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

Biol Rev Camb Philos Soc. 2019 Apr;94(2):439-456. doi: 10.1111/brv.12461. Epub 2018 Sep 6.

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.

Keywords: climate warming; dormancy; functional traits; germination; global change; phenotypic plasticity; seed mass and number; seedling establishment; thermal time.

Publication types

  • Meta-Analysis
  • Research Support, Non-U.S. Gov't
  • Review

MeSH terms

  • Adaptation, Physiological / physiology
  • Climate Change*
  • Germination
  • Multivariate Analysis
  • Phylogeny
  • Plant Dormancy / physiology
  • Plant Physiological Phenomena*
  • Publication Bias
  • Reproduction
  • Seedlings / growth & development
  • Seeds / physiology*
  • Temperature
  • Time Factors