Plant responses to stress impacts: the C we do not see.

The flux of soluble organic carbon (C) from roots to soil (hereafter ‘root exudation’) is believed to have profound effects on C and nutrient cycling in ecosystems. Root exudates can comprise up to 10% of net primary productivity (NPP) in forests (Grayston et al. 1997, Phillips et al. 2011) and may accelerate C and nutrient cycling by up to 30% (Brzostek et al. 2013, Yin et al. 2014, Finzi et al. 2015) through their effects on microbial activity and mineral dissolution (Sulman et al. 2014, Keiluweit et al. 2015). However, despite their importance in altering decomposition and NPP, the primary drivers of exudation remain poorly understood. A primary reason for this is that root exudates are notoriously difficult to collect, especially in field studies. Most exudates are low molecular weight organic compounds that are rapidly assimilated by root-associated soil microbes upon their release into the root apoplast or soil solution. Thus, most of what is known about exudation comes from short-term studies of roots suspended in sterile liquid culture or artificial soil matrices (Phillips et al. 2008). A second impediment to understanding the drivers of exudation is that there are dozens of compounds released by roots (Bais et al. 2006), and the flux of each may depend on whether the exudates are released passively (i.e., via diffusion) or actively (i.e., as an energy dependent process). Given that exudation rates can be driven by environmental conditions, resource availability and plant physiology—factors that may operate alone or in conjunction with one another in nature —it is perhaps unsurprising that we lack a unifying framework for understanding the factors that control this important process. One approach to improving our understanding of exudation in forests is to expose tree seedlings to a range of environmental conditions and develop relationships between exudation rates and other physiological responses. For example, nitrogen (N) stress often increases mass-specific exudation in trees (Aitkenhead-Peterson 2005, Phillips et al. 2009), indicating that tree nutritional status is likely an important regulator of this flux. Similarly, when trees are exposed to elevated CO2, specific exudation rates have been shown to increase, but only under low N (Phillips et al. 2009). While these studies suggest that exudation rates may be driven by a tree’s nutritional status, there have been few investigations of whether other environmental stressors (e.g., low water availability, cold temperatures) also impact exudation. In this issue, Karst et al. report on two overlooked factors that may impact exudation rates in trees: stress and root sugar concentrations. Most root exudates are derived from root nonstructural carbohydrates (NSCs), and are released via the concentration gradients that exist between root cells and the root apoplast (Farrar and Jones 2000, Farrar et al. 2003). Consequently, environmental stressors that alter root sugar concentrations or physically damage roots (Badri and Vivanco 2009) should also impact exudation rates. Karst et al. quantified the relationship between root sugars and exudation—and their interaction with environmental stress—by exposing Populus tremuloides seedlings to three stress treatments (drought, shade and cold), and compared these with non-stressed controls. To facilitate the collection of exudates, the authors grew the seedlings in cuvettes filled with sterile glass beads that provide mechanical impedance to roots, but do not sorb or release C. In general, stressed seedlings exuded more C, with the largest enhancement of specific exudation (fourfold) occurring in trees exposed to cold temperatures. Notably, the increases in exudation occurred despite lower assimilation rates (which can be inferred from the reduced growth rates during the experimental period). Further, the authors found a significant linear relationship between root sugars and exudation across all treatments. These