Flowering in Chenopodium and Related Amaranths

Part of the Compendium of Plant Genomes book series (CPG)


The transition from the vegetative to the reproductive phase is a crucial event in plant development. The floral induction is tightly controlled at multiple levels. While physiological and anatomical studies of flowering have begun in the nineteenth century, the genetic basis of the floral induction remained concealed until the end of the twentieth century. The molecular regulatory pathways mediating the responses to environmental and endogenous cues were first revealed in the model plant Arabidopsis thaliana, later in Oryza sativa (rice), and other crops. Knowledge on flowering in wild species proceeded in much slower pace. Little research was devoted to the family Amaranthaceae, except for the agriculturally important sugar beet. Nowadays, this picture starts to change owing to the availability of genomic and transcriptomic resources in non-model organisms. This review outlines basic characteristics of the regulation of flowering in model plants and summarizes current knowledge on this topic in the genus Chenopodium and its relatives.



The author is grateful to James D. Stone for critically reading the manuscript and for linguistic correction. This study was supported by the Czech Science Foundation (13-02290S).


  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 309:1052–1056PubMedCrossRefGoogle Scholar
  2. Allard HA, Garner WW (1940) Further observations on the response of various species of plants to length of day. US Department of Agriculture Technical Bulletin, p 727Google Scholar
  3. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61:1001–1013PubMedCrossRefGoogle Scholar
  4. An H, Roussot C, Suárez-López P et al (2004) CONSTANS acts in the phloem to regulate a systemic signal that induces photoperiodic flowering of Arabidopsis. Development 131:3615–3626PubMedCrossRefGoogle Scholar
  5. Andres F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639PubMedCrossRefGoogle Scholar
  6. Arnao MB, Hernandez-Ruiz J (2015) Functions of melatonin in plants: a review. J Pineal Res 59:133–150PubMedCrossRefGoogle Scholar
  7. 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
  8. Bendevis MA, Sun YJ, Shabala S, Rosenqvist E, Liu FL, Jacobsen SE (2014) Differentiation of photoperiod-induced ABA and soluble sugar responses of two Quinoa (Chenopodium quinoa Willd.) Cultivars. J Plant Growth Regul 33:562–570CrossRefGoogle Scholar
  9. Benlloch R, Berbel A, Serrano-Mislata A, Madueno F (2007) Floral initiation and inflorescence architecture: a comparative view. Ann Bot 100:659–676PubMedPubMedCentralCrossRefGoogle Scholar
  10. Bertero HD, King RW, Hall AJ (1999a) Photoperiod-sensitive development phases in quinoa (Chenopodium quinoa Willd.). Field Crop Res 60:231–243CrossRefGoogle Scholar
  11. Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993) Physiological signals that induce flowering. Plant Cell 5:1147–1155Google Scholar
  12. Bertero HD, King RW, Hall AJ (1999b) Modelling photoperiod and temperature responses of flowering in quinoa (Chenopodium quinoa Willd.). Field Crop Res 63:19–34CrossRefGoogle Scholar
  13. Blackman BK, Strasburg JL, Raduski AR, Michaels SD, Rieseberg LH (2010) The role of recently derived FT paralogs in sunflower domestication. Curr Biol 20:629–635PubMedPubMedCentralCrossRefGoogle Scholar
  14. Blažková A, Macháčková I, Eder J, Krekule J (2001) Benzyladenine-induced inhibition of flowering in Chenopodium rubrum in vitro is not related to the levels of isoprenoid cytokinins. Plant Growth Regul 34:159–166CrossRefGoogle Scholar
  15. Blazquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171PubMedCrossRefGoogle Scholar
  16. Cháb D, Kolář J, Olson MS, Štorchová H (2008) Two Flowering Locus T (FT) homologs in Chenopodium rubrum differ in expression patterns. Planta 228:929–940PubMedCrossRefGoogle Scholar
  17. Chailakhyan MK (1936) New facts in support of the hormonal theory of plant development C R Acad Sci URSS 13:79–83Google Scholar
  18. Chia TYP, Muller A, Jung C, Mutasa-Gottgens ES (2008) Sugar beet contains a large CONSTANS-LIKE gene family including a CO homologue that is independent of the early-bolting (B) gene locus. J Exp Bot 59:2735–2748PubMedPubMedCentralCrossRefGoogle Scholar
  19. Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J 90:708–719PubMedCrossRefGoogle Scholar
  20. Christiansen JL, Jacobsen SE, Jorgensen ST (2010) Photoperiodic effect on flowering and seed development in quinoa (Chenopodium quinoa Willd.). Acta Agric Scand Sect B-Soil Plant Sci 60:539–544Google Scholar
  21. Corbesier L, Vincent C, Jang SH, Fornara F, Fan QZ et al (2007) FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–1033PubMedCrossRefGoogle Scholar
  22. Cumming BG (1959) Extreme sensitivity of germination and photoperiodic reaction in the genus Chenopodium (Tourn) L Nature 184:1044–1045Google Scholar
  23. Cumming BG, Hendricks SB, Borthwick HA (1965) Rhythmic flowering responses and phytochrome changes in a selection of Chenopodium rubrum. Can J Bot 43:825–853CrossRefGoogle Scholar
  24. Cumming BG (1967) Early-flowering plants. In: Wilt FH, Wessels NK (eds) Methods in developmental biology. Crowell Co, New York, pp 277–299Google Scholar
  25. Dally N, Xiao K, Holtgraewe D, Jung C (2014) The B2 flowering time locus of beet encodes a zinc finger transcription factor. Proc Natl Acad Sci USA 111:10365–10370PubMedCrossRefGoogle Scholar
  26. Deng WW, 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 108:6680–6685PubMedCrossRefGoogle Scholar
  27. 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-Iike gene expression independently of Hd1. Genes Dev 18:926–936Google Scholar
  28. Drabešová J, Cháb D, Kolář J, Haškovcová K, Štorchová H (2014) A darklight transition triggers expression of the floral promoter CrFTL1 and downregulates CONSTANS-like genes in a short-day plant Chenopodium rubrum. J Exp Bot 65:2137–2146PubMedPubMedCentralCrossRefGoogle Scholar
  29. Drabešová J, Černá L, Mašterová H, Koloušková P, Potocký M, Štorchová H (2016) The evolution of the FT/TFL1 genes in Amaranthaceae and their expression patterns in the course of vegetative growth and flowering in Chenopodium rubrum. G3-genes. Genom Genet 6:3066–3076Google Scholar
  30. Fuentes-Bazan, S, G Mansion, and T Borsch, 2012 Towards a species level tree of the globally diverse genus Chenopodium (Chenopodiaceae) Mol Phylogenet Evol 62: 359–374Google Scholar
  31. Fuller HJ (1949) Photoperiodic responses of Chenopodium quinoa Willd. and Amaranthus caudatus L. Am J Bot 36:175–180CrossRefGoogle Scholar
  32. Hayama R, Agashe B, Luley E, King R, Coupland G (2007) A circadian rhythm set by dusk determines the expression of FT homologs and the short-day photoperiodic flowering response in Pharbitis. Plant Cell 19:2988–3000PubMedPubMedCentralCrossRefGoogle Scholar
  33. Izawa T, Oikawa T, Sugiyama N, Tanisaka T, Yano M, Shimamoto K (2002) Phytochrome mediates the external light signal to repress FT orthologs in photoperiodic flowering of rice. Genes Dev 16:2006–2020PubMedPubMedCentralCrossRefGoogle Scholar
  34. Jacobsen SE, Jensen CR, Liu F (2012) Improving crop production in the arid Mediterranean climate. Field Crop Res 128:34–47CrossRefGoogle Scholar
  35. Jarvis DE, Ho YS, Lightfoot DJ, Schmockel SM, Li B, Borm TJA et al (2017) The genome of Chenopodium quinoa. Nature 542:307–312PubMedCrossRefGoogle Scholar
  36. 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
  37. King RW (1972) Timing in Chenopodium rubrum of export of the floral stimulus from the cotyledons and its action at the shoot apex. Can J Bot 50:697–702CrossRefGoogle Scholar
  38. Kolář J, Johnson CH, Macháčková I (2003) Exogenously applied melatonin (N-acetyl-5-methoxytryptamine) affects flowering of the short-day plant Chenopodium rubrum. Physiol Plant 118:605–612CrossRefGoogle Scholar
  39. Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K (2008) Hd3a and RFT1 are essential for flowering in rice. Development 135:767–774PubMedCrossRefGoogle Scholar
  40. Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T, Araki T, Yano M (2002) Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short day conditions. Plant Cell Physiol 43:1096–1105Google Scholar
  41. Komiya R, Yokoi S, Shimamoto K (2009) A gene network for long-day flowering activates RFT1 encoding a mobile flowering signal in rice. Development 136:3443–3450PubMedCrossRefGoogle Scholar
  42. Koornneef M, Hanhart CJ, Vanderveen JH (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet 229:57–66Google Scholar
  43. Lee R, Baldwin S, Kenel F, McCallum J, Macknight R (2013) FLOWERING LOCUS T genes control onion bulb formation and flowering. Nat Commun 4:2884PubMedCrossRefGoogle Scholar
  44. Lexander K (1980) Present knowledge of sugar beet bolting mechanisms. In: Proceedings of the 43rd winter congress of the International Institute of Sugar Beet Research, pp 245–258Google Scholar
  45. Li C, Dubcovsky J (2008) Wheat FT protein regulates VRN1 transcription through interactions with FDL2. Plant J 55:543–554PubMedPubMedCentralCrossRefGoogle Scholar
  46. Li DM, Lu FB, Zhu GF, Sun YB, Liu HL, Liu JW, Wang Z (2014) Molecular characterization and functional analysis of a FLOWERING LOCUS T homolog gene from a Phalaenopsis orchid. Genet Mol Res 13:5982–5994PubMedCrossRefGoogle Scholar
  47. Lifschitz E, Eviatar T, Rozman A, Shalit A, Goldshmidt A, Amsellem Z, Alvarez JP, Eshed Y (2006) The tomato FT ortholog triggers systemic signals that regulate growth and flowering and substitute for diverse environmental stimuli. Proc Natl Acad Sci USA 103:6398–6403PubMedCrossRefGoogle Scholar
  48. Lifschitz E, Ayre BG, Eshed Y (2014) Florigen and anti-florigen - a systemic mechanism for coordinating growth and termination in flowering plants. Front Plant Sci 5:465PubMedPubMedCentralCrossRefGoogle Scholar
  49. Liu J, Yu J, McIntosh L, Kende H, Zeevaart JA (2001) Isolation of a CONSTANS ortholog from Pharbitis nil and its role in flowering. Plant Physiol 125:1821–1830PubMedPubMedCentralCrossRefGoogle Scholar
  50. Liu L, Liu C, Hou XL, Xi WY, Shen LS, Tao Z, Wang Y, Yu H (2012) FTIP1 is an essential regulator required for florigen transport. PLoS Biol 10:e1001313PubMedPubMedCentralCrossRefGoogle Scholar
  51. Macháčková I, Krekule J, Eder J, Seidlová F, Strnad M (1993) Cytokinins in photoperiodic induction of flowering in Chenopodium species. Physiol Plant 87:160–166CrossRefGoogle Scholar
  52. Matsoukas IG, Massiah AJ, Thomas B (2012) Florigenic and antiflorigenic signaling in plants. Plant Cell Physiol 53:1827–1842PubMedCrossRefGoogle Scholar
  53. Meng X, Muszynski MG, Danilevskaya ON (2011) The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell 23:942–960PubMedPubMedCentralCrossRefGoogle Scholar
  54. Michaels SD (2009) Flowering time regulation produces much fruit. Curr Opin Plant Biol 12:75–80PubMedCrossRefGoogle Scholar
  55. Mutasa-Goettgens E, Hedden P (2009) Gibberellin as a factor in floral regulatory networks. J Exp Bot 60:1979–1989CrossRefGoogle Scholar
  56. Nakatani K, Takayanagi S, Noguchi K (2009) Characterization of photoperiodic sensitivity in the Japanese population of Chenopodium album. Weed Biol Manag 9:79–82CrossRefGoogle Scholar
  57. Pavlová L, Krekule J (1990) The effect of IAA application on endogenous rhythm of flowering in Chenopodium rubrum L. Biol Plant 32:277–287CrossRefGoogle Scholar
  58. Pin PA, Benlloch R, Bonnet D, Wremerth-Weich E, Kraft T, Gielen JJL, Nilsson O (2010) An antagonistic pair of FT homologs mediates the control of flowering time in sugar beet. Science 330:1397–1400PubMedCrossRefGoogle Scholar
  59. Pin PA, Nilsson O (2012) The multifaceted roles of FLOWERING LOCUS T in plant development. Plant, Cell Environ 35:1742–1755CrossRefGoogle Scholar
  60. Randoux M, Davie`re, Jeauffre J, JM et al (2014) RoKSN, a floral repressor, forms protein complexes with RoFD and RoFT to regulate vegetative and reproductive development in rose. New Phytol 202:161–173PubMedCrossRefGoogle Scholar
  61. Risi JC, Galway NW (1984) The Chenopodium grains of the Andes: Inca crops for modern agriculture. Advance Appl Biol 10:145–216Google Scholar
  62. Reiter RJ, Tan DX, Zhou Z, Cruz MHC, Fuentes-Broto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20:7396–7437PubMedPubMedCentralCrossRefGoogle Scholar
  63. Samad AFA, Sajad M, Nazaruddin N, Fauzi IA, Murad AM, Zainal Z, Ismail I (2017) MicroRNA and transcription factor: key players in plant regulatory network. Front Plant Sci 8:565PubMedPubMedCentralCrossRefGoogle Scholar
  64. Seidlová F (1980) Sequential steps of transition to flowering in Chenopodium rubrum L. Physiol Veg 18:477–487Google Scholar
  65. Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proc Natl Acad Sci USA 97:3753–3758PubMedCrossRefGoogle Scholar
  66. Štorchová H, Drabešová J, Cháb D, Kolář J, Jellen EN (2015) The introns in Flowering Locus T-Like (FTL) genes are useful markers for tracking paternity in tetraploid Chenopodium quinoa Willd. Genet Resour Crop Evol 62:913–925CrossRefGoogle Scholar
  67. Suarez-Lopez P, Wheatley K, Robson F, Onouchi H, Valverde F, Coupland G (2001) CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature 410:1116–1120PubMedCrossRefGoogle Scholar
  68. Sun CH, Chen D, Fang J, Wang PR, Deng XJ, Chu CC (2014) Understanding the genetic and epigenetic architecture in complex network of rice flowering pathways. Protein Cell 5:889–898PubMedPubMedCentralCrossRefGoogle Scholar
  69. Ullmann J, Seidlová F, Krekule J, Pavlová L (1985) Chenopodium rubrum as a model plant for testing the flowering effects of PGRs. Biol Plant 27:367–372CrossRefGoogle Scholar
  70. Valverde F, Mouradov A, SoppeW Ravenscroft D, Samach A, Coupland G (2004) Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–1006PubMedCrossRefGoogle Scholar
  71. Vogt SH, Weyens G, Lefebvre M, Bork B, Schechert A, Mueller AE (2014) The FLC-like gene BvFL1 is not a major regulator of vernalization response in biennial beets. Front Plant Sci 5:146PubMedPubMedCentralCrossRefGoogle Scholar
  72. Walsh BM, Adhikary D, Maughan PJ, Emshwiller E, Jellen EN (2015) Chenopodium polyploidy inferences from Salt Overly Sensitive 1 (SOS1) data. Am J Bot 102:533–543PubMedCrossRefGoogle Scholar
  73. Wolf K, Kolář J, Witters E, van Dongen W, van Onckelen H, Macháčková I (2001) Daily profile of melatonin levels in Chenopodium rubrum L. depends on photoperiod. J Plant Physiol 158:1491–1493CrossRefGoogle Scholar
  74. Weller JL, Ortega R (2015) Genetic control of flowering time in legumes. Front Plant Sci 6:207PubMedPubMedCentralCrossRefGoogle Scholar
  75. Wickland DP, Hanzawa Y (2015) The Flowering Locus T/Terminal Flower 1 gene family: functional evolution and molecular mechanisms Mol Plant 8:983–997Google Scholar
  76. Wilson HD (1990) Quinoa and relatives (Chenopodium sect. Chenopodium subsect Cellulata). Econ Bot 44:92–110CrossRefGoogle Scholar
  77. Yamada M, Takeno K (2014) Stress and salicylic acid induce the expression of PnFT2 in the regulation of the stress-induced flowering of Pharbitis nil. J Plant Physiol 171:205–212PubMedCrossRefGoogle Scholar
  78. Yano M, Kojima S, Takahashi Y, Lin H, Sasaki T (2001) Genetic control of flowering time in rice, a short day plant. Plant Physiol 127:1425–1429PubMedPubMedCentralCrossRefGoogle Scholar
  79. Zeevart JAD (1976) Physiology of flower formation. Annu Rev Plant Physiol 27:321–348CrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2021

Authors and Affiliations

  1. 1.Institute of Experimental Botany, Czech Academy of SciencesPrague 6, LysolajeCzech Republic

Personalised recommendations