Emerging Role of the Ubiquitin Proteasome System in the Control of Shoot Apical Meristem Function

Journal of Integrative Plant Biology

Volumn 55, Issue 1, 2013, Pages 7-20

  Di Giacomo, Elisabetta ^a   Serino, Giovanna ^b,c   Frugis, Giovanna ^a  

^a CNR   (Italy)

^b SAPIENZA UNIVERSITY OF ROME   (Italy)

^c NEW YORK BOTANICAL GARDEN   (United States)

Author keywords

Arabidopsis thaliana; Cell differentiation; Protein degradation; Shoot apical meristem; Ubiquitin 26S proteasome system

Indexed keywords

PROTEASOME; UBIQUITIN;

ANGIOSPERM; APICAL DOMINANCE; CYTOLOGY; EMBRYONIC DEVELOPMENT; PROTEIN;

ARTICLE; MERISTEM; PHYSIOLOGY;

MERISTEM; PROTEASOME ENDOPEPTIDASE COMPLEX; UBIQUITIN;

ARABIDOPSIS THALIANA;

EID: 84872823215     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12010     Document Type: Article

References (112)

1. Aguilar-Henonin L, Bravo J, Guzman P (2006) Genetic interactions of a putative Arabidopsis thaliana ubiquitin-ligase with components of the Saccharomyces cerevisiae ubiquitination machinery. Curr. Genet. 50, 257-268.
2. Aida M, Ishida T, Fukaki H, Fujisawa H, Tasaka M (1997) Genes involved in organ separation in Arabidopsis: An analysis of the cup-shaped cotyledon mutant. Plant Cell 9, 841-857.
3. Ariizumi T, Lawrence PK, Steber CM (2011) The role of two f-box proteins, SLEEPY1 and SNEEZY, in Arabidopsis gibberellin signaling. Plant Physiol. 155, 765-775.
4. Barton MK (2010) Twenty years on: The inner workings of the shoot apical meristem, a developmental dynamo. Dev. Biol. 341, 95-113.
5. Bernhardt A, Lechner E, Hano P, Schade V, Dieterle M, Anders M, Dubin MJ, Benvenuto G, Bowler C, Genschik P, Hellmann H (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J. 47, 591-603.
6. Byrne ME, Barley R, Curtis M, Arroyo JM, Dunham M, Hudson A, Martienssen RA (2000) Asymmetric leaves1 mediates leaf patterning and stem cell function in Arabidopsis. Nature 408, 967-971.
7. Causier B, Ashworth M, Guo W, Davies B (2012) The TOPLESS interactome: A framework for gene repression in Arabidopsis. Plant Physiol 158, 423-438.
8. Chen D, Molitor A, Liu C, Shen WH (2010) The Arabidopsis PRC1-like ring-finger proteins are necessary for repression of embryonic traits during vegetative growth. Cell Res. 20, 1332-1344.
9. Chen H, Shen Y, Tang X, Yu L, Wang J, Guo L, Zhang Y, Zhang H, Feng S, Strickland E, Zheng N, Deng XW (2006) Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18, 1991-2004.
10. Cho SK, Ryu MY, Song C, Kwak JM, Kim WT (2008) Arabidopsis PUB22 and PUB23 are homologous U-Box E3 ubiquitin ligases that play combinatory roles in response to drought stress. Plant Cell 20, 1899-1914.
11. Chung K, Tasaka M (2011) RPT2a, a 26S proteasome AAA-ATPase, is directly involved in Arabidopsis CC-NBS-LRR protein uni-1D-induced signaling pathways. Plant Cell Physiol. 52, 1657-1664.
12. Clark SE, Jacobsen SE, Levin JZ, Meyerowitz EM (1996) The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development 122, 1567-1575.
13. Coates JC, Laplaze L, Haseloff J (2006) Armadillo-related proteins promote lateral root development in Arabidopsis. Proc. Natl. Acad. Sci. USA 103, 1621-1626.
14. Consortium AIM (2011) Evidence for network evolution in an Arabidopsis interactome map. Science 333, 601-607.
15. Deng XW, Matsui M, Wei N, Wagner D, Chu AM, Feldmann KA, Quail PH (1992) COP1, an Arabidopsis regulatory gene, encodes a protein with both a zinc-binding motif and a G beta homologous domain. Cell 71, 791-801.
16. Deshaies RJ, Joazeiro CA (2009) RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 78, 399-434.
17. Dharmasiri N, Dharmasiri S, Weijers D, Lechner E, Yamada M, Hobbie L, Ehrismann JS, Jurgens G, Estelle M (2005) Plant development is regulated by a family of auxin receptor F box proteins. Dev. Cell 9, 109-119.
18. Disch S, Anastasiou E, Sharma VK, Laux T, Fletcher JC, Lenhard M (2006) The E3 ubiquitin ligase BIG BROTHER controls Arabidopsis organ size in a dosage-dependent manner. Curr. Biol. 16, 272-279.
19. Elo A, Immanen J, Nieminen K, Helariutta Y (2009) Stem cell function during plant vascular development. Semin. Cell Dev. Biol. 20, 1097-1106.
20. Endrizzi K, Moussian B, Haecker A, Levin JZ, Laux T (1996) The SHOOT MERISTEMLESS gene is required for maintenance of undifferentiated cells in Arabidopsis shoot and floral meristems and acts at a different regulatory level than the meristem genes WUSCHEL and ZWILLE. Plant J. 10, 967-979.
21. Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99, 199-209.
22. Feldman RM, Correll CC, Kaplan KB, Deshaies RJ (1997) A complex of Cdc4p, Skp1p, and Cdc53p/cullin catalyzes ubiquitination of the phosphorylated CDK inhibitor Sic1p. Cell 91, 221-230.
23. Figueroa P, Gusmaroli G, Serino G, Habashi J, Ma L, Shen Y, Feng S, Bostick M, Callis J, Hellmann H, Deng XW (2005) Arabidopsis has two redundant Cullin3 proteins that are essential for embryo development and that interact with RBX1 and BTB proteins to form multisubunit E3 ubiquitin ligase complexes in vivo. Plant Cell 17, 1180-1195.
24. Freemont PS, Hanson IM, Trowsdale J (1991) A novel cysteine-rich sequence motif. Cell 64, 483-484.
25. Frugis G, Giannino D, Mele G, Nicolodi C, Chiappetta A, Bitonti MB, Innocenti AM, Dewitte W, Van Onckelen H, Mariotti D (2001) Overexpression of KNAT1 in lettuce shifts leaf determinate growth to a shoot-like indeterminate growth associated with an accumulation of isopentenyl-type cytokinins. Plant Physiol. 126, 1370-1380.
26. Furutani M, Kajiwara T, Kato T, Treml BS, Stockum C, Torres-Ruiz RA, Tasaka M (2007) The gene MACCHI-BOU 4/ENHANCER OF PINOID encodes a NPH3-like protein and reveals similarities between organogenesis and phototropism at the molecular level. Development 134, 3849-3859.
27. Galinha C, Bilsborough G, Tsiantis M (2009) Hormonal input in plant meristems: A balancing act. Semin. Cell Dev. Biol. 20, 1149-1156.
28. Gilkerson J, Hu J, Brown J, Jones A, Sun TP, Callis J (2009) Isolation and characterization of cul1-7, a recessive allele of CULLIN1 that disrupts SCF function at the C terminus of CUL1 in Arabidopsis thaliana. Genetics 181, 945-963.
29. Gingerich DJ, Gagne JM, Salter DW, Hellmann H, Estelle M, Ma L, Vierstra RD (2005) Cullins 3a and 3b assemble with members of the broad complex/tramtrack/bric-a-brac (BTB) protein family to form essential ubiquitin-protein ligases (E3s) in Arabidopsis. J. Biol. Chem. 280, 18810-18821.
30. Glickman MH, Ciechanover A (2002) The ubiquitin-proteasome proteolytic pathway: Destruction for the sake of construction. Physiol. Rev. 82, 373-428.
31. Gray WM, Hellmann H, Dharmasiri S, Estelle M (2002) Role of the Arabidopsis RING-H2 protein RBX1 in RUB modification and SCF function. Plant Cell 14, 2137-2144.
32. Greve K, La Cour T, Jensen MK, Poulsen FM, Skriver K (2003) Interactions between plant RING-H2 and plant-specific NAC (NAM/ATAF1/2/CUC2) proteins: RING-H2 molecular specificity and cellular localization. Biochem J. 371, 97-108.
33. Ha CM, Jun JH, Nam HG, Fletcher JC (2007) BLADE-ON-PETIOLE 1 and 2 control Arabidopsis lateral organ fate through regulation of LOB domain and adaxial-abaxial polarity genes. Plant Cell 19, 1809-1825.
34. Ha CM, Kim GT, Kim BC, Jun JH, Soh MS, Ueno Y, Machida Y, Tsukaya H, Nam HG (2003) The BLADE-ON-PETIOLE 1 gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130, 161-172.
35. Hareven D, Gutfinger T, Parnis A, Eshed Y, Lifschitz E (1996) The making of a compound leaf: Genetic manipulation of leaf architecture in tomato. Cell 84, 735-744.
36. Hay A, Tsiantis M (2010) KNOX genes: Versatile regulators of plant development and diversity. Development 137, 3153-3165.
37. Higa LA, Wu M, Ye T, Kobayashi R, Sun H, Zhang H (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat. Cell Biol. 8, 1277-1283.
38. Hua Z, Vierstra RD (2011) The cullin-RING ubiquitin-protein ligases. Annu. Rev. Plant Biol. 62, 299-334.
39. Huang W, Huang H (2007) A novel function of the 26S proteasome in repressing class-1 KNOX genes during leaf development. Plant Signal. Behav. 2, 25-27.
40. Huang W, Pi L, Liang W, Xu B, Wang H, Cai R, Huang H (2006) The proteolytic function of the Arabidopsis 26S proteasome is required for specifying leaf adaxial identity. Plant Cell 18, 2479-2492.
41. Husbands AY, Chitwood DH, Plavskin Y, Timmermans MC (2009) Signals and prepatterns: New insights into organ polarity in plants. Genes Dev. 23, 1986-1997.
42. Igari K, Endo S, Hibara K, Aida M, Sakakibara H, Kawasaki T, Tasaka M (2008) Constitutive activation of a CC-NB-LRR protein alters morphogenesis through the cytokinin pathway in Arabidopsis. Plant J. 55, 14-27.
43. Iwakawa H, Ueno Y, Semiarti E, Onouchi H, Kojima S, Tsukaya H, Hasebe M, Soma T, Ikezaki M, Machida C, Machida Y (2002) The ASYMMETRIC LEAVES2 gene of Arabidopsis thaliana, required for formation of a symmetric flat leaf lamina, encodes a member of a novel family of proteins characterized by cysteine repeats and a leucine zipper. Plant Cell Physiol. 43, 467-478.
44. Jasinski S, Piazza P, Craft J, Hay A, Woolley L, Rieu I, Phillips A, Hedden P, Tsiantis M (2005) KNOX action in Arabidopsis is mediated by coordinate regulation of cytokinin and gibberellin activities. Curr. Biol. 15, 1560-1565.
45. Kieffer M, Stern Y, Cook H, Clerici E, Maulbetsch C, Laux T, Davies B (2006) Analysis of the transcription factor WUSCHEL and its functional homologue in Antirrhinum reveals a potential mechanism for their roles in meristem maintenance. Plant Cell 18, 560-573.
46. Kraft E, Bostick M, Jacobsen SE, Callis J (2008) ORTH/VIM proteins that regulate DNA methylation are functional ubiquitin E3 ligases. Plant J. 56, 704-715.
47. Laney JD, Hochstrasser M (2011) Analysis of protein ubiquitination. Curr Protoc. Protein Sci. 66, 14.5.1-14.5.13.
48. Laux T, Mayer KF, Berger J, Jurgens G (1996) The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122, 87-96.
49. Lechner E, Goloubinoff P, Genschik P, Shen WH (2002) A gene trap Dissociation insertion line, associated with a RING-H2 finger gene, shows tissue specific and developmental regulated expression of the gene in Arabidopsis. Gene 290, 63-71.
50. Lee JH, Terzaghi W, Gusmaroli G, Charron JB, Yoon HJ, Chen H, He YJ, Xiong Y, Deng XW (2008) Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 20, 152-167.
51. Leibfried A, To JP, Busch W, Stehling S, Kehle A, Demar M, Kieber JJ, Lohmann JU (2005) WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators. Nature 438, 1172-1175.
52. Levin JZ, Meyerowitz EM (1995) UFO: An Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell 7, 529-548.
53. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of 118 Arabidopsis transcription factor and 30 ubiquitin-ligase genes responding to chitin, a plant-defense elicitor. Mol. Plant Microbe Interact. 20, 900-911.
54. Lin SS, Martin R, Mongrand S, Vandenabeele S, Chen KC, Jang IC, Chua NH (2008) RING1 E3 ligase localizes to plasma membrane lipid rafts to trigger FB1-induced programmed cell death in Arabidopsis. Plant J. 56, 550-561.
55. Liu L, Zhang Y, Tang S, Zhao Q, Zhang Z, Zhang H, Dong L, Guo H, Xie Q (2010) An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. Plant J. 61, 893-903.
56. Long JA, Barton MK (1998) The development of apical embryonic pattern in Arabidopsis. Development 125, 3027-3035.
57. Long JA, Ohno C, Smith ZR, Meyerowitz EM (2006) TOPLESS regulates apical embryonic fate in Arabidopsis. Science 312, 1520-1523.
58. Luo G, Gu H, Liu J, Qu LJ (2012) Four closely-related RING-type E3 ligases, APD1-4, are involved in pollen mitosis II regulation in Arabidopsis. J. Integr. Plant Biol. 54, 814-827.
59. Mayer U, Jurgens G (1998) Pattern formation in plant embryogenesis: A reassessment. Semin. Cell Dev. Biol. 9, 187-193.
60. Mazzucotelli E, Belloni S, Marone D, De Leonardis A, Guerra D, Di Fonzo N, Cattivelli L, Mastrangelo A (2006) The E3 ubiquitin ligase gene family in plants: Regulation by degradation. Curr. Genomics 7, 509-522.
61. Mohd-Sarip A, Lagarou A, Doyen CM, van der Knaap JA, Aslan U, Bezstarosti K, Yassin Y, Brock HW, Demmers JA, Verrijzer CP (2012) Transcription-independent function of polycomb group protein PSC in cell cycle control. Science 336, 744-747.
62. Molinier J, Lechner E, Dumbliauskas E, Genschik P (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet. 4, e1000093.
63. Moon J, Zhao Y, Dai X, Zhang W, Gray WM, Huq E, Estelle M (2007) A new CULLIN 1 mutant has altered responses to hormones and light in Arabidopsis. Plant Physiol. 143, 684-696.
64. Mudgil Y, Shiu SH, Stone SL, Salt JN, Goring DR (2004) A large complement of the predicted Arabidopsis ARM repeat proteins are members of the U-box E3 ubiquitin ligase family. Plant Physiol. 134, 59-66.
65. Ohtsubo M, Yasunaga S, Ohno Y, Tsumura M, Okada S, Ishikawa N, Shirao K, Kikuchi A, Nishitani H, Kobayashi M, Takihara Y (2008) Polycomb-group complex 1 acts as an E3 ubiquitin ligase for geminin to sustain hematopoietic stem cell activity. Proc. Natl. Acad. Sci. USA 105, 10396-10401.
66. Perales M, Reddy GV (2012) Stem cell maintenance in shoot apical meristems. Curr. Opin. Plant Biol. 15, 10-16.
67. Petroski MD, Deshaies RJ (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat. Rev. Mol. Cell Biol. 6, 9-20.
68. Phelps-Durr TL, Thomas J, Vahab P, Timmermans MC (2005) Maize rough sheath2 and its Arabidopsis orthologue ASYMMETRIC LEAVES1 interact with HIRA, a predicted histone chaperone, to maintain knox gene silencing and determinacy during organogenesis. Plant Cell 17, 2886-2898.
69. Qin F, Sakuma Y, Tran LS, Maruyama K, Kidokoro S, Fujita Y, Fujita M, Umezawa T, Sawano Y, Miyazono K, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20, 1693-1707.
70. Rast MI, Simon R (2012) Arabidopsis JAGGED LATERAL ORGANS acts with ASYMMETRIC LEAVES2 to coordinate KNOX and PIN expression in shoot and root meristems. Plant Cell 24, 2917-2933.
71. Reinhardt D, Mandel T, Kuhlemeier C (2000) Auxin regulates the initiation and radial position of plant lateral organs. Plant Cell 12, 507-518.
72. Reinhardt D, Pesce ER, Stieger P, Mandel T, Baltensperger K, Bennett M, Traas J, Friml J, Kuhlemeier C (2003) Regulation of phyllotaxis by polar auxin transport. Nature 426, 255-260.
73. Ren C, Pan J, Peng W, Genschik P, Hobbie L, Hellmann H, Estelle M, Gao B, Peng J, Sun C, Xie D (2005) Point mutations in Arabidopsis Cullin1 reveal its essential role in jasmonate response. Plant J. 42, 514-524.
74. Roberts D, Pedmale UV, Morrow J, Sachdev S, Lechner E, Tang X, Zheng N, Hannink M, Genschik P, Liscum E (2011) Modulation of phototropic responsiveness in Arabidopsis through ubiquitination of phototropin 1 by the CUL3-Ring E3 ubiquitin ligase CRL3(NPH3). Plant Cell 23, 3627-3640.
75. Rochon A, Boyle P, Wignes T, Fobert PR, Despres C (2006) The coactivator function of Arabidopsis NPR1 requires the core of its BTB/POZ domain and the oxidation of C-terminal cysteines. Plant Cell 18, 3670-3685.
76. Roeder AH, Tarr PT, Tobin C, Zhang X, Chickarmane V, Cunha A, Meyerowitz EM (2011) Computational morphodynamics of plants: Integrating development over space and time. Nat. Rev. Mol. Cell Biol. 12, 265-273.
77. Sadanandom A, Bailey M, Ewan R, Lee J, Nelis S (2012) The ubiquitin-proteasome system: Central modifier of plant signalling. New Phytol. 196, 13-28.
78. Santner A, Estelle M (2010) The ubiquitin-proteasome system regulates plant hormone signaling. Plant J. 61, 1029-1040.
79. Sassi M, Lu Y, Zhang Y, Wang J, Dhonukshe P, Blilou I, Dai M, Li J, Gong X, Jaillais Y, Yu X, Traas J, Ruberti I, Wang H, Scheres B, Vernoux T, Xu J (2012) COP1 mediates the coordination of root and shoot growth by light through modulation of PIN1- and PIN2-dependent auxin transport in Arabidopsis. Development 139, 3402-3412.
80. Sato T, Maekawa S, Yasuda S, Sonoda Y, Katoh E, Ichikawa T, Nakazawa M, Seki M, Shinozaki K, Matsui M, Goto DB, Ikeda A, Yamaguchi J (2009) CNI1/ATL31, a RING-type ubiquitin ligase that functions in the carbon/nitrogen response for growth phase transition in Arabidopsis seedlings. Plant J. 60, 852-864.
81. Sawa S, Watanabe K, Goto K, Liu YG, Shibata D, Kanaya E, Morita EH, Okada K (1999) FILAMENTOUS FLOWER, a meristem and organ identity gene of Arabidopsis, encodes a protein with a zinc finger and HMG-related domains. Genes Dev. 13, 1079-1088.
82. Shen WH, Parmentier Y, Hellmann H, Lechner E, Dong A, Masson J, Granier F, Lepiniec L, Estelle M, Genschik P (2002) Null mutation of AtCUL1 causes arrest in early embryogenesis in Arabidopsis. Mol. Biol. Cell 13, 1916-1928.
83. Shen WH, Xu L (2009) Chromatin remodeling in stem cell maintenance in Arabidopsis thaliana. Mol. Plant 2, 600-609.
84. Shuai B, Reynaga-Pena CG, Springer PS (2002) The lateral organ boundaries gene defines a novel, plant-specific gene family. Plant Physiol. 129, 747-761.
85. Siegfried KR, Eshed Y, Baum SF, Otsuga D, Drews GN, Bowman JL (1999) Members of the YABBY gene family specify abaxial cell fate in Arabidopsis. Development 126, 4117-4128.
86. Sijacic P, Liu Z (2010) Novel insights from live-imaging in shoot meristem development. J. Integr. Plant Biol. 52, 393-399.
87. Skylar A, Wu X (2011) Regulation of meristem size by cytokinin signaling. J. Integr. Plant Biol. 53, 446-454.
88. Skowyra D, Craig KL, Tyers M, Elledge SJ, Harper JW (1997) F-box proteins are receptors that recruit phosphorylated substrates to the SCF ubiquitin-ligase complex. Cell 91, 209-219.
89. Sonoda Y, Sako K, Maki Y, Yamazaki N, Yamamoto H, Ikeda A, Yamaguchi J (2009) Regulation of leaf organ size by the Arabidopsis RPT2a 19S proteasome subunit. Plant J. 60, 68-78.
90. Sonoda Y, Yao SG, Sako K, Sato T, Kato W, Ohto MA, Ichikawa T, Matsui M, Yamaguchi J, Ikeda A (2007) SHA1, a novel RING finger protein, functions in shoot apical meristem maintenance in Arabidopsis. Plant J. 50, 586-596.
91. Spinelli SV, Martin AP, Viola IL, Gonzalez DH, Palatnik JF (2011) A mechanistic link between STM and CUC1 during Arabidopsis development. Plant Physiol. 156, 1894-1904.
92. Stahle MI, Kuehlich J, Staron L, von Arnim AG, Golz JF (2009) YABBYs and the transcriptional corepressors LEUNIG and LEUNIG_HOMOLOG maintain leaf polarity and meristem activity in Arabidopsis. Plant Cell 21, 3105-3118.
93. Steeves TA, Sussex IM (1989) Patterns in Plant Development Cambridge University Press, Cambridge, UK.
94. Stirnberg P, Furner IJ, Ottoline Leyser HM (2007) MAX2 participates in an SCF complex which acts locally at the node to suppress shoot branching. Plant J. 50, 80-94.
95. Stone SL, Hauksdottir H, Troy A, Herschleb J, Kraft E, Callis J (2005) Functional analysis of the RING-type ubiquitin ligase family of Arabidopsis. Plant Physiol. 137, 13-30.
96. Szakonyi D, Moschopoulos A, Byrne ME (2010) Perspectives on leaf dorsoventral polarity. J. Plant Res. 123, 281-290.
97. Traas J, Doonan JH (2001) Cellular basis of shoot apical meristem development. Int. Rev. Cytol. 208, 161-206.
98. Traas J, Moneger F (2010) Systems biology of organ initiation at the shoot apex. Plant Physiol. 152, 420-427.
99. Ueda M, Matsui K, Ishiguro S, Sano R, Wada T, Paponov I, Palme K, Okada K (2004) The HALTED ROOT gene encoding the 26S proteasome subunit RPT2a is essential for the maintenance of Arabidopsis meristems. Development 131, 2101-2111.
100. Varshavsky A (2012) The ubiquitin system, an immense realm. Annu. Rev. Biochem. 81, 167-176.
101. Vernoux T, Brunoud G, Farcot E, Morin V, Van den Daele H, Legrand J, Oliva M, Das P, Larrieu A, Wells D, Guedon Y, Armitage L, Picard F, Guyomarc'h S, Cellier C, Parry G, Koumproglou R, Doonan JH, Estelle M, Godin C, Kepinski S, Bennett M, De Veylder L, Traas J (2011) The auxin signalling network translates dynamic input into robust patterning at the shoot apex. Mol. Syst. Biol. 7, 508.
102. Vierstra RD (2009) The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 10, 385-397.
103. Woo HR, Pontes O, Pikaard CS, Richards EJ (2007) VIM1, a methylcytosine-binding protein required for centromeric heterochromatinization. Genes Dev. 21, 267-277.
104. Xie M, Tataw M, Venugopala Reddy G (2009) Towards a functional understanding of cell growth dynamics in shoot meristem stem-cell niche. Semin. Cell Dev. Biol. 20, 1126-1133.
105. Xie Q, Guo HS, Dallman G, Fang S, Weissman AM, Chua NH (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419, 167-170.
106. Xu L, Shen WH (2008) Polycomb silencing of KNOX genes confines shoot stem cell niches in Arabidopsis. Curr. Biol. 18, 1966-1971.
107. Yadav RK, Girke T, Pasala S, Xie M, Reddy GV (2009) Gene expression map of the Arabidopsis shoot apical meristem stem cell niche. Proc. Natl. Acad. Sci. USA 106, 4941-4946.
108. Yanai O, Shani E, Dolezal K, Tarkowski P, Sablowski R, Sandberg G, Samach A, Ori N (2005) Arabidopsis KNOXI proteins activate cytokinin biosynthesis. Curr. Biol. 15, 1566-1571.
109. Yasuhara M, Mitsui S, Hirano H, Takanabe R, Tokioka Y, Ihara N, Komatsu A, Seki M, Shinozaki K, Kiyosue T (2004) Identification of ASK and clock-associated proteins as molecular partners of LKP2 (LOV kelch protein 2) in Arabidopsis. J. Exp. Bot. 55, 2015-2027.
110. Yoshida S, Mandel T, Kuhlemeier C (2011) Stem cell activation by light guides plant organogenesis. Genes Dev. 25, 1439-1450.
111. Zhang Z, Wang H, Luo D, Zeng M, Huang H, Cui X (2011) Convergence of the 26S proteasome and the REVOLUTA pathways in regulating inflorescence and floral meristem functions in Arabidopsis. J. Exp. Bot. 62, 359-369.
112. Zhuang M, Calabrese MF, Liu J, Waddell MB, Nourse A, Hammel M, Miller DJ, Walden H, Duda DM, Seyedin SN, Hoggard T, Harper JW, White KP, Schulman BA (2009) Structures of SPOP-substrate complexes: Insights into molecular architectures of BTB-Cul3 ubiquitin ligases. Mol. Cell 36, 39-50.