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Flowering Time as a Model Trait to Bridge Proximate and Evolutionary Questions

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Mathematical Modelling in Plant Biology

Abstract

The transition from vegetative to reproductive growth is a key developmental event that is directly linked to reproductive success in plants. To understand this developmental trait in the context of evolution, the synthesis of molecular/genetic studies and ecology/evolutionary studies is necessary. In this chapter, we present a mathematical approach for synthesizing this body of knowledge to consider different flowering strategies. We model plant life history based on molecular mechanisms of the underlying gene regulatory network of flowering. We then extend the model to predict future flowering phenology under a changing climate and end with conclusions and perspectives.

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References

  1. Tinbergen N (1963) On aims and methods of ethology. Ethology 20(4):410–433

    Google Scholar 

  2. Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408(6814):796

    Article  Google Scholar 

  3. Goff SA, Ricke D, Lan TH, Presting G, Wang R, Dunn M, Glazebrook J, Sessions A, Oeller P, Varma H, Hadley D (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. japonica). Science 296(5565):92–100

    Article  CAS  PubMed  Google Scholar 

  4. Yu J, Hu S, Wang J, Wong GKS, Li S, Liu B, Deng Y, Dai L, Zhou Y, Zhang X, Cao M (2002) A draft sequence of the rice genome (Oryza sativa L. ssp. indica). Science 296(5565):79–92

    Article  CAS  PubMed  Google Scholar 

  5. Smith JM (1978) Optimization theory in evolution. Annu Rev Ecol Syst 9(1):31–56

    Article  Google Scholar 

  6. Satake A, Sakurai G, Kinoshita T (2015) Modeling strategies for plant survival, growth and reproduction. Plant Cell Physiol 56:583–585

    Article  CAS  PubMed  Google Scholar 

  7. Bateson P, Laland KN (2013) Tinbergen’s four questions: an appreciation and an update. Trends Ecol Evol 28(12):712–718

    Article  PubMed  Google Scholar 

  8. Cohen D (1971) Maximizing final yield when growth is limited by time or by limiting resources. J Theor Biol 33(2):299–307

    Article  CAS  PubMed  Google Scholar 

  9. Cohen D (1976) The optimal timing of reproduction. Am Nat 110(975):801–807

    Article  Google Scholar 

  10. Iwasa Y (2000) Dynamic optimization of plant growth. Evol Ecol Res 2(4):437–455

    Google Scholar 

  11. Iwasa Y, Cohen D (1989) Optimal growth schedule of a perennial plant. Am Nat 133(4):480–505

    Article  Google Scholar 

  12. King D, Roughgarden J (1982) Multiple switches between vegetative and reproductive growth in annual plants. Theor Popul Biol 21(2):194–204

    Article  Google Scholar 

  13. Yamamura N, Tsuji N (1995) Optimal strategy of plant antiherbivore defense: implications for apparency and resource-availability theories. Ecol Res 10(1):19–30

    Article  Google Scholar 

  14. Yamauchi A, Yamamura N (2004) Herbivory promotes plant production and reproduction in nutrient-poor conditions: effects of plant adaptive phenology. Am Nat 163(1):138–153

    Article  PubMed  Google Scholar 

  15. Metcalf CJE, Rose KE, Childs DZ, Sheppard AW, Grubb PJ, Rees M (2008) Evolution of flowering decisions in a stochastic, density-dependent environment. Proc Natl Acad Sci 105(30):10466–10470

    Article  CAS  PubMed  Google Scholar 

  16. Rees M, Rose KE (2002) Evolution of flowering strategies in Oenothera glazioviana: an integral projection model approach. Proc R Soc Lond B Biol Sci 269(1499):1509–1515

    Article  Google Scholar 

  17. Bowman JL, Smyth DR, Meyerowitz EM (1991) Genetic interactions among floral homeotic genes of Arabidopsis. Development 112(1):1–20

    CAS  PubMed  Google Scholar 

  18. Carpenter R, Coen ES (1990) Floral homeotic mutations produced by transposon-mutagenesis in Antirrhinum majus. Genes Dev 4(9):1483–1493

    Article  CAS  PubMed  Google Scholar 

  19. 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(4983):931

    Article  CAS  PubMed  Google Scholar 

  20. Koornneef M, Alonso-Blanco C, Peeters AJ, Soppe W (1998) Genetic control of flowering time in Arabidopsis. Annu Rev Plant Biol 49(1):345–370

    Article  CAS  Google Scholar 

  21. Koornneef M, Hanhart CJ, Veen J (1991) A genetic and physiological analysis of late flowering mutants in Arabidopsis thaliana. Mol Gen Genet MGG 229(1):57–66

    Article  CAS  PubMed  Google Scholar 

  22. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61(6):1001–1013

    Article  CAS  PubMed  Google Scholar 

  23. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13(9):627–639

    Article  PubMed  Google Scholar 

  24. Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125(4):655–664

    Article  PubMed  Google Scholar 

  25. Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296(5566):285–289

    Article  CAS  PubMed  Google Scholar 

  26. Blackman BK (2017) Changing responses to changing seasons: natural variation in the plasticity of flowering time. Plant Physiol 173(1):16–26

    Article  CAS  PubMed  Google Scholar 

  27. Fournier-Level A, Perry EO, Wang JA, Braun PT, Migneault A, Cooper MD, Metcalf CJE, Schmitt J (2016) Predicting the evolutionary dynamics of seasonal adaptation to novel climates in Arabidopsis thaliana. Proc Natl Acad Sci 113(20):E2812–E2821 p.201517456

    Article  CAS  PubMed  Google Scholar 

  28. Dennis ES, Peacock WJ (2007) Epigenetic regulation of flowering. Curr Opin Plant Biol 10(5):520–527

    Article  CAS  PubMed  Google Scholar 

  29. Sung S, Amasino RM (2005) Remembering winter: toward a molecular understanding of vernalization. Annu Rev Plant Biol 56:491–508

    Article  CAS  PubMed  Google Scholar 

  30. Burn JE, Bagnall DJ, Metzger JD, Dennis ES, Peacock WJ (1993) DNA methylation, vernalization, and the initiation of flowering. Proc Natl Acad Sci 90(1):287–291

    Article  CAS  PubMed  Google Scholar 

  31. Clarke JH, Dean C (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Mol Gen Genet MGG 242(1):81–89

    CAS  PubMed  Google Scholar 

  32. Koornneef M, Vries H, Hanhart C, Soppe W, Peeters T (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild-type. Plant J 6(6):911–919

    Article  CAS  Google Scholar 

  33. Lee I, Bleecker A, Amasino R (1993) Analysis of naturally occurring late flowering in Arabidopsis thaliana. Mol Gen Genet MGG 237(1):171–176

    CAS  PubMed  Google Scholar 

  34. Napp-Zinn K (1987) Vernalization-environmental and genetic regulation. In: Atherton JG (ed) Manipulation of flowering. Butterworths, London

    Google Scholar 

  35. Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172

    Article  CAS  PubMed  Google Scholar 

  36. Sung S, Amasino RM (2004) Vernalization and epigenetics: how plants remember winter. Curr Opin Plant Biol 7(1):4–10

    Article  CAS  PubMed  Google Scholar 

  37. Lempe J, Balasubramanian S, Sureshkumar S, Singh A, Schmid M, Weigel D (2005) Diversity of flowering responses in wild Arabidopsis thaliana strains. PLoS Genet 1(1):e6

    Article  PubMed Central  Google Scholar 

  38. 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(2):1163–1173

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays C, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proc Natl Acad Sci U S A 101(13):4712–4717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. Plant Cell 11(5):949–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 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(4):935–941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. 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(3):445–458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Kardailsky I, Shukla VK, Ahn JH, Dagenais N, Christensen SK, Nguyen JT, Chory J, Harrison MJ, Weigel D (1999) Activation tagging of the floral inducer FT. Science 286(5446):1962–1965

    Article  CAS  PubMed  Google Scholar 

  44. Kobayashi Y, Kaya H, Goto K, Iwabuchi M, Araki T (1999) A pair of related genes with antagonistic roles in mediating flowering signals. Science 286(5446):1960–1962

    Article  CAS  PubMed  Google Scholar 

  45. Mandel MA, Yanofsky MF (1995) A gene triggering flower formation in Arabidopsis. Nature 377(6549):522

    Article  CAS  PubMed  Google Scholar 

  46. Weigel D, Alvarez J, Smyth DR, Yanofsky MF, Meyerowitz EM (1992) LEAFY controls floral meristem identity in Arabidopsis. Cell 69(5):843–859

    Article  CAS  PubMed  Google Scholar 

  47. Ferrándiz C, Gu Q, Martienssen R, Yanofsky MF (2000) Redundant regulation of meristem identity and plant architecture by FRUITFULL, APETALA1 and CAULIFLOWER. Development 127(4):725–734

    PubMed  Google Scholar 

  48. Scarcelli N, Cheverud JM, Schaal BA, Kover PX (2007) Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proc Natl Acad Sci 104(43):16986–16991

    Article  CAS  PubMed  Google Scholar 

  49. Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proc Natl Acad Sci 100(17):10102–10107

    Article  CAS  PubMed  Google Scholar 

  50. Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170(3):1197–1207

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 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 107(25):11632–11637

    Article  CAS  PubMed  Google Scholar 

  52. 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(7245):423–427

    Article  CAS  PubMed  Google Scholar 

  53. Satake A (2010) Diversity of plant life cycles is generated by dynamic epigenetic regulation in response to vernalization. J Theor Biol 266(4):595–605

    Article  PubMed  Google Scholar 

  54. Bastow R, Mylne JS, Lister C, Lippman Z, Martienssen RA, Dean C (2004) Vernalization requires epigenetic silencing of FLC by histone methylation. Nature 427(6970):164–167

    Article  CAS  PubMed  Google Scholar 

  55. Finnegan JE, Kovac KA, Jaligot E, Sheldon CC, James Peacock W, Dennis ES (2005) The downregulation of FLOWERING LOCUS C (FLC) expression in plants with low levels of DNA methylation and by vernalization occurs by distinct mechanisms. Plant J 44(3):420–432

    Article  CAS  Google Scholar 

  56. 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 105(2):411–416

    Article  CAS  PubMed  Google Scholar 

  57. 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(6):706–710

    Article  CAS  PubMed  Google Scholar 

  58. Angel A, Song J, Dean C, Howard M (2011) A Polycomb-based switch underlying quantitative epigenetic memory. Nature 476(7358):105–108

    Article  CAS  PubMed  Google Scholar 

  59. Satake A, Iwasa Y (2012) A stochastic model of chromatin modification: cell population coding of winter memory in plants. J Theor Biol 302:6–17

    Article  CAS  PubMed  Google Scholar 

  60. Angel A, Song J, Yang H, Questa JI, Dean C, Howard M (2015) Vernalizing cold is registered digitally at FLC. Proc Natl Acad Sci 112(13):4146–4151

    Article  CAS  PubMed  Google Scholar 

  61. Dodd IB, Micheelsen MA, Sneppen K, Thon G (2007) Theoretical analysis of epigenetic cell memory by nucleosome modification. Cell 129(4):813–822

    Article  CAS  PubMed  Google Scholar 

  62. Krzymuski M, Andrés F, Cagnola JI, Jang S, Yanovsky MJ, Coupland G, Casal JJ (2015) The dynamics of FLOWERING LOCUS T expression encodes long-day information. Plant J 83(6):952–961

    Article  CAS  PubMed  Google Scholar 

  63. Miyazaki Y, Maruyama Y, Chiba Y, Kobayashi MJ, Joseph B, Shimizu KK, Mochida K, Hiura T, Kon H, Satake A (2014) Nitrogen as a key regulator of flowering in Fagus crenata: understanding the physiological mechanism of masting by gene expression analysis. Ecol Lett 17(10):1299–1309

    Article  PubMed  Google Scholar 

  64. Miyazaki Y, Satake A (2017) Relationship between seasonal progression of floral meristem development and FLOWERING LOCUS T expression in the deciduous tree Fagus crenata. Ecol Res 32(4):627–631

    Article  CAS  Google Scholar 

  65. Satake A, Kawagoe T, Saburi Y, Chiba Y, Sakurai G, Kudoh H (2013) Forecasting flowering phenology under climate warming by modelling the regulatory dynamics of flowering-time genes. Nat Commun 4:2303

    Article  PubMed  Google Scholar 

  66. Charlesworth B (1980) Evolution in age-structured populations. Cambridge University Press, Cambridge

    Google Scholar 

  67. Chen IC, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333(6045):1024–1026

    Article  CAS  PubMed  Google Scholar 

  68. Root TL, MacMynowski DP, Mastrandrea MD, Schneider SH (2005) Human-modified temperatures induce species changes: joint attribution. Proc Natl Acad Sci U S A 102(21):7465–7469

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Rosenzweig C, Karoly D, Vicarelli M, Neofotis P, Wu Q, Casassa G, Menzel A, Root TL, Estrella N, Seguin B, Tryjanowski P (2008) Attributing physical and biological impacts to anthropogenic climate change. Nature 453(7193):353–357

    Article  CAS  PubMed  Google Scholar 

  70. Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Carvalho L, Clutton-Brock TIM (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Glob Chang Biol 16(12):3304–3313

    Article  Google Scholar 

  71. Anderson JT, Inouye DW, McKinney AM, Colautti RI, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc R Soc Lond B Biol Sci 279(1743):3843–3852

    Article  Google Scholar 

  72. Franks SJ, Sim S, Weis AE (2007) Rapid evolution of flowering time by an annual plant in response to a climate fluctuation. Proc Natl Acad Sci 104(4):1278–1282

    Article  CAS  PubMed  Google Scholar 

  73. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421(6918):37–42

    Article  CAS  PubMed  Google Scholar 

  74. Post ES, Pedersen C, Wilmers CC, Forchhammer MC (2008) Phenological sequences reveal aggregate life history response to climatic warming. Ecology 89(2):363–370

    Article  PubMed  Google Scholar 

  75. Springer CJ, Ward JK (2007) Flowering time and elevated atmospheric CO2. New Phytol 176(2):243–255

    Article  CAS  PubMed  Google Scholar 

  76. Kudoh H (2015) Molecular phenology in plants: in natura systems biology for the comprehensive understanding of seasonal responses under natural environments. New Phytol 210(2):399–412

    Article  PubMed  Google Scholar 

  77. Kobayashi MJ, Takeuchi Y, Kenta T, Kume T, Diway B, Shimizu KK (2013) Mass flowering of the tropical tree Shorea beccariana was preceded by expression changes in flowering and drought-responsive genes. Mol Ecol 22(18):4767–4782

    Article  PubMed  PubMed Central  Google Scholar 

  78. Chan HT (1981) Reproductive biology of some Malaysian dipterocarps, 3: breeding systems. Malaysian Forester, Kepong

    Google Scholar 

  79. Janzen DH (1974) Tropical Blackwater rivers, animals, and mast fruiting by the Dipterocarpaceae. Biotropica 6(2):69–103

    Article  Google Scholar 

  80. Appanah S (1985) General flowering in the climax rain forests of south-East Asia. J Trop Ecol 1(03):225–240

    Article  Google Scholar 

  81. Fitter AH, Fitter RSR (2002) Rapid change in flowering time in British plants. Science 296:1689–1691

    Article  CAS  PubMed  Google Scholar 

  82. 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 151(6):1358–1369

    Article  CAS  PubMed  Google Scholar 

  83. Nagahama A, Kubota Y, Satake (2018) A Climate warming shortens flowering duration: a comprehensive assessment of plant phenological responses based on gene expression analyses and mathematical modeling. Ecol Resg:1059–1068

    Article  CAS  Google Scholar 

  84. Yeoh SH, Satake A, Numata S, Ichie T, Lee SL, Basherudin N, Muhammad N, Kondo T, Otani T, Hashim M, Tani N (2017) Unraveling proximate cues of mass flowering in the tropical forests of Southeast Asia from gene expression analyses. Mol Ecol 26:5074–5085

    Article  CAS  PubMed  Google Scholar 

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Satake, A. (2018). Flowering Time as a Model Trait to Bridge Proximate and Evolutionary Questions. In: Morris, R. (eds) Mathematical Modelling in Plant Biology. Springer, Cham. https://doi.org/10.1007/978-3-319-99070-5_9

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