Out of step: The function of TALE homeodomain transcription factors that regulate shoot meristem maintenance and meristem identity
Received date: 08 Sep 2011
Accepted date: 12 Oct 2011
Published date: 01 Apr 2012
Copyright
The indeterminate growth pattern displayed by shoots is mediated by the proper maintenance of the shoot meristem. Meristem maintenance is dependent upon the balance of stem cell perpetuation in the central zone (CZ) and organogenesis in the peripheral zone (PZ). Although the mechanisms that coordinate CZ and PZ function is not understood, meristem cell fate is likely achieved by the spatial interplay between gene regulatory networks and hormone signaling pathways. During shoot maturation, the identity of the shoot meristem as well as the lateral organs are transformed during the vegetative and reproductive transitions. Studies in model plant systems indicate that three amino acid extension (TALE) homeodomain proteins integrate signaling events that transform the identity of the shoot meristem and establish reproductive patterns of growth. This review will highlight the function of TALE homeodomain transcription factors that regulate shoot meristem cell fate and also function with phase specific regulators to maintain shoot meristem identity.
Key words: shoot development; meristem; flowering; patterning; homeodomain
Shang WU , Harley M. S. SMITH . Out of step: The function of TALE homeodomain transcription factors that regulate shoot meristem maintenance and meristem identity[J]. Frontiers in Biology, 2012 , 7(2) : 144 -154 . DOI: 10.1007/s11515-011-1182-y
1 |
Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science, 309(5737): 1052–1056
|
2 |
Aida M, Ishida T, Tasaka M (1999). Shoot apical meristem and cotyledon formation during Arabidopsis embryogenesis: interaction among the CUP-SHAPED COTYLEDON and SHOOT MERISTEMLESS genes. Development, 126(8): 1563–1570
|
3 |
Aida M, Tasaka M (2006). Morphogenesis and patterning at the organ boundaries in the higher plant shoot apex. Plant Mol Biol, 60(6): 915–928
|
4 |
Amasino R (2010). Seasonal and developmental timing of flowering. Plant J, 61(6): 1001–1013
|
5 |
Barton M K (2010). Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol, 341(1): 95–113
|
6 |
Barton M K, Poethig R S (1993). Formation of the shoot apical meristem in Arabidopsis thaliana: an analysis of development in the wild type and in the shoot meristemless mutant. Development, 119(16): 823–831
|
7 |
Becker A, Theissen G (2003). The major clades of MADS-box genes and their role in the development and evolution of flowering plants. Mol Phylogenet Evol, 29(3): 464–489
|
8 |
Belles-Boix E, Hamant O, Witiak S M, Morin H, Traas J, Pautot V (2006). KNAT6: an Arabidopsis homeobox gene involved in meristem activity and organ separation. Plant Cell, 18(8): 1900–1907
|
9 |
Bernier G (1988). The Control of Floral Evocation and Morphogenesis. Annu Rev Plant Physiol Plant Mol Biol, 39(1): 175–219
|
10 |
Bernier G (2011). My favourite flowering image: the role of cytokinin as a flowering signal. J Exp Bot, (In press)
|
11 |
Bhatt A M, Etchells J P, Canales C, Lagodienko A, Dickinson H (2004). VAAMANA—a BEL1-like homeodomain protein, interacts with KNOX proteins BP and STM and regulates inflorescence stem growth in Arabidopsis. Gene, 328: 103–111
|
12 |
Bleckmann A, Simon R (2009). Interdomain signaling in stem cell maintenance of plant shoot meristems. Mol Cells, 27(6): 615–620
|
13 |
Bolduc N, Hake S (2009). The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell, 21(6): 1647–1658
|
14 |
Bonhomme F, Kurz B, Melzer S, Bernier G, Jacqmard A (2000). Cytokinin and gibberellin activate SaMADS A, a gene apparently involved in regulation of the floral transition in Sinapis alba. Plant J, 24(1): 103–111
|
15 |
Bowman J L, Alvarez J, Weigel D, Meyerowitz E M, Smyth D R (1993). Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development, 119(3): 721–743
|
16 |
Brambilla V, Battaglia R, Colombo M, Masiero S, Bencivenga S, Kater M M, Colombo L (2007). Genetic and molecular interactions between BELL1 and MADS box factors support ovule development in Arabidopsis. Plant Cell, 19(8): 2544–2556
|
17 |
Braybrook S A, Kuhlemeier C (2010). How a plant builds leaves. Plant Cell, 22(4): 1006–1018
|
18 |
Byrne M E, Groover A T, Fontana J R, Martienssen R A (2003). Phyllotactic pattern and stem cell fate are determined by the Arabidopsis homeobox gene BELLRINGER. Development, 130(17): 3941–3950
|
19 |
Byrne M E, Simorowski J, Martienssen R A (2002). ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development, 129(8): 1957–1965
|
20 |
Chae E, Tan Q K, Hill T A, Irish V F (2008). An Arabidopsis F-box protein acts as a transcriptional co-factor to regulate floral development. Development, 135(7): 1235–1245
|
21 |
Chen H, Banerjee A K, Hannapel D J (2004). The tandem complex of BEL and KNOX partners is required for transcriptional repression of ga20ox1. Plant J, 38(2): 276–284
|
22 |
Clark S E, Jacobsen S E, Levin J Z, Meyerowitz E M (1996). The CLAVATA and SHOOT MERISTEMLESS loci competitively regulate meristem activity in Arabidopsis. Development, 122(5): 1567–1575
|
23 |
Crevillén P, Dean C (2011). Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol, 14(1): 38–44
|
24 |
D’Aloia M, Bonhomme D, Bouché F, Tamseddak K, Ormenese S, Torti S, Coupland G, Périlleux C (2011). Cytokinin promotes flowering of Arabidopsis via transcriptional activation of the FT paralogue TSF. Plant J, 65(6): 972–979
|
25 |
de Folter S, Immink R G, Kieffer M, Parenicová L, Henz S R, Weigel D, Busscher M, Kooiker M, Colombo L, Kater M M, Davies B, Angenent G C (2005). Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell, 17(5): 1424–1433
|
26 |
Dodsworth S (2009). A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol, 336(1): 1–9
|
27 |
Dubcovsky J, Loukoianov A, Fu D, Valarik M, Sanchez A, Yan L (2006). Effect of photoperiod on the regulation of wheat vernalization genes VRN1 and VRN2. Plant Mol Biol, 60(4): 469–480
|
28 |
Endrizzi K, Moussian B, Haecker A, Levin J Z, 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(6): 967–979
|
29 |
Eriksson S, Böhlenius H, Moritz T, Nilsson O (2006). GA4 is the active gibberellin in the regulation of LEAFY transcription and Arabidopsis floral initiation. Plant Cell, 18(9): 2172–2181
|
30 |
Ferrándiz C, Gu Q, Martienssen R, Yanofsky M F (2000). Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development, 127(4): 725–734
|
31 |
Fornara F, de Montaigu A, Coupland G (2010). SnapShot: Control of flowering in Arabidopsis. Cell 141(3): 550, 550 e1–2
|
32 |
Gómez-Mena C, Sablowski R (2008). ARABIDOPSIS THALIANA HOMEOBOX GENE1 establishes the basal boundaries of shoot organs and controls stem growth. Plant Cell, 20(8): 2059–2072
|
33 |
Gregis V, Sessa A, Colombo L, Kater M M (2008). AGAMOUS-LIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J, 56(6): 891–902
|
34 |
Gustafson-Brown C, Savidge B, Yanofsky M F (1994). Regulation of the arabidopsis floral homeotic gene APETALA1. Cell, 76(1): 131–143
|
35 |
Hake S, Smith H M, Holtan H, Magnani E, Mele G, Ramirez J (2004). The role of knox genes in plant development. Annu Rev Cell Dev Biol, 20(1): 125–151
|
36 |
Hamant O, Pautot V (2010). Plant development: a TALE story. C R Biol, 333(4): 371–381
|
37 |
Hay A, Tsiantis M (2009). A KNOX family TALE. Curr Opin Plant Biol, 12(5): 593–598
|
38 |
Hay A, Tsiantis M (2010). KNOX genes: versatile regulators of plant development and diversity. Development, 137(19): 3153–3165
|
39 |
Helliwell C, Wood C, Robertson M, Peacock J, Dennis E (2006). The Arabidopsis FLC protein interacts directly in vivo with SOC1 and FT chromatin and is part of a high-molecularweight protein complex. The Plant Journal, 46(2), 183–192
|
40 |
Hepworth S, Valverde F, Ravenscroft D, Mouradov A, Coupland G (2002). Antagonistic regulation of flowering-time gene SOC1 by CONSTANS and FLC via separate promoter motifs. The EMBO Journal, 21(16): 4327–4337
|
41 |
Itoh H, Ueguchi-Tanaka M, Matsuoka M (2008). Molecular biology of gibberellins signaling in higher plants. Int Rev Cell Mol Biol, 268: 191–221
|
42 |
Jackson D, Veit B, Hake S (1994). Expression of maize KNOTTED1 related homeobox genes in the shoot apical meristem predicts patterns of morphogenesis in the vegetative shoot. Development, 120: 405–413
|
43 |
Jang S, Torti S, Coupland G (2009). Genetic and spatial interactions between FT, TSF and SVP during the early stages of floral induction in Arabidopsis. Plant J, 60(4): 614–625
|
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(17): 1560–1565
|
45 |
Kanrar S, Bhattacharya M, Arthur B, Courtier J, Smith H M (2008). Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis. Plant J, 54(5): 924–937
|
46 |
Kanrar S, Onguka O, Smith H M S (2006). Arabidopsis inflorescence architecture requires the activities of KNOX-BELL homeodomain heterodimers. Planta, 224(5): 1163–1173
|
47 |
Kerstetter R A, Laudencia-Chingcuanco D, Smith L G, Hake S (1997). Loss-of-function mutations in the maize homeobox gene, knotted1, are defective in shoot meristem maintenance. Development, 124(16): 3045–3054
|
48 |
King R W, Evans L T (2003). Gibberellins and flowering of grasses and cereals: prizing open the lid of the “florigen” black box. Annu Rev Plant Biol, 54(1): 307–328
|
49 |
Kobayashi Y, Weigel D (2007). Move on up, it’s time for change—mobile signals controlling photoperiod-dependent flowering. Genes Dev, 21(19): 2371–2384
|
50 |
Kyozuka J (2007). Control of shoot and root meristem function by cytokinin. Curr Opin Plant Biol, 10(5): 442–446
|
51 |
Lal S, Pacis L B, Smith H M (2011). Regulation of the SQUAMOSA PROMOTER-BINDING PROTEIN-LIKE genes/microRNA156 Module by the Homeodomain Proteins PENNYWISE and POUND-FOOLISH in Arabidopsis. Mol Plant, (In press)
|
52 |
Lee H, Suh S S, Park E, Cho E, Ahn J H, Kim S G, Lee J S, Kwon Y M, Lee I (2000). The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes Dev, 14(18): 2366–2376
|
53 |
Lee J, Lee I (2010). Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot, 61(9): 2247–2254
|
54 |
Lee J, Oh M, Park H, Lee I (2008). SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J, 55(5): 832–843
|
55 |
Liljegren S J, Gustafson-Brown C, Pinyopich A, Ditta G S, Yanofsky M F (1999). Interactions among APETALA1, LEAFY, and TERMINAL FLOWER1 specify meristem fate. Plant Cell, 11(6): 1007–1018
|
56 |
Liu C, Chen H, Er H L, Soo H M, Kumar P P, Han J H, Liou Y C, Yu H (2008). Direct interaction of AGL24 and SOC1 integrates flowering signals in Arabidopsis. Development, 135(8): 1481–1491
|
57 |
Liu C, Zhou J, Bracha-Drori K, Yalovsky S, Ito T, Yu H (2007). Specification of Arabidopsis floral meristem identity by repression of flowering time genes. Development, 134(10): 1901–1910
|
58 |
Long J A, Barton M K (1998). The development of apical embryonic pattern in Arabidopsis. Development, 125(16): 3027–3035
|
59 |
Long J A, Moan E I, Medford J I, Barton M K (1996). A member of the KNOTTED class of homeodomain proteins encoded by the STM gene of Arabidopsis. Nature, 379(6560): 66–69
|
60 |
Lyndon R F (1998). The shoot apical meristem, Its growth and development. (Cambridge: Cambridge University Press).
|
61 |
Mandel M A, Yanofsky M F (1995). The Arabidopsis AGL8 MADS box gene is expressed in inflorescence meristems and is negatively regulated by APETALA1. Plant Cell, 7(11): 1763–1771
|
62 |
Martínez-Zapater J M, Jarillo J A, Cruz-Alvarez M, Roldan M, Salinas J (1995). Arabidopsis late-flowering fve mutants are affected in both vegetative and reproductive development. Plant J, 7(4): 543–551
|
63 |
Messenguy F, Dubois E (2003). Role of MADS box proteins and their cofactors in combinatorial control of gene expression and cell development. Gene, 316: 1–21
|
64 |
Michaels S D, Amasino R M (1999). FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell, 11(5): 949–956
|
65 |
Michaels S D, Ditta G, Gustafson-Brown C, Pelaz S, Yanofsky M, Amasino R M (2003). AGL24 acts as a promoter of flowering in Arabidopsis and is positively regulated by vernalization. Plant J, 33(5): 867–874
|
66 |
Moens C B, Selleri L (2006). Hox cofactors in vertebrate development. Dev Biol, 291(2): 193–206
|
67 |
Mukherjee K, Brocchieri L, Bürglin T R (2009). A comprehensive classification and evolutionary analysis of plant homeobox genes. Mol Biol Evol, 26(12): 2775–2794
|
68 |
Parcy F, Nilsson O, Busch M A, Lee I, Weigel D (1998). A genetic framework for floral patterning. Nature, 395(6702): 561–566
|
69 |
Pnueli L, Gutfinger T, Hareven D, Ben-Naim O, Ron N, Adir N, Lifschitz E (2001). Tomato SP-interacting proteins define a conserved signaling system that regulates shoot architecture and flowering. Plant Cell, 13(12): 2687–2702
|
70 |
Proveniers M, Rutjens B, Brand M, Smeekens S (2007). The Arabidopsis TALE homeobox gene ATH1 controls floral competency through positive regulation of FLC. Plant J, 52(5): 899–913
|
71 |
Purwestri Y A, Ogaki Y, Tamaki S, Tsuji H, Shimamoto K (2009). The 14-3-3 protein GF14c acts as a negative regulator of flowering in rice by interacting with the florigen Hd3a. Plant Cell Physiol, 50(3): 429–438
|
72 |
Ragni L, Belles-Boix E, Günl M, Pautot V (2008). Interaction of KNAT6 and KNAT2 with BREVIPEDICELLUS and PENNYWISE in Arabidopsis inflorescences. Plant Cell, 20(4): 888–900
|
73 |
Ramirez J, Bolduc N, Lisch D, Hake S (2009). Distal expression of knotted1 in maize leaves leads to reestablishment of proximal/distal patterning and leaf dissection. Plant Physiol, 151(4): 1878–1888
|
74 |
Roeder A H, Ferrándiz C, Yanofsky M F (2003). The role of the REPLUMLESS homeodomain protein in patterning the Arabidopsis fruit. Curr Biol, 13(18): 1630–1635
|
75 |
Ruiz-García L, Madueño F, Wilkinson M, Haughn G, Salinas J, Martínez-Zapater J M (1997). Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell, 9(11): 1921–1934
|
76 |
Rutjens B, Bao D, van Eck-Stouten E, Brand M, Smeekens S, Proveniers M (2009). Shoot apical meristem function in Arabidopsis requires the combined activities of three BEL1-like homeodomain proteins. Plant J, 58(4): 641–654
|
77 |
Saddic L A, Huvermann B, Bezhani S, Su Y, Winter C M, Kwon C S, Collum R P, Wagner D (2006). The LEAFY target LMI1 is a meristem identity regulator and acts together with LEAFY to regulate expression of CAULIFLOWER. Development, 133(9): 1673–1682
|
78 |
Sakamoto T, Kamiya N, Ueguchi-Tanaka M, Iwahori S, Matsuoka M (2001). KNOX homeodomain protein directly suppresses the expression of a gibberellin biosynthetic gene in the tobacco shoot apical meristem. Genes Dev, 15(5): 581–590
|
79 |
Samach A, Onouchi H, Gold S E, Ditta G S, Schwarz-Sommer Z, Yanofsky M F, Coupland G (2000). Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science, 288(5471): 1613–1616
|
80 |
Schmid M, Uhlenhaut N H, Godard F, Demar M, Bressan R, Weigel D, Lohmann J U (2003). Dissection of floral induction pathways using global expression analysis. Development, 130(24): 6001–6012
|
81 |
Schultz E A, Haughn G W (1993). Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development, 119: 745–765
|
82 |
Scofield S, Murray J A (2006). KNOX gene function in plant stem cell niches. Plant Mol Biol, 60(6): 929–946
|
83 |
Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino R A, Coupland G (2006). The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev, 20(7): 898–912
|
84 |
Shalit A, Rozman A, Goldshmidt A, Alvarez J P, Bowman J L, Eshed Y, Lifschitz E (2009). The flowering hormone florigen functions as a general systemic regulator of growth and termination. Proc Natl Acad Sci USA, 106(20): 8392–8397
|
85 |
Shani E, Yanai O, Ori N (2006). The role of hormones in shoot apical meristem function. Curr Opin Plant Biol, 9(5): 484–489
|
86 |
Shen W H, Xu L (2009). Chromatin remodeling in stem cell maintenance in Arabidopsis thaliana. Mol Plant, 2(4): 600–609
|
87 |
Smith H M, Campbell B C, Hake S (2004). Competence to respond to floral inductive signals requires the homeobox genes PENNYWISE and POUND-FOOLISH. Curr Biol, 14(9): 812–817
|
88 |
Smith H M, Hake S (2003). The interaction of two homeobox genes, BREVIPEDICELLUS and PENNYWISE, regulates internode patterning in the Arabidopsis inflorescence. Plant Cell, 15(8): 1717–1727
|
89 |
Smith H M, Ung N, Lal S, Courtier J (2011). Specification of reproductive meristems requires the combined function of SHOOT MERISTEMLESS and floral integrators FLOWERING LOCUS T and FD during Arabidopsis inflorescence development. J Exp Bot, 62(2): 583–593
|
90 |
Smith H M S, Boschke I, Hake S (2002). Selective interaction of plant homeodomain proteins mediates high DNA-binding affinity. Proc Natl Acad Sci USA, 99(14): 9579–9584
|
91 |
Smith L G, Greene B, Veit B, Hake S (1992). A dominant mutation in the maize homeobox gene, Knotted-1, causes its ectopic expression in leaf cells with altered fates. Development, 116(1): 21–30
|
92 |
Souer E, Rebocho A B, Bliek M, Kusters E, de Bruin R A, Koes R (2008). Patterning of inflorescences and flowers by the F-Box protein DOUBLE TOP and the LEAFY homolog ABERRANT LEAF AND FLOWER of petunia. Plant Cell, 20(8): 2033–2048
|
93 |
Steeves T A, Sussex I M (1989). Patterns in Plant Development. (Cambridge: Cambridge University Press).
|
94 |
Takada S, Hibara K i, Ishida T, Tasaka M (2001). The CUP-SHAPED COTYLEDON1 gene of Arabidopsis regulates shoot apical meristem formation. Development, 128(7): 1127–1135
|
95 |
Takano S, Niihama M, Smith H M, Tasaka M, Aida M (2010). gorgon, a novel missense mutation in the SHOOT MERISTEMLESS gene, impairs shoot meristem homeostasis in Arabidopsis. Plant Cell Physiol, 51(4): 621–634
|
96 |
Taoka K I, Ohki I, Tsuji H, Furuita K, Hayashi K, Yanase T, Yamaguchi M, Nakashima C, Purwestri Y A, Tamaki S, Ogaki Y, Shimada C, Nakagawa A, Kojima C, Shimamoto K (2011). 14-3-3 proteins act as intracellular receptors for rice Hd3a florigen. Nature, 476(7360): 332–335
|
97 |
Telfer A, Bollman K M, Poethig R S (1997). Phase change and the regulation of trichome distribution in Arabidopsis thaliana. Development, 124(3): 645–654
|
98 |
Teper-Bamnolker P, Samach A (2005). The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell, 17(10): 2661–2675
|
99 |
Trevaskis B, Hemming M N, Peacock W J, Dennis E S (2006). HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol, 140(4): 1397–1405
|
100 |
Ung N, Lal S, Smith H M (2011). The role of PENNYWISE and POUND-FOOLISH in the maintenance of the shoot apical meristem in Arabidopsis. Plant Physiol, 156(2): 605–614
|
101 |
van der Schoot C, Rinne P L (2011). Dormancy cycling at the shoot apical meristem: transitioning between self-organization and self-arrest. Plant Sci, 180(1): 120–131
|
102 |
van der Valk P, Proveniers M C G, Pertijs J H, Lamers J T W H, van Dun C M P, Smeekens J C M (2004). Late heading of perennial ryegrass caused by introducing an Arabidopsis homeobox gene. Plant Breed, 123(6): 531–535
|
103 |
Vernoux T, Besnard F, Traas J (2010). Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol, 2(4): a001487
|
104 |
Vollbrecht E, Reiser L, Hake S (2000). Shoot meristem size is dependent on inbred background and presence of the maize homeobox gene, knotted1. Development, 127(14): 3161–3172
|
105 |
Wagner D, Sablowski R W M, Meyerowitz E M (1999). Transcriptional activation of APETALA1 by LEAFY. Science, 285(5427): 582–584
|
106 |
Wang J W, Czech B, Weigel D (2009). miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell, 138(4): 738–749
|
107 |
Weigel D, Alvarez J, Smyth D R, Yanofsky M F, Meyerowitz E M (1992). LEAFY controls floral meristem identity in Arabidopsis. Cell, 69(5): 843–859
|
108 |
Wigge P A, Kim M C, Jaeger K E, Busch W, Schmid M, Lohmann J U, Weigel D (2005). Integration of spatial and temporal information during floral induction in Arabidopsis. Science, 309(5737): 1056–1059
|
109 |
William D A, Su Y, Smith M R, Lu M, Baldwin D A, Wagner D (2004). Genomic identification of direct target genes of LEAFY. Proc Natl Acad Sci USA, 101(6): 1775–1780
|
110 |
Willmann M R, Poethig R S (2011). The effect of the floral repressor FLC on the timing and progression of vegetative phase change in Arabidopsis. Development, 138(4): 677–685
|
111 |
Winter C M, Austin R S, Blanvillain-Baufumé S, Reback M A, Monniaux M, Wu M F, Sang Y, Yamaguchi A, Yamaguchi N, Parker J E, Parcy F, Jensen S T, Li H, Wagner D (2011). LEAFY target genes reveal floral regulatory logic, cis motifs, and a link to biotic stimulus response. Dev Cell, 20(4): 430–443
|
112 |
Yamaguchi A, Wu M F, Yang L, Wu G, Poethig R S, Wagner D (2009). The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell, 17(2): 268–278
|
113 |
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen J L, Echenique V, Dubcovsky J (2004). The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science, 303(5664): 1640–1644
|
114 |
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(17): 1566–1571
|
115 |
Yu H, Ito T, Wellmer F, Meyerowitz E M (2004). Repression of AGAMOUS-LIKE 24 is a crucial step in promoting flower development. Nat Genet, 36(2): 157–161
|
116 |
Yu H, Xu Y, Tan E L, Kumar P P (2002). AGAMOUS-LIKE 24, a dosage-dependent mediator of the flowering signals. Proc Natl Acad Sci USA, 99(25): 16336–16341
|
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