Getting to the root of plant biology: Impact of the Arabidopsis genome sequence on root research

Plant Journal

Volumn 61, Issue 6, 2010, Pages 992-1000

  Benfey, Philip N ^a   Bennett, Malcolm ^b   Schiefelbein, John ^c  

^a DUKE UNIVERSITY   (United States)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Arabidopsis; Development; Genetics; Genomics; Root biology; Transcriptome

Indexed keywords

AGAR MEDIA; ARABIDOPSIS; ARABIDOPSIS GENOME; CELL TYPES; CONCENTRIC CYLINDERS; DIMENSIONAL PROBLEMS; EXPERIMENTAL STRATEGY; GENETIC RESEARCH; GENOME SEQUENCES; GENOMICS; LONGITUDINAL AXIS; PLANT BIOLOGY; PRIMARY ROOTS; ROOT BIOLOGY; ROOT DEVELOPMENT; SPATIAL DIMENSION; TRANSCRIPTOMES; TWO-DIMENSIONAL PROBLEM; VASCULAR TISSUE;

CRACK PROPAGATION; ELASTIC MODULI; GENES; RESEARCH; STEM CELLS; TWO DIMENSIONAL;

BIOLOGY;

ARABIDOPSIS; ARTICLE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GENOMICS; GROWTH, DEVELOPMENT AND AGING; PLANT GENOME; PLANT ROOT;

ARABIDOPSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENE REGULATORY NETWORKS; GENOME, PLANT; GENOMICS; PLANT ROOTS;

ARABIDOPSIS;

EID: 77950410675     PISSN: 09607412     EISSN: 1365313X     Source Type: Journal    
DOI: 10.1111/j.1365-313X.2010.04129.x     Document Type: Article

References (71)

1. Aida, M., Beis, D., Heidstra, R., Willemsen, V., Blilou, I., Galinha, C., Nussaume, L., Noh, Y.S., Amasino, R. Scheres, B. (2004) The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell, 119, 109 120.
2. Armengaud, P., Zambaux, K., Hills, A., Sulpice, R., Pattison, R.J., Blatt, M.R. Amtmann, A. (2008) Ez-Rhizo: integrated software for the fast and accurate measurement of root system architecture. Plant J. 57, 945 956.
3. Baxter, I., Muthukumar, B., Park, H.C. et al. (2008) Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1). PLoS Genet. 4 (2 e1000004.
4. Baxter, I., Hosmani, P.S., Rus, A., Lahner, B., Borevitz, J.O., Muthukumar, B., Micklebart, M.V., Schreiber, L., Franke, R.B. Salt, D.E. (2009) Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet. 5 (5 e1000492.
5. Benfey, P.N. Schiefelbein, J.W. (1994) Getting to the root of plant development: the genetics of Arabidopsis root formation. Trends Genet. 10, 84 88.
6. Bernhardt, C., Zhao, M., Gonzalez, A., Lloyd, A. Schiefelbein, J. (2005) The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis. Development, 132, 291 298.
7. Birnbaum, K., Shasha, D.E., Wang, J.Y., Jung, J.W., Lambert, G.M., Galbraith, D.W. Benfey, P.N. (2003) A gene expression map of the Arabidopsis root. Science, 302, 1956 1960.
8. Brady, S.M., Orlando, D.A., Lee, J.Y., Wang, J.Y., Koch, J., Dinneny, J.R., Mace, D., Ohler, U. Benfey, P.N. (2007) A high-resolution root spatiotemporal map reveals dominant expression patterns. Science, 318, 801 806.
9. Chen, Z.H., Nimmo, G.A., Jenkins, G.I. Nimmo, H.G. (2007) BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis. Biochem. J. 405, 191 198.
10. Clark, R.M., Schweikert, G., Toomajian, C. et al. (2007) Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana. Science, 317, 338 342.
11. DeSmet, I., Vassileva, V., DeRybel, B. et al. (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science, 322, 594 597.
12. Devaiah, B.N., Karthikeyan, A.S. Raghothama, K.G. (2007a) WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis. Plant Physiol. 143, 1789 1801.
13. Devaiah, B.N., Nagarajan, V.K. Raghothama, K.G. (2007b) Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6. Plant Physiol. 145, 147 159.
14. Dinneny, J.R., Long, T.A., Wang, J.Y., Jung, J.W., Mace, D., Pointer, S., Barron, C., Brady, S.M., Schiefelbein, J. Benfey, P.N. (2008) Cell identity mediates the response of Arabidopsis roots to abiotic stress. Science, 320, 942 945.
15. Dolan, L. Roberts, K. (1995) Plant development: pulled up by the roots. Curr. Opin. Genet. Dev. 5, 432 438.
16. Galinha, C., Hofhuis, H., Luijten, M., Willemsen, V., Blilou, I., Heidstra, R. Scheres, B. (2007) PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature, 449, 1053 1057.
17. Gifford, M.L., Dean, A., Gutierrez, R.A., Coruzzi, G.M. Birnbaum, K.D. (2008) Cell-specific nitrogen responses mediate developmental plasticity. Proc. Natl Acad. Sci. USA, 105, 803 808.
18. Grieneisen, V.A., Xu, J., Maree, A.F.M., Hogeweg, P. Scheres, B. (2007) Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature, 449, 1008 1013.
19. Grigg, S.P., Galinha, C., Kornet, N., Canales, C., Scheres, B. Tsiantis, M. (2009) Repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr. Biol. 19, 1485 1490.
20. Guimil, S. Dunand, C. (2007) Cell growth and differentiation in Arabidopsis epidermal cells. J. Exp. Bot. 58, 3829 3840.
21. Hochholdinger, F. Zimmermann, R. (2008) Conserved and diverse mechanisms in root development. Curr. Opin. Plant Biol. 11, 70 74.
22. Hochholdinger, F., Park, W.J., Sauer, M. Woll, K. (2004) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci. 9, 42 48.
23. Hu, J., Shibata, Y., Zhu, P.P., Voss, C., Rismanchi, N., Prinz, W.A., Rapoport, T.A. Blackstone, C. (2009) A class of dynamin-like GTPases involved in the generation of the tubular ER network. Cell, 138, 549 561.
24. Huang, L., Yang, S., Zhang, S. et al. (2009) The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root. Plant J. 60, 666 678.
25. Inukai, Y., Sakamoto, T., Ueguchi-Tanaka, M., Shibata, Y., Gomi, K., Umemura, I., Hasegawa, Y., Ashikari, M., Kitano, H. Matsuoka, M. (2005) Crown rootless1, which is essential for crown root formation in rice, is a target of an auxin response factor in auxin signaling. Plant Cell, 17, 1387 1396.
26. Ishida, T., Kurata, T., Okada, K. Wada, T. (2008) A genetic regulatory network in the development of trichomes and root hairs. Annu. Rev. Plant Biol. 59, 365 386.
27. Jiao, Y., Tausta, S.L., Gandotra, N. et al. (2009) A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies. Nat. Genet. 41, 258 263.
28. Jones, M.A., Raymond, M.J. 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.
29. Jones, A.R., Kramer, E.M., Knox, K., Swarup, R., Bennett, M.J., Lazarus, C.M., Leyser, H.M.O. Grierson, C.S. (2008) Auxin transport through non-hair cells sustains root-hair development. Nat. Cell Biol. 11, 78 84.
30. Kerk, N.M., Ceserani, T., Tausta, S.L., Sussex, I.M. Nelson, T.M. (2003) Laser capture microdissection of cells from plant tissues. Plant Physiol. 132, 27 35.
31. Koshino-Kimura, Y., Wada, T., Tachibana, T., Tsugeki, R., Ishiguro, S. Okada, K. (2005) Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. Plant Cell Physiol. 46, 817 826.
32. Kurata, T., Ishida, T., Kawabata-Awai, C. et al. (2005) Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development, 132, 5387 5398.
33. Lahner, B., Gong, J., Mahmoudian, M. et al. (2003) Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana. Nat. Biotechnol. 21, 1215 1221.
34. Laplaze, L., Parizot, B., Baker, A., Ricaud, L., Martiniere, A., Auguy, F., Franche, C., Nussaume, L., Bogusz, D. Haseloff, J. (2005) GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana. J. Exp. Bot. 56, 2433 2442.
35. Laskowski, M., Biller, S., Stanley, K., Kajstura, T. Prusty, R. (2006) Expression profiling of auxin treated Arabidopsis roots: toward a molecular analysis of lateral root emergence. Plant Cell Physiol. 47, 778 792.
36. Laskowski, M., Grieneisen, V.A., Hofhuis, H., TenHove, C.A., Hogeweg, P., Marer, A.F.M. Scheres, B. (2008) Root system architecture from coupling cell shape to auxin transport. PLoS Biol. 6, e307.
37. Lehar, J., Stockwell, B., Giaever, G. Nislow, C. (2008) Combination chemical genetics. Nat. Chem. Biol. 4, 674 681.
38. Levesque, M.P., Vernoux, T., Busch, W. et al. (2006) Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 4, e143.
39. Little, D.Y., Rao, H., Oliva, S., Daniel-Vedele, F., Krapp, A. 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.
40. Liu, H., Wang, S., Yu, X., Yu, J., He, X., Zhang, S., Shou, H. Wu, P. (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J. 43, 47 56.
41. Middleton, A.M., King, J.R., Bennett, M.J. Owen, M.R. (2009) Mathematical modelling of the Aux/IAA negative feedback loop. Bull. Math. Biol., doi:.
42. Misson, J., Raghothama, K.G., Jain, A. et al. (2005) A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation. Proc. Natl Acad. Sci. USA, 102, 11934 11939.
43. Mouchel, C.F., Osmont, K.S. Hardtke, C.S. (2006) BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth. Nature, 443, 458 461.
44. Nakajima, K., Sena, G., Nawy, T. Benfey, P.N. (2001) Intercellular movement of the putative transcription factor SHR in root patterning. Nature, 413, 307 311.
45. Nawy, T., Lee, J.Y., Colinas, J., Wang, J.Y., Thongrod, S.C., Malamy, J.E., Birnbaum, K. Benfey, P.N. (2005) Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell, 17, 1908 1925.
46. Nordborg, M., Hu, T.T., Ishino, Y. et al. (2005) The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3, e196.
47. Okushima, Y., Fukaki, H., Onoda, M., Theologis, A. Tasaka, M. (2007) ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis. Plant Cell, 19, 118 130.
48. Oliva, M. Dunand, C. (2007) Waving and skewing: how gravity and the surface of growth media affect root development in Arabidopsis. New Phytol. 176, 37 43.
49. Osmont, K.S., Sibout, R. Hardtke, C.S. (2007) Hidden branches: developments in root system architecture. Annu. Rev. Plant Biol. 58, 93 113.
50. Petricka, J.J. Benfey, P.N. (2008) Root layers: complex regulation of developmental patterning. Curr. Opin. Genet. Dev. 18, 354 361.
51. Ryu, K.H., Kang, Y.H., Park, Y.H., Hwang, I., Schiefelbein, J. Lee, M.M. (2005) The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis. Development, 132, 4765 4775.
52. Savage, N., Walker, T., Wieckowski, T., Schiefelbein, J., Dolan, L. Monk, N.A.M. (2008) A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis. PLoS Biol. 6, e235.
53. Scacchi, E., Osmont, K.S., Beuchat, J., Salinas, P., Navarrete- Gómez, M., Trigueros, M., Ferrándiz, C. Hardtke, C.S. (2009) Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX. Development, 136, 2059 2067.
54. Schmid, K.J., Sorenson, T.R., Stracke, R., Torjek, O., Altmann, T., Mitchell-Olds, T. Weisshaar, B. (2003) Large scale identification of genome wide single nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res. 13, 1250 1257.
55. Sergeeva, L.I., Keurentjes, J.J.B., Bentsink, L., Vonk, J., Van der Plas, L.W., Koornneef, M. Vreughenhil, D. (2006) Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis. Proc. Natl Acad. Sci. USA, 103, 2994 2999.
56. Shaw, P. Dolan, L. (2008) Chromatin and Arabidopsis root development. Semin. Cell Dev. Biol. 19, 580 585.
57. Simon, M., Lee, M.M., Lin, Y., Gish, L. Schiefelbein, J. (2007) Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev. Biol. 311, 566 578.
58. Stahl, Y., Wink, R.H., Ingram, G.C. Simon, R. (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr. Biol. 19, 909 914.
59. Svistoonoff, S., Creff, A., Reymond, M., Sigoillot-Claude, C., Ricaud, L., Blanchet, A., Nussaume, L. Desnos, T. (2007) Root tip contact with low-phosphate media reprograms plant root architecture. Nat. Genet. 39, 792 796.
60. Swarup, R., Kramer, E.M., Perry, P., Knox, K., Leyser, H.M.O., Haseloff, J., Beemster, G.T.S., Bhalerao, R. Bennett, M.J. (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat. Cell Biol. 7, 1057 1065.
61. Swarup, K., Benkova, E., Swarup, R. et al. (2008) The auxin influx carrier LAX3 promotes lateral root emergence. Nat. Cell Biol. 10, 946 954.
62. Tominaga, R., Iwata, M., Sano, R., Inoue, K., Okada, K. Wada, T. (2008) Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation. Development, 135, 1335 1345.
63. Tominaga-Wada, R., Iwata, M., Sugiyama, J., Kotake, T., Ishida, T., Yokoyama, R., Nishitani, K., Okada, K. Wada, T. (2009) The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots. Plant J. 60, 564 574.
64. Wada, T., Kurata, T., Tominaga, R., Koshino-Kimura, Y., Tachibana, T., Goto, K., Marks, M.D., Shimura, Y. Okada, K. (2002) Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation. Development, 129, 5409 5419.
65. Wang, H., Lockwood, S.K., Hoeltzel, M.F. Schiefelbein, J.W. (1997) The ROOT HAIR DEFECTIVE3 gene encodes an evolutionarily conserved protein with GTP-binding motifs and is required for regulated cell enlargement in Arabidopsis. Genes Dev. 11, 799 811.
66. Wildwater, M., Campilho, A., Perez-Perez, J.M., Heidstra, R., Blilou, I., Korthout, H., Chatterjee, J., Mariconti, L., Gruissem, W. Scheres, B. (2005) The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell, 123, 1337 1349.
67. Willemsen, V., Bauch, M., Bennett, T., Campilho, A., Wolkenfelt, H., Xu, J., Haseloff, J. Scheres, B. (2008) The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev. Cell, 15, 913 922.
68. Won, S.K., Lee, Y.J., Lee, H.Y., Heo, Y.K., Cho, M. Cho, H.T. (2009) Cis-element- and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis. Plant Physiol. 150, 1459 1473.
69. Yant, L., Mathieu, J. Schmid, M. (2009) Just say no: floral repressors help Arabidopsis bide the time. Curr. Opin. Plant Biol. 12, 580 586.
70. Zanetti, M.E., Chang, I.F., Gong, F., Galbraith, D.W. Bailey-Serres, J. (2005) Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression. Plant Physiol. 138, 624 635.
71. Zheng, H., Kunst, L., Hawes, C. Moore, I. (2004) A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus. Plant J. 37, 398 414.