Survival below zero: overlooked aspects of freezing-tolerance in photosynthetic fern tissues

The consequences of climate change on the ecophysiology of cryptogams, generally, and in ferns, particularly, are understudied. Phenomena induced by climate change, such as increased frequency of extreme weather events, shifts in precipitation patterns and temperature fluctuations, can significantly impact the physiology and distribution of ferns. The clade of ferns evolved about 400 million years ago and represents the sister group of seed plants. Given their long evolutionary history, ferns offer insights into the resilience and adaptability of plant lineages over geological time scales. Both from an evolutionary and functional perspective, ferns represent a crucial group with intermediate physiological properties between earlier-evolving bryophytes and spermatophytes. Additionally, their life cycle with single-celled reproductive spores and with two independent generations, gametophyte and sporophyte, which have strong anatomical and physiological differences and even different ecological requirements, make ferns a unique case study. While most ferns avoid freezing by living in the tropics or shedding their fronds, wintergreen species deal with sub-zero temperatures in temperate and cold ecosystems. Additionally, the chlorophyll-containing spores and/or gametophytes of many species also face subzero temperature. Despite all this, our current knowledge of low temperature- and freezing-tolerance mechanisms in ferns is minimal. In this review we make a comprehensive compilation and re-evaluation of the available knowledge in this topic with a focus on photosynthetic cells/organs of ferns (class Polypodiopsida). We include some recent and relevant findings, identify major gaps and provide baseline for future lines of research.