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Memory of Temperature in the Seasonal Control of Flowering Time: An Unexplored Link Between Meteorology and Molecular Biology

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Abstract

Organismal response to a specific environmental signal should have a property that is sensitive to the useful cue but insensitive to other erroneous noises. Because adaptive characteristics of an organism have been shaped by natural selection, their functions should be evaluated in the natural habitats. In the study of flowering time, recent emergence of in natura systems biology i.e. combined applications of molecular biology and statistical modeling in natural habitats, bridges biometeorology and molecular biology. Especially, expression of genes with known function can be analyzed by conventional time-series analyses that have been frequently used in biometeorological studies. Here, by comparing knowledge from (1) meteorology, (2) molecular biology (3) in natura systems biology, and (4) biometeorology, we showed how signal properties in natural temperature fluctuation correspond to mechanistic property of flowering-time regulation. Meteorological data indicate that seasonal signal in temperature is a pattern over multiple weeks or months with short-term serious noises. It predicts that molecular machinery of flowering-time control should refer past temperatures for 4–6 weeks or longer. Molecular biology on the regulation of a key flowering repressor, FLC, in Arabidopsis thaliana revealed that molecular machinery of vernalization response is a representative example that corresponds to the meteorological properties of the seasonal temperature signal. In natura systems biology has revealed that the machinery of vernalization response serves as memory of past temperature that extract seasonal signal from natural complex fluctuation. The referring periods of past temperatures suggested by meteorology, molecular biology and in natura systems biology correspond to the lengths of proceeding periods during which temperature affect first flowering dates of diverse plants. Therefore, we should not take yearly variation of flowering date as a mealy passive developmental effect of preceding temperatures. It includes more active responses of plants that have been evolved to control flowering-time in the noisy temperature fluctuations in the natural habitats.

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References

  • Aikawa S, Kobayashi MJ, Satake A, Shimizu KK, Kudoh H (2010) Robust control of the seasonal expression of the Arabidopsis FLC gene in a fluctuating environment. Proc Natl Acad Sci USA 107:11632–11637

    Article  PubMed  CAS  Google Scholar 

  • Ahas R, Jaagus J, Aasa A (2000) The phenological calendar of Estonia and its correlation with mean air temperature. Int J Biometeorol 44:159–166

    Article  PubMed  CAS  Google Scholar 

  • Akam M (1987) The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1–22

    PubMed  CAS  Google Scholar 

  • Albani MC, Coupland G (2010) Comparative analysis of flowering in annual and perennial plants. Curr Top Dev Biol 91:323–348

    Article  PubMed  CAS  Google Scholar 

  • Amasino R (2004) Vernalization, competence, and the epigenetic memory of winter. Plant Cell 16:2553–2559

    Article  PubMed  CAS  Google Scholar 

  • Anderson JV, Gesch RW, Jia Y, Chao WS, Horvath DP (2005) Seasonal shifts in dormancy status, carbohydrate metabolism, and related gene expression in crown buds of leafy spurge. Plant Cell Environ 28:1567–1578

    Article  CAS  Google Scholar 

  • Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13:627–639

    Article  PubMed  Google Scholar 

  • Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476:105–108

    Article  PubMed  CAS  Google Scholar 

  • Bastow R et al (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427:164–167

    Article  PubMed  CAS  Google Scholar 

  • Battey NH (2000) Aspects of seasonality. J Exp Bot 51:1769–1780

    Article  PubMed  CAS  Google Scholar 

  • Bemer M, Grossniklaus U (2012) Dynamic regulation of Polycomb group activity during plant development. Curr Opin Plant Biol 15:523–529

    Article  PubMed  CAS  Google Scholar 

  • Bernier G (1988) The control of floral evocation and morphogenesis. Annu Rev Plant Physiol 39:175–219

    Article  Google Scholar 

  • Bielenberg DG, Wang Y, Li Z, Zhebentyayeva T, Fan S, Reighard GL, Scorza R, Abbott AG (2008) Sequencing and annotation of the evergrowing locus in peach [Prunus persica (L.) Batsch] reveals a cluster of six MADS-box transcription factors as candidate genes for regulation of terminal bud formation. Tree Genet Genomes 4:495–507

    Article  Google Scholar 

  • Bradley NL, Leopold AC, Ross J, Huffaker W (1999) Phenological changes reflect climate change in Winsconsin. Proc Natl Acad Sci USA 96:9701–9704

    Article  PubMed  CAS  Google Scholar 

  • Censi CA, Ceschia M (2000) Forecasting of the flowering time for wild species observed at Guidonia, central Italy. Int J Biometeorol 44:88–96

    Article  Google Scholar 

  • Chanvivattana Y, Bishopp A, Schubert D, Stock C, Moon Y-H, Sung ZR, Goodrich J (2004) Interaction of Polycomb-group proteins controlling flowering in Arabidopsis. Development 131:5263–5276

    Article  PubMed  CAS  Google Scholar 

  • Chew YH, Wilczek AM, Williams M, Welch SM, Schmitt J, Halliday K (2012) An augmented Arabidopsis phenology model reveals seasonal temperature control of flowering time. New Pytol 194:654–665

    Article  Google Scholar 

  • Choi J, Hyun Y, Kang MJ, In Yun H, Yun JY, Lister C, Dean C, Amasino RM, Noh B, Noh YS, Choi Y (2009) Resetting and regulation of FLOWERING LOCUS C expression during Arabidopsis reproductive development. Plant J 57:918–931

    Article  PubMed  CAS  Google Scholar 

  • Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol 11:191–238

    Article  CAS  Google Scholar 

  • Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evolut 22:357–365

    Article  Google Scholar 

  • De Lucia F, Crevillen P, Jones AME, Greb T, Dean C (2008) A PHD-polycomb repressive complex 2 triggers the epigenetic silencing of FLC during vernalization. Proc Natl Acad Sci USA 105:16831–16836

    Article  PubMed  Google Scholar 

  • Fitter AH, Peat HJ (1994) The ecological flora database. J Ecol 82:415–425

    Article  Google Scholar 

  • Fitter AH, Fitter RSR, Harris ITB, Williamson MH (1995) Relationships between first flowering date and temperature in the flora of a locality in central England. Func Ecol 9:55–60

    Article  Google Scholar 

  • Finnegan EJ, Dennis ES (2007) Vernalization-induced trimethylation of histone H3 lysine 27 at FLC is not maintained in mitotically quiescent cells. Curr Biol 17:1978–1983

    Article  PubMed  CAS  Google Scholar 

  • Flood RG, Halloran GM (1984) Basic development rate in spring wheat. Agro J 76:260–264

    Article  Google Scholar 

  • 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 17:73–78

    Article  PubMed  CAS  Google Scholar 

  • Hemming MN, Trevaskis B (2011) Make hay when the sun shines: the role of MADS-box genes in temperature-dependant seasonal flowering responses. Plant Sci 180:447–453

    Article  PubMed  CAS  Google Scholar 

  • Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331:76–79

    Article  PubMed  CAS  Google Scholar 

  • Izawa T (2012) Physiological significance of the plant circadian clock in natural field conditions. Plant Cell Environ 35:1729–1741

    Article  PubMed  Google Scholar 

  • Jiménez S, Reighard GL, Bielenberg DG (2010) Gene expression of DAM5 and DAM6 is suppressed by chilling temperatures and inversely correlated with bud break rate. Plant Mol Biol 73:157–167

    Article  PubMed  Google Scholar 

  • Jones PD, New M, Parker DE, Martin S, Rigor IG (1999) Surface air temperature and its changes over the past 150 years. Rev Geophys 37:173–199

    Article  Google Scholar 

  • Kemi U, Niittyvuopio A, Toivainen T, Pasanen A, Quilot-Turion B, Holm K, Lagercrantz U, Savolainen O, Kuittinen H (2013) Role of vernalization and of duplicated FLOWERING LOCUS C in the perennial Arabidopsis lyrata. New Phytol 197:323–335

    Article  PubMed  CAS  Google Scholar 

  • Lang A (1952) Physiology of flowering. Ann Rev Plant Physiol 3:265–306

    Article  Google Scholar 

  • Lanzuolo C, Orlando V (2012) Memories from the Polycomb group proteins. Annu Rev Gen 46:561–589

    Article  CAS  Google Scholar 

  • Levy YY, Mesnage S, Mylne JS, Gendall AR, Dean C (2002) Multiple roles of Arabidopsis VRN1 in vernalization and flowering time control. Science 297:243–246

    Article  PubMed  CAS  Google Scholar 

  • Lee R (1970) Latitude and photoperiodism. Arch Met Geoph Biokl Ser B 18:325–332

    Article  Google Scholar 

  • Lewis P (1960) The use of moving average in the analysis of time-series. Weather 15:121–126

    Article  Google Scholar 

  • Li D, Liu C, Shen L, Wu Y, Chen H, Robertson M, Helliwell CA, Ito T, Meyerowitz E, Yu H (2008) A repressor complex governs the Integration of flowering signals in Arabidopsis. Dev Cell 15:110–120

    Article  PubMed  CAS  Google Scholar 

  • Li Z, Reighard GL, Abbott AG, Bielenberg DG (2009) Dormancy-associated MADS genes from the EVG locus of peach [Prunus persica (L.) Batsch] have distinct seasonal and photoperiodic expression patterns. J Exp Bot 60:3521–3530

    Article  PubMed  CAS  Google Scholar 

  • Lin S, Wang J, Poon S, Su C, Wang S, Chiou T (2005) Differential regulation of expression by vernalization FLOWERING LOCUS C in cabbage and Arabidopsis. Plant Physiol 137:1037–1048

    Article  PubMed  CAS  Google Scholar 

  • Luedeling E, Kunz A, Blanke MM (2012) Identification of chilling and heat requirements of cherry trees—a statistical approach. Int J Biometeorol. doi:10.1007/s00484-012-0594-y

    Google Scholar 

  • Manitašević S, Dunđerski J, Matić G, Tucić B (2007) Seasonal variation in heat shock proteins Hsp70 and Hsp90 expression in an exposed and a shaded habitat of Iris pumila. Plant Cell Env 30:1–11

    Article  Google Scholar 

  • Marletto V, Branzi GP, Sirotti M (1992) Forecasting flowering dates of lawn species with air temperature: Application boundaries of the linear approach. Aerobiologia 8:75–83

    Article  Google Scholar 

  • Mayrhofer S, Teuber M, Zimmer I, Louis S, Fischbach RJ, Schnitzler J-P (2005) Diurnal and seasonal variation of isoprene biosynthesis-related genes in grey poplar leaves. Plant Physiol 139:474–484

    Article  PubMed  CAS  Google Scholar 

  • Merquiol E, Pnueli L, Cohen M, Simovitch M, Rachmilevitch S, Goloubinoff P, Kaplan A, Mittler R (2002) Seasonal and diurnal variations in gene expression in the desert legume Retam raetam. Plant Cell Env 25:1627–1638

    Article  CAS  Google Scholar 

  • Margueron R, Reinberg D (2011) The Polycomb complex PRC2 and its mark in life. Nature 469:343–349

    Article  PubMed  CAS  Google Scholar 

  • Mylne JS, Barrett L, Tessadori F, Mesnage S, Johnson L, Bernatavichute YV, Jacobsen SE, Fransz P, Dean C (2006) LHP1, the Arabidopsis homologue of heterochromatin protein 1, is required for epigenetic silencing of FLC. Proc Natl Acad Sci USA 103:5012–5017

    Article  PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11:949–956

    PubMed  CAS  Google Scholar 

  • Michaels SD, Amasino RM (2000) Memories of winter: vernalization and the competence to flower. Plant Cell Environ 23:1145–1153

    Article  Google Scholar 

  • Munguia-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecol Letters 14:511–521

    Article  Google Scholar 

  • Nagano AJ, Sato Y, Mihara M, Antonio BA, Motoyama R, Itoh H, Nagamura Y, Izawa T (2012) Deciphering and prediction of transcriptome dynamics under fluctuating field conditions. Cell 51:1358–1369

    Article  Google Scholar 

  • Pearson JC, Lemons D, McGinnis W (2005) Modulating Hox gene functions during animal body patterning. Nat Rev Gen 6:893–904

    Article  CAS  Google Scholar 

  • Penfield S (2008) Temperature perception and signal transduction in plants. New Phytol 179:615–628

    Article  PubMed  CAS  Google Scholar 

  • Peñulelas J, Filella I (2001) Responses to a warming world. Science 294:793–794

    Article  Google Scholar 

  • Prescott JA, Collins JA (1951) The lag of temperature behind solar radiation. Quart J Roy Meteorol Soc 77:121–126

    Article  Google Scholar 

  • Preston JC, Kellogg EA (2006) Reconstructing the evolutionary history of paralogous APETALA1/ FRUITFULL-like genes in grasses (Poaceae). Genetics 174:421–437

    Article  PubMed  CAS  Google Scholar 

  • Quintana-Murci L, Alcaïs A, Abel L, Casanova J-L (2007) Immunology in natura: clinical, epidemiological and evolutionary genetics of infectious diseases. Nat Immunol 8:1165–1171

    Article  PubMed  CAS  Google Scholar 

  • Richards CL, Hanzawa Y, Katari MS, Ehrenreich IM, Engelmann KE, Purugganan MD (2009) Perspective on ecological and evolutionary systems biology. Annu Plant Rev 35:331–351

    CAS  Google Scholar 

  • Richards CL, Rosas U, Banta J, Bhambhra N, Purugganan MD (2012) Genome-wide patterns of Arabidopsis gene expression in nature. PLoS Genet 8:e1002662

    Article  PubMed  CAS  Google Scholar 

  • Ringrose L, Paro R (2004) Epigenetic regulation of cellular memory by the poycomb and trithorax group proteins. Annu Rev Gen 38:413–443

    Article  CAS  Google Scholar 

  • Roberts AMI (2008) Exploring relationships between phenological and weather data using smoothing. Int J Biometeorol 53:463–470

    Article  Google Scholar 

  • Rodríguez-Rajo FJ, Frenguelli G, Jato MV (2003) Effect of air temperature on forecasting the start of the Betula pollen season at two contrasting sites in the south of Europe (1995–2001). Int J Biometeorol 47:117–125

    PubMed  Google Scholar 

  • Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA (2003) Fingerprints of global warming on wild animals and plants. Nature 421:57–60

    Article  PubMed  CAS  Google Scholar 

  • Salisbury FB (1963) The flowering process. Pergamon, Oxford

    Google Scholar 

  • Schmitz RJ, Sung S, Amasino RM (2008) Histone arginine methylation is required for vernalization-induced epigenetic silencing of FLC in winter-annual Arabidopsis thaliana. Proc Natl Acad Sci USA 105:411–416

    Article  PubMed  CAS  Google Scholar 

  • Schwartz MD (2003) Phenology: an integrative environmental science. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • Shimizu KK, Kudoh H, Kobayashi MJ (2011) Plant sexual reproduction during climate change: gene function in natura studied by ecological and evolutionary systems biology. Ann Bot 108:777–787

    Article  PubMed  CAS  Google Scholar 

  • Searle I, He Y, Turck F, Vincent C, Fornara F, Kröber S, Amasino RA, Coupland G (2006) The transcription factor FLC confers a flowering response to vernalization by repressing meristem competence and systemic signaling in Arabidopsis. Genes Dev 20:898–912

    Article  PubMed  CAS  Google Scholar 

  • 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 11:445–458

    PubMed  CAS  Google Scholar 

  • 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 97:3753–3758

    Article  PubMed  CAS  Google Scholar 

  • Shindo C, Lister C, Crevillen P, Nordborg M, Dean C (2006) Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes Dev 20:3079–3083

    Article  PubMed  CAS  Google Scholar 

  • Simpson G, Dean C (2002) Arabidopsis: the Rosetta stone of flowering time? Science 296:285–289

    Article  PubMed  CAS  Google Scholar 

  • Song J, Angel A, Howard M, Dean C (2012) Vernalization—a cold-induced epigenetic switch. J Cell Sci 125:1–9

    Article  Google Scholar 

  • Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int J Biometeorol 44:82–87

    Article  PubMed  CAS  Google Scholar 

  • Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164

    Article  PubMed  CAS  Google Scholar 

  • Sung S, He Y, Eshoo TW, Tamada Y, Johnson L, Nakahigashi K, Goto K, Jacobsen SE, Amasino RM (2006) Epigenetic maintenance of the vernalized state in Arabidopsis thaliana requires LIKE HETEROCHROMATIN PROTEIN 1. Nat Genet 38:706–710

    Article  PubMed  CAS  Google Scholar 

  • Swiezewski S, Liu F, Magusin A, Dean C (2009) Cold-induced silencing by long antisense transcripts of an Arabidopsis Polycomb target. Nature 462:799–802

    Article  PubMed  CAS  Google Scholar 

  • Takahashi R, Yasuda S (1971) Genetics of earliness and growth habit in barley. In: Nilan RA (ed) Barley genetics II (proceedings of the second international barley genetics symposium). Washington State University Press, Pullman, pp 388–408

    Google Scholar 

  • Tooke F, Battey NH (2010) Temperate flowering phenology. J Exp Bot 61:2853–2862

    Article  PubMed  CAS  Google Scholar 

  • Trenberth KE (1983) What are the seasons? Bull Amer Meteorol Soc 64:1276–1282

    Article  Google Scholar 

  • Trevaskis B, Hemming MN, Dennis ES, Peacock WJ (2007) The molecular basis of vernalization-induced flowering in cereals. Trends Plant Sci 12:352–357

    Article  PubMed  CAS  Google Scholar 

  • Turck F, Roudier F, Farrona S, Martin-Magniette M-L, Guillaume E, Buisine N, Gagnot S, Martienssen RA, Coupland G, Colot V (2007) Arabidopsis TFL2/LHP1 specifically associates with genes marked by trimethylation of histone H3 lysine 27. PLoS Genet 3:e86

    Article  PubMed  Google Scholar 

  • Turner BM (2002) Cellular memory and the histone code. Cell 111:285–291

    Article  PubMed  CAS  Google Scholar 

  • Wahba G (1990) Spline model for observation data. Society for Industrial and Applied Mathematics, Philadelphia

    Book  Google Scholar 

  • Walther G-R, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin J-M, Hoegh-Guldberg O, Bairlein F (2002) Ecological response to recent climate change. Nature 416:389–395

    Article  PubMed  CAS  Google Scholar 

  • 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 459:423–427

    Article  PubMed  CAS  Google Scholar 

  • Wilczek AM, Roe JL, Knapp MC, Cooper MD, Lopez-Gallego C, Martin LJ, Muir CD, Sim S, Walker A, Anderson J, Egan JF, Moyers BT, Petipas R, Giakountis A, Charbit E, Coupland G, Welch SM, Schmitt J (2009) Effects of genetic perturbation on seasonal life history plasticity. Science 323:930–934

    Article  PubMed  CAS  Google Scholar 

  • Wilczek AM, Burghardt LT, Cobb AR, Cooper MD, Welch SM, Schmitt J (2010) Genetic and physiological bases for phenological responses to current and predicted climates. Philos Trans R Soc B 365:3129–3147

    Article  CAS  Google Scholar 

  • Withrow RB (1959) A kinetic analysis of photoperiodism. In: Withrow RB (ed) Photoperiodism and related phenomena in plants and animals. American Association for Advancement of Science, Washington, pp 439–471

    Google Scholar 

  • Wood CC, Robertson M, Tanner G, Peacock WJ, Dennis ES, Helliwell CA (2006) The Arabidopsis thaliana vernalization response requires a polycomb-like protein complex that also includes VERNALIZATION INSENSITIVE 3. Proc Natl Acad Sci USA 103:14631–14636

    Article  PubMed  Google Scholar 

  • Yan L, Loukoianov A, Tranquilli G, Helguera M, Fahima T, Dubcovsky J (2003) Positional cloning of the wheat vernalisation gene VRN1. Proc Natl Acad Sci USA 100:6263–6268

    Article  PubMed  CAS  Google Scholar 

  • Yanovsky MJ, Kay SA (2003) Living by the calendar: how plants know when to flower. Nat Rev Mol Cell Biol 4:265–275

    Article  PubMed  CAS  Google Scholar 

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Kudoh, H., Nagano, A.J. (2013). Memory of Temperature in the Seasonal Control of Flowering Time: An Unexplored Link Between Meteorology and Molecular Biology. In: Pontarotti, P. (eds) Evolutionary Biology: Exobiology and Evolutionary Mechanisms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-38212-3_13

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