Flowering season of vernal herbs is shortened at elevated temperatures with reduced precipitation in early spring

Walther, G. et al. Ecological responses to recent climate change. Nature 416, 389–395. https://doi.org/10.1038/416389a (2002).

ADS  CAS  Article  PubMed  Google Scholar 

Pereira, H. M. et al. Scenarios for global biodiversity in the 21st century. Science 330, 1496–1501. https://doi.org/10.1126/science.1196624 (2010).

ADS  CAS  Article  PubMed  Google Scholar 

Carter, S. K., Saenz, D. & Rudolf, V. H. W. Shifts in phenological distributions reshape interaction potential in natural communities. Ecol. Lett. 21, 1143–1151. https://doi.org/10.1111/ele.13081 (2018).

Article  PubMed  Google Scholar 

Kahl, S. M., Lenhard, M. & Joshi, J. Compensatory mechanisms to climate change in the widely distributed species Silene vulgaris. J. Ecol. 107, 1918–1930. https://doi.org/10.1111/1365-2745.13133 (2019).

Article  Google Scholar 

Easterling, D. R. et al. Climate extremes: observations, modeling, and impacts. Science 289, 2068–2074. https://doi.org/10.1126/science.289.5487.2068 (2000).

ADS  CAS  Article  PubMed  Google Scholar 

IPCC. Global Warming of 1.5°C: An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty https://www.ipcc.ch/sr15/ (2018).

Wolkovich, et al. Warming experiments underpredict plant phenological responses to climate change. Nature 485, 494–497. https://doi.org/10.1038/nature11014 (2012).

ADS  CAS  Article  PubMed  Google Scholar 

Ahammed, G. J., Li, X., Wan, H., Zhou, G. & Cheng, Y. SlWRKY81 reduces drought tolerance by attenuating proline biosynthesis in tomato. Sci. Hortic. 270, 109444. https://doi.org/10.1016/j.scienta.2020.109444 (2020).

CAS  Article  Google Scholar 

Dorji, T. et al. Impacts of climate change on flowering phenology and production in alpine plants: the importance of end of flowering. Agric. Ecosyst. Environ. 291, 106795. https://doi.org/10.1016/j.agee.2019.106795 (2020).

Article  Google Scholar 

Bertin, R. I. Plant phenology and distribution in relation to recent climate change. J. Torrey Bot. Soc. 135, 126–146. https://doi.org/10.3159/07-RP-035R.1 (2008).

Article  Google Scholar 

Lawson, C. R., Vindenes, Y., Bailey, L. & van de Poll, M. Environmental variation and population responses to global change. Ecol. Lett. 18, 724–736. https://doi.org/10.1111/ele.12437 (2015).

Article  PubMed  Google Scholar 

Sherry, R. A. et al. Divergence of reproductive phenology under climate warming. Proc. Nat. Acad. Sci. USA 104, 198–202. https://doi.org/10.1073/pnas.0605642104 (2007).

ADS  CAS  Article  PubMed  Google Scholar 

Nicotra, A. B. et al. Plant phenotypic plasticity in a changing climate. Trends Plant Sci. 15, 684–692. https://doi.org/10.1016/j.tplants.2010.09.008 (2010).

CAS  Article  PubMed  Google Scholar 

Prevéy, J. S. et al. Warming shortens flowering seasons of tundra plant communities. Nat. Ecol. Evol. 3, 45–52. https://doi.org/10.1038/s41559-018-0745-6 (2019).

Article  PubMed  Google Scholar 

Ahammed, G. J., Li, X., Liu, A. & Chen, S. Physiological and defense responses of tea plants to elevated CO₂: a review. Front. Plant Sci. 11, 305. https://doi.org/10.3389/fpls.2020.00305 (2020).

Article  PubMed  PubMed Central  Google Scholar 

Fogelström, E. & Ehrlén, J. Phenotypic but not genotypic selection for earlier flowering in a perennial herb. J. Ecol. 107, 2650–2659. https://doi.org/10.1111/1365-2745.13240 (2019).

Article  Google Scholar 

Badeck, F. et al. Responses of spring phenology to climate change. New Phytol. 162, 295–309. https://doi.org/10.1111/j.1469-8137.2004.01059.x (2004).

Article  Google Scholar 

Ehrlén, J., Raabova, J. & Dahlgren, J. P. Flowering schedule in a perennial plant: life-history trade-offs, seed predation, and total offspring fitness. Ecology 96, 2280–2288. https://doi.org/10.1890/14-1860.1 (2015).

Article  PubMed  Google Scholar 

Körner, C. & Basler, D. Phenology under global warming. Science 327, 1461–1462. https://doi.org/10.1126/science.1186473 (2010).

ADS  Article  PubMed  Google Scholar 

Gerst, K. L., Rossington, N. L. & Mazer, S. J. Phenological responsiveness to climate differs among four species of Quercus in North America. J. Ecol. 105, 1610–1622. https://doi.org/10.1111/1365-2745.12774 (2017).

Article  Google Scholar 

Grossiord, C. et al. Precipitation, not air temperature, drives functional responses of trees in semi-arid ecosystems. J. Ecol. 105, 163–175. https://doi.org/10.1111/1365-2745.12662 (2017).

Article  Google Scholar 

Crimmins, T. M., Crimmins, M. A. & Bertelsen, C. D. Onset of summer flowering in a ‘Sky Island’ is driven by monsoon moisture. New Phytol. 191, 468–479. https://doi.org/10.1111/j.1469-8137.2011.03705.x (2011).

Article  PubMed  Google Scholar 

Meng, F. D. et al. Changes in flowering functional group affect responses of community phenological sequences to temperature change. Ecology 98, 734–740. https://doi.org/10.1002/ecy.1685 (2017).

CAS  Article  PubMed  Google Scholar 

Dunne, J. A., Harte, J. & Taylor, K. J. Subalpine meadow flowering phenology responses to climate change: integrating experimental and gradient methods. Ecol. Monogr. 73, 69–86. https://doi.org/10.1890/0012-9615(2003)073[0069:SMFPRT]2.0.CO;2 (2003).

Article  Google Scholar 

Gugger, S., Kesselring, H., Stöcklin, J. & Hamann, E. Lower plasticity exhibited by high- versus mid- elevation species in their phenological responses to manipulated temperature and drought. Annu. Bot. 116, 953–962. https://doi.org/10.1093/aob/mcv155 (2015).

Article  Google Scholar 

Richardson, A. D. et al. Ecosystem warming extends vegetation activity but heightens vulnerability to cold temperatures. Nature 560, 368–371. https://doi.org/10.1038/s41586-018-0399-1 (2018).

ADS  CAS  Article  PubMed  Google Scholar 

Fenner, M. The phenology of growth and reproduction in plants. Perspect. Plant Ecol. 1, 78–91. https://doi.org/10.1078/1433-8319-00053 (1998).

Article  Google Scholar 

Lee, H. & Kang, H. Temperature-driven changes of pollinator assemblage and activity of Megaleranthis saniculifolia (Ranunculaceae) at high altitudes on Mt. Sobaeksan, South Korea. J. Ecol. Environ. 42, 31. https://doi.org/10.1186/s41610-018-0092-1 (2018).

Article  Google Scholar 

Yu, H., Luedeling, E. & Xu, J. Winter and spring warming result in delayed spring phenology on the Tibetan Plateau. Proc. Nat. Acad. Sci. USA 107, 22151–22156. https://doi.org/10.1073/pnas.1012490107 (2010).

ADS  Article  PubMed  Google Scholar 

Cook, B. I., Wolkovich, E. M. & Parmesan, C. Divergent responses to spring and winter warming drive community level flowering trends. Proc. Nat. Acad. Sci. USA 109, 9000–9005. https://doi.org/10.1073/pnas.1118364109 (2012).

ADS  Article  PubMed  Google Scholar 

Meier, A. J., Bratton, S. P. & Duffy, D. C. Possible ecological mechanisms for loss of vernal-herb diversity in logged eastern deciduous forests. Ecol. Appl. 5, 935–946. https://doi.org/10.2307/2269344 (1995).

Article  Google Scholar 

Sung, J. et al. Growth environment and vegetation structure of native habitat of Corydalis cornupetala. Korean J. Environ. Ecol. 27, 271–279 (2013).

Google Scholar 

Augspurger, C. K. & Salk, C. F. Constraints of cold and shade on the phenology of spring ephemeral herb species. J. Ecol. 105, 246–254. https://doi.org/10.1111/1365-2745.12651 (2017).

CAS  Article  Google Scholar 

Rizhsky, L. et al. When defense pathways collide: the response of Arabidopsis to a combination of drought and heat stress. Plant Physiol. 134, 1683–1696. https://doi.org/10.1104/pp.103.033431 (2004).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Su, Z. et al. Flower development under drought stress: morphological and transcriptomic analyses reveal acute response of long-term acclimation in Arabidopsis. Plant Cell 25, 3785–3807. https://doi.org/10.1105/tpc.113.115428 (2013).

CAS  Article  PubMed  PubMed Central  Google Scholar 

Vallales, F., Wright, S. J., Lasso, E., Kitajima, K. & Pearcy, R. W. Plastic phenotypic response to light of 16 congeneric shrubs from a Panamanian rainforest. Ecology 81, 1925–1936. https://doi.org/10.1890/0012-9658(2000)081[1925:PPRTLO]2.0.CO;2 (2000).

Article  Google Scholar 

Valladares, F., Sanchez-Gomez, D. & Zavala, M. A. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. J. Ecol. 94, 1103–1116. https://doi.org/10.1111/j.1365-2745.2006.01176.x (2006).

Article  Google Scholar 

CaraDonna, P. J., Iler, A. M. & Inouye, D. W. Shifts in flowering phenology reshape a subalpine plant community. Proc. Nat. Acad. Sci. USA 111, 13. https://doi.org/10.1073/pnas.1323073111 (2014).

CAS  Article  Google Scholar 

Forrest, J. & Miller-Rushing, A. J. Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos. Trans. Biol. Sci. 365, 3101–3112. https://doi.org/10.1098/rstb.2010.0145 (2010).

Article  Google Scholar 

Richardson, A. D. et al. Climate change, phenology, and phenological control of vegetation feedbacks to the climate system. Agric. For. Meteorol. 169, 156–173. https://doi.org/10.1016/j.agrformet.2012.09.012 (2013).

ADS  Article  Google Scholar 

Richards, F. J. A flexible growth function for empirical use. J. Exp. Bot. 29, 290–300. https://doi.org/10.1093/jxb/10.2.290 (1959).

Article  Google Scholar 

Barnabás, B., Jäger, K. & Fehér, A. The effect of drought and heat stress on reproductive processes in cereals. Plant Cell Environ. 31, 11–38. https://doi.org/10.1111/j.1365-3040.2007.01727.x (2008).

CAS  Article  PubMed  Google Scholar 

Limousin, J.-M. et al. Morphological and phenological shoot plasticity in a Mediterranean evergreen oak facing long-term increased drought. Oecologia 169, 565–577. https://doi.org/10.1007/s00442-011-2221-8 (2012).

ADS  Article  PubMed  Google Scholar 

Li, X. et al. Exogeneous melatonin improves tea quality under moderate high temperatures by increasing epigallacatechin-3-gallate and theanine biosynthesis in Camellia sinensis L. J. Plant Physiol. 253, 153273. https://doi.org/10.1016/j.jplph.2020.153273 (2020).

CAS  Article  PubMed  Google Scholar 

Wheeler, J. A. et al. The snow and the willows: earlier spring snowmelt reduces performance in the low-lying alpine shrub Salix herbacea. J. Ecol. 104, 1041–1050. https://doi.org/10.1111/1365-2745.12579 (2016).

CAS  Article  Google Scholar 

Llorens, L. & Peñuelas, J. Experimental evidence of future drier and warmer conditions affecting flowering of two co-occurring Mediterranean shrubs. Int. J. Plant Sci. 166, 235–245. https://doi.org/10.1086/427480 (2005).

Article  Google Scholar 

Bernal, M., Estiarte, M. & Penuelas, J. Drought advances spring growth phenology of the Mediterranean shrub Erica multiflora. Plant Biol. 13, 252–257. https://doi.org/10.1111/j.1438-8677.2010.00358.x (2011).

CAS  Article  PubMed  Google Scholar 

Shavrukov, Y. et al. Early flowering as a drought escape mechanism in plants: how can it aid wheat production?. Front. Plant Sci. 8, 1950. https://doi.org/10.3389/fpls.2017.01950 (2017).

Article  PubMed  PubMed Central  Google Scholar 

Sherry, R. A. et al. Changes in duration of reproductive phases and lagged phenological response to experimental climate warming. Plant Ecol. Divers. 4, 23–35. https://doi.org/10.1080/17550874.2011.557669 (2011).

Article  Google Scholar 

Prasad, P. V. V., Pisipati, S. R., Momčilović, I. & Ristic, Z. Independent and combined effects of high temperature and drought stress during grain filling on plant yield and chloroplast EF-Tu expression in spring wheat. J. Agric. Crop Sci. 197(430–441), 2011. https://doi.org/10.1111/j.1439-037X.2011.00477.x (2011).

CAS  Article  Google Scholar 

Zong, J.-M. et al. The AaDREB1 transcription factor from the cold-tolerant plant Adonis amurensis enhances abiotic stress tolerance in transgenic plant. Int. J. Mol. Sci. 17, 611. https://doi.org/10.3390/ijms17040611 (2016).

ADS  CAS  Article  PubMed Central  Google Scholar 

Żuraw, B., Rysiak, K. & Szymczak, G. Ecology and morphology of the flowers of Hepatica nobilisSchreb. (Ranunculaceae). Mod. Phytomorphol. 4, 39–43. https://doi.org/10.5281/zenodo.161177 (2013).

Article  Google Scholar 

Kalliovirta, M., Ryttäri, T. & Heikkinen, R. K. Population structure of a threatened plant, Pulsatilla patens, in boreal forests: modeling relationships to overgrowth and site closure. Biodivers. Conserv. 15, 3095–3108. https://doi.org/10.1007/s10531-005-5403-z (2006).

Article  Google Scholar 

Inghe, O. & Tamm, C. O. Survival and flowering of perennial herbs. IV. The behavior of Hepatica nobilis and Sanicula europaea on permanent plots during 1943–1981. Oikos 45, 400–420. https://doi.org/10.2307/3565576 (1985).

Article  Google Scholar 

Lee, T. B. Colored Flora of Korea (Hyangmunsa, Seoul, 2003).

Google Scholar 

Kang, H. & Jang, S. Flowering patterns among angiosperm species in Korea: diversity and constraints. J. Plant Biol. 47, 348–355. https://doi.org/10.1007/BF03030550 (2004).

Article  Google Scholar 

Culley, T. M. Reproductive biology and delayed selfing in Viola pubscens (Violaceae), an understory herb with chasmogamous and cleistogamous flowers. Int. J. Plant Sci. 163, 113–122. https://doi.org/10.1086/324180 (2002).

Article  Google Scholar 

R Core Team. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, https://www.R-project.org (2017).