Repeated colonization of alpine habitats by Arabidopsis arenosa viewed through freezing resistance and ice management strategies

Success or failure of plants to cope with freezing temperatures can critically influence plant distribution and adaptation to new habitats. Especially in alpine environments, frost is a likely major selective force driving adaptation. In Arabidopsis arenosa (L.) Lawalrée, alpine populations have evolved independently in different mountain ranges, enabling studying mechanisms of acclimation and adaptation to alpine environments. We tested for heritable, parallel differentiation in freezing resistance, cold acclimation potential and ice management strategies using eight alpine and eight foothill populations. Plants from three European mountain ranges (Niedere Tauern, Făgăraș and Tatra Mountains) were grown from seeds of tetraploid populations in four common gardens, together with diploid populations from the Tatra Mountains. Freezing resistance was assessed using controlled freezing treatments and measuring effective quantum yield of photosystem II, and ice management strategies by infrared video thermography and cryomicroscopy. The alpine ecotype had a higher cold acclimation potential than the foothill ecotype, whereby this differentiation was more pronounced in tetraploid than diploid populations. However, no ecotypic differentiation was found in one region (Făgăraș), where the ancient lineage had a different evolutionary history. Upon freezing, an ice lens within a lacuna between the palisade and spongy parenchyma tissues was formed by separation of leaf tissues, a mechanism not previously reported for herbaceous species. The dynamic adjustment of freezing resistance to temperature conditions may be particularly important in alpine environments characterized by large temperature fluctuations. Furthermore, the formation of an extracellular ice lens may be a useful strategy to avoid tissue damage during freezing.