1932

Abstract

Photoperiod-measuring mechanisms allow organisms to anticipate seasonal changes to align reproduction and growth with appropriate times of the year. This review provides historical and modern context to studies of plant photoperiodism. We describe how studies of photoperiodic flowering in plants led to the first theoretical models of photoperiod-measuring mechanisms in any organism. We discuss how more recent molecular genetic studies in and rice have revisited these concepts. We then discuss how photoperiod transcriptomics provides new lessons about photoperiodic gene regulatory networks and the discovery of noncanonical photoperiod-measuring systems housed in metabolic networks of plants. This leads to an examination of nonflowering developmental processes controlled by photoperiod, including metabolism and growth. Finally, we highlight the importance of understanding photoperiodism in the context of climate change, delving into the rapid latitudinal migration of plant species and the potential role of photoperiod-measuring systems in generating photic barriers during migration.

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2023-05-22
2024-06-25
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Literature Cited

  1. 1.
    Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A et al. 2005. FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex. Science 309:1052–56
    [Google Scholar]
  2. 2.
    Alabadi D, Oyama T, Yanovsky MJ, Harmon FG, Mas P, Kay SA. 2001. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293:880–83
    [Google Scholar]
  3. 3.
    Alexandre Moraes T, Mengin V, Peixoto B, Encke B, Krohn N et al. 2022. The circadian clock mutant lhy cca1 elf3 paces starch mobilization to dawn despite severely disrupted circadian clock function. Plant Physiol. 189:2332–56
    [Google Scholar]
  4. 4.
    Andrés F, Coupland G. 2012. The genetic basis of flowering responses to seasonal cues. Nat. Rev. Genet. 13:627–39
    [Google Scholar]
  5. 5.
    Baerenfaller K, Massonnet C, Hennig L, Russenberger D, Sulpice R et al. 2015. A long photoperiod relaxes energy management in Arabidopsis leaf six. Curr. Plant Biol. 2:34–45
    [Google Scholar]
  6. 6.
    Bauerle WL, Oren R, Way DA, Qian SS, Stoy PC et al. 2012. Photoperiodic regulation of the seasonal pattern of photosynthetic capacity and the implications for carbon cycling. PNAS 109:8612–17
    [Google Scholar]
  7. 7.
    Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P. 1993. Physiological signals that induce flowering. Plant Cell 5:1147–55
    [Google Scholar]
  8. 8.
    Black M, Wareing PF. 1954. Photoperiodic control of germination in seed of birch (Betula pubescens Ehrh.). Nature 174:705–6
    [Google Scholar]
  9. 9.
    Bocobza SE, Malitsky S, Araújo WL, Nunes-Nesi A, Meir S et al. 2013. Orchestration of thiamin biosynthesis and central metabolism by combined action of the thiamin pyrophosphate riboswitch and the circadian clock in Arabidopsis. Plant Cell 25:288–307
    [Google Scholar]
  10. 10.
    Brachi B, Faure N, Horton M, Flahauw E, Vazquez A et al. 2010. Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLOS Genet. 6:e1000940
    [Google Scholar]
  11. 11.
    Brulfert J, Guerrier D, Queiroz O. 1982. Photoperiodism and Crassulacean acid metabolism: II. Relations between leaf aging and photoperiod in Crassulacean acid metabolism induction. Planta 154:332–38
    [Google Scholar]
  12. 12.
    Brulfert J, Müller D, Kluge M, Queiroz O. 1982. Photoperiodism and Crassulacean acid metabolism: I. Immunological and kinetic evidences for different patterns of phosphoenolpyruvate carboxylase isoforms in photoperiodically inducible and non-inducible Crassulacean acid metabolism plants. Planta 154:326–31
    [Google Scholar]
  13. 13.
    Brulfert J, Queiroz O. 1982. Photoperiodism and Crassulacean acid metabolism: III. Different characteristics of the photoperiod-sensitive and non-sensitive isoforms of phosphoenolpyruvate carboxylase and Crassulacean acid metabolism operation. Planta 154:339–43
    [Google Scholar]
  14. 14.
    Bünning E. 1936. Die endogene Tagesrhythmik als Grundlage der photoperiodischen Reaktion. Ber. Dtsch. Bot. Ges. 54:590–607The first connection between the circadian clock and photoperiod measurement.
    [Google Scholar]
  15. 15.
    Campoli C, Shtaya M, Davis SJ, von Korff M 2012. Expression conservation within the circadian clock of a monocot: natural variation at barley Ppd-H1 affects circadian expression of flowering time genes, but not clock orthologs. BMC Plant Biol. 12:97
    [Google Scholar]
  16. 16.
    Caspar T, Huber SC, Somerville C. 1985. Alterations in growth, photosynthesis, and respiration in a starchless mutant of Arabidopsis thaliana (L.) deficient in chloroplast phosphoglucomutase activity 1. Plant Physiol. 79:11–17
    [Google Scholar]
  17. 17.
    Chailakhyan MK. 1936. New facts in support of the hormonal theory of plant development. C. R. Acad. Sci. URSS 13:79–83
    [Google Scholar]
  18. 18.
    Chapman MA. 2022. Putting the pea in photoPEAriod. J. Exp. Bot. 73:3825–27
    [Google Scholar]
  19. 19.
    Chatterton NJ, Silvius JE. 1979. Photosynthate partitioning into starch in soybean leaves: I. Effects of photoperiod versus photosynthetic period duration. Plant Physiol. 64:749–53Plants measure photosynthetic period to control photosynthate partitioning.
    [Google Scholar]
  20. 20.
    Chatterton NJ, Silvius JE. 1980. Acclimation of photosynthate partitioning and photosynthetic rates to changes in length of the daily photosynthetic period. Ann. Bot. 46:739–45
    [Google Scholar]
  21. 21.
    Chatterton NJ, Silvius JE. 1981. Photosynthate partitioning into starch in soybean leaves: II. Irradiance level and daily photosynthetic period duration effects. Plant Physiol. 67:257–60
    [Google Scholar]
  22. 22.
    Chen A, Li C, Hu W, Lau MY, Lin H et al. 2014. PHYTOCHROME C plays a major role in the acceleration of wheat flowering under long-day photoperiod. PNAS 111:10037–44
    [Google Scholar]
  23. 23.
    Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD. 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–26
    [Google Scholar]
  24. 24.
    Cookson SJ, Chenu K, Granier C. 2007. Day length affects the dynamics of leaf expansion and cellular development in Arabidopsis thaliana partially through floral transition timing. Ann. Bot. 99:703–11
    [Google Scholar]
  25. 25.
    Corbesier L, Vincent C, Jang S, Fornara F, Fan Q et al. 2007. FT protein movement contributes to long-distance signaling in floral induction of Arabidopsis. Science 316:1030–33Demonstration that FT itself is the mobile florigen.
    [Google Scholar]
  26. 26.
    Covington MF, Maloof JN, Straume M, Kay SA, Harmer SL. 2008. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biol. 9:R130
    [Google Scholar]
  27. 27.
    Díaz-Riquelme J, Grimplet J, Martínez-Zapater JM, Carmona MJ. 2012. Transcriptome variation along bud development in grapevine (Vitis vinifera L.). BMC Plant Biol. 12:181
    [Google Scholar]
  28. 28.
    Dodd AN, Salathia N, Hall A, Kevei E, Toth R et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–33
    [Google Scholar]
  29. 29.
    Doi K, Izawa T, Fuse T, Yamanouchi U, Kubo T et al. 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. 18:926–36
    [Google Scholar]
  30. 30.
    Duplat-Bermúdez L, Ruiz-Medrano R, Landsman D, Mariño-Ramírez L, Xoconostle-Cázares B. 2016. Transcriptomic analysis of Arabidopsis overexpressing flowering locus T driven by a meristem-specific promoter that induces early flowering. Gene 587:120–31
    [Google Scholar]
  31. 31.
    Exposito-Alonso M, 500 Genomes Field Exp. Team, Burbano HA, Bossdorf O, Nielsen R, Weigel D 2019. Natural selection on the Arabidopsis thaliana genome in present and future climates. Nature 573:126–29
    [Google Scholar]
  32. 32.
    Fankhauser C, Staiger D. 2002. Photoreceptors in Arabidopsis thaliana: light perception, signal transduction and entrainment of the endogenous clock. Planta 216:1–16
    [Google Scholar]
  33. 33.
    Fernandez O, Ishihara H, George GM, Mengin V, Flis A et al. 2017. Leaf starch turnover occurs in long days and in falling light at the end of the day. Plant Physiol. 174:2199–212
    [Google Scholar]
  34. 34.
    Fichtner F, Lunn JE. 2021. The role of trehalose 6-phosphate (Tre6P) in plant metabolism and development. Annu. Rev. Plant Biol. 72:737–60
    [Google Scholar]
  35. 35.
    Figueroa CM, Lunn JE. 2016. A tale of two sugars: trehalose 6-phosphate and sucrose. Plant Physiol. 172:7–27
    [Google Scholar]
  36. 36.
    Flis A, Mengin V, Ivakov AA, Mugford ST, Hubberten H-M et al. 2019. Multiple circadian clock outputs regulate diel turnover of carbon and nitrogen reserves. Plant Cell Environ. 42:549–73
    [Google Scholar]
  37. 37.
    Flis A, Sulpice R, Seaton DD, Ivakov AA, Liput M et al. 2016. Photoperiod-dependent changes in the phase of core clock transcripts and global transcriptional outputs at dawn and dusk in Arabidopsis. Plant Cell Environ. 39:1955–81
    [Google Scholar]
  38. 38.
    Gao H, Zheng X-M, Fei G, Chen J, Jin M et al. 2013. Ehd4 encodes a novel and Oryza-genus-specific regulator of photoperiodic flowering in rice. PLOS Genetics 9:e1003281
    [Google Scholar]
  39. 39.
    Gao M, Geng F, Klose C, Staudt A-M, Huang H et al. 2019. Phytochromes measure photoperiod in Brachypodium. bioRxiv 697169. https://doi.org/10.1101/697169
  40. 40.
    Garner WW, Allard HA. 1920. Effect of the relative length of day and night and other factors of the environment on growth and reproduction in plants. J. Agric. Res. 18:553–606Demonstration that plants measure photoperiod to control development.
    [Google Scholar]
  41. 41.
    Gendron JM, Leung CC, Liu W. 2021. Energy as a seasonal signal for growth and reproduction. Curr. Opin. Plant Biol. 63:102092
    [Google Scholar]
  42. 42.
    Gibon Y, Pyl E-T, Sulpice R, Lunn JE, Höhne M et al. 2009. Adjustment of growth, starch turnover, protein content and central metabolism to a decrease of the carbon supply when Arabidopsis is grown in very short photoperiods. Plant Cell Environ. 32:859–74
    [Google Scholar]
  43. 43.
    Gnesutta N, Kumimoto RW, Swain S, Chiara M, Siriwardana C et al. 2017. CONSTANS imparts DNA sequence specificity to the histone fold NF-YB/NF-YC dimer. Plant Cell 29:1516–32
    [Google Scholar]
  44. 44.
    Graf A, Schlereth A, Stitt M, Smith AM. 2010. Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. PNAS 107:9458–63
    [Google Scholar]
  45. 45.
    Hamner KC, Takimoto A. 1964. Circadian rhythms and plant photoperiodism. Am. Nat. 98:295–322
    [Google Scholar]
  46. 46.
    Harmer SL. 2009. The circadian system in higher plants. Annu. Rev. Plant Biol. 60:357–77
    [Google Scholar]
  47. 47.
    Harmer SL, Hogenesch JB, Straume M, Chang H-S, Han B et al. 2000. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock. Science 290:2110–13
    [Google Scholar]
  48. 48.
    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 19:2988–3000
    [Google Scholar]
  49. 49.
    Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. 2003. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature 422:719–22
    [Google Scholar]
  50. 50.
    Heintzen C, Fischer R, Melzer S, Kappeler S, Apel K, Staiger D. 1994. Circadian oscillations of a transcript encoding a germin-like protein that is associated with cell walls in young leaves of the long-day plant Sinapis alba L. Plant Physiol. 106:905–15
    [Google Scholar]
  51. 51.
    Heintzen C, Melzer S, Fischer R, Kappeler S, Apel K, Staiger D. 1994. A light- and temperature-entrained circadian clock controls expression of transcripts encoding nuclear proteins with homology to RNA-binding proteins in meristematic tissue. Plant J. 5:799–813
    [Google Scholar]
  52. 52.
    Hernando CE, Romanowski A, Yanovsky MJ. 2017. Transcriptional and post-transcriptional control of the plant circadian gene regulatory network. Biochim. Biophys. Acta Gene Regul. Mech. 1860:84–94
    [Google Scholar]
  53. 53.
    Huffeldt NP. 2020. Photic barriers to poleward range-shifts. Trends Ecol. Evol. 35:652–55
    [Google Scholar]
  54. 54.
    Huffeldt NP. 2021. Importance of photic constraints depends on the population. Trends Ecol. Evol. 36:480–81
    [Google Scholar]
  55. 55.
    Imaizumi T, Auge G, Donohue K. 2017. Photoperiod throughout the maternal life cycle, not photoperiod during seed imbibition, influences germination in Arabidopsis thaliana. Am. J. Bot. 104:516–26
    [Google Scholar]
  56. 56.
    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 309:293–97
    [Google Scholar]
  57. 57.
    Ito T, Nishio H, Tarutani Y, Emura N, Honjo MN et al. 2019. Seasonal stability and dynamics of DNA methylation in plants in a natural environment. Genes 10:544
    [Google Scholar]
  58. 58.
    Itoh H, Nonoue Y, Yano M, Izawa T. 2010. A pair of floral regulators sets critical day length for Hd3a florigen expression in rice. Nat. Genet. 42:635–38
    [Google Scholar]
  59. 59.
    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 16:2006–20
    [Google Scholar]
  60. 60.
    Izumi M, Hidema J, Makino A, Ishida H. 2013. Autophagy contributes to nighttime energy availability for growth in Arabidopsis. Plant Physiol. 161:1682–93
    [Google Scholar]
  61. 61.
    Jaeger KE, Wigge PA. 2007. FT protein acts as a long-range signal in Arabidopsis. Curr. Biol. 17:1050–54
    [Google Scholar]
  62. 62.
    Jung C, Pillen K, Staiger D, Coupland G, von Korff M 2016. Recent advances in flowering time control. Front. Plant Sci. 7:2011
    [Google Scholar]
  63. 63.
    Kicia M, Gola EM, Janska H. 2010. Mitochondrial protease AtFtsH4 protects ageing Arabidopsis rosettes against oxidative damage under short-day photoperiod. Plant Signal. Behav. 5:126–28
    [Google Scholar]
  64. 64.
    Kim H, Kim Y, Yeom M, Lim J, Nam HG. 2016. Age-associated circadian period changes in Arabidopsis leaves. J. Exp. Bot. 67:2665–73
    [Google Scholar]
  65. 65.
    Kippes N, VanGessel C, Hamilton J, Akpinar A, Budak H et al. 2020. Effect of phyB and phyC loss-of-function mutations on the wheat transcriptome under short and long day photoperiods. BMC Plant Biol. 20:297
    [Google Scholar]
  66. 66.
    Klepikova AV, Logacheva MD, Dmitriev SE, Penin AA 2015. RNA-seq analysis of an apical meristem time series reveals a critical point in Arabidopsis thaliana flower initiation. BMC Genom. 16:466
    [Google Scholar]
  67. 67.
    Kojima S, Takahashi Y, Kobayashi Y, Monna L, Sasaki T et al. 2002. Hd3a, a rice ortholog of the Arabidopsis FT gene, promotes transition to flowering downstream of Hd1 under short-day conditions. Plant Cell Physiol. 43:1096–105
    [Google Scholar]
  68. 68.
    Koller D, Mayer AM, Poljakoff-Mayber A, Klein S. 1962. Seed germination. Annu. Rev. Plant Physiol. 13:437–64
    [Google Scholar]
  69. 69.
    Komiya R, Ikegami A, Tamaki S, Yokoi S, Shimamoto K. 2008. Hd3a and RFT1 are essential for flowering in rice. Development 135:767–74
    [Google Scholar]
  70. 70.
    Laubinger S, Marchal V, Gentilhomme J, Wenkel S, Adrian J et al. 2006. Arabidopsis SPA proteins regulate photoperiodic flowering and interact with the floral inducer CONSTANS to regulate its stability. Development 133:3213–22
    [Google Scholar]
  71. 71.
    Lemmer B. 2009. Discoveries of rhythms in human biological functions: a historical review. Chronobiol. Int. 26:1019–68
    [Google Scholar]
  72. 72.
    Lepistö A, Kangasjärvi S, Luomala E-M, Brader G, Sipari N et al. 2009. Chloroplast NADPH-thioredoxin reductase interacts with photoperiodic development in Arabidopsis. Plant Physiol. 149:1261–76
    [Google Scholar]
  73. 73.
    Lepistö A, Pakula E, Toivola J, Krieger-Liszkay A, Vignols F, Rintamäki E. 2013. Deletion of chloroplast NADPH-dependent thioredoxin reductase results in inability to regulate starch synthesis and causes stunted growth under short-day photoperiods. J. Exp. Bot. 64:3843–54
    [Google Scholar]
  74. 74.
    Leung CC, Tarté DA, Oliver LS, Gendron JM. 2022. Diverse photoperiodic gene expression patterns are likely mediated by distinct transcriptional systems in Arabidopsis. bioRxiv 2022.10.05.510993. https://doi.org/10.1101/2022.10.05.510993
  75. 75.
    Li M-W, Liu W, Lam H-M, Gendron JM. 2018. Characterization of two growth period QTLs reveals modification of PRR3 genes during soybean domestication. Plant Cell Physiol. 60:407–20
    [Google Scholar]
  76. 76.
    Liu W, Feke A, Leung CC, Tarté DA, Yuan W et al. 2021. A metabolic daylength measurement system mediates winter photoperiodism in plants. Dev. Cell 56:2501–15.e5Identification of the metabolic daylength measurement system for short-day gene expression and fitness in Arabidopsis.
    [Google Scholar]
  77. 77.
    Lu Y, Gehan JP, Sharkey TD. 2005. Daylength and circadian effects on starch degradation and maltose metabolism. Plant Physiol. 138:2280–91
    [Google Scholar]
  78. 78.
    Luccioni L, Krzymuski M, Sánchez-Lamas M, Karayekov E, Cerdán PD, Casal JJ. 2019. CONSTANS delays Arabidopsis flowering under short days. Plant J. 97:923–32
    [Google Scholar]
  79. 79.
    Lumsden PJ, Furuya M. 1986. Evidence for two actions of light in the photoperiodic induction of flowering in Pharbitis nil. Plant Cell Physiol. 27:1541–51
    [Google Scholar]
  80. 80.
    Manechini JRV, Santos PHdSS, Romanel E, Brito MDS, Scarpari MdS et al. 2021. Transcriptomic analysis of changes in gene expression during flowering induction in sugarcane under controlled photoperiodic conditions. Front. Plant Sci. 12:635784
    [Google Scholar]
  81. 81.
    Martín G, Rovira A, Veciana N, Soy J, Toledo-Ortiz G et al. 2018. Circadian waves of transcriptional repression shape PIF-regulated photoperiod-responsive growth in Arabidopsis. Curr. Biol. 28:311–18.e5
    [Google Scholar]
  82. 82.
    Martín G, Veciana N, Boix M, Rovira A, Henriques R, Monte E 2020. The photoperiodic response of hypocotyl elongation involves regulation of CDF1 and CDF5 activity. Physiol. Plant. 169:480–90
    [Google Scholar]
  83. 83.
    Mathieu J, Warthmann N, Kuttner F, Schmid M. 2007. Export of FT protein from phloem companion cells is sufficient for floral induction in Arabidopsis. Curr. Biol. 17:1055–60This work demonstrated that the FT protein could be exported from companion cells to induce flowering.
    [Google Scholar]
  84. 84.
    Maurya JP, Miskolczi PC, Mishra S, Singh RK, Bhalerao RP. 2020. A genetic framework for regulation and seasonal adaptation of shoot architecture in hybrid aspen. PNAS 117:11523–30
    [Google Scholar]
  85. 85.
    McClung CR. 2019. The plant circadian oscillator. Biology 8:14
    [Google Scholar]
  86. 86.
    McClung CR. 2021. Circadian clock components offer targets for crop domestication and improvement. Genes 12:374
    [Google Scholar]
  87. 87.
    McWatters HG, Bastow RM, Hall A, Millar AJ. 2000. The ELF3 zeitnehmer regulates light signalling to the circadian clock. Nature 408:716–20
    [Google Scholar]
  88. 88.
    Melzer S, Majewski DM, Apel K. 1990. Early changes in gene expression during the transition from vegetative to generative growth in the long-day plant Sinapis alba. Plant Cell 2:953–61
    [Google Scholar]
  89. 89.
    Mengin V, Pyl E-T, Alexandre Moraes T, Sulpice R, Krohn N et al. 2017. Photosynthate partitioning to starch in Arabidopsis thaliana is insensitive to light intensity but sensitive to photoperiod due to a restriction on growth in the light in short photoperiods. Plant Cell Environ. 40:2608–27
    [Google Scholar]
  90. 90.
    Michael TP, Breton G, Hazen SP, Priest H, Mockler TC et al. 2008. A morning-specific phytohormone gene expression program underlying rhythmic plant growth. PLOS Biol. 6:e225
    [Google Scholar]
  91. 91.
    Millar AJ, Straume M, Chory J, Chua NH, Kay SA. 1995. The regulation of circadian period by phototransduction pathways in Arabidopsis. Science 267:1163–66
    [Google Scholar]
  92. 92.
    Mockler TC, Michael TP, Priest HD, Shen R, Sullivan CM et al. 2007. The Diurnal Project: diurnal and circadian expression profiling, model-based pattern matching, and promoter analysis. Cold Spring Harbor. Symp. Quant. Biol. 72:353–63
    [Google Scholar]
  93. 93.
    Moraes TA, Mengin V, Annunziata MG, Encke B, Krohn N et al. 2019. Response of the circadian clock and Diel starch turnover to one day of low light or low CO2. Plant Physiol. 179:1457–78
    [Google Scholar]
  94. 94.
    Mugford ST, Fernandez O, Brinton J, Flis A, Krohn N et al. 2014. Regulatory properties of ADP glucose pyrophosphorylase are required for adjustment of leaf starch synthesis in different photoperiods. Plant Physiol. 166:1733–47
    [Google Scholar]
  95. 95.
    Müller NA, Wijnen CL, Srinivasan A, Ryngajllo M, Ofner I et al. 2016. Domestication selected for deceleration of the circadian clock in cultivated tomato. Nat. Genet. 48:89–93
    [Google Scholar]
  96. 96.
    Nagano AJ, Kawagoe T, Sugisaka J, Honjo MN, Iwayama K, Kudoh H. 2019. Annual transcriptome dynamics in natural environments reveals plant seasonal adaptation. Nat. Plants 5:74–83
    [Google Scholar]
  97. 97.
    Nanda KK, Hamner KC. 1958. Studies on the nature of the endogenous rhythm affecting photoperiodic response of Biloxi soybean. Bot. Gaz. 120:14–25
    [Google Scholar]
  98. 98.
    Nathan R, Horvitz N, He Y, Kuparinen A, Schurr FM, Katul GG. 2011. Spread of North American wind-dispersed trees in future environments. Ecol. Lett. 14:211–19
    [Google Scholar]
  99. 99.
    Navarro C, Abelenda JA, Cruz-Oró E, Cuéllar CA, Tamaki S et al. 2011. Control of flowering and storage organ formation in potato by FLOWERING LOCUS T. Nature 478:119–22
    [Google Scholar]
  100. 100.
    Nishida H, Ishihara D, Ishii M, Kaneko T, Kawahigashi H et al. 2013. Phytochrome C is a key factor controlling long-day flowering in barley. Plant Physiol. 163:804–14
    [Google Scholar]
  101. 101.
    Niwa Y, Yamashino T, Mizuno T. 2009. Circadian clock regulates photoperiodic response of hypocotyl elongation through a coincidence mechanism in Arabidopsis thaliana. Plant Cell Physiol. 50:838–54
    [Google Scholar]
  102. 102.
    Nozue K, Covington MF, Duek PD, Lorrain S, Fankhauser C et al. 2007. Rhythmic growth explained by coincidence between internal and external cues. Nature 448:358–63Demonstration that the PIF proteins are part of a coincidence mechanism that controls hypocotyl growth.
    [Google Scholar]
  103. 103.
    Nunes MV, Saunders D. 1999. Photoperiodic time measurement in insects: a review of clock models. J. Biol. Rhythms 14:84–104
    [Google Scholar]
  104. 104.
    Osugi A, Itoh H, Ikeda-Kawakatsu K, Takano M, Izawa T. 2011. Molecular dissection of the roles of phytochrome in photoperiodic flowering in rice. Plant Physiol. 157:1128–37
    [Google Scholar]
  105. 105.
    Pal SK, Liput M, Piques M, Ishihara H, Obata T et al. 2013. Diurnal changes of polysome loading track sucrose content in the rosette of wild-type Arabidopsis and the starchless pgm mutant. Plant Physiol. 162:1246–65
    [Google Scholar]
  106. 106.
    Pankin A, Campoli C, Dong X, Kilian B, Sharma R et al. 2014. Mapping-by-sequencing identifies HvPHYTOCHROME C as a candidate gene for the early maturity 5 locus modulating the circadian clock and photoperiodic flowering in barley. Genetics 198:383–96
    [Google Scholar]
  107. 107.
    Pearce S, Kippes N, Chen A, Debernardi JM, Dubcovsky J. 2016. RNA-seq studies using wheat PHYTOCHROME B and PHYTOCHROME C mutants reveal shared and specific functions in the regulation of flowering and shade-avoidance pathways. BMC Plant Biol. 16:141
    [Google Scholar]
  108. 108.
    Pittendrigh CS. 1972. Circadian surfaces and the diversity of possible roles of circadian organization in photoperiodic induction. PNAS 69:2734–37
    [Google Scholar]
  109. 109.
    Pittendrigh CS, Minis DH. 1964. The entrainment of circadian oscillations by light and their role as photoperiodic clocks. Am. Nat. 98:261–94
    [Google Scholar]
  110. 110.
    Plantenga FDM, Heuvelink E, Rienstra JA, Visser RGF, Bachem CWB, Marcelis LFM. 2019. Coincidence of potato CONSTANS (StCOL1) expression and light cannot explain night-break repression of tuberization. Physiol. Plant. 167:250–63
    [Google Scholar]
  111. 111.
    Putterill J, Robson F, Lee K, Simon R, Coupland G. 1995. The CONSTANS gene of Arabidopsis promotes flowering and encodes a protein showing similarities to zinc finger transcription factors. Cell 80:847–57The identification and cloning of the CONSTANS gene in Arabidopsis.
    [Google Scholar]
  112. 112.
    Qiu L, Wu Q, Wang X, Han J, Zhuang G et al. 2021. Forecasting rice latitude adaptation through a daylength-sensing-based environment adaptation simulator. Nat. Food 2:348–62
    [Google Scholar]
  113. 113.
    Rensing L, Meyer-Grahle U, Ruoff P. 2001. Biological timing and the clock metaphor: oscillatory and hourglass mechanisms. Chronobiol. Int. 18:329–69
    [Google Scholar]
  114. 114.
    Rosado-Souza L, Proost S, Moulin M, Bergmann S, Bocobza SE et al. 2019. Appropriate thiamin pyrophosphate levels are required for acclimation to changes in photoperiod. Plant Physiol. 180:185–97
    [Google Scholar]
  115. 115.
    Ruttink T, Arend M, Morreel K, Storme V, Rombauts S et al. 2007. A molecular timetable for apical bud formation and dormancy induction in poplar. Plant Cell 19:2370–90
    [Google Scholar]
  116. 116.
    Saikkonen K, Taulavuori K, Hyvönen T, Gundel PE, Hamilton CE et al. 2012. Climate change-driven species' range shifts filtered by photoperiodism. Nat. Clim. Change 2:239–42
    [Google Scholar]
  117. 117.
    Saji H, Furuya M, Takimoto A. 1984. Role of the photoperiod preceding a flower-inductive dark period in dark-grown seedlings of Pharbitis nil Choisy. Plant Cell Physiol. 25:715–20
    [Google Scholar]
  118. 118.
    Salazar JD, Saithong T, Brown PE, Foreman J, Locke JC et al. 2009. Prediction of photoperiodic regulators from quantitative gene circuit models. Cell 139:1170–79
    [Google Scholar]
  119. 119.
    Samach A, Onouchi H, Gold SE, Ditta GS, Schwarz-Sommer Z et al. 2000. Distinct roles of CONSTANS target genes in reproductive development of Arabidopsis. Science 288:1613–36
    [Google Scholar]
  120. 120.
    Sapey E, Jiang B, Liu L, Yuan S, Wu T et al. 2022. Transcriptome profile of a long-juvenile soybean genotype Huaxia-3 under short and long photoperiod. Plant Mol. Biol. Rep. 40:433–45
    [Google Scholar]
  121. 121.
    Sawa M, Nusinow DA, Kay SA, Imaizumi T. 2007. FKF1 and GIGANTEA complex formation is required for day-length measurement in Arabidopsis. Science 318:261–65
    [Google Scholar]
  122. 122.
    Schaffer R, Ramsay N, Samach A, Putterill J, Carre IA, Coupland G. 1998. The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93:1219–29
    [Google Scholar]
  123. 123.
    Seaton DD, Graf A, Baerenfaller K, Stitt M, Millar AJ, Gruissem W. 2018. Photoperiodic control of the Arabidopsis proteome reveals a translational coincidence mechanism. Mol. Syst. Biol. 14:e7962
    [Google Scholar]
  124. 124.
    Settele J, Bishop J, Potts SG. 2016. Climate change impacts on pollination. Nat. Plants 2:16092
    [Google Scholar]
  125. 125.
    Smith AM, Zeeman SC. 2020. Starch: a flexible, adaptable carbon store coupled to plant growth. Annu. Rev. Plant Biol. 71:217–45
    [Google Scholar]
  126. 126.
    Somers DE, Schultz TF, Milnamow M, Kay SA 2000. ZEITLUPE encodes a novel clock-associated PAS protein from Arabidopsis. Cell 101:319–29
    [Google Scholar]
  127. 127.
    Song YH, Kubota A, Kwon MS, Covington MF, Lee N et al. 2018. Molecular basis of flowering under natural long-day conditions in Arabidopsis. Nat. Plants 4:824–35
    [Google Scholar]
  128. 128.
    Staiger D. 2001. RNA-binding proteins and circadian rhythms in Arabidopsis thaliana. Philo. Trans. R. Soc. Lond. B. 356:1755–59
    [Google Scholar]
  129. 129.
    Staiger D, Shin J, Johansson M, Davis SJ. 2013. The circadian clock goes genomic. Genome Biol. 14:208
    [Google Scholar]
  130. 130.
    Suárez-López 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 410:1116–20Discovery that CONSTANS is at the intersection of the circadian clock and flowering time.
    [Google Scholar]
  131. 131.
    Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N et al. 2014. Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol. Plant 7:137–55
    [Google Scholar]
  132. 132.
    Takimoto A, Ikeda K. 1961. Effect of twilight on photoperiodic induction in some short day plants. Plant Cell Physiol. 2:213–29
    [Google Scholar]
  133. 133.
    Tarancon C, Gonzalez-Grandio E, Oliveros JC, Nicolas M, Cubas P 2017. A conserved carbon starvation response underlies bud dormancy in woody and herbaceous species. Front. Plant Sci. 8:788
    [Google Scholar]
  134. 134.
    Thomas B, Vince-Prue D. 1997. Photoperiodism in Plants London: Academic
    [Google Scholar]
  135. 135.
    Thomson G, Taylor J, Putterill J. 2019. The transcriptomic response to a short day to long day shift in leaves of the reference legume Medicago truncatula. PeerJ 7:e6626
    [Google Scholar]
  136. 136.
    Tian H, Li Y, Wang C, Xu X, Zhang Y et al. 2021. Photoperiod-responsive changes in chromatin accessibility in phloem companion and epidermis cells of Arabidopsis leaves. Plant Cell 33:475–91
    [Google Scholar]
  137. 137.
    Tougeron K. 2021. How constraining are photic barriers to poleward range-shifts?. Trends Ecol. Evol. 36:478–79
    [Google Scholar]
  138. 138.
    Tournois J. 2014. Études sur la sexualite du houblon. Ann. Sci. Nat. 19:49–189
    [Google Scholar]
  139. 139.
    Turner A, Beales J, Faure S, Dunford RP, Laurie DA 2005. The pseudo-response regulator Ppd-H1 provides adaptation to photoperiod in barley. Science 310:1031–34
    [Google Scholar]
  140. 140.
    Tylewicz S, Petterle A, Marttila S, Miskolczi P, Azeez A et al. 2018. Photoperiodic control of seasonal growth is mediated by ABA acting on cell-cell communication. Science 360:212–15
    [Google Scholar]
  141. 141.
    Valverde F, Mouradov A, Soppe W, Ravenscroft D, Samach A, Coupland G. 2004. Photoreceptor regulation of CONSTANS protein in photoperiodic flowering. Science 303:1003–6
    [Google Scholar]
  142. 142.
    Vince-Prue D. 1994. The duration of light and photoperiodic responses. Photomorphogenesis in Plants RE Kendrick, GHM Kronenberg 447–90. Dordrecht, Neth: Springer
    [Google Scholar]
  143. 143.
    Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T et al. 2013. Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–7
    [Google Scholar]
  144. 144.
    Walther G-R, Roques A, Hulme PE, Sykes MT, Pyšek P et al. 2009. Alien species in a warmer world: risks and opportunities. Trends Ecol. Evol. 24:686–93
    [Google Scholar]
  145. 145.
    Wang Q, Liu W, Leung CC, Tarte DA, Gendron J. 2023. Parallel mechanisms detect different photoperiods to independently control seasonal flowering and growth in plants. bioRxiv 2023.02.10.528016. https://doi.org/10.1101/2023.02.10.528016
  146. 146.
    Wang Z-Y, Tobin EM. 1998. Constitutive expression of the CIRCADIAN CLOCK ASSOCIATED1 (CCA1) gene disrupts circadian rhythms and suppresses its own expression. Cell 93:1207–17
    [Google Scholar]
  147. 147.
    Wei X, Xu J, Guo H, Jiang L, Chen S et al. 2010. DTH8 suppresses flowering in rice, influencing plant height and yield potential simultaneously. Plant Physiol. 153:1747–58
    [Google Scholar]
  148. 148.
    Weng X, Lovell JT, Schwartz SL, Cheng C, Haque T et al. 2019. Complex interactions between day length and diurnal patterns of gene expression drive photoperiodic responses in a perennial C4 grass. Plant Cell Environ. 42:2165–82
    [Google Scholar]
  149. 149.
    Wigge PA, Kim MC, Jaeger KE, Busch W, Schmid M et al. 2005. Integration of spatial and temporal information during floral induction in Arabidopsis. Science 309:1056–59
    [Google Scholar]
  150. 150.
    Wu W, Zheng X-M, Lu G, Zhong Z, Gao H et al. 2013. Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. PNAS 110:2775–80
    [Google Scholar]
  151. 151.
    Xiang Y, Sapir T, Rouillard P, Ferrand M, Jiménez-Gómez JM. 2022. Interaction between photoperiod and variation in circadian rhythms in tomato. BMC Plant Biol. 22:187
    [Google Scholar]
  152. 152.
    Xue W, Xing Y, Weng X, Zhao Y, Tang W et al. 2008. Natural variation in Ghd7 is an important regulator of heading date and yield potential in rice. Nat. Genet. 40:761–67
    [Google Scholar]
  153. 153.
    Yan J, Kim YJ, Somers DE. 2021. Post-translational mechanisms of plant circadian regulation. Genes 12:325
    [Google Scholar]
  154. 154.
    Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L et al. 2000. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell 12:2473–84
    [Google Scholar]
  155. 155.
    Yanovsky MJ, Kay SA. 2002. Molecular basis of seasonal time measurement in Arabidopsis. Nature 419:308–12Discovery that the circadian clock is a required component for CONSTANS photoperiod measurement.
    [Google Scholar]
  156. 156.
    Yu B, He X, Tang Y, Chen Z, Zhou L et al. 2023. Photoperiod controls plant seed size in a CONSTANS-dependent manner. Nat. Plants 9:343–54
    [Google Scholar]
  157. 157.
    Zhang B, Holmlund M, Lorrain S, Norberg M, Bakó L et al. 2017. BLADE-ON-PETIOLE proteins act in an E3 ubiquitin ligase complex to regulate PHYTOCHROME INTERACTING FACTOR 4 abundance. eLife 6:e26759
    [Google Scholar]
  158. 158.
    Zhao Y, Zhao B, Xie Y, Jia H, Li Y et al. 2022. The evening complex promotes maize flowering and adaptation to temperate regions. Plant Cell 35:369–89
    [Google Scholar]
  159. 159.
    Zierer W, Rüscher D, Sonnewald U, Sonnewald S. 2021. Tuber and tuberous root development. Annu. Rev. Plant Biol. 72:551–80
    [Google Scholar]
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