Abstract
Global warming affects various environmental factors, including temperature, precipitation, drought, and flooding. Temperature rise is mainly due to increased levels of carbon dioxide (CO2), which was increased by approximately 50% since the industrialization period. Here, we review the effect of global climate changes on the alteration of flowering time. High temperature during vernalization delays flowering mainly due to increased expression of FLOWERING LOCUS C and TaVERNALIZATION 2 encoding floral repressors in Arabidopsis and winter wheat, respectively. Increased ambient temperature promotes flowering in many plant species, especially in spring-flowering plants. In Arabidopsis, higher temperature induces SHORT VEGETATIVE PHASE–FLOWERING LOCUS M (FLM)-δ complex that promotes FLOWERING LOCUS T (FT) expression. Moreover, high temperatures suppress a floral repressor FLM and disturb the stability of the evening complex that is an inhibitor of PHYTOCHROME INTERACTING FACTOR 4, which induces FT expression. Drought induces or delays flowering depending on plant species, growing season, and developmental stage. In Arabidopsis, drought induces flowering by promoting the GIGANTEA-CONSTANS (CO) pathway, whereas the stress delays flowering under short-day conditions via ABSCISIC ACID-INSENSITIVE 1. Plants also alter flowering time to avoid wet conditions, including flooding and precipitation. Increased CO2 concentration accelerates flowering, probably by increasing the rate of photosynthesis. We also reviewed the effect of climate change on pollination.
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References
Abrha H (2019) Climate change impact on coffee and the pollinator bee suitable area interaction in Raya Azebo. Ethiopia Environ Hazards 18(5):400–413
Adeyemo OS, Hyde PT, Setter TL (2019) Identification of FT family genes that respond to photoperiod, temperature and genotype in relation to flowering in cassava (Manihot esculenta, Crantz). Plant Reprod 32:181–191
Anderson J, Inouye D, Iler A, Colautti R, Mitchell-Olds T (2012) Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change. Proc Biol Sci 279:3843–3852
Baena-González E, Rolland F, Thevelein JM, Sheen J (2007) A central integrator of transcription networks in plant stress and energy signaling. Nature 448:938–942
Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2(e106–e106):980–989
Benscoter A, Miller-Rushing A, Inouye D (2010) Changes in snowmelt date and summer precipitation affect the flowering phenology of Erythronium grandiflorum (glacier lily; Liliaceae). Am J Bot 97:1431–1437
Bernal M, Estiarte M, Penuelas J (2011) Drought advances spring growth phenology of the Mediterranean shrub Erica multiflora. Plant Biol Stuttg Ger 13:252–257
Bernier G, Havelange A, Houssa C, Petitjean A, Lejeune P (1993) Physiological signals that induce flowering. Plant Cell 5:1147–1155
Blázquez MA, Ahn JH, Weigel D (2003) A thermosensory pathway controlling flowering time in Arabidopsis thaliana. Nat Genet 33:168–171
Brotherton S, Joyce C, Berg M, Awcock G (2019) Resilience to extreme flooding shown by both hydric and mesic wetland plant species. Ecohydrology: 12e2158
Bustamante E, Burquez A (2008) Effects of plant size and weather on the flowering phenology of the organ pipe cactus (Stenocereus thurberi). Ann Bot 102:1019–1030
Capovilla G, Schmid M, Posé D (2014) Control of flowering by ambient temperature. J Exp Bot 66:59–69
Cho LH, Yoon J, An G (2017) The control of flowering time by environmental factors. Plant J Cell Mol Biol 90:708–719
Chouard P (1960) Vernalization and its relations to dormancy. Annu Rev Plant Physiol 11:191–238
Christmann S (2019) Do we realize the full impact of pollinator loss on other ecosystem services and the challenges for any restoration in terrestrial areas? Restor Ecol 27:720–725
Claire J, Maria B, Bluz K, Thomas D, Serena M, Mereu V, Michetti M (2019) Climate change adaptation in the agriculture sector in Europe, 1–112
Cramer W, Yohe GW, Auffhammer M, Huggel C (2014) Chapter 18: Detection and Attribution of Observed Impacts. IPCC AR5 WG2 A 2014, 979–1037
Craufurd PQ, Wheeler TR (2009) Climate change and the flowering time of annual crops. J Exp Bot 60:2529–2539
Curtis PS, Wang X (1998) A meta-analysis of elevated CO2 effects on woody plant mass, form, and physiology. Oecologia 113:299–313
Dahanayake SR, Galwey NW (1998) Effects of interactions between low and high temperature treatments on flowering of spring rape (Brassica napus var. annua). Ann Bot 81:609–617
Dixon L, Karsai I, Kiss T, Adamski N, Liu Z, Ding Y, Allard V, Boden S, Griffiths S (2019) VERNALIZATION1 controls developmental responses of winter wheat under high ambient temperatures. Development 146(dev172684):1–10
Doyle MR, Davis SJ, Bastow RM, McWatters HG, Kozma-Bognár L, Nagy F, Millar AJ, Amasino RM (2002) The ELF4 gene controls circadian rhythms and flowering time in Arabidopsis thaliana. Nature 419:74–77
Du H, Huang F, Wu N, Li X, Hu H, Xiong L (2018) Integrative regulation of drought escape through ABA-dependent and independent pathways in Rice. Mol Plant 11:584–597
Dyer AG, Whitney HM, Arnold SEJ, Glover BJ, Chittka L (2006) Bees associate warmth with floral colour. Nature 442:525–525
Elers B, Wiebe HJ (1984) Flower formation of Chinese cabbage. II Anti-vernalization and short-day treatment. Sci Hortic 22:327–332
Evans LT, Wardlaw IF, Fischer RA (1975) Wheat. In: Evans LT (ed) Crop physiology. Cambridge University Press, Cambridge, pp 101–149
Fernández V, Takahashi Y, Le Gourrierec J, Coupland G (2016) Photoperiodic and thermosensory pathways interact through CONSTANS to promote flowering at high temperature under short days. Plant J 86:426–440
Fettell N, Bowden P, McNee T (2010) Barley growth & development. Industry & Investment NSW: 1–82
Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691
Fox N, Jönsson AM (2019) Climate effects on the onset of flowering in the United Kingdom. Environ Sci Eur 31:89
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 104:1278
Fukao T, Barrera-Figueroa BE, Juntawong P, Peña-Castro JM (2019) Submergence and waterlogging stress in plants: a review highlighting research opportunities and understudied Aspects. Front Plant Sci 10:340
Galbiati F, Chiozzotto R, Locatelli F, Spada A, Genga A, Fornara F (2016) Hd3a, RFT1 and Ehd1 integrate photoperiodic and drought stress signals to delay the floral transition in rice. Plant Cell Environ 39(9):1982–1993
Gendall AR, Levy YY, Wilson A (2001) Dean C (2001) The VERNALIZATION 2 gene mediates the epigenetic regulation of vernalization in Arabidopsis. Cell 107(4):525–535
Gérard M, Vanderplanck M, Wood T, Michez D (2020) Global warming and plant–pollinator mismatches. Emerg Top Life Sci 4:77–86
Giannini TC, Costa WF, Borges RC, Miranda L, da Costa CPW, Saraiva AM, Imperatriz Fonseca VL (2020) Climate change in the Eastern Amazon: crop-pollinator and occurrence-restricted bees are potentially more affected. Reg Environ Change 20:9
Gol L, Haraldsson EB, Von Korff M (2020) Ppd-H1 integrates drought stress signals to control spike development and flowering time in barley. J Exp Bot: eraa261
Gregory FG, Purvis ON (1948) Reversal of vernalization by high temperature. Nature 161:859–860
Guo T, Mu Q, Wang J, Vanous A, Onogi A, Iwata H, Li X, Yu J (2020) Dynamic effects of interacting genes underlying rice flowering-time phenotypic plasticity and global adaptation. Genome Res 30:673–683
Han Y, Zhang X, Wang Y, Ming F (2013) The Suppression of WRKY44 by GIGANTEA-miR172 pathway is involved in drought response of Arabidopsis thaliana. PLoS ONE 8:e73541
Hattori Y, Nagai K, Furukawa S, Song XJ, Kawano R, Sakakibara H, Wu J, Matsumoto T, Yoshimura A, Kitano H, Matsuoka M, Mori H, Ashikari M (2009) The ethylene response factors SNORKEL1 and SNORKEL2 allow rice to adapt to deep water. Nature 7258:1026–1030
Hazen SP, Schultz TF, Pruneda-Paz JL, Borevitz JO, Ecker JR, Kay SA (2005) LUX ARRHYTHMO encodes a Myb domain protein essential for circadian rhythms. Proc Natl Acad Sci USA 102:10387
Hicks KA, Millar AJ, Carré IA, Somers DE, Straume M, Meeks-Wagner DR, Kay SA (1996) Conditional circadian dysfunction of the Arabidopsis early-flowering 3 mutant. Science 274:790–792
Hu Q, Weiss A, Feng S, Baenziger PS (2005) Earlier winter wheat heading dates and warmer spring in the U.S. Great Plains Agric For Meteorol 135:284–290
Hwang K, Susila H, Nasim Z, Jung JY, Ahn JH (2019) Arabidopsis ABF3 and ABF4 transcription factors act with the NF-YC complex to regulate SOC1 expression and mediate drought-accelerated flowering. Mol Plant 12:489–505
IPCC (2007) Summary for Policymakers. In: Climate Change 2007: The Physical Science Basis. Contribution of Working Group I to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Cambridge University Press
IPCC (2018) Summary for Policymakers. IPCC SR15 2018: 3–24
Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot 96:501–505
Jagadish SVK, Bahuguna RN, Djanaguiraman M, Gamuyao R, Prasad PVV, Craufurd PQ (2016) Implications of high temperature and elevated CO2 on flowering time in plants. Front Plant Sci 7:913
Jentsch A, Kreyling J, Boettcher-Treschkow J, Beierkuhnlein C (2008) Beyond gradual warming: Extreme weather events alter flower phenology of European grassland and heath species. Glob Change Biol 15:837–849
Jeong DH, Schmidt S, Rymarquis L, Park S, Ganssmann M, German M, Accerbi M, Zhai J, Fahlgren N, Fox S, Garvin D, Mockler T, Carrington J, Meyers B, Green P (2013) Parallel analysis of RNA ends enhances global investigation of microRNAs and target RNAs of Brachypodium distachyon. Genome Biol 14:145
Johnston A, Reekie E (2008) Regardless of whether rising atmospheric carbon dioxide levels increase air temperature, flowering phenology will be affected. Int J Plant Sci 169:1210–1218
Jung JH, Barbosa AD, Hutin S, Kumita JR, Gao M, Derwort D, Silva CS, Lai X, Pierre E, Geng F, Kim SB, Baek S, Zubieta C, Jaeger KE, Wigge PA (2020) A prion-like domain in ELF3 functions as a thermosensor in Arabidopsis. Nature 585:256–260
Kato K, Yokoyama H (1992) Geographical variation in heading characters among wheat landraces, Triticum aestivum L., and its implication for their adaptability. Theor Appl Genet 84:259–265
Kehrberger S, Holzschuh A (2019) How does timing of flowering affect competition for pollinators, flower visitation and seed set in an early spring grassland plant? Sci Rep 9:15593
Kigel J, Konsens I, Rosen N, Rotem G, Kon A, Fragman-Sapir O (2013) Relationships between flowering time and rainfall gradients across Mediterranean-desert transects. Isr J Ecol Evol 57:91–109
Kim DH, Sung S (2013) Coordination of the vernalization response through a VIN3 and FLC Gene Family Regulatory Network in Arabidopsis. Plant Cell 25:454
Kim DH, Sung S (2014) Genetic and epigenetic mechanisms underlying vernalization. Arab Book 12:e0171–e0171
Kjøhl M, Nielsen A, Stenseth NC (2011) Potential effects of climate change on crop pollination. Food and Agriculture Organization of the United Nations. FAO, Rome
Kleemola J, Peltonen J, Peltonensainio P (1994) Apical development and growth of barley under different CO2 and nitrogen regimes. J Agron Crop Sci 173:79–92
Koini MA, Alvey L, Allen T, Tilley CA, Harberd NP, Whitelam GC, Franklin KA (2009) High temperature-mediated adaptations in plant architecture require the bHLH transcription factor PIF4. Curr Biol 19:408–413
Kooyers NJ (2015) The evolution of drought escape and avoidance in natural herbaceous populations. Plant Sci 234:155–162
Kudo G, Nishikawa Y, Kasagi T, Kosuge S (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecol Res 19:255–259
Kumar SV, Lucyshyn D, Jaeger K, Alos E, Alvey E, Harberd N, Wigge P (2012) Transcription factor PIF4 controls the thermosensory activation of flowering. Nature 484:242–245
Labandera AM, Tedds HM, Bailey M, Sprigg C, Etherington RD, Akintewe O, Kalleechurn G, Holdsworth MJ, Gibbs DJ (2020) The PRT6 N-degron pathway restricts VERNALIZATION 2 to endogenous hypoxic niches to modulate plant development. New Phytol.
Lawson DA, Rands SA (2019) The effects of rainfall on plant–pollinator interactions. Arthropod-Plant Interact 13:561–569
Lee JH, Lee JS, Ahn JH (2008) Ambient temperature signaling in plants: An emerging field in the regulation of flowering time. J Plant Biol 5:321–326
Lee JH, Ryu HS, Chung KS, Posé D, Kim S, Schmid M, Ahn JH (2013) Regulation of temperature-responsive flowering by MADS-Box transcription factor repressors. Science 342(6158):628–632
Lin CC, Chao YT, Chen WC, Ho HY, Chou MY, Li YR (2019) Regulatory cascade involving transcriptional and N-end rule pathways in rice under submergence. Proc Nat Acad Sci USA 116:3300–3309
Long S, Ainsworth E, Rogers A, Ort D (2004) Rising atmospheric carbon dioxide: plants face the future. Annu Rev Plant Biol 55:591–628
Luan W, Chen H, Fu Y, Si H, Peng W, Song S, Liu W, Hu G, Sun Z, Xie D, Sun C (2009) The effect of the crosstalk between photoperiod and temperature on the Heading-Date in Rice. PLoS ONE 4:e5891
Lutz U, Posé D, Pfeifer M, Gundlach H, Hagmann J, Wang C, Weigel D, Mayer KFX, Schmid M, Schwechheimer C (2015) Modulation of ambient temperature-dependent flowering in Arabidopsis thaliana by natural variation of FLOWERING LOCUS M. PLOS Genet 11:e1005588
Madrid E, Chandler JW, Coupland G (2020) Gene regulatory networks controlled by FLOWERING LOCUS C that confer variation in seasonal flowering and life history. J Exp Bot 5:eraa216
McClung CR, Lou P, Hermand V, Kim JA (2016) The importance of ambient temperature to growth and the induction of flowering. Front Plant Sci 7:1266–1266
Melgar JC, Dunlop J, Albrigo G, Syvertsen J (2010) Winter drought stress can delay flowering and avoid immature fruit loss during late-season mechanical harvesting of “Valencia” Oranges. Hortic Sci 45:271–276
Menzel A, Sparks T, Estrella N, Koch E, Aasa A, Ahas R (2006) European phenological response to climate change matches be warming pattern. Global Change Biol 12:1969–1976
Mohandass D, Zhao JL, Xia YM, Campbell M, Li Q (2015) Increasing temperature causes flowering onset time changes of alpine ginger Roscoea in the Central Himalayas. J Asia Pac Biodivers 8:191–198
Monroe JG, Powell T, Price N, Mullen JL, Howard A, Evans K, Lovell JT, McKay JK (2018) Drought adaptation in Arabidopsis thaliana by extensive genetic loss-of-function. Elife 6:e41038
Moore LM, Lauenroth WK (2017) Differential effects of temperature and precipitation on early- vs. late-flowering species. Ecosphere 8: e01819
Morton EM, Rafferty NE (2017) Plant–pollinator interactions under climate change: The use of spatial and temporal transplants. Appl Plant Sci 5: apps.1600133
Nagatoshi Y, Fujita Y (2019) Accelerating Soybean BREEDING in a CO2-supplemented growth chamber. Plant Cell Physiol 60:77–84
Nagy L, Kreyling J, Gellesch E, Beierkuhnlein C, Jentsch A (2012) Recurring weather extremes alter the flowering phenology of two common temperate shrubs. Int J Biometeorol 57(4):579–588
Nakano Y, Higuchi Y, Sumitomo K, Hisamatsu T (2013) Flowering retardation by high temperature in chrysanthemums: involvement of FLOWERING LOCUS T-like 3 gene repression. J Exp Bot 64:909–920
Nakano Y, Date M, Sumitomo K, Oda A, Hisamatsu T (2015) Delay of flowering by high temperature in chrysanthemum: Heat-sensitive time-of-day and heat effects on CsFTL3 and CsAFT gene expression. J Hortic Sci Biotechnol 90:143–149
Norgate M, Boyd-Gerny S, Simonov V, Rosa MGP, Heard TA, Dyer AG (2010) Ambient temperature influences Australian native stingless bee (Trigona carbonaria) Preference for Warm Nectar. PLoS ONE 5:e12000
Ohnishi T, Yoshino M, Yamakawa H, Kinoshita T (2011) The biotron breeding system: a rapid and reliable procedure for genetic studies and breeding in rice. Plant Cell Physiol 52:1249–1257
Peña-Castro JM, Van Zanten M, Lee SC, Patel MR, Voesenek LAJC, Fukao T, Bailey-Serres J (2011) Expression of rice SUB1A and SUB1C transcription factors in Arabidopsis uncovers flowering inhibition as a submergence tolerance mechanism. Plant J 67:434–446
Philips B, Goldy R, Brainard D, Michigan State University Extension (2020) Bolting in spring vegetables. https://www.canr.msu.edu/news/bolting-in-spring-vegetables#sources
Posé D, Verhage L, Ott F, Yant L, Mathieu J, Angenent G, Immink R, Schmid M (2013) Temperature-dependent regulation of flowering by antagonistic FLM variants. Nature 503.
Prentice I, Farquhar G, Fasham M, Goulden M, Heimann M, Jaramillo V, Kheshgi H, Le Quéré C, Scholes R, Wallace DWR (2001) The carbon cycle and atmospheric carbon dioxide, in: Climate Change 2001: The Scientific Basis.
Rafferty NE, Diez JM, Bertelsen CD (2020) Changing climate drives divergent and nonlinear shifts in flowering phenology across elevations. Curr Biol 30:432–441
Rehman A, Jingdong L, Du Y, Khatoon R, Wagan SA, Khan S (2015) Flood disaster in Pakistan and its impact on agriculture growth. Glob Adv Res J Agric Sci 4:827–830
Rezazadeh A, Harkess R, Telmadarrehei T (2018) The Effect of light intensity and temperature on flowering and morphology of potted red firespike. Horticulturae 4:36
Riboni M, Galbiati M, Tonelli C, Conti L (2013) GIGANTEA Enables Drought Escape Response via Abscisic Acid-Dependent Activation of the Florigens and SUPPRESSOR OF OVEREXPRESSION OF CONSTANS1. Plant Physiol 162:1706
Riboni M, Robustelli Test A, Galbiati M, Tonelli C, Conti L (2016) ABA-dependent control of GIGANTEA signalling enables drought escape via up-regulation of FLOWERING LOCUS T in Arabidopsis thaliana. J Exp Bot 67:6309–6322
Richman SK, Levine JM, Stefan L, Johnson CA (2020) Asynchronous range shifts drive alpine plant–pollinator interactions and reduce plant fitness. Glob Change Biol 26:3052–3064
Rietveld P, Wilkinson C, Franssen H, Balk PA, Plas L, Weisbeek P, Boer AD (2000) Low temperature sensing in tulip (Tulipa gesneriana L.) is mediated through an increased response to auxin. J Exp Bot 51:587–594
Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: Conserved and Novel Mechanisms. Annu Rev Plant Biol 57:675–709
Rosenthal SJ, McCarty R (2019) Switching winter and summer photoperiods in an animal model of bipolar disorder. Neuropsychopharmacol 44:1677–1678
Ruperti B, Botton A, Populin F, Eccher G, Brilli M, Quaggiotti S, Trevisan S, Cainelli N, Guarracino P, Schievano E, Meggio F (2019) Flooding responses on grapevine: a physiological, transcriptional, and metabolic perspective. Front Plant Sci 10:339
Sánchez-Bermejo E, Zhu W, Tasset C, Eimer H, Sureshkumar S, Singh R, Sundaramoorthi V, Colling L, Balasubramanian S (2015) Genetic architecture of natural variation in thermal responses of Arabidopsis. Plant Physiol 169
Satake A, Kawagoe T, Saburi Y, Chiba Y, Sakurai G, Kudoh H (2013) Forecasting flowering phenology under climate warming by modelling regulatory dynamics of flowering-time genes. Nat Commun 4:2303
Sawa M, Kay SA (2011) GIGANTEA directly activates FLOWERING LOCUS T in Arabidopsis thaliana. Proc Natl Acad Sci 108:11698
Scaven VL, Rafferty NE (2013) Physiological effects of climate warming on flowering plants and insect pollinators and potential consequences for their interactions. Curr Zool 59:418–426
Scortecci K, Michaels S, Amasino R (2001) Identification of a MADS-box gene, FLOWERING LOCUS M, that represses flowering. Plant J Cell Mol Biol 26:229–236
Seneweera S, Milham P, Conroy J (1994) Influence of elevated CO2 and phosphorus nutrition on the growth and yield of a short-duration rice (Oryza sativa L. cv. Jarrah). Aust J Plant Physiol 21:281–292
Seo PJ, Ryu J, Kang SK, Park CM (2011) Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis. Plant J 65:418–429
Shavrukov Y, Kurishbayev A, Jatayev S, Shvidchenko V, Zotova L, Koekemoer F, de Groot S, Soole K, Langridge P (2017) Early flowering as a drought escape mechanism in plants: how can it aid wheat production? Front Plant Sci 8:1950–1950
Shim JS, Jang G (2020) Environmental signal-dependent regulation of flowering time in rice. Int J Mol Sci 21(17):6155
Siegmund J, Wiedermann M, Donges J, Donner R (2016) Impact of temperature and precipitation extremes on the flowering dates of four German wildlife shrub species. Biogeosciences 13:5541–5555
Silva CS, Nayak A, Lai X, Hutin S, Hugouvieux V, Jung JH, López-Vidriero I, Franco-Zorrilla JM, Panigrahi KCS, Nanao MH, Wigge PA, Zubieta C (2020) Molecular mechanisms of evening complex activity in Arabidopsis. Proc Natl Acad Sci 117:6901
Song X, Kristie DN, Reekie EG (2009) Why does elevated CO2 affect time of flowering? An exploratory study using the photoperiodic flowering mutants of Arabidopsis thaliana. New Phytol 181:339–346
Song Y, Gao Z, Luan W (2012) Interaction between temperature and photoperiod in regulation of flowering time in rice. China Life Sci 55:241–249
Springer C, Ward J (2007) Flowering time and elevated CO2. New Phytol 176:243–255
Stocker TF, Qin D, Plattner GK, Alexander LV (2013) Technical Summary (PDF). IPCC AR5 WG1 2013, pp 33–115
Sung S, Amasino RM (2004) Vernalization in Arabidopsis thaliana is mediated by the PHD finger protein VIN3. Nature 427:159–164
Sureshkumar S, Dent C, Seleznev A, Tasset C, Balasubramanian S (2016) Nonsense-mediated mRNA decay modulates FLM-dependent thermosensory flowering response in Arabidopsis. Nat Plants 2:16055
Susila H, Nasim Z, Ahn JH (2018) Ambient temperature-responsive mechanisms coordinate regulation of flowering time. Int J Mol Sci 19:3196
Takeno K (2016) Stress-induced flowering: the third category of flowering response. J Exp Bot 67:4925–4934
Tanaka J, Hayashi T, Iwata H (2016) A practical, rapid generation-advancement system for rice breeding using simplified biotron breeding system. Breed Sci 66:542–551
Teng N, Wang J, Chen T, Wu X, Wang Y, Lin J (2006) Elevated CO2 induces physiological, biochemical and structural changes in leaves of Arabidopsis thaliana. New Phytol 172:92–103
Thompson M, Gamage D, Hirotsu N, Martin A, Seneweera S (2017) Effects of elevated carbon dioxide on photosynthesis and carbon partitioning: a perspective on root sugar sensing and hormonal crosstalk. Front Physiol 8:578
Van Moerkercke A, Duncan O, Zander M, Šimura J, Broda M, Vanden Bossche R, Lewsey MG, Lama S, Singh KB, Ljung K, Ecker JR, Goossens A, Millar AH, Van Aken O (2019) A MYC2/MYC3/MYC4-dependent transcription factor network regulates water spray-responsive gene expression and jasmonate levels. Proc Natl Acad Sci 116:23345
Voesenek LA, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73
Wahl V, Ponnu J, Schlereth A, Arrivault S, Langenecker T, Franke A, Feil R, Lunn JE, Stitt M, Schmid M (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–707
Walker SM, Ward JK (2018) Interactions between rising CO2 and temperature drive accelerated flowering in model plants under changing conditions of the last century. Oecologia 187:911–919
Wang R, Farrona S, Vincent C, Joecker A, Schoof H, Turck F, Alonso-Blanco C, Coupland G, Albani M (2009) PEP1 regulates perennial flowering in Arabis alpina. Nat V459:423–427
Wang H, Li Y, Pan J, Lou D, Hu Y, Yu D (2017) The bHLH Transcription Factors MYC2, MYC3, and MYC4 Are Required for Jasmonate-Mediated Inhibition of Flowering in Arabidopsis. Mol Plant 10(11):1461–1464
White MD, Klecker M, Hopkinson RJ, Weits DA, Mueller C, Naumann C (2017) Plant cysteine oxidases are dioxygenases that directly enable arginyl transferase-catalysed arginylation of N-end rule targets. Nat Commun 8:14690
Whitney H, Dyer A, Chittka L, Rands S, Glover B (2008) The interaction of temperature and sucrose concentration on foraging preferences in bumblebees. Naturwissenschaften 95:845–850
Wiebe HJ (1990) Vernalization of vegetable crops—a review. Acta Hortic 267:323–328
World Meteorological Organization (2019) WMO Statement on the State of the Global Climate in 2018. Geneva WMO-No. 1233.
Wu X, Liu H, Li X, Tian Y, Mahecha MD (2017) Responses of winter wheat yields to warming-mediated vernalization variations across temperate Europe. Front Ecol Evol 5:126
Xu K, Xu X, Fukao T, Canlas P, Maghirang-Rodriguez R, Heuer S, Ismail AM, Bailey-Serres J, Ronald PC, Mackill DJ (2006) SUB1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442(7103):705–708
Yan L, Loukoianov A, Blechl A, Tranquilli G, Ramakrishna W, SanMiguel P, Bennetzen JL, Echenique V, Dubcovsky J (2004) The wheat VRN2 gene is a flowering repressor down-regulated by vernalization. Science 303:1640–1644
Yan L, Fu D, Li C, Blechl A, Tranquilli G, Bonafede M, Sanchez A, Valarik M, Yasuda S, Dubcovsky J (2006) The wheat and barley vernalization gene VRN3 is an orthologue of FT. Proc Natl Acad Sci 103:19581
Yan Y, Shen L, Chen Y, Bao S, Yu TZ, H, (2014) A MYB-domain protein EFM mediates flowering responses to environmental cues in Arabidopsis. Dev Cell 30:437–448
Yoon J, Cho LH, Tun W, Jeon JS, An G (2021) Sucrose signaling in higher plants. Plant Sci 302:110703
Zhang C, Liu J, Zhao T, Gomez A, Li C, Yu C, Li H, Lin J, Yang Y, Liu B, Lin C (2016) A drought-inducible transcription factor delays reproductive timing in rice. Plant Physiol 171:334
Zhang J, Yi Q, Xing F, Tang C, Wang L, Ye W, Ng I, Chan T, Chen H, Liu D (2018) Rapid shifts of peak flowering phenology in 12 species under the effects of extreme climate events in Macao. Sci Rep 8:13950
Zheng Y, Luo L, Liu Y, Yang Yunqiang, Wang C, Xiang K, Yang Yongping (2018) Effect of vernalization on tuberization and flowering in the Tibetan turnip is associated with changes in the expression of FLC homologues. Plant Divers 40
Zheng S, Hu H, Ren H, Yang Z, Qiu Q, Qi W, Liu X, Chen X, Cui X, Li S, Zhou B, Sun D, Cao X, Du J (2019) The Arabidopsis H3K27me3 demethylase JUMONJI 13 is a temperature and photoperiod dependent flowering repressor. Nat Commun 10:1303
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This study was supported in part by grants from the National Research Foundation of Korea (NRF-2020R1A2C2006826 to G.A.; NRF-2020R1A2C2012976 to J.J.).
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J-SJ and GA designed the project; TW, JY, J-SJ and GA wrote the paper.
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Tun, W., Yoon, J., Jeon, JS. et al. Influence of Climate Change on Flowering Time. J. Plant Biol. 64, 193–203 (2021). https://doi.org/10.1007/s12374-021-09300-x
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DOI: https://doi.org/10.1007/s12374-021-09300-x
Keywords
- Climate change
- Global warming
- Flowering time
- Pollinator interaction