Advertisement

Evolution of the Flowering Pathways

  • Eva Lucas-Reina
  • M Isabel Ortiz-Marchena
  • Francisco J. Romero-Campero
  • Myriam Calonje
  • José M. Romero
  • Federico ValverdeEmail author
Chapter
Part of the Progress in Botany book series (BOTANY, volume 77)

Abstract

Flowering plants are some of the most successful organisms on Earth, particularly those used in agriculture due to the widespread distribution produced by farming activities. The correct moment of the year to flower is a crucial decision as it strongly compromises the success of the progeny and is thus strictly controlled. Crops have been artificially selected to flower in those conditions better adapted for human production, and many genes related to flowering time are selected as targets for breeding programs. These characteristics reflect a complex regulatory pathway that has to respond both to predictable and unexpected changes in the environment. This plasticity confers the flowering plants with a genetic toolkit to adapt to varied habitats and changing environmental conditions. Recent advances in massive acquisition of data from many different species belonging to the green eukaryotic lineage allow us to make an evolutionary approach to the main mechanisms that influence the floral transition and how flowers are formed in modern plants. This work will review some of these aspects from the floral transition to the floral organogenesis.

Keywords

Circadian Clock Floral Organ Shoot Apical Meristem Floral Meristem Floral Transition 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

The authors would like to thank the help from the coordinated projects BIO2011-28847-C02-00 and BIO2014-52425-P to FV and JMR, the BIO2013-44078-P project to MC, and the TRANSPLANTA Consolider 28317 project from Spanish Ministry of Economy and Innovation (MINECO). The help from the Marie Curie Grant ID333748 to MC and from the Excellence Project P08-AGR-03582 and CVI-281 to FV from the Andalusian Government is also acknowledged. The authors regret the exclusion, due to lack of space, of excellent works from other colleagues that could not be referred in this review.

References

  1. Aagaard JE, Willis JH, Phillips PC (2006) Relaxed selection among duplicate floral regulatory genes in Lamiales. J Mol Evol 63:493–503PubMedCrossRefGoogle Scholar
  2. Alvarez J, Guli CL, Yu X-H, Smyth DR (1992) Terminal flower: a gene affecting inflorescence development in Arabidopsis thaliana. Plant J 2:103–116CrossRefGoogle Scholar
  3. Alvarez-Buylla ER, Liljegren SJ, Pelaz S, Gold SE, Burgeff C, Ditta GS, Vergara-Silva F, Yanofsky MF (2000a) MADS-box gene evolution beyond flowers: expression in pollen, endosperm, guard cells, roots and trichomes. Plant J 24:457–466PubMedCrossRefGoogle Scholar
  4. Alvarez-Buylla ER, Pelaz S, Liljegren SJ, Gold SE, Burgeff C, Ditta GS, Ribas de Pouplana L, Martinez-Castilla L, Yanofsky MF (2000b) An ancestral MADS-box gene duplication occurred before the divergence of plants and animals. Proc Natl Acad Sci USA 97:5328–5333PubMedPubMedCentralCrossRefGoogle Scholar
  5. Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559PubMedPubMedCentralCrossRefGoogle Scholar
  6. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013PubMedCrossRefGoogle Scholar
  7. Amasino RM, Michaels SD (2010) The timing of flowering. Plant Physiol 154:516–520PubMedPubMedCentralCrossRefGoogle Scholar
  8. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639PubMedCrossRefGoogle Scholar
  9. Arazi T, Talmor-Neiman M, Stav R, Riese M, Huijser P, Baulcombe DC (2005) Cloning and characterization of micro-RNAs from moss. Plant J 43:837–848PubMedCrossRefGoogle Scholar
  10. Aukerman MJ, Sakai H (2003) Regulation of flowering time and floral organ identity by a MicroRNA and its APETALA2-like target genes. Plant Cell 15:2730–2741PubMedPubMedCentralCrossRefGoogle Scholar
  11. Avonce N, Wuyts J, Verschooten K, Vandesteene L, Van Dijck P (2010) The Cytophaga hutchinsonii ChTPSP: first characterized bifunctional TPS-TPP protein as putative ancestor of all eukaryotic trehalose biosynthesis proteins. Mol Biol Evol 27:359–369PubMedCrossRefGoogle Scholar
  12. Axtell MJ, Bowman JL (2008) Evolution of plant microRNAs and their targets. Trends Plant Sci 13:343–349PubMedCrossRefGoogle Scholar
  13. Baena-González E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482PubMedPubMedCentralCrossRefGoogle Scholar
  14. Bajguz A, Piotrowska-Niczyporuk A (2013) Synergistic effect of auxins and brassinosteroids on the growth and regulation of metabolite content in the green alga Chlorella vulgaris (Trebouxiophyceae). Plant Physiol Biochem 71:290–297PubMedCrossRefGoogle Scholar
  15. Balasubramanian S, Weigel D (2006) Temperature induced flowering in Arabidopsis thaliana. Plant Signal Behav 1:227–228PubMedPubMedCentralCrossRefGoogle Scholar
  16. Bartlett ME, Kirchoff BK, Specht CD (2008) Epi-illumination microscopy coupled to in situ hybridization and its utility in the study of evolution and development in non-model species. Dev Genes Evol 218:273–279PubMedCrossRefGoogle Scholar
  17. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167PubMedCrossRefGoogle Scholar
  18. 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 29:464–489PubMedCrossRefGoogle Scholar
  19. Beel B, Müller N, Kottke T, Mittag M (2013) News about cryptochrome photoreceptors in algae. Plant Signal Behav 8:e22870PubMedPubMedCentralCrossRefGoogle Scholar
  20. Benlloch R, Berbel A, Serrano-Mislata A, Madueño F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot 100:659–676PubMedPubMedCentralCrossRefGoogle Scholar
  21. Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993) Physiological signals that induce flowering. Plant Cell 5:1147–1155PubMedPubMedCentralCrossRefGoogle Scholar
  22. Blazquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171PubMedCrossRefGoogle Scholar
  23. Blazquez MA, Ferrándiz C, Madueño F, Parcy F (2006) How floral meristems are built. Plant Mol Biol 60:855–870PubMedCrossRefGoogle Scholar
  24. Böhlenius H, Huang T, Charbonnel-Campaa L, Brunner AM, Jansson S, Strauss SH, Nilsson O (2006) CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312:1040–1043PubMedCrossRefGoogle Scholar
  25. Bomblies K, Wang RL, Ambrose BA, Schmidt RJ, Meeley RB, Doebley J (2003) Duplicate FLORICAULA/LEAFY homologs zfl1 and zfl2 control inflorescence architecture and flower patterning in maize. Development 130:2385–2395PubMedCrossRefGoogle Scholar
  26. Bouget FY, Lefranc M, Thommen Q, Pfeuty B, Lozano JC, Schatt P, Botebol H, Vergé V (2014) Transcriptional versus non-transcriptional clocks: a case study in Ostreococcus. Mar Genomics 14:1–6CrossRefGoogle Scholar
  27. Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112:1–20PubMedGoogle Scholar
  28. Bowman JL, Alvarez J, Weigel D, Meyerowitz EM, Smyth DR (1993) Control of flower development in Arabidopsis thaliana by APETALA1 and interacting genes. Development 119:721–743Google Scholar
  29. Bradley D, Carpenter R, Copsey L, Vincent C, Rothstein S, Coen E (1996) Control of inflorescence architecture in Antirrhinum. Nature 379:791–797PubMedCrossRefGoogle Scholar
  30. Bradshaw WE, Holzapfel CM (2007) Evolution of animal photoperiodism. Annu Rev Ecol Evol Syst 38:1–25CrossRefGoogle Scholar
  31. Busch MA, Bomblies K, Weigel D (1999) Activation of a floral homeotic gene in Arabidopsis. Science 285:585–587PubMedCrossRefGoogle Scholar
  32. Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4:1483–1493PubMedCrossRefGoogle Scholar
  33. Carretero-Paulet L, Galstyan A, Roig-Villanova I, Martínez-García JF, Bilbao-Castro JR, Robertson DL (2010) Genome-wide classification and evolutionary analysis of the bHLH family of transcription factors in Arabidopsis, poplar, rice, moss, and algae. Plant Physiol 153:1398–1412PubMedPubMedCentralCrossRefGoogle Scholar
  34. Casal JJ, Fankhauser C, Coupland G, Blázquez MA (2004) Signalling for developmental plasticity. Trends Plant Sci 9:309–314PubMedCrossRefGoogle Scholar
  35. Castro Marin I, Loef I, Bartetzko L, Searle I, Coupland G, Stitt M, Osuna D (2011) Nitrate regulates floral induction in Arabidopsis, acting independently of light, gibberellin and autonomous pathways. Planta 233:539–552PubMedPubMedCentralCrossRefGoogle Scholar
  36. Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol 11:47CrossRefGoogle Scholar
  37. Coen ES (1991) The role of homeotic genes in flower development and evolution. Annu Rev Plant Physiol Plant Mol Biol 42:241–279CrossRefGoogle Scholar
  38. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37PubMedCrossRefGoogle Scholar
  39. Coen ES, Romero JM, Doyle S, Elliott R, Murphy G, Carpenter R (1990) Floricaula: a homeotic gene required for flower development in antirrhinum majus. Cell 63:1311–1322PubMedCrossRefGoogle Scholar
  40. Coen ES, Doyle S, Romero JM, Elliott R, Magrath R, Carpenter R (1991) Homeotic genes controlling flower development in Antirrhinum. Development 113:149–155Google Scholar
  41. Corbesier L, Lejeune P, Bernier G (1998) The role of carbohydrates in the induction of flowering in Arabidopsis thaliana: comparison between the wild type and a starchless mutant. Planta 206:131–137PubMedCrossRefGoogle Scholar
  42. Corellou F, Schwartz C, Motta JP, Djouani-Tahri EB, Sanchez F, Bouget FY (2009) Clocks in the green lineage: comparative functional analysis of the circadian architecture of the picoeukaryote ostreococcus. Plant Cell 21:3436–3449PubMedPubMedCentralCrossRefGoogle Scholar
  43. Corrales AR, Nebauer SG, Carrillo L, Fernández-Nohales P, Marqués J, Renau-Morata B, Granell A, Pollmann S, Vicente-Carbajosa J, Molina RV, Medina J (2014) Characterization of tomato Cycling Dof Factors reveals conserved and new functions in the control of flowering time and abiotic stress responses. J Exp Bot 65:995–1012PubMedCrossRefGoogle Scholar
  44. Crespo JL (2012) BiP links TOR signaling to ER stress in Chlamydomonas. Plant Signal Behav 7:273–275PubMedPubMedCentralCrossRefGoogle Scholar
  45. Crespo L, Díaz-Troya S, Florencio FJ (2005) Inhibition of target of rapamycin signaling by rapamycin in the unicellular green alga. Plant Physiol 139:1736–1749PubMedPubMedCentralCrossRefGoogle Scholar
  46. Crevillen P, Dean C (2011) Regulation of the floral repressor gene FLC: the complexity of transcription in a chromatin context. Curr Opin Plant Biol 14:38–44PubMedCrossRefGoogle Scholar
  47. Crevillen P, Sonmez C, Wu Z, Dean C (2013) A gene loop containing the floral repressor FLC is disrupted in the early phase of vernalization. EMBO J 32:140–148PubMedPubMedCentralCrossRefGoogle Scholar
  48. Cuperus JT, Fahlgren N, Carrington JC (2011) Evolution and functional diversification of MIRNA genes. Plant Cell 23:431–442PubMedPubMedCentralCrossRefGoogle Scholar
  49. Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638PubMedPubMedCentralCrossRefGoogle Scholar
  50. De Bodt S, Raes J, Florquin K, Rombauts S, Rouze P, Theissen G, Van de Peer Y (2003) Genome-wide structural annotation and evolutionary analysis of the type I MADS-box genes in plants. J Mol Evol 56:573–586PubMedCrossRefGoogle Scholar
  51. De Bodt S, Maere S, Van de Peer Y (2005) Genome duplication and the origin of angiosperms. Trends Ecol Evol 20:591–597PubMedCrossRefGoogle Scholar
  52. de Folter S, Immink RG, Kieffer M, Parenicova L, Henz SR, Weigel D, Busscher M, Kooiker M, Colombo L, Kater MM, Davies B, Angenent GC (2005) Comprehensive interaction map of the Arabidopsis MADS Box transcription factors. Plant Cell 17:1424–1433PubMedPubMedCentralCrossRefGoogle Scholar
  53. De Lucia F, Crevillen P, Jones AM, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105:16831–16836PubMedPubMedCentralCrossRefGoogle Scholar
  54. Debast S, Nunes-Nesi A, Hajirezaei MR, Hofmann J, Sonnewald U, Fernie AR, Bornke F (2011) Altering trehalose-6-phosphate content in transgenic potato tubers affects tuber growth and alters responsiveness to hormones during sprouting. Plant Physiol 156:1754–1771PubMedPubMedCentralCrossRefGoogle Scholar
  55. Della Pina S, Souer E, Koes R (2014) Arguments in the evo-devo debate: say it with flowers! J Exp Bot 65:2231–2242PubMedCrossRefGoogle Scholar
  56. Deng W, Ying H, Helliwell CA, Taylor JM, Peacock WJ, Dennis ES (2011) FLOWERING LOCUS C (FLC) regulates development pathways throughout the life cycle of Arabidopsis. Proc Natl Acad Sci USA 108:6680–6685PubMedPubMedCentralCrossRefGoogle Scholar
  57. Deng Y, Wang X, Guo H, Duan D (2014) A trehalose-6-phosphate synthase gene from Saccharina japonica (Laminariales, Phaeophyceae). Mol Biol Rep 41:529–536PubMedCrossRefGoogle Scholar
  58. Deprost D, Yao L, Sormani R, Moreau M, Leterreus G, Nicolai M, Bedu M, Robaglia C, Meyer C (2007) The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep 8:864–870PubMedPubMedCentralCrossRefGoogle Scholar
  59. Derkacheva M, Hennig L (2014) Variations on a theme: polycomb group proteins in plants. J Exp Bot 65:2769–2784PubMedCrossRefGoogle Scholar
  60. Dickens CWS, Staden JV (1988) The in vitro flowering of Kalanchöe blossfeldiana Poellnitz: I. Role of culture conditions and nutrients. J Exp Bot 39:461–471CrossRefGoogle Scholar
  61. Distelfeld A, Li C, Dubcovsky J (2009) Regulation of flowering in temperate cereals. Curr Opin Plant Biol 12:178–184PubMedCrossRefGoogle Scholar
  62. Ditta G, Pinyopich A, Robles P, Pelaz S, Yanofsky MF (2004) The SEP4 gene of Arabidopsis thaliana functions in floral organ and meristem identity. Curr Biol 14:1935–1940PubMedCrossRefGoogle Scholar
  63. Djouani-Tahri EB, Christie JM, Sanchez-Ferandin S, Sanchez F, Bouget FY, Corellou F (2011) A eukaryotic LOV-histidine kinase with circadian clock function in the picoalga Ostreococcus. Plant J 65:578–588CrossRefGoogle Scholar
  64. Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T, Shimatani Z, Yano M, Yoshimura A (2004) Ehd1, a B-type response regulator in rice, confers short-day promotion of flowering and controls FT-like gene expression independently of Hd1. Genes Dev 2:926–936CrossRefGoogle Scholar
  65. Dornelas MC, Patreze CM, Angenent GC, Immink RG (2011) MADS: the missing link between identity and growth? Trends Plant Sci 16:89–97PubMedCrossRefGoogle Scholar
  66. 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 60:469–480PubMedPubMedCentralCrossRefGoogle Scholar
  67. Egea-Cortines M, Saedler H, Sommer H (1999) Ternary complex formation between the MADS-box proteins SQUAMOSA, DEFICIENS and GLOBOSA is involved in the control of floral architecture in Antirrhinum majus. EMBO J 18:5370–5379PubMedPubMedCentralCrossRefGoogle Scholar
  68. Erdmann R, Gramzow L, Melzer R, Theissen G, Becker A (2010) GORDITA (AGL63) is a young paralog of the Arabidopsis thaliana B(sister) MADS box gene ABS (TT16) that has undergone neofunctionalization. Plant J 63:914–924PubMedCrossRefGoogle Scholar
  69. Espinosa-Soto C, Padilla-Longoria P, Alvarez-Buylla ER (2004) A gene regulatory network model for cell-fate determination during Arabidopsis thaliana flower development that is robust and recovers experimental gene expression profiles. Plant Cell 16:2923–2939PubMedPubMedCentralCrossRefGoogle Scholar
  70. Fang Q, Liu J, Xu Z, Song R (2008) Cloning and characterization of a flowering time gene from Thellungiella halophila. Acta Biochim Biophys Sin (Shanghai) 40:747–753CrossRefGoogle Scholar
  71. Fattash I, Voss B, Reski R, Hess WR, Frank W (2007) Evidence for the rapid expansion of microRNA-mediated regulation in early land plant evolution. BMC Plant Biol 7:13PubMedPubMedCentralCrossRefGoogle Scholar
  72. Ferrandiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127:725–734PubMedGoogle Scholar
  73. Finnegan EJ, Dennis ES (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17:1978–1983PubMedCrossRefGoogle Scholar
  74. Fornara F, Panigrahi KCS, Gissot L, Sauerbrunn N, Rühl M, Jarillo JA, Coupland G (2009) Arabidopsis DOF transcription factors act redundantly to reduce CONSTANS expression and are essential for a photoperiodic flowering response. Dev Cell 17:75–86PubMedCrossRefGoogle Scholar
  75. Fornara F, de Montaigu A, Coupland G (2010) SnapShot: control of flowering in Arabidopsis. Cell 141:551–552CrossRefGoogle Scholar
  76. Frink CR, Waggoner PE, Ausubel JH (1999) Nitrogen fertilizer: retrospect and prospect. Proc Natl Acad Sci USA 96:1175–1180PubMedPubMedCentralCrossRefGoogle Scholar
  77. Frohlich MW (2003) An evolutionary scenario for the origin of flowers. Nat Rev Genet 4:559–566PubMedCrossRefGoogle Scholar
  78. Frohlich MW (2006) Recent developments regarding the evolutionary origin of flowers. In: Soltis DE, Callow JA (eds) Advances in botanical research, vol 44. Academic Press, San Diego, CA, pp 63–127Google Scholar
  79. Frohlich MW, Estabrook GF (2000) Wilkinson support calculated with exact probabilities: an example using Floricaula/LEAFY amino acid sequences that compares three hypotheses involving gene gain/loss in seed plants. Mol Biol Evol 17:1914–1925PubMedCrossRefGoogle Scholar
  80. Fu D, Dunbar M, Dubcovsky J (2007) Wheat VIN3-like PHD finger genes are up-regulated by vernalization. Mol Genet Genomics 277:301–313PubMedCrossRefGoogle Scholar
  81. Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiol 132:1107–1114PubMedPubMedCentralCrossRefGoogle Scholar
  82. Geraldo N, Baurle I, Kidou S, Hu X, Dean C (2009) FRIGIDA delays flowering in Arabidopsis via a cotranscriptional mechanism involving direct interaction with the nuclear cap-binding complex. Plant Physiol 150:1611–1618PubMedPubMedCentralCrossRefGoogle Scholar
  83. Gibson SI (2004) Sugar and phytohormone response pathways: navigating a signalling network. J Exp Bot 55:253–264PubMedCrossRefGoogle Scholar
  84. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H et al (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  85. González-Schain ND, Díaz-Mendoza M, Zurczak M, Suárez-López P (2012) Potato CONSTANS is involved in photoperiodic tuberization in a graft-transmissible manner. Plant J 70:678–690PubMedCrossRefGoogle Scholar
  86. Goodenough U, Lin H, Lee JH (2007) Sex determination in Chlamydomonas. Semin Cell Dev Biol 18:350–361PubMedCrossRefGoogle Scholar
  87. Graham LE, Cook ME, Busse JS (2000) The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc Natl Acad Sci USA 97:4535–4540PubMedPubMedCentralCrossRefGoogle Scholar
  88. Gramzow L, Theissen G (2010) A hitchhiker’s guide to the MADS world of plants. Genome Biol 11:214PubMedPubMedCentralCrossRefGoogle Scholar
  89. Greb T, Mylne JS, Crevillen P, Geraldo N, An H, Gendall AR, Dean C (2007) The PHD finger protein VRN5 functions in the epigenetic silencing of Arabidopsis FLC. Curr Biol 17:73–78PubMedCrossRefGoogle Scholar
  90. Greenup AG, Sasani S, Oliver SN, Walford SA, Millar AA, Trevaskis B (2011) Transcriptome analysis of the vernalization response in barley (Hordeum vulgare) seedlings. PLoS One 6:e17900PubMedPubMedCentralCrossRefGoogle Scholar
  91. Grossman A (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224PubMedCrossRefGoogle Scholar
  92. Halliday KJ, Salter MG, Thingnaes E, Whitelam GC (2003) Phytochrome control of flowering is temperature sensitive and correlates with expression of the floral integrator FT. Plant J 33:875–885PubMedCrossRefGoogle Scholar
  93. Hames C, Ptchelkine D, Grimm C, Thevenon E, Moyroud E, Gerard F, Martiel JL, Benlloch R, Parcy F, Muller CW (2008) Structural basis for LEAFY floral switch function and similarity with helix-turn-helix proteins. EMBO J 27:2628–2637PubMedPubMedCentralCrossRefGoogle Scholar
  94. Hartmann U, Hohmann S, Nettesheim K, Wisman E, Saedler H, Huijser P (2000) Molecular cloning of SVP: a negative regulator of the floral transition in Arabidopsis. Plant J 21:351–360PubMedCrossRefGoogle Scholar
  95. Haughn GW, Somerville CR (1988) Genetic control of morphogenesis in Arabidopsis. Dev Genet 9:73–89CrossRefGoogle Scholar
  96. Henschel K, Kofuji R, Hasebe M, Saedler H, Munster T, Theissen G (2002) Two ancient classes of MIKC-type MADS-box genes are present in the moss Physcomitrella patens. Mol Biol Evol 19:801–814PubMedCrossRefGoogle Scholar
  97. Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79PubMedCrossRefGoogle Scholar
  98. Higgins J, Bailey PC, Laurie DA (2010) Comparative genomics of flowering time pathways using Brachypodium distachyon as a model for the temperate grasses. PLoS One 5:e10065PubMedPubMedCentralCrossRefGoogle Scholar
  99. Himi S, Sano R, Nishiyama T, Tanahashi T, Kato M, Ueda K, Hasebe M (2001) Evolution of MADS-box gene induction by FLO/LFY genes. J Mol Evol 53:387–393PubMedCrossRefGoogle Scholar
  100. Honma T, Goto K (2001) Complexes of MADS-box proteins are sufficient to convert leaves into floral organs. Nature 409:525–529PubMedCrossRefGoogle Scholar
  101. Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138:4117–4129PubMedCrossRefGoogle Scholar
  102. Huijser P, Klein J, Lonnig WE, Meijer H, Saedler H, Sommer H (1992) Bracteomania, an inflorescence anomaly, is caused by the loss of function of the MADS-box gene squamosa in Antirrhinum majus. EMBO J 11:1239–1249PubMedPubMedCentralGoogle Scholar
  103. Imaizumi T, Schultz TF, Harmon FG, Ho LA, Kay SA (2005) FKF1 F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science 309:293–297PubMedCrossRefGoogle Scholar
  104. Irish VF (2010) The flowering of Arabidopsis flower development. Plant J 61:1014–1028PubMedCrossRefGoogle Scholar
  105. Irwin JA, Lister C, Soumpourou E, Zhang Y, Howell EC, Teakle G, Dean C (2012) Functional alleles of the flowering time regulator FRIGIDA in the Brassica oleracea genome. BMC Plant Biol 12:21PubMedPubMedCentralCrossRefGoogle Scholar
  106. Ito T (2011) Coordination of flower development by homeotic master regulators. Curr Opin Plant Biol 14:53–59PubMedCrossRefGoogle Scholar
  107. Ito S, Song YH, Josephson-Day AR, Miller RJ, Breton G, Olmstead RG, Imaizumi T (2012) FLOWERING BHLH transcriptional activators control expression of the photoperiodic flowering regulator CONSTANS in Arabidopsis. Proc Natl Acad Sci USA 109:3582–3587PubMedPubMedCentralCrossRefGoogle Scholar
  108. Izawa T, Takahashi Y, Yano M (2003) Comparative biology comes into bloom: genomic and genetic comparison of flowering pathways in rice and Arabidopsis. Curr Opin Plant Biol 6:113–120PubMedCrossRefGoogle Scholar
  109. Jack T (2001) Plant development going MADS. Plant Mol Biol 46:515–520PubMedCrossRefGoogle Scholar
  110. Jang S, Marchal V, Panigrahi KCS, Wenkel S, Soppe W, Deng XW, Valverde F, Coupland G (2008) Arabidopsis COP1 shapes the temporal pattern of CO accumulation conferring a photoperiodic flowering response. EMBO J 27:1277–1288PubMedPubMedCentralCrossRefGoogle Scholar
  111. Jetha K, Theissen G, Melzer R (2015) Arabidopsis SEPALLATA proteins differ in cooperative DNA-binding during the formation of floral quartet-like complexes. Nucleic Acids Res 42:10927–10942CrossRefGoogle Scholar
  112. Jofuku KD, den Boer BG, Van Montagu M, Okamuro JK (1994) Control of Arabidopsis flower and seed development by the homeotic gene APETALA2. Plant Cell 6:1211–1225PubMedPubMedCentralCrossRefGoogle Scholar
  113. Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290:344–347PubMedCrossRefGoogle Scholar
  114. Jossier M, Bouly JP, Meimoun P, Arjmand A, Lessard P, Hawley S, Grahame Hardie D, Thomas M (2009) SnRK1 (SNF1-related kinase 1) has a central role in sugar and ABA signalling in Arabidopsis thaliana. Plant J 59:316–328PubMedCrossRefGoogle Scholar
  115. Kang IH, Steffen JG, Portereiko MF, Lloyd A, Drews GN (2008) The AGL62 MADS domain protein regulates cellularization during endosperm development in Arabidopsis. Plant Cell 20:635–647PubMedPubMedCentralCrossRefGoogle Scholar
  116. Kanrar S, Bhattacharya M, Arthur B, Courtier J, Smith HM (2008) Regulatory networks that function to specify flower meristems require the function of homeobox genes PENNYWISE and POUND-FOOLISH in Arabidopsis. Plant J 54:924–937PubMedCrossRefGoogle Scholar
  117. Kant S, Peng M, Rothstein SJ (2011) Genetic regulation by NLA and microRNA827 for maintaining nitrate-dependent phosphate homeostasis in Arabidopsis. PLoS Genet 7:e1002021PubMedPubMedCentralCrossRefGoogle Scholar
  118. Kato Y, Imamura N (2008) Effect of sugars on amino acid transport by symbiotic Chlorella. Plant Physiol Biochem 46:911–917PubMedCrossRefGoogle Scholar
  119. Kaufmann K, Melzer R, Theissen G (2005) MIKC-type MADS-domain proteins: structural modularity, protein interactions and network evolution in land plants. Gene 347:183–198PubMedCrossRefGoogle Scholar
  120. Kaufmann K, Muino JM, Jauregui R, Airoldi CA, Smaczniak C, Krajewski P, Angenent GC (2009) Target genes of the MADS transcription factor SEPALLATA3: integration of developmental and hormonal pathways in the Arabidopsis flower. PLoS Biol 7:e1000090PubMedPubMedCentralCrossRefGoogle Scholar
  121. Kaufmann K, Wellmer F, Muino JM, Ferrier T, Wuest SE, Kumar V, Serrano-Mislata A, Madueno F, Krajewski P, Meyerowitz EM, Angenent GC, Riechmann JL (2010) Orchestration of floral initiation by APETALA1. Science 328:85–89PubMedCrossRefGoogle Scholar
  122. Keller SR, Levsen N, Ingvarsson PK, Olson MS, Tiffin P (2011) Local selection across a latitudinal gradient shapes nucleotide diversity in balsam poplar, Populus balsamifera L. Genetics 188:941–952PubMedPubMedCentralCrossRefGoogle Scholar
  123. Kim DH, Sung S (2013) Coordination of the vernalization response through a VIN3 and FLC gene family regulatory network in Arabidopsis. Plant Cell 25:454–469PubMedPubMedCentralCrossRefGoogle Scholar
  124. Kim DH, Sung S (2014) Genetic and epigenetic mechanisms underlying vernalization. Arabidopsis Book 12:e0171PubMedPubMedCentralCrossRefGoogle Scholar
  125. Kim DH, Doyle MR, Sung S, Amasino RM (2009) Vernalization: winter and the timing of flowering in plants. Annu Rev Cell Dev Biol 25:277–299PubMedCrossRefGoogle Scholar
  126. Kim JJ, Lee JH, Kim W, Jung HS, Huijser P, Ahn JH (2012) The microRNA156-SQUAMOSA PROMOTER BINDING PROTEIN-LIKE3 module regulates ambient temperature-responsive flowering via FLOWERING LOCUS T in Arabidopsis. Plant Physiol 159:461–478PubMedPubMedCentralCrossRefGoogle Scholar
  127. Kloosterman B, Abelenda JA, Gomez MDMC, Oortwijn M, de Boer JM, Kowitwanich K, Horvath BM, van Eck HJ, Smaczniak C, Prat S, Visser RGF, Bachem CWB (2013) Naturally occurring allele diversity allows potato cultivation in northern latitudes. Nature 495:246–250PubMedCrossRefGoogle Scholar
  128. Kofuji R, Sumikawa N, Yamasaki M, Kondo K, Ueda K, Ito M, Hasebe M (2003) Evolution and divergence of the MADS-box gene family based on genome-wide expression analyses. Mol Biol Evol 20:1963–1977PubMedCrossRefGoogle Scholar
  129. Kovach JD, Lamb RS (2014) There can be only one. Science 343:623–624PubMedCrossRefGoogle Scholar
  130. Koyama K, Hatano H, Nakamura J, Takumi S (2012) Characterization of three VERNALIZATION INSENSITIVE3-like (VIL) homologs in wild wheat, Aegilops tauschii Coss. Hereditas 149:62–71PubMedCrossRefGoogle Scholar
  131. Kramer EM, Hall JC (2005) Evolutionary dynamics of genes controlling floral development. Curr Opin Plant Biol 8:13–18PubMedCrossRefGoogle Scholar
  132. Krizek BA, Fletcher JC (2005) Molecular mechanisms of flower development: an armchair guide. Nat Rev Genet 6:688–698PubMedCrossRefGoogle Scholar
  133. Kuittinen H, Niittyvuopio A, Rinne P, Savolainen O (2008) Natural variation in Arabidopsis lyrata vernalization requirement conferred by a FRIGIDA indel polymorphism. Mol Biol Evol 25:319–329PubMedCrossRefGoogle Scholar
  134. Kumar SV, Wigge PA (2010) H2A.Z-containing nucleosomes mediate the thermosensory response in Arabidopsis. Cell 140:136–147PubMedCrossRefGoogle Scholar
  135. Kumar SV, Lucyshyn D, Jaeger KE, Alos E, Alvey E, Harberd NP, Wigge PA (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245PubMedCrossRefGoogle Scholar
  136. Kwantes M, Liebsch D, Verelst W (2012) How MIKC* MADS-box genes originated and evidence for their conserved function throughout the evolution of vascular plant gametophytes. Mol Biol Evol 29:293–302PubMedCrossRefGoogle Scholar
  137. Lamb RS, Hill TA, Tan QK, Irish VF (2002) Regulation of APETALA3 floral homeotic gene expression by meristem identity genes. Development 129:2079–2086PubMedGoogle Scholar
  138. Lawlor DW, Paul MJ (2014) Source/sink interactions underpin crop yield: the case for trehalose 6-phosphate/SnRK1 in improvement of wheat. Front Plant Sci 5:418. doi: 10.3389/fpls.2014.00418 PubMedPubMedCentralCrossRefGoogle Scholar
  139. Lazaro A, Valverde F, Pineiro M, Jarillo JA (2012) The Arabidopsis E3 Ubiquitin Ligase HOS1 negatively regulates CONSTANS abundance in the photoperiodic control of flowering. Plant Cell 24:982–999PubMedPubMedCentralCrossRefGoogle Scholar
  140. Lebon G, Wojnarowiez G, Holzapfel B, Fontaine F, Vaillant-Gaveau N, Clement C (2008) Sugars and flowering in the grapevine (Vitis vinifera L.). J Exp Bot 59:2565–2578PubMedCrossRefGoogle Scholar
  141. Ledger S, Strayer C, Ashton F, Sa K, Putterill J (2001) Analysis of the function of two circadian-regulated CONSTANS-LIKE genes. Plant J 26:15–22PubMedCrossRefGoogle Scholar
  142. Lee JH, Park SH, Lee JS, Ahn JH (2007) A conserved role of SHORT VEGETATIVE PHASE (SVP) in controlling flowering time of Brassica plants. Biochim Biophys Acta 1769:455–461PubMedCrossRefGoogle Scholar
  143. Lee J, Oh M, Park H, Lee I (2008) SOC1 translocated to the nucleus by interaction with AGL24 directly regulates leafy. Plant J 55:832–843PubMedCrossRefGoogle Scholar
  144. Lee H, Yoo SJ, Lee JH, Kim W, Yoo SK, Fitzgerald H, Carrington JC, Ahn JH (2010) Genetic framework for flowering-time regulation by ambient temperature-responsive miRNAs in Arabidopsis. Nucleic Acids Res 38:3081–3093PubMedPubMedCentralCrossRefGoogle Scholar
  145. Lee JH, Ryu HS, Chung KS, Pose D, Kim S, Schmid M, Ahn JH (2013) Regulation of temperature-responsive flowering by MADS-box transcription factor repressors. Science 342:628–632PubMedCrossRefGoogle Scholar
  146. Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243–246PubMedCrossRefGoogle Scholar
  147. Li Y, Huang J, Sandmann G, Chen F (2008) Glucose sensing and the mitochondrial alternative pathway are involved in the regulation of astaxanthin biosynthesis in the dark-grown Chlorella zofingiensis (Chlorophyceae). Planta 228:735–743PubMedCrossRefGoogle Scholar
  148. Li D, Yang C, Li X, Gan Q, Zhao X, Zhu L (2009) Functional characterization of rice OsDof12. Planta 229:1159–1169PubMedCrossRefGoogle Scholar
  149. Li P, Filiault D, Box MS, Kerdaffrec E, van Oosterhout C, Wilczek AM, Schmitt J, McMullan M, Bergelson J, Nordborg M et al (2014) Multiple FLC haplotypes defined by independent cis-regulatory variation underpin life history diversity in Arabidopsis thaliana. Genes Dev 28:1635–1640PubMedPubMedCentralCrossRefGoogle Scholar
  150. Lisso J, Schroder F, Mussig C (2013) EXO modifies sucrose and trehalose responses and connects the extracellular carbon status to growth. Front Plant Sci 4:219PubMedPubMedCentralCrossRefGoogle Scholar
  151. Liu C, Xi W, Shen L, Tan C, Yu H (2009) Regulation of floral patterning by flowering time genes. Dev Cell 16:711–722PubMedCrossRefGoogle Scholar
  152. Liu T, Li Y, Ren J, Qian Y, Yang X, Duan W, Hou X (2013) Nitrate or NaCl regulates floral induction in Arabidopsis thaliana. Biologia 68:215–222Google Scholar
  153. Loeppky HA, Coulman BE (2001) Residue removal and nitrogen fertilization affects tiller development and flowering in meadow bromegrass. Agron J 93:891–895CrossRefGoogle Scholar
  154. Lohmann JU, Weigel D (2002) Building beauty: the genetic control of floral patterning. Dev Cell 2:135–142PubMedCrossRefGoogle Scholar
  155. Lohmann JU, Hong RL, Hobe M, Busch MA, Parcy F, Simon R, Weigel D (2001) A molecular link between stem cell regulation and floral patterning in Arabidopsis. Cell 105:793–803PubMedCrossRefGoogle Scholar
  156. Loreti E, Matsukura C, Gubler F, Alpi A, Yamaguchi J, Perata P (2000) Glucose repression of alpha-amylase in barley embryos is independent of GAMYB transcription. Plant Mol Biol 44:85–90PubMedCrossRefGoogle Scholar
  157. Lovell JT, Juenger TE, Michaels SD, Lasky JR, Platt A, Richards JH, Yu X, Easlon HM, Sen S, McKay JK (2013) Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation. Proc Biol Sci 280:20131043PubMedPubMedCentralCrossRefGoogle Scholar
  158. Lucas-Reina E, Romero-Campero FJ, Romero JM, Valverde F (2015) An evolutionarily conserved DOF-CONSTANS module controls plant photoperiodic signalling. Plant Physiol 168(2):561–574. doi: 10.1104/pp.15.00321 PubMedPubMedCentralCrossRefGoogle Scholar
  159. Luo M, Platten D, Chaudhury A, Peacock WJ, Dennis ES (2009) Expression, imprinting, and evolution of rice homologs of the polycomb group genes. Mol Plant 2:711–723PubMedCrossRefGoogle Scholar
  160. Maizel A, Busch MA, Tanahashi T, Perkovic J, Kato M, Hasebe M, Weigel D (2005) The floral regulator LEAFY evolves by substitutions in the DNA binding domain. Science 308:260–263PubMedCrossRefGoogle Scholar
  161. Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377:522–524PubMedCrossRefGoogle Scholar
  162. Mandel MA, Gustafson-Brown C, Savidge B, Yanofsky MF (1992) Molecular characterization of the Arabidopsis floral homeotic gene APETALA1. Nature 360:273–277PubMedCrossRefGoogle Scholar
  163. Martinez-Barajas E, Delatte T, Schluepmann H, de Jong GJ, Somsen GW, Nunes C, Primavesi LF, Coello P, Mitchel RAC, Paul MJ (2011) Wheat grain development is characterized by remarkable trehalose 6-phosphate accumulation pregrain filling: tissue distribution and relationship to SNF1-related protein kinase1 activity. Plant Physiol 156:373–381PubMedPubMedCentralCrossRefGoogle Scholar
  164. Martínez-García JF, Virgós-Soler A, Prat S (2002) Control of photoperiod-regulated tuberization in potato by the Arabidopsis flowering-time gene CONSTANS. Proc Natl Acad Sci USA 99:15211–15216PubMedPubMedCentralCrossRefGoogle Scholar
  165. Masiero S, Colombo L, Grini PE, Schnittger A, Kater MM (2011) The emerging importance of type I MADS box transcription factors for plant reproduction. Plant Cell 23:865–872PubMedPubMedCentralCrossRefGoogle Scholar
  166. Matsoukas IG, Massiah AJ, Thomas B (2012) Florigenic and antiflorigenic signaling in plants. Plant Cell Physiol 53:1827–1842PubMedCrossRefGoogle Scholar
  167. Matsuo T, Ishiura M (2011) Chlamydomonas reinhardtii as a new model system for studying the molecular basis of the circadian clock. FEBS Lett 585:1495–1502PubMedCrossRefGoogle Scholar
  168. McClung CR (2014) Wheels within wheels: new transcriptional feedback loops in the Arabidopsis circadian clock. F1000Prime Rep 6:2PubMedPubMedCentralCrossRefGoogle Scholar
  169. McKim S, Hay A (2010) Patterning and evolution of floral structures—marking time. Curr Opin Genet Dev 20:448–453PubMedCrossRefGoogle Scholar
  170. Mellerowicz EJ, Horgan K, Walden A, Coker A, Walter C (1998) PRFLL—a Pinus radiata homologue of FLORICAULA and LEAFY is expressed in buds containing vegetative shoot and undifferentiated male cone primordia. Planta 206:619–629PubMedCrossRefGoogle Scholar
  171. Melzer R, Theissen G (2009) Reconstitution of ‘floral quartets’ in vitro involving class B and class E floral homeotic proteins. Nucleic Acids Res 37:2723–2736PubMedPubMedCentralCrossRefGoogle Scholar
  172. Melzer S, Lens F, Gennen J, Vanneste S, Rohde A, Beeckman T (2008) Flowering-time genes modulate meristem determinacy and growth form in Arabidopsis thaliana. Nat Genet 40:1489–1492PubMedCrossRefGoogle Scholar
  173. Melzer R, Verelst W, Theissen G (2009) The class E floral homeotic protein SEPALLATA3 is sufficient to loop DNA in ‘floral quartet’-like complexes in vitro. Nucleic Acids Res 37:144–157PubMedPubMedCentralCrossRefGoogle Scholar
  174. Meyerowitz EM (1997) Plants and the logic of development. Genetics 145:5–9PubMedPubMedCentralGoogle Scholar
  175. Michaels SD, Amasino RM (1999) The gibberellic acid biosynthesis mutant ga1-3 of Arabidopsis thaliana is responsive to vernalization. Dev Genet 25:194–198PubMedCrossRefGoogle Scholar
  176. Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. Plant Cell 13:935–941PubMedPubMedCentralCrossRefGoogle Scholar
  177. Michel G, Tonon T, Scornet D, Cock JM, Kloareg B (2010) Central and storage carbon metabolism of the brown alga Ectocarpus siliculosus: insights into the origin and evolution of storage carbohydrates in Eukaryotes. New Phytol 188:67–81PubMedCrossRefGoogle Scholar
  178. Moore B, Zhou L, Rolland F, Hall Q, Cheng WH, Liu YX, Hwang I, Jones T, Sheen J (2003) Role of the Arabidopsis glucose sensor HXK1 in nutrient, light, and hormonal signaling. Science 300:332–336PubMedCrossRefGoogle Scholar
  179. Moreno-Risueño MA, Martínez M, Vicente-Carbajosa J, Carbonero P (2007) The family of DOF transcription factors: from green unicellular algae to vascular plants. Mol Genet Genomics 277:379–390PubMedCrossRefGoogle Scholar
  180. Mouradov A, Glassick T, Hamdorf B, Murphy L, Fowler B, Marla S, Teasdale RD (1998) NEEDLY, a Pinus radiata ortholog of FLORICAULA/LEAFY genes, expressed in both reproductive and vegetative meristems. Proc Natl Acad Sci USA 95:6537–6542PubMedPubMedCentralCrossRefGoogle Scholar
  181. Moyroud E, Tichtinsky G, Parcy F (2009) The LEAFY floral regulators in Angiosperms: conserved proteins with diverse roles. J Plant Biol 52:177–185CrossRefGoogle Scholar
  182. Moyroud E, Kusters E, Monniaux M, Koes R, Parcy F (2010) LEAFY blossoms. Trends Plant Sci 15:346–352PubMedCrossRefGoogle Scholar
  183. Murphy RL, Klein RR, Morishige DT, Brady JA, Rooney WL, Miller FR, Dugas DV, Klein PE, Mullet JE (2011) Coincident light and clock regulation of pseudoresponse regulator protein 37 (PRR37) controls photoperiodic flowering in sorghum. Proc Natl Acad Sci USA 108:16469–16474PubMedPubMedCentralCrossRefGoogle Scholar
  184. Nakamura Y, Kato T, Yamashino T, Murakami M, Mizuno T (2007) Characterization of a set of phytochrome-interacting factor-like bHLH proteins in Oryza sativa. Biosci Biotech Biochem 71:1183–1191CrossRefGoogle Scholar
  185. Navarro C, Ja A, Cruz-Oró E, Cuéllar Ca Tamaki S, Silva J, Shimamoto K, Prat S (2011) Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–122PubMedCrossRefGoogle Scholar
  186. Ng M, Yanofsky MF (2001) Function and evolution of the plant MADS-box gene family. Nat Rev Genet 2:186–195PubMedCrossRefGoogle Scholar
  187. Noguero M, Atif RM, Ochatt S, Thompson RD (2013) The role of the DNA-binding One Zinc Finger (DOF) transcription factor family in plants. Plant Sci 209:32–45PubMedCrossRefGoogle Scholar
  188. Nunes C, Primavesi LF, Patel MK, Martinez-Barajas E, Powers SJ, Sagar R et al (2013) Inhibition of SnRK1 by metabolites: tissue-dependent effects and cooperative inhibition by glucose1-phosphate in combination with trehalose-6-phosphate. Plant Physiol Biochem 63:89–98PubMedCrossRefGoogle Scholar
  189. Núñez-Elisea R, Caldeira ML (1988) Induction of flowering in mango (Mangifera indica L.) within ammonium nitrate sprays. HortSci 23:883Google Scholar
  190. O’Maoileidigh DS, Graciet E, Wellmer F (2014) Gene networks controlling Arabidopsis thaliana flower development. New Phytol 201:16–30PubMedCrossRefGoogle Scholar
  191. Oesterhelt C, Gross W (2014) Different sugar kinases are involved in the sugar sensing of Galdieria sulphuraria. Plant Physiol 128:291–299CrossRefGoogle Scholar
  192. Ohto M, Onai K, Furukawa Y, Aoki E, Araki T, Nakamura K (2001) Effects of sugar on vegetative development and floral transition in Arabidopsis. Plant Physiol 127:252–261PubMedPubMedCentralCrossRefGoogle Scholar
  193. Okamuro JK, Caster B, Villarroel R, Van Montagu M, Jofuku KD (1997) The AP2 domain of APETALA2 defines a large new family of DNA binding proteins in Arabidopsis. Proc Natl Acad Sci USA 94:7076–7081PubMedPubMedCentralCrossRefGoogle Scholar
  194. Oliver SN, Finnegan EJ, Dennis ES, Peacock WJ, Trevaskis B (2009) Vernalization-induced flowering in cereals is associated with changes in histone methylation at the VERNALIZATION1 gene. Proc Natl Acad Sci USA 106:8386–8391PubMedPubMedCentralCrossRefGoogle Scholar
  195. Oliver SN, Deng W, Casao MC, Trevaskis B (2013) Low temperatures induce rapid changes in chromatin state and transcript levels of the cereal VERNALIZATION1 gene. J Exp Bot 64:2413–2422PubMedPubMedCentralCrossRefGoogle Scholar
  196. Ortiz-Marchena MI, Albi T, Lucas-Reina E, Said FE, Romero-Campero FJ, Cano B, Ruiz MT, Romero JM, Valverde F (2014) Photoperiodic control of carbon distribution during the floral transition in Arabidopsis thaliana. Plant Cell 26:565–584PubMedPubMedCentralCrossRefGoogle Scholar
  197. Pade N, Linka N, Ruth W, Weber APM, Hagemann M (2014) Floridoside and isofloridoside are synthesized by trehalose 6-phosphate synthase-like enzymes in the red alga Galdieria sulphuraria. New Phytol 205(3):1227–1238. doi: 10.1111/nph.13108 PubMedCrossRefGoogle Scholar
  198. Parcy F, Nilsson O, Busch MA, Lee I, Weigel D (1998) A genetic framework for floral patterning. Nature 395:561–566PubMedCrossRefGoogle Scholar
  199. Parenicova L, de Folter S, Kieffer M, Horner DS, Favalli C, Busscher J, Cook HE, Ingram RM, Kater MM, Davies B, Angenent GC, Colombo L (2003) Molecular and phylogenetic analyses of the complete MADS-box transcription factor family in Arabidopsis: new openings to the MADS world. Plant Cell 15:1538–1551PubMedPubMedCentralCrossRefGoogle Scholar
  200. Pego V, Kortstee AJ, Huijser C, Smeekens SCM (2000) Photosynthesis, sugars and the regulation of gene expression. J Exp Bot 51:407–416PubMedCrossRefGoogle Scholar
  201. Pelaz S, Ditta GS, Baumann E, Wisman E, Yanofsky MF (2000) B and C floral organ identity functions require SEPALLATA MADS-box genes. Nature 405:200–203PubMedCrossRefGoogle Scholar
  202. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJ, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–1400PubMedCrossRefGoogle Scholar
  203. Piñeiro M, Jarillo JA (2013) Ubiquitination in the control of photoperiodic flowering. Plant Sci 198:98–109PubMedCrossRefGoogle Scholar
  204. Pires N, Dolan L (2010) Early evolution of bHLH proteins in plants. Plant Signal Behav 5:911–912PubMedPubMedCentralCrossRefGoogle Scholar
  205. Poethig RS (2013) Vegetative phase change and shoot maturation in plants. Curr Top Dev Biol 105:125–152PubMedPubMedCentralCrossRefGoogle Scholar
  206. Portereiko MF, Lloyd A, Steffen JG, Punwani JA, Otsuga D, Drews GN (2006) AGL80 is required for central cell and endosperm development in Arabidopsis. Plant Cell 18:1862–1872PubMedPubMedCentralCrossRefGoogle Scholar
  207. Pose D, Yant L, Schmid M (2012) The end of innocence: flowering networks explode in complexity. Curr Opin Plant Biol 15:45–50PubMedCrossRefGoogle Scholar
  208. Pose D, Verhage L, Ott F, Yant L, Mathieu J, Angenent GC, Immink RG, Schmid M (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503:414–417PubMedCrossRefGoogle Scholar
  209. Preston JC, Sandve SR (2013) Adaptation to seasonality and the winter freeze. Front Plant Sci 4:167PubMedPubMedCentralGoogle Scholar
  210. Pugsley AT (1971) A genetic analysis of the spring-winter habit of growth in wheat. Aust J Agric Res 22:10CrossRefGoogle Scholar
  211. Ratcliffe OJ, Nadzan GC, Reuber TL, Riechmann JL (2001) Regulation of flowering in Arabidopsis by an FLC homologue. Plant Physiol 126:122–132PubMedPubMedCentralCrossRefGoogle Scholar
  212. Ratcliffe OJ, Kumimoto RW, Wong BJ, Riechmann JL (2003) Analysis of the Arabidopsis MADS AFFECTING FLOWERING gene family: MAF2 prevents vernalization by short periods of cold. Plant Cell 15:1159–1169PubMedPubMedCentralCrossRefGoogle Scholar
  213. Ream TS, Woods DP, Amasino RM (2012) The molecular basis of vernalization in different plant groups. Cold Spring Harb Symp Quant Biol 77:105–115PubMedCrossRefGoogle Scholar
  214. Ream TS, Woods DP, Schwartz CJ, Sanabria CP, Mahoy JA, Walters EM, Kaeppler HF, Amasino RM (2014) Interaction of photoperiod and vernalization determines flowering time of Brachypodium distachyon. Plant Physiol 164:694–709PubMedPubMedCentralCrossRefGoogle Scholar
  215. Reeves PA, He Y, Schmitz RJ, Amasino RM, Panella LW, Richards CM (2007) Evolutionary conservation of the FLOWERING LOCUS C-mediated vernalization response: evidence from the sugar beet (Beta vulgaris). Genetics 176:295–307PubMedPubMedCentralCrossRefGoogle Scholar
  216. Reisdorph NA, Small GD (2004) The CPH1 gene of Chlamydomonas reinhardtii encodes two forms of cryptochrome whose levels are controlled by light-induced proteolysis 1 [w]. Plant Physiol 134:1546–1554PubMedPubMedCentralCrossRefGoogle Scholar
  217. Riaño-Pachón DM, Corrêa LGG, Trejos-Espinosa R, Mueller-Roeber B (2008) Green transcription factors: a chlamydomonas overview. Genetics 179:31–39PubMedPubMedCentralCrossRefGoogle Scholar
  218. Riechmann JL, Meyerowitz EM (1997) MADS domain proteins in plant development. Biol Chem 378:1079–1101PubMedGoogle Scholar
  219. Riechmann JL, Meyerowitz EM (1998) The AP2/EREBP family of plant transcription factors. Biol Chem 379:633–646PubMedGoogle Scholar
  220. Risk JM, Laurie RE, Macknight RC, Day CL (2010) FRIGIDA and related proteins have a conserved central domain and family specific N- and C-terminal regions that are functionally important. Plant Mol Biol 73:493–505PubMedCrossRefGoogle Scholar
  221. Robaglia C, Thomas M, Meyer C (2012) Sensing nutrient and energy status by SnRK1 and TOR kinases. Curr Opin Plant Biol 57:301–307CrossRefGoogle Scholar
  222. Rockwell NC, Duanmu D, Martin SS, Bachy C, Price DC, Bhattacharya D, Worden AZ, Lagarias JC (2014) Eukaryotic algal phytochromes span the visible spectrum. Proc Natl Acad Sci USA 111:3871–3876PubMedPubMedCentralCrossRefGoogle Scholar
  223. Roldan M, Gomez-Mena C, Ruiz-Garcia L, Salinas J, Martinez-Zapater JM (1999) Sucrose availability on the aerial part of the plant promotes morphogenesis and flowering of Arabidopsis in the dark. Plant J 20:581–590PubMedCrossRefGoogle Scholar
  224. Rolland F, Baena-González E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709PubMedCrossRefGoogle Scholar
  225. Romero JM, Valverde F (2009) Evolutionarily conserved photoperiod mechanisms in plants. Plant Signal Behav 4:642–644PubMedPubMedCentralCrossRefGoogle Scholar
  226. Romero-Campero FJ, Lucas-Reina E, Said FE, Romero JM, Valverde F (2013) A contribution to the study of plant development evolution based on gene co-expression networks. Front Plant Sci 4:1–17CrossRefGoogle Scholar
  227. Rubio V, Deng XW (2007) Plant science: standing on the shoulders of GIGANTEA. Science 318:206–207PubMedCrossRefGoogle Scholar
  228. Ruelens P, de Maagd RA, Proost S, Theissen G, Geuten K, Kaufmann K (2013) FLOWERING LOCUS C in monocots and the tandem origin of angiosperm-specific MADS-box genes. Nat Commun 4:2280PubMedCrossRefGoogle Scholar
  229. Samach A, Wigge PA (2005) Ambient temperature perception in plants. Curr Opin Plant Biol 8:483–486PubMedCrossRefGoogle Scholar
  230. Sawa M, Kay SA (2011) GIGANTEA directly activates Flowering Locus T in Arabidopsis thaliana. Proc Natl Acad Sci USA 28:11698–11703CrossRefGoogle Scholar
  231. Sayou C, Monniaux M, Nanao MH, Moyroud E, Brockington SF, Thevenon E, Chahtane H, Warthmann N, Melkonian M, Zhang Y, Wong GK, Weigel D, Parcy F, Dumas R (2014) A promiscuous intermediate underlies the evolution of LEAFY DNA binding specificity. Science 343:645–648PubMedCrossRefGoogle Scholar
  232. Schluepmann H, Pellny T, van Dijken A, Smeekens S, Paul M (2003) Trehalose 6-phosphate is indispensable for carbohydrate utilization and growth in Arabidopsis thaliana. Proc Natl Acad Sci USA 100:6849–6854PubMedPubMedCentralCrossRefGoogle Scholar
  233. Schranz ME, Quijada P, Sung SB, Lukens L, Amasino R, Osborn TC (2002) Characterization and effects of the replicated flowering time gene FLC in Brassica rapa. Genetics 162:1457–1468PubMedPubMedCentralGoogle Scholar
  234. Schroder F, Lisso J, Lange P, Mussig C (2009) The extracellular EXO protein mediates cell expansion in Arabidopsis leaves. BMC Plant Biol 9:20PubMedPubMedCentralCrossRefGoogle Scholar
  235. Schultz EA, Haughn GW (1991) LEAFY, a homeotic gene that regulates inflorescence development in Arabidopsis. Plant Cell 3:771–781PubMedPubMedCentralCrossRefGoogle Scholar
  236. Schulze T, Prager K, Dathe H, Kelm J, Kiessling P, Mittag M (2010) How the green alga Chlamydomonas reinhardtii keeps time. Protoplasma 244:3–14PubMedCrossRefGoogle Scholar
  237. Schwarz-Sommer Z, Huijser P, Nacken W, Saedler H, Sommer H (1990) Genetic control of flower development by homeotic genes in Antirrhinum majus. Science 250:931–936PubMedCrossRefGoogle Scholar
  238. Scortecci KC, Michaels SD, Amasino RM (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J 26:229–236PubMedCrossRefGoogle Scholar
  239. Serrano G, Herrera-palau R, Romero JM, Serrano A, Coupland G, Valverde F (2009) Chlamydomonas CONSTANS and the evolution of plant photoperiodic signaling. Curr Biol 19:359–368PubMedCrossRefGoogle Scholar
  240. Sharma KK, Schuhmann H, Schenk PM (2012) High lipid induction in microalgae for biodiesel production. Energies 5:1532–1553CrossRefGoogle Scholar
  241. Sheldon CC, Burn JE, Perez PP, Metzger J, Edwards JA, Peacock WJ, Dennis ES (1999) The FLF MADS box gene: a repressor of flowering in Arabidopsis regulated by vernalization and methylation. Plant Cell 11:445–458PubMedPubMedCentralCrossRefGoogle Scholar
  242. Shindo S, Sakakibara K, Sano R, Ueda K, Hasebe M (2001) Characterization of a FLORICAULA/LEAFY homologue of Gnetum parvifolium and its implications for the evolution of reproductive organs in seed plants. Int J Plant Sci 162:1199–1209CrossRefGoogle Scholar
  243. Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiol 138:1163–1173PubMedPubMedCentralCrossRefGoogle Scholar
  244. Simonini S, Roig-Villanova I, Gregis V, Colombo B, Colombo L, Kater MM (2012) Basic pentacysteine proteins mediate MADS domain complex binding to the DNA for tissue-specific expression of target genes in Arabidopsis. Plant Cell 24:4163–4172PubMedPubMedCentralCrossRefGoogle Scholar
  245. Slotte T, Huang H, Lascoux M, Ceplitis A (2008) Polyploid speciation did not confer instant reproductive isolation in Capsella (Brassicaceae). Mol Biol Evol 25:1472–1481PubMedCrossRefGoogle Scholar
  246. Smaczniak C, Immink RG, Angenent GC, Kaufmann K (2012a) Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139:3081–3098PubMedCrossRefGoogle Scholar
  247. Smaczniak C, Immink RG, Muino JM, Blanvillain R, Busscher M, Busscher-Lange J, Dinh QD, Liu S, Westphal AH, Boeren S, Parcy F, Xu L, Carles CC, Angenent GC, Kaufmann K (2012b) Characterization of MADS-domain transcription factor complexes in Arabidopsis flower development. Proc Natl Acad Sci USA 109:1560–1565PubMedPubMedCentralCrossRefGoogle Scholar
  248. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13:274–279PubMedCrossRefGoogle Scholar
  249. Smith HM, 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 62:583–593PubMedPubMedCentralCrossRefGoogle Scholar
  250. Sommer H, Beltran JP, Huijser P, Pape H, Lonnig WE, Saedler H, Schwarz-Sommer Z (1990) Deficiens, a homeotic gene involved in the control of flower morphogenesis in Antirrhinum majus: the protein shows homology to transcription factors. EMBO J 9:605–613PubMedPubMedCentralGoogle Scholar
  251. Song J, Angel A, Howard M, Dean C (2012a) Vernalization—a cold-induced epigenetic switch. J Cell Sci 125:3723–3731PubMedCrossRefGoogle Scholar
  252. Song Y, Gao Z, Luan W (2012b) Interaction between temperature and photoperiod. Sci China Life Sci 55:241–249PubMedCrossRefGoogle Scholar
  253. Song YH, Smith RW, To BJ, Millar AJ, Imaizumi T (2012c) FKF1 conveys timing information for CONSTANS stabilization in photoperiodic flowering. Science 336:1045–1049PubMedPubMedCentralCrossRefGoogle Scholar
  254. Song XM, Huang ZN, Duan WK, Ren J, Liu TK, Li Y, Hou XL (2014) Genome-wide analysis of the bHLH transcription factor family in Chinese cabbage (Brassica rapa ssp. pekinensis). Mol Genet Genomics 289:77–91PubMedCrossRefGoogle Scholar
  255. Srikanth A, Schmid M (2011) Regulation of flowering time: all roads lead to Rome. Cell Mol Life Sci 68:2013–2037PubMedCrossRefGoogle Scholar
  256. Steffen JG, Kang IH, Portereiko MF, Lloyd A, Drews GN (2008) AGL61 interacts with AGL80 and is required for central cell development in Arabidopsis. Plant Physiol 148:259–268PubMedPubMedCentralCrossRefGoogle Scholar
  257. Sung S, Amasino RM (2004a) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7:4–10PubMedCrossRefGoogle Scholar
  258. Sung S, Amasino RM (2004b) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164PubMedCrossRefGoogle Scholar
  259. Sung S, Schmitz RJ, Amasino RM (2006) A PHD finger protein involved in both the vernalization and photoperiod pathways in Arabidopsis. Genes Dev 20:3244–3248PubMedPubMedCentralCrossRefGoogle Scholar
  260. Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802PubMedCrossRefGoogle Scholar
  261. Tadege M, Sheldon CC, Helliwell CA, Stoutjesdijk P, Dennis ES, Peacock WJ (2001) Control of flowering time by FLC orthologues in Brassica napus. Plant J 28:545–553PubMedCrossRefGoogle Scholar
  262. Tanabe Y, Hasebe M, Sekimoto H, Nishiyama T, Kitani M, Henschel K, Munster T, Theissen G, Nozaki H, Ito M (2005) Characterization of MADS-box genes in charophycean green algae and its implication for the evolution of MADS-box genes. Proc Natl Acad Sci USA 102:2436–2441PubMedPubMedCentralCrossRefGoogle Scholar
  263. Tanahashi T, Sumikawa N, Kato M, Hasebe M (2005) Diversification of gene function: homologs of the floral regulator FLO/LFY control the first zygotic cell division in the moss Physcomitrella patens. Development 132:1727–1736PubMedCrossRefGoogle Scholar
  264. Theissen G (2001) Development of floral organ identity: stories from the MADS house. Curr Opin Plant Biol 4:75–85PubMedCrossRefGoogle Scholar
  265. Theissen G, Melzer R (2007a) Combinatorial control of floral organ identity by MADS-domain transcription factors. In: Annual plant reviews, vol 29: regulation of transcription in plants. Blackwell, Oxford, pp 253–265Google Scholar
  266. Theissen G, Melzer R (2007b) Molecular mechanisms underlying origin and diversification of the angiosperm flower. Ann Bot 100:603–619PubMedPubMedCentralCrossRefGoogle Scholar
  267. Theissen G, Saedler H (2001) Plant biology. Floral quartets. Nature 409:469–471PubMedCrossRefGoogle Scholar
  268. Theissen G, Becker A, Di Rosa A, Kanno A, Kim JT, Munster T, Winter KU, Saedler H (2000) A short history of MADS-box genes in plants. Plant Mol Biol 42:115–149PubMedCrossRefGoogle Scholar
  269. Trevaskis B, Bagnall DJ, Ellis MH, Peacock WJ, Dennis ES (2003) MADS box genes control vernalization-induced flowering in cereals. Proc Natl Acad Sci USA 100:13099–13104PubMedPubMedCentralCrossRefGoogle Scholar
  270. Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357PubMedCrossRefGoogle Scholar
  271. Tsai AYL, Gazzarrini S (2014) Trehalose-6-phosphate and SnRK1 kinases in plant development and signalling: the emerging picture. Front Plant Sci 5:119. doi: 10.3389/fpls.2014.00119 PubMedPubMedCentralCrossRefGoogle Scholar
  272. Turck F, Fornara F, Coupland G (2008) Regulation and identity of florigen: FLOWERING LOCUS T moves center stage. Annu Rev Plant Biol 59:573–594PubMedCrossRefGoogle Scholar
  273. Valverde F (2011) CONSTANS and the evolutionary origin of photoperiodic timing of flowering. J Exp Bot 62:2453–2463PubMedCrossRefGoogle Scholar
  274. Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006PubMedCrossRefGoogle Scholar
  275. Valverde F, Ortega JM, Losada M, Serrano A (2005) Sugar-mediated transcriptional regulation of the Gap gene system and concerted photosystem II functional modulation in the microalga Scenedesmus vacuolatus. Planta 221:937–952PubMedCrossRefGoogle Scholar
  276. van Mourik S, van Dijk A, de Gee M, Immink R, Kaufmann K, Angenent G, van Ham R, Molenaar J (2010) Continuous-time modeling of cell fate determination in Arabidopsis flowers. BMC Syst Biol 4:101PubMedPubMedCentralCrossRefGoogle Scholar
  277. Vandenbussche M, Zethof J, Souer E, Koes R, Tornielli GB, Pezzotti M, Ferrario S, Angenent GC, Gerats T (2003) Toward the analysis of the petunia MADS box gene family by reverse and forward transposon insertion mutagenesis approaches: B, C, and D floral organ identity functions require SEPALLATA-like MADS box genes in petunia. Plant Cell 15:2680–2693PubMedPubMedCentralCrossRefGoogle Scholar
  278. Verhage L, Angenent GC, Immink RG (2014) Research on floral timing by ambient temperature comes into blossom. Trends Plant Sci 9:583–591CrossRefGoogle Scholar
  279. Wagner D, Sablowski RW, Meyerowitz EM (1999) Transcriptional activation of APETALA1 by LEAFY. Science 285:582–584PubMedCrossRefGoogle Scholar
  280. Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–707PubMedCrossRefGoogle Scholar
  281. Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani MC (2009) PEP1 regulates perennial flowering in Arabis alpina. Nature 459:423–427PubMedCrossRefGoogle Scholar
  282. Wang H, Zhang Z, Li H, Zhao X, Liu X, Ortiz M, Lin C, Liu B (2013) CONSTANS-LIKE 7 regulates branching and shade avoidance response in Arabidopsis. J Exp Bot 64:1017–1024PubMedPubMedCentralCrossRefGoogle Scholar
  283. Weigel D (1995) The APETALA2 domain is related to a novel type of DNA binding domain. Plant Cell 7:388–389PubMedPubMedCentralCrossRefGoogle Scholar
  284. Weigel D, Nilsson O (1995) A developmental switch sufficient for flower initiation in diverse plants. Nature 377:495–500PubMedCrossRefGoogle Scholar
  285. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69:843–859PubMedCrossRefGoogle Scholar
  286. Wellmer F, Graciet E, Riechmann JL (2014) Specification of floral organs in Arabidopsis. J Exp Bot 65:1–9PubMedCrossRefGoogle Scholar
  287. Werner JD, Borevitz JO, Warthmann N, Trainer GT, Ecker JR, Chory J, Weigel D (2005) Quantitative trait locus mapping and DNA array hybridization identify an FLM deletion as a cause for natural flowering-time variation. Proc Natl Acad Sci USA 102:2460–2465PubMedPubMedCentralCrossRefGoogle Scholar
  288. Westerman JM, Lawrence MJ (1970) Genotype-environment interaction and developmental regulation in Arabidopsis thaliana. I. Inbred lines; description. Heredity 25:18Google Scholar
  289. Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M, Lohmann JU, Weigel D (2005) Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–1059PubMedCrossRefGoogle Scholar
  290. Wu L, Birch RG (2010) Physiological basis for enhanced sucrose accumulation in an engineered sugarcane cell line. Funct Plant Biol 37:1161–1174CrossRefGoogle Scholar
  291. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133:3539–3547PubMedPubMedCentralCrossRefGoogle Scholar
  292. Wynne J, Treisman R (1992) SRF and MCM1 have related but distinct DNA binding specificities. Nucleic Acids Res 20:3297–3303PubMedPubMedCentralCrossRefGoogle Scholar
  293. Xiao J, Xu S, Li C, Xu Y, Xing L, Niu Y, Huan Q, Tang Y, Zhao C, Wagner D et al (2014) O-GlcNAc-mediated interaction between VER2 and TaGRP2 elicits TaVRN1 mRNA accumulation during vernalization in winter wheat. Nat Commun 5:4572PubMedPubMedCentralCrossRefGoogle Scholar
  294. Xue W, Xing Y, Weng X, Zhao Y, Tang W, Wang L, Zhou H, Yu S, Xu C, Li X, Zhang Q (2008) Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat Genet 40:761–767PubMedCrossRefGoogle Scholar
  295. Yamaguchi A, Wu MF, Yang L, Wu G, Poethig RS, Wagner D (2009) The microRNA-regulated SBP-Box transcription factor SPL3 is a direct upstream activator of LEAFY, FRUITFULL, and APETALA1. Dev Cell 17:268–278PubMedPubMedCentralCrossRefGoogle Scholar
  296. Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalization gene VRN1. Proc Natl Acad Sci USA 100:6263–6268PubMedPubMedCentralCrossRefGoogle Scholar
  297. Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644PubMedPubMedCentralCrossRefGoogle Scholar
  298. Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci USA 103:19581–19586PubMedPubMedCentralCrossRefGoogle Scholar
  299. Yang J, Yang MF, Zhang WP, Chen F, Shen SH (2011) A putative flowering-time-related Dof transcription factor gene, JcDof3, is controlled by the circadian clock in Jatropha curcas. Plant Sci 181:667–674PubMedCrossRefGoogle Scholar
  300. Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T (2000) Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–2484PubMedPubMedCentralCrossRefGoogle Scholar
  301. Yanofsky MF, Ma H, Bowman JL, Drews GN, Feldmann KA, Meyerowitz EM (1990) The protein encoded by the Arabidopsis homeotic gene agamous resembles transcription factors. Nature 346:35–39PubMedCrossRefGoogle Scholar
  302. Zhang B, Pan X, Cannon CH, Cobb GP, Anderson TA (2006) Conservation and divergence of plant microRNA genes. Plant J 46:243–259PubMedCrossRefGoogle Scholar
  303. Zhang Y, Primavesi LF, Jhurreea D, Andraloja PC, Mitchell RA, Powers SJ, Schluepmann H, Delatte T, Wingler A, Paul MJ (2009) Inhibition of SNF1-related protein kinase 1 and regulation of metabolic pathway by trehalose. Plant Physiol 149:1860–1871PubMedPubMedCentralCrossRefGoogle Scholar
  304. Zhou L, Jang JC, Jones TL, Sheen J (1998) Glucose and ethylene signal transduction crosstalk revealed by an Arabidopsis glucose-insensitive mutant. Proc Natl Acad Sci USA 95:10294–10299PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Eva Lucas-Reina
    • 1
  • M Isabel Ortiz-Marchena
    • 1
  • Francisco J. Romero-Campero
    • 2
  • Myriam Calonje
    • 1
  • José M. Romero
    • 1
  • Federico Valverde
    • 1
    Email author
  1. 1.Institute for Plant Biochemistry and PhotosynthesisPlant Development Unit, CSIC and Universidad de SevillaSevilleSpain
  2. 2.Department of Computational Sciences and Artificial IntelligenceResearch Group in Natural Computing, Universidad de SevillaSevilleSpain

Personalised recommendations