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PMID: 20409273 Published · ppublish English Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S. Review

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

The Plant journal : for cell and molecular biology ·Vol. 61 ·No. 6 ·2010-03-00 ·Pages 992-1000

Benfey PN, Bennett M, Schiefelbein J

Abstract

Prior to the availability of the genome sequence, the root of Arabidopsis had attracted a small but ardent group of researchers drawn to its accessibility and developmental simplicity. Roots are easily observed when grown on the surface of nutrient agar media, facilitating analysis of responses to stimuli such as gravity and touch. Developmental biologists were attracted to the simple radial organization of primary root tissues, which form a series of concentric cylinders around the central vascular tissue. Equally attractive was the mode of propagation, with stem cells at the tip giving rise to progeny that were confined to cell files. These properties of root development reduced the normal four-dimensional problem of development (three spatial dimensions and time) to a two-dimensional problem, with cell type on the radial axis and developmental time along the longitudinal axis. The availability of the complete Arabidopsis genome sequence has dramatically accelerated traditional genetic research on root biology, and has also enabled entirely new experimental strategies to be applied. Here we review examples of the ways in which availability of the Arabidopsis genome sequence has enhanced progress in understanding root biology.

MeSH Terms
Arabidopsis/genetics,growth & development Gene Expression Profiling Gene Expression Regulation, Developmental Gene Expression Regulation, Plant Gene Regulatory Networks Genome, Plant Genomics Plant Roots/genetics,growth & development
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Benfey Philip N
Department of Biology, Institute for Genome Sciences & Policy, Center for Systems Biology, Duke University, Durham, NC, USA. [email protected]
Bennett Malcolm
Schiefelbein John
References (71)
71 references, click to expand
  1. A high-resolution root spatiotemporal map reveals dominant expression patterns.
    Science. 2007 Nov 2;318(5851):801-6 PMID: 17975066
  2. Plant development: pulled up by the roots.
    Curr Opin Genet Dev. 1995 Aug;5(4):432-8 PMID: 7580133
  3. Root layers: complex regulation of developmental patterning.
    Curr Opin Genet Dev. 2008 Aug;18(4):354-61 PMID: 18617392
  4. BHLH32 modulates several biochemical and morphological processes that respond to Pi starvation in Arabidopsis.
    Biochem J. 2007 Jul 1;405(1):191-8 PMID: 17376028
  5. Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis.
    Plant Cell Physiol. 2005 Jun;46(6):817-26 PMID: 15795220
  6. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells.
    Dev Cell. 2008 Dec;15(6):913-22 PMID: 19081078
  7. The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis.
    Development. 2005 Nov;132(21):4765-75 PMID: 16207757
  8. Expression profiling of auxin-treated Arabidopsis roots: toward a molecular analysis of lateral root emergence.
    Plant Cell Physiol. 2006 Jun;47(6):788-92 PMID: 16621846
  9. A signaling module controlling the stem cell niche in Arabidopsis root meristems.
    Curr Biol. 2009 Jun 9;19(11):909-14 PMID: 19398337
  10. Just say no: floral repressors help Arabidopsis bide the time.
    Curr Opin Plant Biol. 2009 Oct;12(5):580-6 PMID: 19695946
  11. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development.
    Nature. 2007 Oct 25;449(7165):1053-7 PMID: 17960244
  12. Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal.
    Nat Cell Biol. 2005 Nov;7(11):1057-65 PMID: 16244669
  13. Conserved and diverse mechanisms in root development.
    Curr Opin Plant Biol. 2008 Feb;11(1):70-4 PMID: 18006363
  14. Immunopurification of polyribosomal complexes of Arabidopsis for global analysis of gene expression.
    Plant Physiol. 2005 Jun;138(2):624-35 PMID: 15955926
  15. ARF7 and ARF19 regulate lateral root formation via direct activation of LBD/ASL genes in Arabidopsis.
    Plant Cell. 2007 Jan;19(1):118-30 PMID: 17259263
  16. A genome-wide transcriptional analysis using Arabidopsis thaliana Affymetrix gene chips determined plant responses to phosphate deprivation.
    Proc Natl Acad Sci U S A. 2005 Aug 16;102(33):11934-9 PMID: 16085708
  17. Transcriptional profile of the Arabidopsis root quiescent center.
    Plant Cell. 2005 Jul;17(7):1908-25 PMID: 15937229
  18. Getting to the root of plant development: the genetics of Arabidopsis root formation.
    Trends Genet. 1994 Mar;10(3):84-8 PMID: 8178369
  19. Crown rootless1, which is essential for crown root formation in rice, is a target of an AUXIN RESPONSE FACTOR in auxin signaling.
    Plant Cell. 2005 May;17(5):1387-96 PMID: 15829602
  20. Laser capture microdissection of cells from plant tissues.
    Plant Physiol. 2003 May;132(1):27-35 PMID: 12746508
  21. Dynamic, auxin-responsive plasma membrane-to-nucleus movement of Arabidopsis BRX.
    Development. 2009 Jun;136(12):2059-67 PMID: 19465596
  22. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation.
    Development. 2005 Dec;132(24):5387-98 PMID: 16291794
  23. The putative high-affinity nitrate transporter NRT2.1 represses lateral root initiation in response to nutritional cues.
    Proc Natl Acad Sci U S A. 2005 Sep 20;102(38):13693-8 PMID: 16157886
  24. Intercellular movement of the putative transcription factor SHR in root patterning.
    Nature. 2001 Sep 20;413(6853):307-11 PMID: 11565032
  25. Root system architecture from coupling cell shape to auxin transport.
    PLoS Biol. 2008 Dec 16;6(12):e307 PMID: 19090618
  26. WRKY75 transcription factor is a modulator of phosphate acquisition and root development in Arabidopsis.
    Plant Physiol. 2007 Apr;143(4):1789-801 PMID: 17322336
  27. Auxin transport is sufficient to generate a maximum and gradient guiding root growth.
    Nature. 2007 Oct 25;449(7165):1008-13 PMID: 17960234
  28. ARL1, a LOB-domain protein required for adventitious root formation in rice.
    Plant J. 2005 Jul;43(1):47-56 PMID: 15960615
  29. A GFP-based assay reveals a role for RHD3 in transport between the endoplasmic reticulum and Golgi apparatus.
    Plant J. 2004 Feb;37(3):398-414 PMID: 14731265
  30. The bHLH genes GL3 and EGL3 participate in an intercellular regulatory circuit that controls cell patterning in the Arabidopsis root epidermis.
    Development. 2005 Jan;132(2):291-8 PMID: 15590742
  31. A gene expression map of the Arabidopsis root.
    Science. 2003 Dec 12;302(5652):1956-60 PMID: 14671301
  32. Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root.
    Science. 2008 Oct 24;322(5901):594-7 PMID: 18948541
  33. Chromatin and Arabidopsis root development.
    Semin Cell Dev Biol. 2008 Dec;19(6):580-5 PMID: 18824115
  34. Repression of apical homeobox genes is required for embryonic root development in Arabidopsis.
    Curr Biol. 2009 Sep 15;19(17):1485-90 PMID: 19646874
  35. Cell identity mediates the response of Arabidopsis roots to abiotic stress.
    Science. 2008 May 16;320(5878):942-5 PMID: 18436742
  36. Cell-specific nitrogen responses mediate developmental plasticity.
    Proc Natl Acad Sci U S A. 2008 Jan 15;105(2):803-8 PMID: 18180456
  37. BRX mediates feedback between brassinosteroid levels and auxin signalling in root growth.
    Nature. 2006 Sep 28;443(7110):458-61 PMID: 17006513
  38. A transcriptome atlas of rice cell types uncovers cellular, functional and developmental hierarchies.
    Nat Genet. 2009 Feb;41(2):258-63 PMID: 19122662
  39. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning.
    Dev Biol. 2007 Nov 15;311(2):566-78 PMID: 17931617
  40. Genomic scale profiling of nutrient and trace elements in Arabidopsis thaliana.
    Nat Biotechnol. 2003 Oct;21(10):1215-21 PMID: 12949535
  41. EZ-Rhizo: integrated software for the fast and accurate measurement of root system architecture.
    Plant J. 2009 Mar;57(5):945-56 PMID: 19000163
  42. GAL4-GFP enhancer trap lines for genetic manipulation of lateral root development in Arabidopsis thaliana.
    J Exp Bot. 2005 Sep;56(419):2433-42 PMID: 16043452
  43. Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis.
    PLoS Genet. 2009 May;5(5):e1000492 PMID: 19461889
  44. Root tip contact with low-phosphate media reprograms plant root architecture.
    Nat Genet. 2007 Jun;39(6):792-6 PMID: 17496893
  45. Cis-element- and transcriptome-based screening of root hair-specific genes and their functional characterization in Arabidopsis.
    Plant Physiol. 2009 Jul;150(3):1459-73 PMID: 19448035
  46. A mutual support mechanism through intercellular movement of CAPRICE and GLABRA3 can pattern the Arabidopsis root epidermis.
    PLoS Biol. 2008 Sep 23;6(9):e235 PMID: 18816165
  47. 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. 1997 Mar 15;11(6):799-811 PMID: 9087433
  48. Arabidopsis CAPRICE-LIKE MYB 3 (CPL3) controls endoreduplication and flowering development in addition to trichome and root hair formation.
    Development. 2008 Apr;135(7):1335-45 PMID: 18305006
  49. Analysis of the root-hair morphogenesis transcriptome reveals the molecular identity of six genes with roles in root-hair development in Arabidopsis.
    Plant J. 2006 Jan;45(1):83-100 PMID: 16367956
  50. Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana.
    Genome Res. 2003 Jun;13(6A):1250-7 PMID: 12799357
  51. Phosphate homeostasis and root development in Arabidopsis are synchronized by the zinc finger transcription factor ZAT6.
    Plant Physiol. 2007 Sep;145(1):147-59 PMID: 17631527
  52. Mathematical modelling of the Aux/IAA negative feedback loop.
    Bull Math Biol. 2010 Aug;72(6):1383-407 PMID: 20135237
  53. From weeds to crops: genetic analysis of root development in cereals.
    Trends Plant Sci. 2004 Jan;9(1):42-8 PMID: 14729218
  54. The pattern of polymorphism in Arabidopsis thaliana.
    PLoS Biol. 2005 Jul;3(7):e196 PMID: 15907155
  55. The GLABRA2 homeodomain protein directly regulates CESA5 and XTH17 gene expression in Arabidopsis roots.
    Plant J. 2009 Nov;60(3):564-74 PMID: 19619157
  56. The auxin influx carrier LAX3 promotes lateral root emergence.
    Nat Cell Biol. 2008 Aug;10(8):946-54 PMID: 18622388
  57. Cell growth and differentiation in Arabidopsis epidermal cells.
    J Exp Bot. 2007;58(14):3829-40 PMID: 18162628
  58. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche.
    Cell. 2004 Oct 1;119(1):109-20 PMID: 15454085
  59. Role of a positive regulator of root hair development, CAPRICE, in Arabidopsis root epidermal cell differentiation.
    Development. 2002 Dec;129(23):5409-19 PMID: 12403712
  60. Common sequence polymorphisms shaping genetic diversity in Arabidopsis thaliana.
    Science. 2007 Jul 20;317(5836):338-42 PMID: 17641193
  61. Combination chemical genetics.
    Nat Chem Biol. 2008 Nov;4(11):674-81 PMID: 18936752
  62. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis.
    PLoS Biol. 2006 May;4(5):e143 PMID: 16640459
  63. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots.
    Cell. 2005 Dec 29;123(7):1337-49 PMID: 16377572
  64. A genetic regulatory network in the development of trichomes and root hairs.
    Annu Rev Plant Biol. 2008;59:365-86 PMID: 18257710
  65. Waving and skewing: how gravity and the surface of growth media affect root development in Arabidopsis.
    New Phytol. 2007;176(1):37-43 PMID: 17692076
  66. The Arabidopsis SUMO E3 ligase AtMMS21, a homologue of NSE2/MMS21, regulates cell proliferation in the root.
    Plant J. 2009 Nov;60(4):666-78 PMID: 19682286
  67. Auxin transport through non-hair cells sustains root-hair development.
    Nat Cell Biol. 2009 Jan;11(1):78-84 PMID: 19079245
  68. Variation in molybdenum content across broadly distributed populations of Arabidopsis thaliana is controlled by a mitochondrial molybdenum transporter (MOT1).
    PLoS Genet. 2008 Feb 29;4(2):e1000004 PMID: 18454190
  69. Hidden branches: developments in root system architecture.
    Annu Rev Plant Biol. 2007;58:93-113 PMID: 17177637
  70. Vacuolar invertase regulates elongation of Arabidopsis thaliana roots as revealed by QTL and mutant analysis.
    Proc Natl Acad Sci U S A. 2006 Feb 21;103(8):2994-9 PMID: 16481625
  71. A class of dynamin-like GTPases involved in the generation of the tubular ER network.
    Cell. 2009 Aug 7;138(3):549-61 PMID: 19665976
Article Info
Journal
The Plant journal : for cell and molecular biology
Abbr.
Plant J
ISSN
1365-313X
Published
2010-03-00
Pages
992-1000
Language
English
Region
England
NLM ID
9207397
PMCID
PMC2967761
Subset
IM
Grants
Biotechnology and Biological Sciences Research Council · BB/G023972/1 · United Kingdom
NIGMS NIH HHS · R01 GM043778-21 · United States
NIGMS NIH HHS · P50 GM081883-020003 · United States
NIGMS NIH HHS · R01 GM043778 · United States
Biotechnology and Biological Sciences Research Council · BB/D019613/1 · United Kingdom
NIGMS NIH HHS · P50 GM081883-030003 · United States
NIGMS NIH HHS · R01 GM043778-19 · United States
NIGMS NIH HHS · P50 GM081883 · United States
NIGMS NIH HHS · R01 GM043778-20 · United States
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