Temporal heterogeneity of cold acclimation phenotypes in Arabidopsis leaves

To predict the effects of temperature changes on plant growth and performance, it is crucial to understand the impact of thermal history on leaf morphology, anatomy and physiology. Here, we document a comprehensive range of leaf phenotypes in 25/20 degrees C-grown Arabidopsis thaliana plants that were shifted to 5 degrees C for up to 2 months. When warm-grown, pre-existing (PE) leaves were exposed to cold, leaf thickness increased due to an increase in mesophyll cell size. Leaves that were entirely cold-developed (CD) were twice as thick (eight cell layers) as their warm-developed (WD) counterparts (six layers), and also had higher epidermal and stomatal cell densities. After 4 d of cold, PE leaves accumulated high levels of total non-structural carbohydrates (TNC). However, glucose and starch levels declined thereafter, and after 45 d in the cold, PE leaves exhibited similar TNC to CD leaves. A similar phenomenon was observed in delta(13)C and a range of photosynthetic parameters. In cold-treated PE leaves, an increase in respiration (R(dark)) with cold exposure time was evident when measured at 25 degrees C but not 5 degrees C. Cold acclimation was associated with a large increase in the ratio of leaf R(dark) to photosynthesis. The data highlight the importance of understanding developmental thermal history in determining individual phenotypic traits.