Transcriptional Switches Direct Plant Organ Formation and Patterning

Current Topics in Developmental Biology

Volumn 98, Issue , 2012, Pages 229-257

  Moreno Risueno, Miguel A ^a   Van Norman, Jaimie M ^a   Benfey, Philip N ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Arabidopsis; Asymmetric cell division; Biological clock; Cell fate specification; Organ patterning; Oscillating gene expression; Stem cells; Transcriptional regulation

Indexed keywords

EID: 84856416305     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-386499-4.00009-4     Document Type: Chapter

References (71)

1. Agusti J., Lichtenberger R., Schwarz M., Nehlin L., Greb T. Characterization of transcriptome remodeling during cambium formation identifies MOL1 and RUL1 as opposing regulators of secondary growth. PLoS Genet. 2011, 7:e1001312.
2. Aida M., Beis D., Heidstra R., Willemsen V., Blilou I., Galinha C., Nussaume L., Noh Y.S., Amasino R., Scheres B. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell 2004, 119:109-120.
3. Benfey P.N., Linstead P.J., Roberts K., Schiefelbein J.W., Hauser M.T., Aeschbacher R.A. Root development in Arabidopsis: Four mutants with dramatically altered root morphogenesis. Development 1993, 119:57-70.
4. Bishopp A., Help H., El-Showk S., Weijers D., Scheres B., Friml J., Benkova E., Mahonen A.P., Helariutta Y. A mutually inhibitory interaction between auxin and cytokinin specifies vascular pattern in roots. Curr. Biol. 2011, 21:917-926.
5. Bishopp A., Lehesranta S., Vaten A., Help H., El-Showk S., Scheres B., Helariutta K., Mahonen A.P., 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.
6. Brady S.M., Orlando D.A., Lee J.Y., Wang J.Y., Koch J., Dinneny J.R., Mace D., Ohler U., Benfey P.N. A high-resolution root spatiotemporal map reveals dominant expression patterns. Science 2007, 318:801-806.
7. 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.
8. Cano-Delgado A., Lee J.Y., Demura T. Regulatory mechanisms for specification and patterning of plant vascular tissues. Annu. Rev. Cell Dev. Biol. 2010, 26:605-637.
9. Carlsbecker A., Lee J.Y., Roberts C.J., Dettmer J., Lehesranta S., Zhou J., Lindgren O., Moreno-Risueno M.A., Vaten A., Thitamadee S., et al. Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature 2010, 465:316-321.
10. Cooke J., Zeeman E.C. A clock and wavefront model for control of the number of repeated structures during animal morphogenesis. J. Theor. Biol. 1976, 58:455-476.
11. Cui H., Levesque M.P., Vernoux T., Jung J.W., Paquette A.J., Gallagher K.L., Wang J.Y., Bilou I., Scheres B., Benfey P.N. An evolutionarily conserved mechanism delimiting SHR movement defines a single layer of endodermis in plants. Science 2007, 316:421-425.
12. De Rybel B., Vassileva V., Parizot B., Demeulenaere M., Grunewald W., Audenaert D., Van Campenhout J., Overvoorde P., Jansen L., Vanneste S., et al. A novel aux/IAA28 signaling cascade activates GATA23-dependent specification of lateral root founder cell identity. Curr. Biol. 2010, 20:1697-1706.
13. De Smet I., Tetsumura T., De Rybel B., Frey N.F., Laplaze L., Casimiro I., Swarup R., Naudts M., Vanneste S., Audenaert D., et al. Auxin-dependent regulation of lateral root positioning in the basal meristem of Arabidopsis. Development 2007, 134:681-690.
14. Di Laurenzio L., Wysocka-Diller J., Malamy J.E., Pysh L., Helariutta Y., Freshour G., Hahn M.G., Feldmann K.A., Benfey P.N. 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.
15. 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.
16. Donner T.J., Sherr I., Scarpella E. Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 2009, 136:3235-3246.
17. Dreher K.A., Brown J., Saw R.E., Callis J. The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. Plant Cell 2006, 18:699-714.
18. Engstrom E.M., Izhaki A., Bowman J.L. Promoter bashing, microRNAs, and Knox genes. New insights, regulators, and targets-of-regulation in the establishment of lateral organ polarity in Arabidopsis. Plant Physiol. 2004, 135:685-694.
19. Esau K. Anatomy of Seed Plants 1977, Wiley, New York.
20. Faure J.E., Rotman N., Fortune P., Dumas C. Fertilization in Arabidopsis thaliana wild type: Developmental stages and time course. Plant J. 2002, 30:481-488.
21. 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.
22. 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.
23. Gallagher K.L., Benfey P.N. Both the conserved GRAS domain and nuclear localization are required for SHORT-ROOT movement. Plant J. 2009, 57:785-797.
24. Gallagher K.L., Paquette A.J., Nakajima K., Benfey P.N. Mechanisms regulating SHORT-ROOT intercellular movement. Curr. Biol. 2004, 14:1847-1851.
25. Galweiler L., Guan C., Muller A., Wisman E., Mendgen K., Yephremov A., Palme K. Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 1998, 282:2226-2230.
26. Goldbeter A., Gonze D., Pourquie O. Sharp developmental thresholds defined through bistability by antagonistic gradients of retinoic acid and FGF signaling. Dev. Dyn. 2007, 236:1495-1508.
27. 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.
28. Hamant O., Heisler M.G., Jonsson H., Krupinski P., Uyttewaal M., Bokov P., Corson F., Sahlin P., Boudaoud A., Meyerowitz E.M., et al. Developmental patterning by mechanical signals in Arabidopsis. Science 2008, 322:1650-1655.
29. Hamant O., Traas J., Boudaoud A. Regulation of shape and patterning in plant development. Curr. Opin. Genet. Dev. 2010, 20:454-459.
30. Heidstra R., Welch D., Scheres B. Mosaic analyses using marked activation and deletion clones dissect Arabidopsis SCARECROW action in asymmetric cell division. Genes Dev. 2004, 18:1964-1969.
31. Heisler M.G., Ohno C., Das P., Sieber P., Reddy G.V., Long J.A., Meyerowitz E.M. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr. Biol. 2005, 15:1899-1911.
32. Heisler M.G., Hamant O., Krupinski P., Uyttewaal M., Ohno C., Jonsson H., Traas J., Meyerowitz E.M. Alignment between PIN1 polarity and microtubule orientation in the shoot apical meristem reveals a tight coupling between morphogenesis and auxin transport. PLoS Biol. 2010, 8:e1000516.
33. Helariutta Y., Fukaki H., Wysocka-Diller J., Nakajima K., Jung J.W., Sena G., Hauser M.-T., Benfey P.N. The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell 2000, 101:555-567.
34. Hirakawa Y., Kondo Y., Fukuda H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis. Plant Cell 2010, 22:2618-2629.
35. Hirakawa Y., Kondo Y., Fukuda H. Establishment and maintenance of vascular cell communities through local signaling. Curr. Opin. Plant Biol. 2011, 14:17-23.
36. Ilegems M., Douet V., Meylan-Bettex M., Uyttewaal M., Brand L., Bowman J.L., Stieger P.A. Interplay of auxin, KANADI and Class III HD-ZIP transcription factors in vascular tissue formation. Development 2010, 137:975-984.
37. Jenik P.D., Gillmor C.S., Lukowitz W. Embryonic patterning in Arabidopsis thaliana. Annu. Rev. Cell Dev. Biol. 2007, 23:207-236.
38. Jurgens G. Apical-basal pattern formation in Arabidopsis embryogenesis. EMBO J. 2001, 20:3609-3616.
39. Krol A.J., Roellig D., Dequeant M.L., Tassy O., Glynn E., Hattem G., Mushegian A., Oates A.C., Pourquie O. Evolutionary plasticity of segmentation clock networks. Development 2011, 138:2783-2792.
40. 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.
41. Levesque M.P., Vernoux T., Busch W., Cui H., Wang J.Y., Bilou I., Hassan H., Nakajima K., Matsumoto N., Lohmann J.U., et al. Whole-genome analysis of the SHORT-ROOT developmental pathway in Arabidopsis. PLoS Biol. 2006, 4:e143.
42. Leyser O. Dynamic integration of auxin transport and signalling. Curr. Biol. 2006, 16:R424-R433.
43. Long J.A., Woody S., Poethig S., Meyerowitz E.M., Barton M.K. Transformation of shoots into roots in Arabidopsis embryos mutant at the TOPLESS locus. Development 2002, 129:2797-2806.
44. Long J.A., Ohno C., Smith Z.R., Meyerowitz E.M. TOPLESS regulates apical embryonic fate in Arabidopsis. Science 2006, 312:1520-1523.
45. Lukowitz W., Roeder A., Parmenter D., Somerville C. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 2004, 116:109-119.
46. Mahonen A.P., Bonke M., Kauppinen L., Riikonen M., Benfey P.N., Helariutta Y. A novel two-component hybrid molecule regulates vascular morphogenesis of the Arabidopsis root. Genes Dev. 2000, 14:2938-2943.
47. Mahonen A.P., Bishopp A., Higuchi M., Nieminen K.M., Kinoshita K., Tormakangas K., Ikeda Y., Oka A., Kakimoto T., Helariutta Y. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science 2006, 311:94-98.
48. Miyashima S., Koi S., Hashimoto T., Nakajima K. Non-cell-autonomous microRNA165 acts in a dose-dependent manner to regulate multiple differentiation status in the Arabidopsis root. Development 2011, 138:2303-2313.
49. Moreno-Risueno M.A., Benfey P.N. Time-based patterning in development: The role of oscillating gene expression. Transcription 2011, 2:124-129.
50. Moreno-Risueno M.A., Van Norman J.M., Moreno A., Zhang J., Ahnert S.E., Benfey P.N. Oscillating gene expression determines competence for periodic Arabidopsis root branching. Science 2010, 329:1306-1311.
51. Nakajima K., Sena G., Nawy T., Benfey P.N. Intercellular movement of the putative transcription factor SHR in root patterning. Nature 2001, 413:307-311.
52. Ohashi-Ito K., Fukuda H. Transcriptional regulation of vascular cell fates. Curr. Opin. Plant Biol. 2010, 13:670-676.
53. Ohashi-Ito K., Oda Y., Fukuda H. Arabidopsis VASCULAR-RELATED NAC-DOMAIN6 directly regulates the genes that govern programmed cell death and secondary wall formation during xylem differentiation. Plant Cell 2010, 22:3461-3473.
54. Petersson S.V., Johansson A.I., Kowalczyk M., Makoveychuk A., Wang J.Y., Moritz T., Grebe M., Benfey P.N., Sandberg G., Ljung K. An auxin gradient and maximum in the Arabidopsis root apex shown by high-resolution cell-specific analysis of IAA distribution and synthesis. Plant Cell 2009, 21:1659-1668.
55. Petrasek J., Mravec J., Bouchard R., Blakeslee J.J., Abas M., Seifertova D., Wisniewska J., Tadele Z., Kubes M., Covanova M., et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science 2006, 312:914-918.
56. Petricka J.J., Van Norman J.M., Benfey P.N. Symmetry breaking in plants: Molecular mechanisms regulating asymmetric cell divisions in Arabidopsis. Cold Spring Harb. Perspect. Biol. 2009, 1:a000497.
57. Prigge M.J., Otsuga D., Alonso J.M., Ecker J.R., Drews G.N., Clark S.E. Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell 2005, 17:61-76.
58. Pysh L.D., Wysocka-Diller J.W., Camilleri C., Bouchez D., Benfey P.N. The GRAS gene family in Arabidopsis: Sequence characterization and basic expression analysis of the SCARECROW-LIKE genes. Plant J. 1999, 18:111-119.
59. Reinhardt D., Pesce E.R., Stieger P., Mandel T., Baltensperger K., Bennett M., Traas J., Friml J., Kuhlemeier C. Regulation of phyllotaxis by polar auxin transport. Nature 2003, 426:255-260.
60. Rogg L.E., Lasswell J., Bartel B. A gain-of-function mutation in IAA28 suppresses lateral root development. Plant Cell 2001, 13:465-480.
61. Scheres B., Wolkenfelt H., Willemsen V., Terlouw M., Lawson E., Dean C., Weisbeek P. Embryonic origin of the Arabidopsis primary root and root meristem initials. Development 1994, 120:2475-2487.
62. Schlereth A., Moller B., Liu W., Kientz M., Flipse J., Rademacher E.H., Schmid M., Jurgens G., Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature 2010, 464:913-916.
63. Sena G., Jung J.W., Benfey P.N. A broad competence to respond to SHORT ROOT revealed by tissue-specific ectopic expression. Development 2004, 131:2817-2826.
64. Smith Z.R., Long J.A. Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature 2010, 464:423-426.
65. Soyano T., Thitamadee S., Machida Y., Chua N.H. ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. Plant Cell 2008, 20:3359-3373.
66. Sozzani R., Cui H., Moreno-Risueno M.A., Busch W., Van Norma J.M., Vernoux T., Brady S.M., Dewitte W., Murray J.A.H., Benfey P.N. Spatiotemporal regulation of cell-cycle genes by SHORTROOT links patterning and growth. Nature 2010, 466:128-132.
67. Ueda M., Zhang Z., Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev. Cell 2011, 20:264-270.
68. 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.
69. Wu X., Chory J., Weigel D. Combinations of WOX activities regulate tissue proliferation during Arabidopsis embryonic development. Dev. Biol. 2007, 309:306-316.
70. 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. 2011, 66:579-590.
71. Zhang J., Elo A., Helariutta Y. Arabidopsis as a model for wood formation. Curr. Opin. Biotechnol. 2011, 22:293-299.