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The scarcity of C4 plants in cool climates is usually attributed to their lower photosynthetic efficiency than C3 species at low temperatures. However, a lower freezing resistance may also decrease the competitive advantage of C4 plants by reducing canopy duration, especially in continental steppe grasslands, where a short, hot growing season is bracketed by frost events. This paper reports an experimental test of the hypothesis that cold acclimation is negligible in C4 grasses, leading to greater frost damage than in C3 species. The experiments exposed six C3 and three C4 Mongolian steppe grasses to 20 d chilling or control pre-treatments, followed by a high-light freezing event. Leaf resistance to freezing injury was independent of photosynthetic type. Three C3 species showed constitutive freezing resistance characterized by <20% leaf mortality, associated with high photosynthetic carbon fixation and electron transport rates and low leaf osmotic potential. One freezing-sensitive C4 species showed the expected pattern of chilling-induced damage to photosynthesis and >95% leaf mortality after the freezing event. However, three C3 and two C4 species displayed a cold acclimation response, showing significant decreases in osmotic potential and photosynthesis after exposure to chilling, and a 30–72% reduction of leaf freezing injury. This result suggested that down-regulation of osmotic potential may be involved in the cold acclimation process, and demonstrated that there is no inherent barrier to the development of cold acclimation in C4 species from this ecosystem. Cold acclimation via osmoregulation represents a previously undescribed mechanism to explain the persistence of C4 plants in cool climates. [ABSTRACT FROM PUBLISHER]

Globally, C4 plants dominate hot, open environments, but this general pattern is underpinned by important differences in the biogeography of C4 lineages. In particular, the species richness of C4 Poaceae (grasses) increases strongly with increasing temperature, whereas that of the major C4 eudicot group Chenopodiaceae correlates positively with aridity. Freezing tolerance is a crucial determinant of biogeographical relationships with temperature and is mediated by photodamage and cellular disruption by desiccation, but little is known about differences between C4 families. This study hypothesized that there is a greater risk of freezing damage via these mechanisms in C4 Poaceae than Chenopodiaceae, that freezing protection differs between the taxonomic groups, and that freezing tolerance of species is linked to arid habitat preference. Chlorophyll fluorescence, water relations, and freezing injury were compared in four C3 and six C4 species of Poaceae and Chenopodiaceae from the same Mongolian flora. Contrary to expectations, freezing-induced leaf mortality and photodamage were lower in Poaceae than Chenopodiaceae species, and unrelated to photosynthetic pathway. The freezing resistance of Poaceae species resulted from constitutive protection and cold acclimation and an ability to protect the photosynthetic apparatus from photodamage. Freezing protection was associated with low osmotic potential and low tissue elasticity, and freezing damage was accompanied by electrolyte leakage, consistent with cell-membrane disruption by ice. Both Chenopodiaceae and Poaceae had the potential to develop cold acclimation and withstand freezing during the growing season, which conflicted with the hypothesis. Instead, freezing tolerance was more closely associated with life history and ecological preference in these Mongolian species.