Out of step: The function of TALE homeodomain transcription factors that regulate shoot meristem maintenance and meristem identity

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 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 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 Amasino R (2010). Seasonal and developmental timing of flowering. Plant J, 61(6): 1001–1013 Barton M K (2010). Twenty years on: the inner workings of the shoot apical meristem, a developmental dynamo. Dev Biol, 341(1): 95–113 Barton MK, 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 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 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 Bernier G (1988). The Control of Floral Evocation and Morphogenesis. Annu Rev Plant Physiol Plant Mol Biol, 39(1): 175–219 Bernier G (2011). My favourite flowering image: the role of cytokinin as a flowering signal. J Exp Bot, (In press) 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 Bleckmann A, Simon R (2009). Interdomain signaling in stem cell maintenance of plant shoot meristems. Mol Cells, 27(6): 615–620 Bolduc N, Hake S (2009). The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell, 21(6): 1647–1658 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 Bowman J L, Alvarez J, Weigel D, Meyerowitz EM, Smyth D R (1993). Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development, 119(3): 721–743 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 Braybrook S A, Kuhlemeier C (2010). How a plant builds leaves. Plant Cell, 22(4): 1006–1018 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 Byrne M E, Simorowski J, Martienssen R A (2002). ASYMMETRIC LEAVES1 reveals knox gene redundancy in Arabidopsis. Development, 129(8): 1957–1965 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 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 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 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 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 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 Dodsworth S (2009). A diverse and intricate signalling network regulates stem cell fate in the shoot apical meristem. Dev Biol, 336(1): 1–9 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 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 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 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 Fornara F, de Montaigu A, Coupland G (2010). SnapShot: Control of flowering in Arabidopsis. Cell 141(3): 550, 550 e1-2 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 Gregis V, Sessa A, Colombo L, Kater M M (2008). AGAMOUSLIKE24 and SHORT VEGETATIVE PHASE determine floral meristem identity in Arabidopsis. Plant J, 56(6): 891–902 Gustafson-Brown C, Savidge B, Yanofsky MF (1994). Regulation of the arabidopsis floral homeotic gene APETALA1. Cell, 76(1): 131–143 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 Hamant O, Pautot V (2010). Plant development: a TALE story. C R Biol, 333(4): 371–381 Hay A, Tsiantis M(2009). A KNOX family TALE. Curr Opin Plant Biol, 12(5): 593–598 Hay A, Tsiantis M (2010). KNOX genes: versatile regulators of plant development and diversity. Development, 137(19): 3153–3165 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 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 Itoh H, Ueguchi-Tanaka M, Matsuoka M (2008). Molecular biology of gibberellins signaling in higher plants. Int Rev Cell Mol Biol, 268: 191–221 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 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 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 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 POUNDFOOLISH in Arabidopsis. Plant J, 54(5): 924–937 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 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 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 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 Kyozuka J (2007). Control of shoot and root meristem function by cytokinin. Curr Opin Plant Biol, 10(5): 442–446 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) 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 Lee J, Lee I (2010). Regulation and function of SOC1, a flowering pathway integrator. J Exp Bot, 61(9): 2247–2254 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 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 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 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 Long J A, Barton M K (1998). The development of apical embryonic pattern in Arabidopsis. Development, 125(16): 3027–3035 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 Lyndon R F (1998). The shoot apical meristem, Its growth and development. (Cambridge: Cambridge University Press). 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 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 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 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 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 Moens C B, Selleri L (2006). Hox cofactors in vertebrate development. Dev Biol, 291(2): 193–206 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 Parcy F, Nilsson O, Busch M A, Lee I, Weigel D (1998). A genetic framework for floral patterning. Nature, 395(6702): 561–566 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 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 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 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 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 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 Ruiz-García L, Madueño F, Wilkinson M, Haughn G, Salinas J, Martínez-Zapater JM (1997). Different roles of flowering-time genes in the activation of floral initiation genes in Arabidopsis. Plant Cell, 9(11): 1921–1934 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 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 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 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 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 Schultz E A, Haughn GW (1993). Genetic analysis of the floral initiation process (FLIP) in Arabidopsis. Development, 119: 745–765 Scofield S, Murray J A (2006). KNOX gene function in plant stem cell niches. Plant Mol Biol, 60(6): 929–946 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 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 Shani E, Yanai O, Ori N (2006). The role of hormones in shoot apical meristem function. Curr Opin Plant Biol, 9(5): 484–489 Shen W H, Xu L (2009). Chromatin remodeling in stem cell maintenance in Arabidopsis thaliana. Mol Plant, 2(4): 600–609 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 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 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 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 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 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 Steeves T A, Sussex I M (1989). Patterns in Plant Development. (Cambridge: Cambridge University Press). 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 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 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 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 Teper-Bamnolker P, Samach A (2005). The flowering integrator FT regulates SEPALLATA3 and FRUITFULL accumulation in Arabidopsis leaves. Plant Cell, 17(10): 2661–2675 Trevaskis B, Hemming MN, Peacock WJ, Dennis E S (2006). HvVRN2 responds to daylength, whereas HvVRN1 is regulated by vernalization and developmental status. Plant Physiol, 140(4): 1397–1405 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 van der Schoot C, Rinne P L (2011). Dormancy cycling at the shoot apical meristem: transitioning between self-organization and selfarrest. Plant Sci, 180(1): 120–131 van der Valk P, ProveniersMC G, Pertijs J H, Lamers J TWH, 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 Vernoux T, Besnard F, Traas J (2010). Auxin at the shoot apical meristem. Cold Spring Harb Perspect Biol, 2(4): a001487 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 Wagner D, Sablowski R W M, Meyerowitz E M (1999). Transcriptional activation of APETALA1 by LEAFY. Science, 285(5427): 582–584 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 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 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 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 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 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 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 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 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 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 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