Past studies have shown that flowering times have accelerated over the last century. These responses are often attributed to rising temperature, although short-term field experiments with warming treatments have under-estimated accelerations in flowering time that have been observed in long-term field surveys. Thus, there appears to be a missing factor(s) for explaining accelerated flowering over the last century. Rising atmospheric CO2 concentration ([CO2]) is a possible candidate, and its contributions to affecting flowering time over historic periods are not well understood. This is likely because rising [CO2] is confounded with temperature in the field and preindustrial [CO2] studies are relatively rare. To address this, we tested the individual and interactive effects of rising [CO2] and temperature between preindustrial and modern periods on flowering time in the model system, Arabidopsis thaliana. We used a variety of genotypes originating from diverse locations, allowing us to test intraspecific responses to last-century climate change. We found that accelerated flowering time between the full-preindustrial and full-modern treatments was mainly driven by an interaction between rising [CO2] and temperature, rather than through the individual effects of either factor in isolation. Furthermore, accelerated flowering time was driven by enhanced plant growth rates and not through changes in plant size at flowering. Thus, the interaction between rising [CO2] and temperature may be key for explaining large accelerations in flowering times that have been observed over the last century and that could not be explained by rising temperature alone.
This is a preview of subscription content,to check access.
Access this article
Similar content being viewed by others
Ainsworth EE, Rogers A (2007) The response of photosynthesis and stomatal conductance to rising [CO2]: mechanisms and environmental interactions. Plant Cell Environ 30:258–270. https://doi.org/10.1111/j.1365-3040.2007.01641.x
Allen JM et al (2014) Modeling daily flowering probabilities: expected impact of climate change on Japanese cherry phenology. Glob Chang Biol 20:1251–1263
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 B Biol Sci 279:3843–3852. https://doi.org/10.1098/rspb.2012.1051
Balasubramanian S, Sureshkumar S, Lempe J, Weigel D (2006) Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet 2:980–989. https://doi.org/10.1371/journal.pgen.0020106
Bartomeus I et al (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc Natl Acad Sci USA 108:20645–20649. https://doi.org/10.1073/pnas.1115559108
Bunce JA (2008) Acclimation of photosynthesis to temperature in Arabidopsis thaliana and Brassica oleracea. Photosynthetica 46:517–524
Burghardt LT et al (2015) Fluctuating, warm temperatures decrease the effect of a key floral repressor on flowering time in Arabidopsis thaliana. New Phytol 210:564–576
Carter EB, Theodorou MD, Morris P (1997) Responses to Lotus corniculatus to environmental change. 1. Effects of elevated CO2, temperature and drought on growth and plant development. New Phytol 136:245–253
Cleland EE, Chiariello NR, Loarie SR, Mooney HA, Field CB (2006) Diverse responses of phenology to global changes in a grassland ecosystem. Proc Natl Acad Sci USA 103:13740–13744. https://doi.org/10.1073/pnas.0600815103
Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365. https://doi.org/10.1016/j.tree.2007.04.003
Craufurd PQ, Wheeler TR (2009) Climate change and the flowering time of annual crops. J Exp Bot 60:2529–2539
Dunnell KL, Travers SE (2011) Shifts in the flowering phenology of the Northern Great Plains: patterns over 100 years. Am J Bot 98:935–945. https://doi.org/10.3732/ajb.1000363
Easlon HM, Carlisle E, Mckay JK, Bloom AJ (2015) Does low stomatal conductance or photosynthetic capacity enhance growth at elevated CO2 in Arabidopsis? Plant Physiol. https://doi.org/10.1104/pp.114.245241
Ellwood ER, Temple SA, Primack RB, Bradley NL, Davis CC (2013) Record-breaking early flowering in the eastern United States. PLoS ONE 8:e53788
Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22:432–439
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345
Felton AJ, Smith MD (2017) Integrating plant and ecological responses to climate extremes from individual to ecosystem levels. Philos Trans R Soc B 372:20160142
Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296:1689–1691. https://doi.org/10.1126/science.1071617
Footitt S, Huang Z, Ölcer-Footitt H, Clay H, Finch-Savage WE (2018) The impact of global warming on germination and seedling emergence in Alliaria petiolata a woodland species with dormancy loss dependent on low temperature. Plant Biol. https://doi.org/10.1111/plb.12720
Franks SJ (2015) The unique and multifaceted importance of the timing of flowering. Am J Bot 102:1401–1402
Gerhart LM, Ward JK (2010) Plant responses to low [CO2] of the past. New Phytol 188:674–695
Harris RN, Chapman DS (2001) Mid-latitude (30°–60°N) climatic warming inferred by combining borehole temperatures with surface air temperatures. Geophys Res Lett 28:747–750. https://doi.org/10.1029/2000gl012348
Huang Z, Footitt S, Tang A, Finch-Savage WE (2017) Predicted global warming scenarios impact on the mother plant to alter seed dormancy and germination behaviour in Arabidopsis. Plant Cell Environ 41:2018
IPCC (2007) Summary for policymakers. In: Solomon S, Qin D, Manning M, Chen Z, Marquis M, Averyt KB, Tignor M, Miller HL (eds) 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, Cambridge
IPCC (2013) Summary for policy makers. In: Stocker TF, Qin D, Plattner G-K, Tignor M, Allen SK, Boschung J, Nauels A, Xia Y, Bex V, Midgley PM (eds) Climate change 2013: the physical science basis. Contribution of Working Group 1 to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge
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
Kim SY, He Y, Jacob Y, Noh Y-S, Michaels S, Amasino R (2005) Establishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferase. Am Soc Plant Biol. https://doi.org/10.1105/tpc.105.034645
Kimball BA (2016) Crop responses to elevated CO2 and interactions with H2, N, and temperature. Curr Opin Plant Biol 31:36–43
Koornneef M, Alonso-Blanco C, Vreugdenhil D (2004) Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55:141–172
Lutz U et al (2015) Modulation of ambient temperature-dependent flowering in Arabidopsis thaliana by natural variation of FLOWERING LOCUS M. PLoS Genet 11:e1005588
May P et al (2013) The effects of carbon dioxide and temperature on microRNA expression in Arabidopsis development. Nat Commun 4:2145
Menzel A (2002) Phenology: its importance to the global change community. Clim Chang 54:379–385
Menzel A et al (2006) European phenological response to climate change matches the warming pattern. Glob Chang Biol 12:1969–1976. https://doi.org/10.1111/j.1365-2486.2006.01193.x
Norby RJ, Luo Y (2004) Evaluating ecosystem responses to rising atmospheric CO2 and global warming in a multi-factor world. New Phytol 162:281–293
Primack RB, Miller-Rushing AJ (2011) Broadening the study of phenology and climate change. New Phytol 191:307–309. https://doi.org/10.1111/j.1469-8137.2011.03773.x
Rafferty NE, Ives AR (2012) Pollinator effectiveness varies with experimental shifts in flowering time. Ecology 93:803–814
Rawson HM (1992) Plant responses to temperature under conditions of elevated CO2. Aust J Bot 40:473–490
Richardson BA, Chaney L, Shaw NL, Still SM (2016) Will phenotypic plasticity affecting flowering phenology keep pace with climate change? Glob Chang Biol 23:2499–2508
Rogers CA et al (2006) Interaction of the onset of spring and elevated atmospheric CO2 on ragweed (Ambrosia artemisiifolia L.) pollen production. Environ Health Perspect 116:865–869
Schmalenbach I, Zhang L, Reymond M, Jiménez-Gómez JM (2014) The relationship between flowering time and growth responses to drought in Arabidopsis Landsberg erecta × Antwerp-1 population. Front Plant Sci 5:609
Simpson GG, Dean C (2002) Arabidopsis, the Rosetta stone of flowering time? Science 296:285–289
Springer CJ, Ward JK (2007) Flowering time and elevated atmospheric CO2. New Phytol 176:243–255. https://doi.org/10.1111/j.1469-8137.2007.02196.x
Springer CJ, Orozco RA, Kelly JK, Ward JK (2008) Elevated CO2 influences the expression of floral-initiation genes in Arabidopsis thaliana. New Phytol 178:63–67. https://doi.org/10.1111/j.1469-8137.2008.02387.x
Wadgymar SM, Ogilvie JE, Inouye DW, Weis AE, Anderson JT (2018) Phenological responses to multiple environmental drivers under climate change: insights from a long-term observational study and a manipulative field experiment. New Phytol 218:517–529
Wahl V et al (2013) Regulation of flowering by trehalose-6-phosphate signaling in Arabidopsis thaliana. Science 339:704–707
Wang H, Xiao W, Nui Y, Chai R, Jin C, Zhang Y (2015) Elevated carbon dioxide induces stomatal closure of Arabidopsis thaliana (L.) Heynh. through an increased production of nitric oxide. J Plant Growth Regul 34:372–380
Wang B, Liu DL, Asseng S, Macadam I, Yu Q (2016) Impact of climate change on wheat flowering time in eastern Australia. Agric For Meterol 209–210:11–21
Ward JK, Tissue DT, Thomas RB, Strain BR (1999) Comparative responses of model C3 and C4 plants to drought in low and elevated CO2. Glob Chang Biol 5:857–867
Wolkovich EM et al (2012) Warming experiments underpredict plant phenological responses to climate change. Nature 485:494–497. https://doi.org/10.1038/nature11014
We thank Courtney Bone, Ellen Duffy, Taylor Leibbrandt, Rebecca Orozco, Cedric Clark, and Diondré Jones-Sanders for their technical assistance in completing this project. This work was supported by National Science Foundation GK-12 and IGERT fellowships to SMW as well as National Science Foundation CAREER and NSF IOS awards to JKW. All raw data are available from the corresponding author upon request. JKW would like to thank Distinguished Professor James Ehleringer for his many contributions to science, the amazing training and mentoring that he provided her, and for his wonderful friendship and support over the years. She would also like to thank Edna Ehleringer for her encouragement, support, and friendship during her post-doctoral years and beyond.
Funding was provided by the U.S. National Science Foundation (IOS) and the University of Kansas.
Conflict of interest
The authors declare they have no conflicts of interest.
Communicated by Russell K. Monson.
Using model plants, S. Michael Walker (Ph.D. student) demonstrated that the interaction between rising CO2 and temperature better explains accelerated flowering time over changing conditions of the last century compared with the individual effects of either factor.
Electronic supplementary material
Below is the link to the electronic supplementary material.
About this article
Cite this article
Walker, S.M., Ward, J.K. Interactions between rising CO2 and temperature drive accelerated flowering in model plants under changing conditions of the last century. Oecologia 187, 911–919 (2018). https://doi.org/10.1007/s00442-018-4197-0