Seeds of future past: climate change and the thermal memory of plant reproductive traits

Abstract

Plant persistence and migration in face of climate change depends on successful reproduction by seed, a central aspect of plant life that drives population dynamics, community assembly and species distributions. Plant reproduction by seed is a chain of physiological processes, the rates of which are a function of temperature, and can be modelled using thermal time models. Importantly, while seed reproduction responds to its instantaneous thermal environment, there is also evidence of phenotypic plasticity in response to the thermal history experienced by the plant's recent ancestors, by the reproducing plant since seedling establishment, and by its seeds both before and after their release. This phenotypic plasticity enables a thermal memory of plant reproduction, which allows individuals to acclimatise to their surroundings. This review synthesises current knowledge on the thermal memory of plant reproduction by seed, and highlights its importance for modelling approaches based on physiological thermal time. We performed a comprehensive search in the Web of Science and analysed 533 relevant articles, of which 81 provided material for a meta-analysis of thermal memory in reproductive functional traits based on the effect size Zr. The articles encompassed the topics of seed development, seed yield (mass and number), seed dormancy (physiological, morphological and physical), germination, and seedling establishment. The results of the meta-analysis provide evidence for a thermal memory of seed yield, physiological dormancy and germination. Seed mass and physiological dormancy appear to be the central hubs of this memory. We argue for integrating thermal memory into a predictive framework based on physiological time modelling. This will provide a quantitative assessment of plant reproduction, a complex system that integrates past and present thermal inputs to achieve successful reproduction in changing environments. The effects of a warming environment on plant reproduction cannot be reduced to a qualitative interpretation of absolute positives and negatives. Rather, these effects need to be understood in terms of changing rates and thresholds for the physiological process that underlie reproduction by seed.

Plant behaviour: an evolutionary response to the environment?

“…The ability to interpret favourable environmental conditions for germination selects for the ‘smartest’ seeds. Indeed, before germinating, the seed must evaluate several factors, such as range of temperatures in the different seasons, availability of water, volatile organic compounds in the soil, perception of light, age of the seed and soil mineral availability (Tribouillois et al, 2016; Fernandez‐Pascual et al, 2019). When the seeds wait for more favourable conditions before germinating, they activate dormancy processes, specifically secondary dormancy.…”

Differential Interpretation of Mountain Temperatures by Endospermic Seeds of Three Endemic Species Impacts the Timing of In Situ Germination

“…Similar behaviours have also been identified for the only congeneric species, Ribes sardoum Martelli, which is also present in Sardinia [ 50 ]. However, while the results of this study are based on the assumption that the thermal thresholds for seed germination will remain constant trough climate change, further studies should be carried out on these species to understand how climate change might affect the successive steps of seed production, dispersal, dormancy, and germination, as they also have a thermal memory (via phenotypic plasticity) that incorporates information from past thermal history [ 51 ].…”

Adaptation of Forest Trees to Rapidly Changing Climate

“…Observations of the effects of temperature during ripening on the future features of the germination process suggest that plants' phenological thermal memory allows seeds to adapt their germination phenology to climate change. This phenomenon can help predict climate change [25].…”

“…The role of different stages of thermal history, including previous generations and stages of flowering and seed development, still requires careful investigation [21][22][23][24][25]. The results of some studies suggest that there is an interaction between provenance and climate that has a significant impact on successful development and survival and that phylogenetic signals do not play an important role in this adaptation [26].…”

“…The results of some studies suggest that there is an interaction between provenance and climate that has a significant impact on successful development and survival and that phylogenetic signals do not play an important role in this adaptation [26]. Thermal signals shape the successive steps of seed production, dormancy and germination; however, due to phenotypic plasticity, those processes also have thermal memory that contains their thermal experience from the past [25,27]. Microclimate may be the factor that most affects seed germination and early seedling establishment [13,[28][29][30][31].…”