Environmental (E) plasticity in partitioning between sugar and starch
Immediate response to stress depends on an organism’s ability to plastically adjust trait values to accommodate changing environments. The degree to which an organism can plastically respond will, in many cases, determine its ability to survive stress. Here, we found extensive plastic variation due to environmental response in the proportion of NSC stores in starch versus sugar (Table 2, Figure 3, solid black lines). In Clatskanie an average of 20% of total NSC stores were found in starch, while only half that amount was found in Corvallis (Figure 3).
Clatskanie has a coastal climate with rainfall spread throughout the year and small temperature differences between winter and summer (Figure 2). In contrast, Corvallis has a continental climate which regularly experiences extreme temperatures and long periods without rainfall (Figure 2). Thus, these results may reflect the differential enzymatic sensitivities of starch degradation and synthesis to average climatic conditions at these two sites (Pollock & Lloyd, 1987; Aude Tixier et al., 2019). The warmer average temperatures in Clatskanie could have led to a higher proportion of NSC being left in starch while the colder, more stressful conditions of Corvallis resulted in more sugar storage.
The observed plasticity in proportion of starch storage could also be driven by the weather patterns on the dates of sampling. We happened to collect woody tissues on the coldest days recorded over the past 38 years in Clatskanie and extremely cold days in Corvallis (Figure 3). Low temperatures in Clatskanie fell below -10oC some days and highs never went above 4oC, within the minimum temperature range that starch synthesis and degradation enzymes can work (Pollock & Lloyd, 1987). The sharp drop in temperatures due to the polar vortex may have halted enzymatic activity entirely. Thus, instead of starch steadily degrading to sugar as temperatures drop, the quick temperature change may have prevented starch from degrading further. Conversely, we travelled to Corvallis after sampling in Clatskanie, where the temperature reached just above 5oC on our sample dates; just above the minimum temperature range for enzymatic activity. Thus, starch may have degraded into sugar in trees at this site. Such a quick change could be possible given that starch synthesis and degradation have been observed on diurnal scales (A. Tixier et al., 2018).
It is difficult to pinpoint whether the plasticity in the proportion of NSC in starch between the two gardens was attributable to the average climate of the two sites, or the weather at the time of sampling. However, there is mounting evidence that this plasticity in the synthesis and degradation of starch in plants is critical for seasonal signaling in plants (Gibon et al., 2009; Palacio, Gunter, Sala, Korner, & Millard, 2014; Aude Tixier et al., 2019). Branch NSC stores begin to synthesize from sugar into starch as temperatures rise in spring (Furze et al., 2019; Martínez-Vilalta et al., 2016), and this process likely occurs faster in branches than in roots because branches are exposed to air and not insulated in the soil. Thus, temperature gradients across the plant may drive the movement of carbohydrates upward in spring to support leaf flush and stem growth (Sperling, Silva, Tixier, Theroux-Rancourt, & Zwieniecki, 2017). This synthesis of starch or movement of carbohydrates could be the signal plants sense in spring to break dormancy or initiate leafout. Thus, it may be this plasticity in the conversion of sugar to starch that is in part driving observed plasticity in phenological timing, a key trait for future tree adaptation to climate change (Alberto et al., 2011; Hall et al., 2007; Keller et al., 2011).
While the pattern of plastic variation between gardens is clear, it is not yet known what the biological meaning of a 10% change in the proportion of stores in starch could be as there are few studies of starch variation in response to environment in trees. The degradation of starch and resultant increase in sugars has been demonstrated to confer freezing and drought resistance to herbaceous plants, particularly Arabidopsis (reviewed in Thalmann & Santelia, 2017). However, these studies are conducted in a laboratory on leaf tissues in herbaceous plants using different NSC quantification measures, which makes the ability to draw meaningful comparisons difficult (Landhausser et al., 2018). Of the few studies performed in trees using similar methods to ours, there is evidence that a 10% change in proportion of starch is substantial. In Populus tremuloides clones, the proportion of total stores in starch in branches can vary between 0 and 13% seasonally (Landhäusser & Lieffers, 2003). Additionally, across four deciduous species measured in the dormant season (January), the proportion of stores in starch can vary between 8 and 28% (Furze et al., 2019). Together, these suggest that a 10% difference between the two gardens may be a biologically relevant shift. Overall, our findings highlight the need for more research on starch conversion in tree species in the lab and in situ .