, K., Fujiwara, T. et al. (2014) Identification and characterization of an Arabidopsis mutant with altered localization of NIP5;1, a plasma membrane boric acid channel, reveals the requirement for D-galactose in endomembrane organization. Plant Cell Physiol. 55: 704-714.
73. Vert, G., Grotz, N., Dedaldechamp, 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.
74. Wang, N., Cui, Y., Liu, Y., Fan, H., Du, J., Huang, Z. et al. (2013) Requirement and functional redundancy of Ib subgroup bHLH proteins for iron deficiency responses and uptake in Arabidopsis thaliana. Mol. Plant 6: 503-513.
75. Wang, R., Liu, D. and Crawford, N.M. (1998) The Arabidopsis CHL1 protein plays a major role in high-affinity nitrate uptake. Proc. Natl Acad. Sci. USA 95: 15134-15139.
76. Williamson, L.C., Ribrioux, S.P., Fitter, A.H. and Leyser, H.M. (2001) Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiol. 126: 875-882.
77. Yamaji, N., Sasaki, A., Xia, J.X., Yokosho, K. and Ma, J.F. (2013a) A nodebased switch for preferential distribution of manganese in rice. Nat. Commun. 4: 2442.
78. Yamaji, N., Xia, J., Mitani-Ueno, N., Yokosho, K. and Feng Ma, J. (2013b) Preferential delivery of zinc to developing tissues in rice is mediated by P-type heavy metal ATPase OsHMA2. Plant Physiol. 162: 927-939.
79. Yoshinari, A., Kasai, K., Fujiwara, T., Naito, S. and Takano, J. (2012) Polar localization and endocytic degradation of a boron transporter, BOR1, is dependent on specific tyrosine residues. Plant Signal. Behav. 7: 46-49.
80. Yuan, H.M., Xu, H.H., Liu, W.C. and Lu, Y.T. (2013) Copper regulates primary root elongation through PIN1-mediated auxin redistribution. Plant Cell Physiol. 54: 766-778.
81. Yuan, L., Gu, R., Xuan, Y., Smith-Valle, E., Loque, D., Frommer, W.B. et al. (2013) Allosteric regulation of transport activity by heterotrimerization of Arabidopsis ammonium transporter complexes in vivo. Plant Cell 25: 974-984.
82. Yuan, L., Loque, D., Ye, F., Frommer, W.B. and von Wiren, N. (2007) Nitrogen-dependent posttranscriptional regulation of the ammonium transporter AtAMT1;1. Plant Physiol. 143: 732-744.
83. Yuan, Y., Wu, H., Wang, N., Li, J., Zhao, W., Du, J. et al. (2008) FIT interacts with AtbHLH38 and AtbHLH39 in regulating iron uptake gene expression for iron homeostasis in Arabidopsis. Cell Res. 18: 385-397.
84. Zhang, H.M. and Forde, B.G. (1998) An Arabidopsis MADS box gene that controls nutrient-induced changes in root architecture. Science 279: 407-409.
85. Zheng, L., Yamaji, N., Yokosho, K. and Ma, J.F. (2012) YSL16 is a phloem-localized transporter of the copper-nicotianamine complex that is responsible for copper distribution in rice. Plant Cell 24: 3767-3782.