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• W2103809602 abstract "Plants are poikilothermic organisms. They closely follow the temperature of their immediate surroundings, and as a result, their internal body temperature varies considerably. Both seasonal and diurnal temperature variation has shaped plant traits throughout their 430 million year evolutionary history on land. Thus, it is no surprise that plants evolved specific traits that use temperature variation to boost physiological performance (Nicotra et al., 2010), just as wood physicochemical properties sustain water transport under tension. Yet our homoeothermic point of view often biases notions of how plants could benefit from energy gradients due to temperature variation. Instead, past research has mainly focused on protection mechanisms across high or low thermal extremes. In reality, all plant physical properties (e.g., viscosity of sap or diffusivity) and chemical activities (e.g., solubility or metabolic rates) are functionally related to temperature (Graham and Patterson, 1982), and, consequently, many physiological processes such as respiration, photosynthesis, and carbohydrate balance respond to temperature. Changes in temperature influence all aspects of cellular and physiological functions, even within the range of temperatures regularly experienced by an individual (Larcher, 1995). Moreover, as biochemical pathways are characterized by different thermal kinetics, metabolic processes might be differentially affected by temperature shifts, ultimately altering cellular physiology. The temperature response of biochemical reaction rates is often characterized using the Arrhenius equation (Arrhenius, 1889) and temperature coefficient . Q10 describes the change in reaction rate over 10°C, where and are reaction rates at temperature T1 and T2. In living organisms this coefficient usually varies from 1.5 to 4 for different metabolic reaction and pathways. While in extreme temperatures Q10 may change due to substrate and enzymatic limitations, it is relatively constant within the organism's physiological range of temperatures. For poikilothermic organisms, this range should be relatively wide, e.g., although variable among species (Atkin and Tjoelker, 2003). Because each metabolic pathway has a characteristic Q10, the effective accumulation and degradation of specific products would depend not only on substrate/product availability or quantity of enzyme but also on temperature. For example, the major carbohydrate metabolism pathways of starch degradation and synthesis share substrate–product compounds but differ in participating enzymes. The starch degradation pathway is a spontaneous reaction with Q10 of ∼1.8, while starch synthesis is an ATP-dependent process with Q10 exceeding 3 (Preiss, 1988; Pollock and Lloyd, 1987). Such a large discrepancy of Q10 between starch degradation and synthesis suggests potentially interesting kinetics as temperature changes diurnally and seasonally. It is truly informative to consider the implications of the simple Q10 discrepancy between these two opposing pathways for cellular level carbohydrate management. Assuming similar levels of starch degradation and synthesis in temperature T0 (Fig. 1A), a rise in temperature above T0 will increase starch synthesis activity above starch degradation (Q10 = ∼1.8), due to higher thermal coefficient of the reaction (Q10 > ∼3), and the cell will accumulate starch (T1; Fig. 1A). A drop in temperature below T0 will reduce starch degradation activity less than starch synthesis, and there will be a general shift to accumulate sugars in the cell (T2; Fig. 1A). Thus, a shift between starch accumulation and degradation could be driven by temperature alone, without the need for enzymatic mediation via transcriptional or posttranscriptional control. Of course, the amount of active enzymes would influence the accumulation/degradation temperature threshold and shift the equilibrium temperature to a new value (T3; Fig. 1B). Meanwhile, a potential change in enzyme isoforms could influence the thermal coefficient of the reaction (Volenec et al., 1991) and change the accumulation rate without changing the temperature threshold (T0; Fig. 1B). Moving from the level of the cell to the level of the leaf, one can consider the trend to accumulate starch in leaves during the day (Stitt and Zeeman, 2012). This trend is generally associated with high substrate availability and potentially limited phloem loading capacity, but it can also be related to an increase in leaf temperature during the daytime, which would shift net metabolic activity toward starch accumulation. At night, when temperatures drop below the accumulation threshold, starch would be digested, preparing sugars for nocturnal redistribution. A hypothetical representation of the thermal response of starch metabolism. (A) Starch synthesis and degradation are characterized by two different thermal coefficient where Q10 synthesis > Q10 degradation (gray/black lines). At temperature T0, the processes are in equilibrium (gray circle). However, shifting to a higher temperature (T1) would result in higher activity of starch synthesis than degradation and consequently shift toward starch accumulation, assuming no change in enzyme quantity (blue arrow up). Shifting to a lower temperature (T2) would result in a larger reduction in starch synthesis rate, leading to a net degradation of starch (marked by blue arrow down). (B) Acclimation/active control of starch metabolism can shift due to a change in the quantity of an enzyme or its thermal properties (i.e., the efficiency of the processes). A change in enzyme amount through transcriptional and posttranscriptional modification would shift the equilibrium temperature. In the presented example, a reduction in the concentration of an enzyme for starch synthesis shifts the equilibrium temperature from T0 to T3 (red line and green circle). Modification of enzyme isoforms may result in changes in the ratio of Q10synthesis to Q10degradation (blue line) without shifting the equilibrium point (gray circle). In such a case, the same temperature (compare A and B at T1) might influence net rates of starch accumulation/degradation. The concept of temperature-assisted shifts in carbohydrate metabolism becomes more interesting when we consider the implications for large organisms like trees that must translocate carbohydrates over long distances. Many temperate trees have to survive multiple, often dramatic, thermal events over the course of a year that correspond with critical phenological activities. Specifically, trees must shift and store carbohydrates before dormancy and remobilize them for spring bud break, fruit development, and root growth (Gordon and Dejong, 2007). The soil–atmosphere temperature gradient changes seasonally, undergoing periods when soil is on average warmer then air (fall) and a season when soil is colder than air (spring; Fig. 2). Interestingly, sugars are transported toward roots when the average soil temperature is higher than air (fall) and transported toward the canopy when average temperature of soil is lower than air (spring). Incidentally, this pattern follows the postulated temperature-assisted direction of sugar/starch translocation. Higher soil temperature would promote starch synthesis, and roots would act as a sugar sink, while lower soil temperature would promote starch degradation, and roots would act as sugar source (Fig. 2). Such activities would facilitate cold acclimation in deciduous trees facing long winters (Nguyen et al., 1990) and promote vegetative and reproductive growth in spring (Regier et al., 2010). Diurnally, trees must also redistribute starch across multiple orders of branches. This task may be facilitated by diurnal temperature changes and is potentially linked to stem heat capacity (Stockfors, 2000). Stems could effectively act as a conveyer belt along the shoot-to-roots path that shifts sugar in and out of storage as starch—especially when stem and twig temperatures are out of phase due to differences in their thermal capacitance. Schematic representation of soil/root and tree crown temperature throughout the year. As starch metabolism is characterized by two different thermal coefficients where Q10 synthesis > Q10 degradation, the direction of transport might be facilitated by starch accumulation in the hottest compartment of the tree due to thermal preferences. The metabolic response of trees to diurnal temperature change can broaden our understanding of potential threats to plants under future climate conditions. Climate change may generate extreme weather events that would induce genetically controlled acclimation patterns leading to either survival or mortality. However, with predicted shifts in climate, many environments may become challenging for plants to inhabit when temperature ranges change beyond those needed for maintaining basic homeostasis. According to the sugar/starch temperature-dependent transition and seasonal translocation hypotheses, trees rely on finely tuned spatial temperature differences to accesses stored carbohydrates. Consequently, in a different temperature regime, a lack of access to carbohydrates could amplify stress mortality in trees and could explain why drought-stressed trees die without fully depleting their carbohydrate reserves (Anderegg et al., 2012) or run out of carbohydrates despite relatively mild weather conditions (Sala and Mencuccini, 2014). These examples could possibly result from temperature-related increase in carbohydrate demand for protection (e.g., osmotic adjustment of freezing point depression) and limited accessibility/mobility to storage. Perhaps most relevant to our discussion is the dependency of trees on stored carbohydrates during dormancy, when storage is the only source of energy for any physiological activity. According to our hypothesis, warm winter nights would reduce starch degradation in stems/roots and limit the delivery of sugar to twigs and buds. Inadequate level of sugars near buds would possibly affect bud-break and blooming processes and endanger tree/species survival strategies. In our opinion, the proposed hypothesis of temperature-assisted translocation of carbohydrates in trees opens a novel and exciting research arena. Much can be learned by studying plants as poikilothermic organisms that use basic thermophysical differences among myriads of biological reactions to perform higher-level physiological activities. As our knowledge on transcriptional control of plant biology grows exponentially, we tend to overlook the possibility of direct physiological regulation by physical properties of the environment. Yet, reexamining how basic thermal properties of enzymatic reactions could affect metabolic processes by simply exploiting natural, highly predictable diurnal and seasonal variation in temperature adds new perspective to our understanding of plant physiological adaptation to terrestrial environments. The presented work is supported by California Pistachio Research Board and Almond Board of California to M.Z. We also thank Mason Earles for critical evaluation of the manuscript." @default.
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• W2103809602 title "Temperature-assisted redistribution of carbohydrates in trees" @default.
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