Patterning the primary root in Arabidopsis

Wiley Interdisciplinary Reviews: Developmental Biology

Volumn 1, Issue 5, 2012, Pages 675-691

  Cederholm, Heidi M ^a   Iyer Pascuzzi, Anjali S ^a   Benfey, Philip N ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUXIN; CYTOKININ; TRANSCRIPTION FACTOR;

ARABIDOPSIS; CELL DIVISION; CELL TYPE; EMBRYO DEVELOPMENT; ENDODERMIS; GENE EXPRESSION; HORMONAL REGULATION; MERISTEM; MORPHOGENESIS; NONHUMAN; PLANT DEVELOPMENT; PLANT EPIDERMIS; PLANT ROOT CAP; PROTEIN EXPRESSION; REVIEW; VASCULAR TISSUE;

ARABIDOPSIS; CELL DIVISION; GENE EXPRESSION REGULATION, PLANT; MERISTEM; ORGANOGENESIS, PLANT; PLANT DEVELOPMENT; PLANT GROWTH REGULATORS; PLANT ROOTS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84874935709     PISSN: 17597684     EISSN: 17597692     Source Type: Journal    
DOI: 10.1002/wdev.49     Document Type: Review

References (91)

1. Benfey PN, Scheres B. Root development. Curr Biol 2000, 10:R813-R815.
2. Scheres B. Stem-cell niches: nursery rhymes across kingdoms. Nat Rev Mol Cell Biol 2007, 8:345-354.
3. Dello Ioio R, Nakamura K, Moubayidin L, Perilli S, Taniguchi M, Morita MT, Aoyama T, Costantino P, Sabatini S. A genetic framework for the control of cell division and differentiation in the root meristem. Science 2008, 322:1380-1384.
4. Dello Ioio R, Linhares FS, Scacchi E, Casamitjana-Martinez E, Heidstra R, Costantino P, Sabatini S. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol 2007, 17: 678-682.
5. Moubayidin L, Perilli S, Dello Ioio R, Di Mambro R, Costantino P, Sabatini S. The rate of cell differentiation controls the Arabidopsis root meristem growth phase. Curr Biol 2010, 20:1138-1143.
6. Katsir L, Davies KA, Bergmann DC, Laux T. Peptide signalling in plant development. Curr Biol 2011, 21: R356-R364.
7. Van Norman JM, Breakfield NW, Benfey PN. Intercellular communication during plant development. Plant Cell 2011, 23:855-864.
8. Wang G, Fiers M. CLE peptide signalling during plant development. Protoplasma 2010, 240:33-43.
9. Bennett T, Scheres B. Root development-two meristems for the price of one? Curr Top Dev Biol 2010, 91: 67-102.
10. De Smet I, Lau S, Mayer U, Jurgens G. Embryogenesis - the humble beginnings of plant life. Plant J 2010, 61: 959-970.
11. Peris CI, Rademacher EH, Weijers D. Green beginnings - pattern formation in the early plant embryo. Curr Top Dev Biol 2010, 91:1-27.
12. Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 2004, 131:657-668.
13. Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T. Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell 2008, 14:867-876.
14. Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jurgens G. The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell 2003, 112:219-230.
15. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M. Plant development is regulated by a family of auxin receptor F box proteins. Dev Cell 2005, 9: 109-119.
16. Szemenyei H, Hannon M, Long JA. TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science 2008, 319: 1384-1386.
17. Schlereth A, Moller B, Liu W, Kientz M, Flipse J, Rademacher EH, Schmid M, Jurgens G, Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010, 464:913-916.
18. Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jurgens G. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 2003, 426:147-153.
19. Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh YS, Amasino R, Scheres B. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 2004, 119:109-120.
20. Smith ZR, Long JA. Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 2010, 464:423-426.
21. Grigg SP, Galinha C, Kornet N, Canales C, Scheres B, Tsiantis M. Repression of apical homeobox genes is required for embryonic root development in Arabidopsis. Curr Biol 2009, 19:1485-1490.
22. Muller B, Sheen J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature 2008, 453:1094-1097.
23. Overvoorde P, Fukaki H, Beeckman T. Auxin control of root development. Cold Spring Harb Perspect Biol 2010, 2:a001537.
24. Bishopp A, Help H, Helaruitta Y. Cytokinin signalling during root development. Int Rev Cell Mol Biol 2009, 276:1-48.
25. Itoh H, Ueguchi-Tanaka M, Matsuoka M. Molecular biology of gibberellins signalling in higher plants. Int Rev Cell Mol Biol 2008, 268:191-221.
26. Petrasek J, Friml J. Auxin transport routes in plant development. Development 2009, 136:2675-2688.
27. Feraru E, Friml J. PIN polar targeting. Plant Physiol 2008, 147:1553-1559.
28. Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature 2005, 433: 39-44.
29. Grieneisen VA, Xu J, Maree AF, Hogeweg P, Scheres B. Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature 2007, 449:1008-1013.
30. Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk PB, Ljung K, Sandberg G, et al. A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science 2004, 306:862-865.
31. Friml J, Benkova E, Blilou I, Wisniewska J, Hamann T, Ljung K, Woody S, Sandberg G, Scheres B, Jurgens G, et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell 2002, 108: 661-673.
32. Muller A, Guan C, Galweiler L, Tanzler P, Huijser P, Marchant A, Parry G, Bennett M, Wisman E, Palme K. AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J 1998, 17:6903-6911.
33. Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature 2007, 449:1053-1057.
34. Di Laurenzio L, Wysocka-Diller J, Malamy JE, Pysh L, Helariutta Y, Freshour G, Hahn MG, Feldmann KA, Benfey PN. The SCARECROW gene regulates an asymmetric cell division that is essential for generating the radial organization of the Arabidopsis root. Cell 1996, 86:423-433.
35. Sabatini S, Heidstra R, Wildwater M, Scheres B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem. Genes Dev 2003, 17:354-358.
36. Moubayidin L, Di Mambro R, Sabatini S. Cytokinin-auxin crosstalk. Trends Plant Sci 2009, 14:557-562.
37. Nakajima K, Sena G, Nawy T, Benfey PN. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 2001, 413:307-311.
38. Ruzicka K, Simaskova M, Duclercq J, Petrasek J, Zazimalova E, Simon S, Friml J, Van Montagu MC, Benkova E. Cytokinin regulates root meristem activity via modulation of the polar auxin transport. Proc Natl Acad Sci U S A 2009, 106:4284-4289.
39. Ubeda-Tomas S, Swarup R, Coates J, Swarup K, Laplaze L, Beemster GT, Hedden P, Bhalerao R, Bennett MJ. Root growth in Arabidopsis requires gibberellin/DELLA signalling in the endodermis. Nat Cell Biol 2008, 10:625-628.
40. Ubeda-Tomas S, Federici F, Casimiro I, Beemster GT, Bhalerao R, Swarup R, Doerner P, Haseloff J, Bennett MJ. Gibberellin signaling in the endodermis controls Arabidopsis root meristem size. Curr Biol 2009, 19:1194-1199.
41. Achard P, Gusti A, Cheminant S, Alioua M, Dhondt S, Coppens F, Beemster GT, Genschik P. Gibberellin signaling controls cell proliferation rate in Arabidopsis. Curr Biol 2009, 19:1188-1193.
42. Hacham Y, Holland N, Butterfield C, Ubeda-Tomas S, Bennett MJ, Chory J, Savaldi-Goldstein S. Brassinosteroid perception in the epidermis controls root meristem size. Development 2010, 138:839-848.
43. Gonzalez-Garcia MP, Vilarrasa-Blasi J, Zhiponova M, Divol F, Mora-Garcia S, Russinova E, Cano-Delgado AI. Brassinosteroids control meristem size by promoting cell cycle progression in Arabidopsis roots. Development 2011, 138:849-859.
44. Stepanova AN, Yun J, Likhacheva AV, Alonso JM. Multilevel interactions between ethylene and auxin in Arabidopsis roots. Plant Cell 2007, 19:2169-2185.
45. Swarup R, Perry P, Hagenbeek D, Van Der Straeten D, Beemster GT, Sandberg G, Bhalerao R, Ljung K, Bennett MJ. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell 2007, 19:2186-2196.
46. Ortega-Martinez O, Pernas M, Carol RJ, Dolan L. Ethylene modulates stem cell division in the Arabidopsis thaliana root. Science 2007, 317:507-510.
47. Zhang H, Han W, De Smet I, Talboys P, Loya R, Hassan A, Rong H, Jurgens G, Paul Knox J, Wang MH. ABA promotes quiescence of the quiescent centre and suppresses stem cell differentiation in the Arabidopsis primary root meristem. Plant J 2010, 64:764-774.
48. Chuck G, Candela H, Hake S. Big impacts by small RNAs in plant development. Curr Opin Plant Biol 2009, 12:81-86.
49. Dolan L, Janmaat K, Willemsen V, Linstead P, Poethig S, Roberts K, Scheres B. Cellular organisation of the Arabidopsis thaliana root. Development 1993, 119: 71-84.
50. Mahonen AP, Bonke M, Kauppinen L, Riikonen M, Benfey PN, Helariutta Y. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev 2000, 14:2938-2943.
51. Ohashi-Ito K, Bergmann DC. Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. Development 2007, 134: 2959-2968.
52. Parizot B, Laplaze L, Ricaud L, Boucheron-Dubuisson E, Bayle V, De Smet I, Poethig SR, Helaruitta Y, Haseloff J, Chriqui D, et al. Diarch symmetry of the vascular bundle in Arabidopsis root encompasses the pericycle and is reflected in distich lateral root initiation. Plant Physiol 2008, 146:140-148.
53. Nawy T, Lee JY, Colinas J, Wang JY, Thongrod SC, Malamy JE, Birnbaum K, Benfey PN. Transcriptional profile of the Arabidopsis root quiescent center. Plant Cell 2005, 17:1908-1925.
54. Carlsbecker A, Lee JY, Roberts CJ, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno MA, Vaten A, Thitamadee S, et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 465:316-321.
55. Prigge MJ, Otsuga D, Alonso JM, Ecker JR, Drews GN, Clark SE. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 2005, 17:61-76.
56. Kubo M, Udagawa M, Nishikubo N, Horiguchi G, Yamaguchi M, Ito J, Mimura T, Fukuda H, Demura T. Transcription switches for protoxylem and metaxylem vessel formation. Genes Dev 2005, 19:1855-1860.
57. Yamaguchi M, Kubo M, Fukuda H, Demura T. Vascular-related NAC-DOMAIN7 is involved in the differentiation of all types of xylem vessels in Arabidopsis roots and shoots. Plant J 2008, 55:652-664.
58. Yamaguchi M, Mitsuda N, Ohtani M, Ohme-Takagi M, Kato K, Demura T. VASCULAR-RELATED NAC-DOMAIN7 directly regulates the expression of a broad range of genes for xylem vessel formation. Plant J 2010, 66:579-590.
59. Mahonen AP, Higuchi M, Tormakangas K, Miyawaki K, Pischke MS, Sussman MR, Helariutta Y, Kakimoto T. Cytokinins regulate a bidirectional phosphorelay network in Arabidopsis. Curr Biol 2006, 16: 1116-1122.
60. Bishopp A, Lehesranta S, Vaten A, Help H, El-Showk S, Scheres B, Helariutta K, Mahonen AP, Sakakibara H, Helariutta Y. Phloem-transported cytokinin regulates polar auxin transport and maintains vascular pattern in the root meristem. Curr Biol 2011, 21:927-932.
61. Bishopp A, Help H, El-Showk S, Weijers D, Scheres B, Friml J, Benkova E, Mahonen AP, Helariutta Y. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr Biol 2011, 21:917-926.
62. Bonke M, Thitamadee S, Mahonen AP, Hauser MT, Helariutta Y. APL regulates vascular tissue identity in Arabidopsis. Nature 2003, 426:181-186.
63. Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser MT, Benfey PN. The SHORT-ROOT gene controls radial patterning. Cell 2000, 101:555-567.
64. Cui H, Levesque MP, Vernoux T, Jung JW, Paquette AJ, Gallagher KL, Wang JY, Blilou I, Scheres B, Benfey PN. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 2007, 316:421-425.
65. Welch D, Hassan H, Blilou I, Immink R, Heidstra R, Scheres B. Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev 2007, 21:2196-2204.
66. Sozzani R, Cui H, Moreno-Risueno MA, Busch W, Van Norman JM, Vernoux T, Brady SM, Dewitte W, Murray JA, Benfey PN. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 2010, 466:128-132.
67. Schiefelbein J, Kwak SH, Wieckowski Y, Barron C, Bruex A. The gene regulatory network for root epidermal cell-type pattern formation in Arabidopsis. J Exp Bot 2009, 60:1515-1521.
68. Schellmann S, Hulskamp M, Uhrig J. Epidermal pattern formation in the root and shoot of Arabidopsis. Biochem Soc Trans 2007, 35:146-148.
69. Kwak SH, Shen R, Schiefelbein J. Positional signaling mediated by a receptor-like kinase in Arabidopsis. Science 2005, 307:1111-1113.
70. Kwak SH, Schiefelbein J. The role of the SCRAMBLED receptor-like kinase in patterning the Arabidopsis root epidermis. Dev Biol 2007, 302:118-131.
71. Yadav RK, Fulton L, Batoux M, Schneitz K. The Arabidopsis receptor-like kinase STRUBBELIG mediates inter-cell-layer signaling during floral development. Dev Biol 2008, 323:261-270.
72. Kwak SH, Schiefelbein J. A feedback mechanism controlling SCRAMBLED receptor accumulation and cell-type pattern in Arabidopsis. Curr Biol 2008, 18: 1949-1954.
73. Lee MM, Schiefelbein J. WEREWOLF, a MYB-related protein in Arabidopsis, is a position-dependent regulator of epidermal cell patterning. Cell 1999, 99: 473-483.
74. Payne CT, Zhang F, Lloyd AM. GL3 encodes a bHLH protein that regulates trichome development in Arabidopsis through interaction with GL1 and TTG1. Genetics 2000, 156:1349-1362.
75. Zhang F, Gonzalez A, Zhao M, Payne CT, Lloyd A. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development 2003, 130:4859-4869.
76. Bernhardt C, Lee MM, Gonzalez A, Zhang F, Lloyd A, Schiefelbein J. The bHLH GLABRA3 (GL3) and ENHANCER OF GLABRA3 (EGL3) specify epidermal cell fate in the Arabidopsis root. Development 2003, 130:6431-6439.
77. Lee MM, Schiefelbein J. Cell pattern in the Arabidopsis root epidermis determined by lateral inhibition with feedback. Plant Cell 2002, 14:611-618.
78. Ryu KH, Kang YH, Park YH, Hwang I, Schiefelbein J, Lee MM. The WEREWOLF MYB protein directly regulates CAPRICE transcription during cell fate specification in the Arabidopsis root epidermis. Development 2005, 132:4765-4775.
79. Koshino-Kimura Y, Wada T, Tachibana T, Tsugeki R, Ishiguro S, Okada K. Regulation of CAPRICE transcription by MYB proteins for root epidermis differentiation in Arabidopsis. Plant Cell Physiol 2005, 46: 817-826.
80. Kurata T. Cell-to-cell movement of the CAPRICE protein in Arabidopsis root epidermal cell differentiation. Development 2005, 132:5387-5398.
81. Kirik V, Simon M, Huelskamp M, Schiefelbein J. The ENHANCER OF TRY AND CPC1 gene acts redundantly with TRIPTYCHON and CAPRICE in trichome and root hair cell patterning in Arabidopsis. Dev Biol 2004, 268:506-513.
82. Schellmann S, Schnittger A, Kirik V, Wada T, Okada K, Beermann A, Thumfahrt J, Jurgens G, Hulskamp M. TRIPTYCHON and CAPRICE mediate lateral inhibition during trichome and root hair patterning in Arabidopsis. EMBO J 2002, 21:5036-5046.
83. Simon M, Lee MM, Lin Y, Gish L, Schiefelbein J. Distinct and overlapping roles of single-repeat MYB genes in root epidermal patterning. Dev Biol 2007, 311:566-578.
84. Wada T, Tachibana T, Shimura Y, Okada K. Epidermal cell differentiation in Arabidopsis determined by a Myb homolog, CPC. Science 1997, 277:1113-1116.
85. Ohashi Y, Oka A, Rodrigues-Pousada R, Possenti M, Ruberti I, Morelli G, Aoyama T. Modulation of phospholipid signalling by GLABRA2 in root-hair pattern formation. Science 2003, 300:1427-1430.
86. Willemsen V, Bauch M, Bennett T, Campilho A, Wolkenfelt H, Xu J, Haseloff J, Scheres B. The NAC domain transcription factors FEZ and SOMBRERO control the orientation of cell division plane in Arabidopsis root stem cells. Dev Cell 2008, 15:913-922.
87. Bennett T, van den Toorn A, Sanchez-Perez GF, Campilho A, Willemsen V, Snel B, Scheres B. SOMBRERO, BEARSKIN1, and BEARSKIN2 regulate root cap maturation in Arabidopsis. Plant Cell 2010, 22: 640-654.
88. Wildwater M, Campilho A, Perez-Perez JM, Heidstra R, Blilou I, Korthout H, Chatterjee J, Mariconti L, Gruissem W, Scheres B. The RETINOBLASTOMA-RELATED gene regulates stem cell maintenance in Arabidopsis roots. Cell 2005, 123:1337-1349.
89. Wachsman G, Heidstra R, Scheres B. Distinct cell-autonomous functions of RETINOBLASTOMA-RELATED in Arabidopsis stem cells revealed by the brother of brainbow clonal analysis system. Plant Cell 2011, 23:2581-2591.
90. Phytohormones teaching tools (http://www.plantcell.org/site/teachingtools/TTPB6.xhtml)
91. Small RNAs teaching tools (http://www.plantcell.org/site/teachingtools/TTPB5.xhtml)