Inflorescences of alpine cushion plants freeze autonomously and may survive subzero temperatures by supercooling

Abstract

Freezing patterns in the high alpine cushion plants Saxifraga bryoides, Saxifraga caesia, Saxifraga moschata and Silene acaulis were studied by infrared thermography at three reproductive stages (bud, anthesis, fruit development). The single reproductive shoots of a cushion froze independently in all four species at every reproductive stage. Ice formation caused lethal damage to the respective inflorescence. After ice nucleation, which occurred mainly in the stalk or the base of the reproductive shoot, ice propagated throughout that entire shoot, but not into neighboring shoots. However, anatomical ice barriers within cushions were not detected. The naturally occurring temperature gradient within the cushion appeared to interrupt ice propagation thermally. Consequently, every reproductive shoot needed an autonomous ice nucleation event to initiate freezing. Ice nucleation was not only influenced by minimum temperatures but also by the duration of exposure. At moderate subzero exposure temperatures (−4.3 to −7.7 °C) the number of frozen inflorescences increased exponentially. Due to efficient supercooling, single reproductive shoots remained unfrozen down to −17.4 °C (cooling rate 6 K h−1). Hence, the observed freezing pattern may be advantageous for frost survival of individual inflorescences and reproductive success of high alpine cushion plants, when during episodic summer frosts damage can be avoided by supercooling.

Distribution models for mountain plant species: The value of elevation

“…Indeed, cold temperatures (especially during the growing season) rather than warm temperatures are known to constrain metabolic and developmental processes as well as aboveground productivity through frost damage and nutrient and moisture immobilization (Bliss, 1962;Billings and Mooney, 1968;Rixen et al, 2012). Thus, the factors influencing these processes are likely mediating the reproductive success and distribution of mountain species (Körner, 1999;Taschler and Neuner, 2004;Hacker et al, 2011).…”

How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment

“…Depending on the plant species and on the developmental stage, there is a more or less broad temperature range between first and severe frost damage. For the cushion plants Saxifraga bryoides , S. caesia , S. moschata and Silene acaulis , Hacker et al (2011) could show that ice nucleation occurs independently in each single reproductive shoot—mainly in the stalks, and less frequently in the flower buds and flowers—and ice does not propagate into neighbouring shoots. Anatomical ice barriers have not yet been detected, which suggests that the dense cushion structure provides a thermal block for ice propagation (Hacker and Neuner 2008).…”

“…Sakai and Otsuka 1970; Larcher and Wagner 1976; Squeo et al 1991, 1996; Körner 2003; Taschler and Neuner 2004; Bannister et al 2005; Bannister 2007; Larcher et al 2010). At subzero temperatures, plants may either avoid freezing by supercooling or tolerate extracellular freezing and subsequent freeze-dehydration to a certain extent (Goldstein et al 1985; Rada et al 1987; Squeo et al 1991; Hacker and Neuner 2008; Hacker et al 2011; Neuner and Hacker 2012). As frost resistance is an adaptive trait, its extent differs according to the predictable environmental temperature regime (Sakai and Larcher 1987; Larcher 2005).…”

Advances in physiological and molecular aspects of plant cold tolerance

“…Research about the mechanism of ice initiation in plants has greatly decreased recently because of its essential role in specific aspects of cold hardiness (Gusta et al 2009;Aryal & Neuner 2010;Hacker et al 2011;Walters Jr et al 2011). Ice formation may take place either in the intracellular or extracellular spaces depending on the cooling conditions (Guy 1990).…”